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High functional diversity within species of arbuscular mycorrhizal fungi
New Phytologist
Abstract
• Species of arbuscular mycorrhizal fungi (AMF) differ markedly in their improvement of plant nutrition and health. However, it is not yet possible to relate the diversity of an AMF community to its functional properties due to the lack of information on the functional diversity at each taxonomic level. This study investigates the inter- and intraspecific functional diversity of four Glomus species in relation to a phylogenetic analysis of large ribosomal subunit (LSU) sequences.• Growth and P nutrition of cucumber (Cucumis sativus) associated with 24 different isolates of AMF were measured in a two-compartment system with a 33P-labelled root-free soil compartment.• Intraspecific differences were found in plant growth response and the extension of the fungal mycelium into the root-free soil patch whereas length-specific P uptake of the hyphae remained rather constant within each AMF species. Hence, the length-specific P uptake differed according to species, whereas lower phylogenetic levels were required to match functional characteristics such as fungal growth pattern and plant growth promotion.• The large intraspecific diversity observed for mycelium growth and improvement of P uptake means that AMF communities of low species diversity may still contain considerable functional heterogeneity.
... Differences in AM fungal colonization traits (e.g. hyphal and spore density, size and turnover, intra-and extraradical growth), plant growth, and nutrient patterns (Hart and Reader, 2002;Marro et al., 2022;Munkvold et al., 2004) have been evidenced among AM fungal taxa, but the factors that drive functionality in terms of infectivity and effectiveness are still not fully understood (Hoeksema et al., 2018;Koch et al., 2017;Säle et al., 2021). Functional variability among AM fungal taxa was reported to be determined by the fungal-host combination (Arcidiacono et al., 2023;Yang et al., 2016), fungal phylogeny (Maherali and Klironomos, 2007;Säle et al., 2021), and local adaptation processes (Ji et al., 2013;Johnson et al., 2010). ...
... Functional variability among AM fungal taxa was reported to be determined by the fungal-host combination (Arcidiacono et al., 2023;Yang et al., 2016), fungal phylogeny (Maherali and Klironomos, 2007;Säle et al., 2021), and local adaptation processes (Ji et al., 2013;Johnson et al., 2010). The magnitude and direction of these effects are also highly variable within fungal orders (Marro et al., 2022), families (Arcidiacono et al., 2023;Horsch et al., 2023;Hart and Reader, 2002), genera (Dodd et al., 2000), species (interspecies variability) as well as isolates within species (intraspecies variability) (Avio et al., 2006;Koch et al., 2006Koch et al., , 2017Munkvold et al., 2004;Marro et al., 2022). A great intraspecific variability has been demonstrated by differential responses of the same host (Munkvold et al., 2004;de Novais et al., 2014;Mensah et al., 2015) or different hosts (Koch et al., 2017;Schoen et al., 2021). ...
... The magnitude and direction of these effects are also highly variable within fungal orders (Marro et al., 2022), families (Arcidiacono et al., 2023;Horsch et al., 2023;Hart and Reader, 2002), genera (Dodd et al., 2000), species (interspecies variability) as well as isolates within species (intraspecies variability) (Avio et al., 2006;Koch et al., 2006Koch et al., , 2017Munkvold et al., 2004;Marro et al., 2022). A great intraspecific variability has been demonstrated by differential responses of the same host (Munkvold et al., 2004;de Novais et al., 2014;Mensah et al., 2015) or different hosts (Koch et al., 2017;Schoen et al., 2021). This was also supported by the occurrence of a high genetic variability among isolates of the same AM fungal species (Corradi and Sanders, 2006;Mathieu et al., 2018). ...
Characterization and selection of arbuscular mycorrhizal fungal (AMF) taxa to design inocula tailored to meet a spectrum of needs is a crucial first step to achieve specific beneficial agronomic functions. Commonly, commercial microbial inocula are based on generalist single AM fungal taxa, having low genetic variability and not offering efficiency and stability when applied in agroecosystems. In this study, we investigated the AMF functional variability at inter-and intra-species levels by characterizing colonization traits, host growth, and mineral uptake of single-spore AM fungi isolated from soils with a fertility gradient. Nineteen single-spore cultures, showing high spore density and AMF colonization, were phylogenetically assigned to different isolates of 3 AMF species (i.e. Entrophospora claroidea, Funneliformis mosseae and Archaeospora trappei). A higher functional variability in infectivity and effectiveness was detected among isolates within AMF species (25 % of total variance) than among AMF species. Most of AMF isolates of F. mosseae have a better outcome in terms of plant growth, although with a performance gradient, while the isolates of E. claroidea showed a variable functional pattern, and those of A. trappei a less variable pattern. Overall, isolates originating from the soil of the conventional arable field with higher pH and phosphorous availability promoted the uptake of plant nutrients, while those originating from soils with higher SOM and plant diversity promoted plant growth. On the contrary, the infectivity traits of the AM fungi were more conserved, as they were not affected by the environmental parameters of the soils of origin. Finally, we highlighted that soil pH played an important role in shaping the pattern of AMF functionality. Boosting the isolation and cultivation of AMF taxa, originating from agricultural and natural soils, is shown to be a key step in exploiting AMF diversity and designing the new generation of microbial inoculants.
... It is well known that the benefits to plant growth conferred by AMF vary much depending on AMF species (Munkvold et al., 2004;Long et al., 2010). Some mechanisms have been proposed to explain this variation (Khalil et al., 1999;Yao et al., 2001aYao et al., , 2001bMunkvold et al., 2004;Yang et al., 2015). ...
... It is well known that the benefits to plant growth conferred by AMF vary much depending on AMF species (Munkvold et al., 2004;Long et al., 2010). Some mechanisms have been proposed to explain this variation (Khalil et al., 1999;Yao et al., 2001aYao et al., , 2001bMunkvold et al., 2004;Yang et al., 2015). Our previous study with three wheat genotypes of different P efficiency revealed that plant P efficiency affected the growth promotion by AMF (Yao et al., 2001a). ...
... These mechanisms stand on the side of host plants, but not on the side of AMF. When standing on the side of AMF, Munkvold et al. (2004) reported that AMF external hyphal length determined the hyphal P uptake in association with cucumber, thus affecting the growth promotion by AMF. Similarly, hyphal P uptake rate was also regarded as key factor affecting the growth promotion by AMF in association of wheat (Yao et al., 2001b). ...
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Arbuscular mycorrhizal fungi (AMF) can promote plant growth and enhance plant drought tolerance with varying effect size among different fungal species. However, the linkage between the variation and the lipid metabolism, which is exclusively derived from plants, has been little explored thus far. Here, we established AM symbiosis between tomato (Solanum lycopersicum) plants and three AMF species (Rhizophagus intraradices, Funneliformis mosseae, Rhizophagus irregularis) under well watered (WW) or drought stressed (DS) conditions in pot experiment. The plant biomass, chlorophyll fluorescence Fv/Fm, shoot P content and mycorrhizal colonization were determined. Meanwhile, fatty acid (FA) profiles and relative expression of genes encoding for nutrition exchange (SlPT4, SlPT5, RAM2, STR/STR2) in roots were also monitored. DS significantly decreased plant
biomass while AMF significantly increased it, with three fungal species varying in their growth promoting capacity and drought tolerance capacity. The growth promoting effect of R. irregularis was lower than those of R. intraradices and F. mosseae, and was associated with higher mycorrhizal colonization and more consumption of lipids. However, the drought tolerance capacity of R. irregularis was greater than those of R. intraradices and
F. mosseae, and was associated with less decrease in mycorrhizal colonization and lipid content. We also found that AMF mediated plant drought tolerance via regulating both AM specific FAs and non-AM specific FAs in a complementary manner. These data suggest that lipid metabolism in AM plays a crucial role in plant drought tolerance mediated by AMF.
... Differences in AM fungal colonization traits (e.g. hyphal and spore density, size and turnover, intra-and extraradical growth), plant growth, and nutrient patterns (Hart and Reader, 2002;Marro et al., 2022;Munkvold et al., 2004) have been evidenced among AM fungal taxa, but the factors that drive functionality in terms of infectivity and effectiveness are still not fully understood (Hoeksema et al., 2018;Koch et al., 2017;Säle et al., 2021). Functional variability among AM fungal taxa was reported to be determined by the fungal-host combination (Arcidiacono et al., 2023;Yang et al., 2016), fungal phylogeny (Maherali and Klironomos, 2007;Säle et al., 2021), and local adaptation processes (Ji et al., 2013;Johnson et al., 2010). ...
... Functional variability among AM fungal taxa was reported to be determined by the fungal-host combination (Arcidiacono et al., 2023;Yang et al., 2016), fungal phylogeny (Maherali and Klironomos, 2007;Säle et al., 2021), and local adaptation processes (Ji et al., 2013;Johnson et al., 2010). The magnitude and direction of these effects are also highly variable within fungal orders (Marro et al., 2022), families (Arcidiacono et al., 2023;Horsch et al., 2023;Hart and Reader, 2002), genera (Dodd et al., 2000), species (interspecies variability) as well as isolates within species (intraspecies variability) (Avio et al., 2006;Koch et al., 2006Koch et al., , 2017Munkvold et al., 2004;Marro et al., 2022). A great intraspecific variability has been demonstrated by differential responses of the same host (Munkvold et al., 2004;de Novais et al., 2014;Mensah et al., 2015) or different hosts (Koch et al., 2017;Schoen et al., 2021). ...
... The magnitude and direction of these effects are also highly variable within fungal orders (Marro et al., 2022), families (Arcidiacono et al., 2023;Horsch et al., 2023;Hart and Reader, 2002), genera (Dodd et al., 2000), species (interspecies variability) as well as isolates within species (intraspecies variability) (Avio et al., 2006;Koch et al., 2006Koch et al., , 2017Munkvold et al., 2004;Marro et al., 2022). A great intraspecific variability has been demonstrated by differential responses of the same host (Munkvold et al., 2004;de Novais et al., 2014;Mensah et al., 2015) or different hosts (Koch et al., 2017;Schoen et al., 2021). This was also supported by the occurrence of a high genetic variability among isolates of the same AM fungal species (Corradi and Sanders, 2006;Mathieu et al., 2018). ...
... Our objective was to gain more insight into species-specific effects between AMF and host weeds. Differences in growth response between AMF species or even between isolates have been shown for several crops and other plants [10,[17][18][19][20]. However, investigations specifically on agriculturally relevant weeds are mostly limited to a few AMF species; screenings encompassing many species and isolates from different families are missing. ...
... For S. nigrum, Vatovec, et al. [22] found no significant effect on growth, although under certain environmental conditions, the growth response tended to be negative, which is similar to our results. On the other hand, different isolates from the same AMF species can lead to contrasting results regarding plant growth response [10,[17][18][19][20]. In our study, these effects were less pronounced, i.e., there were also differences among different isolates of the same species, but they were not significant. ...
Arbuscular mycorrhizal fungi (AMF) have multiple functions in agroecosystems and affect many processes below- and aboveground, including plant productivity. Mycorrhizal symbiosis is not necessarily beneficial for the host plant and the growth response can be not only positive but also neutral or negative. Among other factors, the responsiveness of plants to AMF depends on the plant-fungus combination. To find out whether the AMF species or isolate is a decisive factor for growth responses of weeds, 44 AMF isolates were tested in a pot experiment for their effects on three agricultural weeds: Echinochloa crus-galli, Solanum nigrum and Papaver rhoeas. The 44 isolates cover 18 AMF species from 13 genera and all 5 orders of the Glomeromycota. The aboveground biomass of the weeds was determined after different times of growth of each weed. In most cases, the effects of AMF isolates on weed growth were negative or neutral. We conclude that some weed species do not benefit from AMF in terms of growth. AMF species can even cause negative growth responses, an effect that may be of practical interest for organic farming where the aim is to obtain a high diversity and concentration of native AMF for the benefit of the cultivated crops without increasing the labor for mechanical weeding.
... Así, el hongo puede absorber nutrientes del suelo (especialmente P) que luego transporta a la raíz, a través de las hifas(Smith y Read, 2008). Otras funciones asociadas con la respuesta de las plantas a la colonización por hongos micorrícicos arbusculares jugarían potenciales roles en la determinación de la diversidad vegetal, la variabilidad de los ecosistemas y la productividad(Munkvold et al., 2004;Smith et al., 2004).Como se mencionó, la rizósfera es un lugar de elevada actividad microbiana y estudios indican que la micorrizósfera también lo es, y que las bacterias de suelo pueden asociarse a la región extra-radical de las hifas(Toljander et al., 2006;Jansa et al., 2013). Asimismo, se ha descripto la influencia de los hongos micorrícicos arbusculares en la composición de la comunidad bacteriana, tanto in vivo como in vitro.Marschner et al. (2001) estudiaron de qué modo la inoculación con hongos micorrícicos arbusculares modificaba la composición de la comunidad rizosférica de plantas de maíz.Describieron diferencias en las comunidades bacterianas de plantas micorrizadas y no micorrizadas, y corroboraron que estas diferencias aumentaban si los ensayos se prolongaban en el tiempo.Toljander et al. (2007) demostraron que los exudados de hongos micorrícicos arbusculares tenían efecto directo sobre la comunidad bacteriana del suelo.Ordoñes et al. (2016) analizaron la relación entre bacterias solubilizadoras de P y hongos micorrícicos arbusculares y describieron los efectos sobre el crecimiento de diferentes cepas bacterianas y de estas últimas sobre el crecimiento de hifas extra-radiculares, en raíces de zanahoria y de papa. ...
El objetivo fué determinar especies de hongos filamentosos presentes en cuatro sitios con presencia de Vitis spp en la Región de Los Tuxtla del Estado de Veracruz. Metodología El muestreo de suelo se efectuó de acuerdo con la norma NMX-AA-132-SCFI-2006. Las muestras fueron analizadas en el Laboratorio de Investigación de Recursos Acuáticos (LIRA) dentro de las instalaciones del Instituto Tecnológico de Boca del Rio, para su procesamiento y análisis. Para el aislamiento de los hongos filamentosos del suelo se empleó el método de siembra directa. Los datos de carbono orgánico (C.O.) y materia orgánica (M.O.) fueron confrontados con la abundancia de hongos filamentosos, mediante un análisis estadístico ANDEVA. La comparación de medias se realizó atraves de una prueba de Tukey con un p> 0,05. Resultados Los contenidos de M.O. variaron en los sitios de ambos municipios. los hongos filamentosos considerados como potencialmente benéficos para el enriquecimiento de los suelos que se pudieron determinar son los del género: Adsidia spp, Aspergillus spp y Trichoderma spp. Conclusiones Se encontraron tres géneros de hongos con potencial de enriquecimiento de suelos que son: Trichoderma spp, Aspergillus spp, Absidia spp. Los tres sitios de muestreo de Cerro Vigía fueron en los que se encontraron mayor número de colonias de todos los géneros encontrados. De acuerdo con los avances del presente estudio se requiere de seguir realizando investigaciones para determinar que especies corresponden a estos tres géneros aquí reportados y si tienen el potencial de biorremediar suelos contaminados.
... Fertilization often reduces allocation to extraradical hyphae and arbuscules relative to other structures 32 . The genotypes of the organisms involved and the environmental conditions under which they interact determine the functioning of mycorrhizal association along the mutualistic-parasitic continuum [33][34][35][36][37][38][39][40] . A better understanding of the factors is needed. ...
The presence of Arbuscular Mycorrhizal Fungi (AMF) in vascular land plant roots is one of the most ancient of symbioses supporting nitrogen and phosphorus exchange for photosynthetically derived carbon. Here we provide a multi-scale modeling approach to predict AMF colonization of a worldwide crop from a Recombinant Inbred Line (RIL) population derived from Sorghum bicolor and S. propinquum. The high-throughput phenotyping methods of fungal structures here rely on a Mask Region-based Convolutional Neural Network (Mask R-CNN) in computer vision for pixel-wise fungal structure segmentations and mixed linear models to explore the relations of AMF colonization, root niche, and fungal structure allocation. Models proposed capture over 95% of the variation in AMF colonization as a function of root niche and relative abundance of fungal structures in each plant. Arbuscule allocation is a significant predictor of AMF colonization among sibling plants. Arbuscules and extraradical hyphae implicated in nutrient exchange predict highest AMF colonization in the top root section. Our work demonstrates that deep learning can be used by the community for the high-throughput phenotyping of AMF in plant roots. Mixed linear modeling provides a framework for testing hypotheses about AMF colonization phenotypes as a function of root niche and fungal structure allocations.
... Indeed, establishing connections between AM fungal taxa and/or genotypes (e.g., within species) and their functional roles is a laborious process, which is expected to continue in the foreseeable future (Serghi et al. , 2021;Manley et al. , 2023). This is needed due to the complex links between AM fungi and functional outcomes for both hosts (e.g. , plant growth and fitness, nutrient uptake and stress tolerance) and soil functions/properties (e.g. , carbon storage, aggregate stability, biotic diversity), which appear to be highly context dependent and relatively poorly predicted by taxonomy alone (Munkvold et al. , 2004;Koch et al. , 2017;Yang et al. , 2017;Qiu et al. , 2021). However, this effort is also required because AM fungal traits have not been systematically assessed alongside with hypotheses of adaptation or with specific mechanisms in mind. ...
... Moreover, the study revealed a high mycorrhizal dependency of five of the plant species investigated, suggesting that, overall, the limited growth of control plants could be ascribed to the lack of adequate AMF inoculum (Camprubi et al. 2011). As the consortium of native AMF was composed of diverse AMF species, it is conceivable that they reflected a high functional diversity, consistent with previous findings (Munkvold et al. 2004;Mensah et al. 2015;Turrini et al. 2018). ...
Climate change and global warming have contributed to increase terrestrial drought, causing negative impacts on agricultural production. Drought stress may be addressed using novel agronomic practices and beneficial soil microorganisms, such as arbuscular mycorrhizal fungi (AMF), able to enhance plant use efficiency of soil resources and water and increase plant antioxidant defence systems. Specific traits functional to plant resilience improvement in dry conditions could have developed in AMF growing in association with xerophytic plants in maritime sand dunes, a drought-stressed and low-fertility environment. The most studied of such plants are European beachgrass (Ammophila arenaria Link), native to Europe and the Mediterranean basin, and American beachgrass (Ammophila breviligulata Fern.), found in North America. Given the critical role of AMF for the survival of these beachgrasses, knowledge of the composition of AMF communities colonizing their roots and rhizospheres and their distribution worldwide is fundamental for the location and isolation of native AMF as potential candidates to be tested for promoting crop growth and resilience under climate change. This review provides quantitative and qualitative data on the occurrence of AMF communities of A. arenaria and A. breviligulata growing in European, Mediterranean basin and North American maritime sand dunes, as detected by morphological studies, trap culture isolation and molecular methods, and reports on their symbiotic performance. Moreover, the review indicates the dominant AMF species associated with the two Ammophila species and the common species to be further studied to assess possible specific traits increasing their host plants resilience toward drought stress under climate change.
... The biocontrol effect of AMF against PPN depends on several factors. One of them may be the AMF species involved, as different AMF isolates are expected to affect plant growth, nutrition, and stress responses differently (Mensah et al. 2015;Munkvold et al. 2004;Sikes et al. 2009). Most studies testing plant responses to AMF have used Rhizophagus irregularis and Funneliformis mosseae (Glomerales), as they are considered generalists and ubiquitous species; however, these species can be quite heterogeneous in their functionality (Berruti et al. 2016). ...
Arbuscular mycorrhizal fungi (AMF) can increase plant tolerance and/or resistance to pests such as the root-knot nematode Meloidogyne incognita. However, the ameliorative effects may depend on AMF species. The aim of this work was therefore to evaluate whether four AMF species differentially affect plant performance in response to M. incognita infection. Tomato plants grown in greenhouse conditions were inoculated with four different AMF isolates (Claroideoglomus claroideum, Funneliformis mosseae, Gigaspora margarita, and Rhizophagus intraradices) and infected with 100 second stage juveniles of M. incognita at two different times: simultaneously or 2 weeks after the inoculation with AMF. After 60 days, the number of galls, egg masses, and reproduction factor of the nematodes were assessed along with plant biomass, phosphorus (P), and nitrogen concentrations in roots and shoots and root colonization by AMF. Only the simultaneous nematode inoculation without AMF caused a large reduction in plant shoot biomass, while all AMF species were able to ameliorate this effect and improve plant P uptake. The AMF isolates responded differently to the interaction with nematodes, either increasing the frequency of vesicles (C. claroideum) or reducing the number of arbuscules (F. mosseae and Gi. margarita). AMF inoculation did not decrease galls; however, it reduced the number of egg masses per gall in nematode simultaneous inoculation, except for C. claroideum. This work shows the importance of biotic stress alleviation associated with an improvement in P uptake and mediated by four different AMF species, irrespective of their fungal root colonization levels and specific interactions with the parasite.
... This suggests that species belonging to the same family may show high functional variability. This supports previous finding on intra-family variation of plant growth and nutrient uptake (i.e., N and P) along with mycelium size and structure (Hart and Reader 2002;Munkvold et al. 2004). In addition to the intra-family functional variability, a little functional consistency was also previously found at species level (Avio et al. 2006;Börstler et al. 2008Börstler et al. , 2010Hart and Reader 2002;Koch et al. 2006;Mensah et al. 2015). ...
Contrasting life-history characteristics of arbuscular mycorrhizal (AM) fungal families may have important implications for mycorrhizal functioning. Nevertheless, the effect of inoculation with AM fungi having different life-history strategies on the quality parameters of tomato fruits was not investigated. In this study, fruit and sauce quality of two tomato varieties were evaluated in field conditions after inoculation with four AM fungal species belonging to Glomeraceae and Gigasporaceae. The functional relationship between AM fungal traits (i.e., root colonization structures, community diversity) and fruit quality parameters was analyzed. AM fungal inoculation increased total phenols (TPC) and lycopene concentration in fruits of both varieties (47% and 247%, respectively) and antioxidant activity in var. Rio Grande (85%). Gigasporaceae were more effective in increasing TPC and antioxidant activity compared to Glomeraceae in var. Rio Grande. Gigaspora gigantea outperformed Scutellospora pellucida in var. Pisanello for TPC, antioxidant activity, and lycopene. Inoculated strains of G. gigantea, S. pellucida, Funneliformis mosseae, and Sclerocystis sinuosa were molecularly retrieved within tomato roots. In both varieties, a functional relationship between occurrence of arbuscules in roots and fruit quality was found. In var. Rio Grande, the abundance of some native AM fungal taxa shaped the pattern of fruit quality parameters. Gigasporaceae might be of great relevance for the synthesis of health-promoting compounds in tomato and should be included in biostimulant programmes targeting the production of high-quality vegetables.
... Past work examining plant responses to inoculation with individual AMF species suggests that the impact of AMF on nutrient uptake varies by fungal and host species wherein the relationship lies on a spectrum of mutualism to fungal parasitism Klironomos, 2003;Mensah et al., 2015;Munkvold et al., 2004;Smith et al., 2004). This observed variability in the benefits of mycorrhizal inoculation on host plants is likely due to a range in the plant C costs of nutrient return across AMF species. ...
The use of arbuscular mycorrhizal fungi (AMF) as biofertilizers has proven successful in boosting the yield and nutritional quality of a variety of crops. AMF associate with plant roots and exchange soil nutrients for photosynthetically derived C in the form of sugars and lipids. Past research has shown that not all AMF species are equal in their benefit to nutrient uptake and crop health, and that the most beneficial AMF species appear to vary by host species. Although an important human food staple, especially in developing regions where nutrient deficiency is a prevalent threat to public health, little work has been done to test the effectiveness of AMF in enhancing the nutritional quality of common bean ( Phaseolus vulgaris L. ). Therefore, our objective was to determine the most beneficial AMF species for inoculation of this important crop. We inoculated black beans ( Phaseolus vulgaris black turtle beans) with eight individual AMF species and one mixed species inoculum in an outdoor pot trial over 3 months and assessed the extent to which they altered yield, mineral nutrient and anthocyanin concentration of seeds and leaf tissues. Despite seeing no yield effects from inoculation, we found that across treatments percent root length colonized by AMF was positively correlated with plant tissue P, Cu, and Zn concentration. Underlying these broad benefits, seeds from plants inoculated with three AMF species, Claroideoglomus claroideum (+15%), Funneliformis mosseae (+13%), and Gigaspora rosea (+11%) had higher P concentration than non‐mycorrhizal plants. C. claroideum also increased seed potassium (K) and copper (Cu), as well as leaf aluminum (Al) concentration making it a promising candidate to further test the benefit of individual AMF species on black bean growth in field trials.
... According to Opik et al. [79] , for single species inoculation, three AMF species viz. Rhizophagus intraradices, Rhizophagus irregularis and Funneliformis mossae are subjected to most scientific studies because these are extremely versatile symbionts that can colonise a wide range of host plants, maintain long-term storage, disperse widely across the world and quickly and massively reproduce. ...
Arbuscular Mycorrhizal Fungi (AMF) are a group of soil-borne fungi that form symbiotic relationships with the roots of most plants, including crops. In this relationship, the fungus provides the plant with nutrients, such as phosphorus, in exchange for carbohydrates produced by the plant through photosynthesis. The use of AMF as a biofertilizer involves the application of these fungi to soil to enhance plant growth and improve nutrient uptake. Studies have shown that AMF can increase plant growth, drought tolerance, and nutrient uptake, leading to improved crop yields. The fungi form a network of hyphae in the soil, which helps to increase the soil's water-holding capacity, as well as its ability to retain nutrients. This can lead to improved plant growth and health, even in nutrient-poor soils. In addition, the use of AMF as a biofertilizer can help to reduce the dependence on synthetic fertilizers, which can have negative environmental impacts. AMF can help to improve soil fertility, increase plant nutrient uptake, and reduce soil erosion, leading to more sustainable agriculture practices. However, it is important to note that the effectiveness of AMF as a biofertilizer can vary depending on several factors, including the species of AMF used, the type of crop being grown, and the conditions of the soil. Additionally, the proper application and management of AMF is important to ensure its effectiveness. In conclusion, the use of AMF as a biofertilizer has the potential to enhance plant growth, improve nutrient uptake, and promote sustainable agriculture practices.
... Among the AMF orders, the more common were Glomerales, Archaeosporales and Diversisporales. These orders, mainly Glomerales, are generally found in arable fields (Daniell et al., 2001;Higo et al., 2015;Oehl et al., 2010), but their functional differences are not yet well known (Burleigh et al., 2002;Munkvold et al., 2004). Our results show that the legacy of CC determines the abundance, richness and structure of fungal communities associated to the roots of subsequent main crops. ...
Cover crops (CC) can promote nutrient retention and recycling for main crops, yet may also promote soil‐borne pathogens or suppress beneficial root symbionts such as arbuscular mycorrhizal fungi (AMF). We investigated how root fungal communities of main crop are affected by preceding CC monocultures and mixtures and by main crop identity. We expected that AMF abundance and diversity in main crops are promoted by AM‐host CC, and suppressed by non‐AM host CC, and that mixtures of CC species can promote beneficial and suppress pathogenic root fungi. Our full‐factorial field experiment comprised a crop rotation in a sand soil with different CC treatments (monocultures of radish (AM non‐host), ryegrass, clover, vetch (AM‐hosts), mixtures of radish+vetch, ryegrass+clover, and fallow), and two main crops (oat and endive). At peak crop growth we investigated the root fungal communities in the main crops using microscopy and high throughput sequencing (Illumina MiSeq). Cover crop identity was of prime importance and CC legacy overruled main crop identity in determining root fungal communities in main crops. Compared to fallow CC with ryegrass increased AMF colonization and richness in both main crops and of non‐AMF in oat. Legacies of ryegrass, ryegrass+clover and vetch resulted in distinct root fungal communities in the main crops, while the legacy of CC with radish were similar to the legacy of fallow. Root fungal community in crops after clover had highest abundance of representative fungal pathogens in contrast with the other CC treatments that resulted in fungal communities where pathogens were scarce. Oppositely to expected, CC mixtures did not enhance fungal symbionts or suppressed pathogens. Overall, fungal communities in roots of the main crops in our field experiment, were determined by the preceding CC species in monoculture, rather than by the CC AMF preference or functional group. This research highlights that the choice of CC determines the root fungal community in main crop which may influence crop quality.
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... Ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) fungi are two main plant mycorrhizal symbionts for woody plant species in forests [25]. EcM fungi and AM fungi could improve the P absorption of EcM and AM plants [26][27][28] and further affect plant species diversity [29,30]. P addition can cause changes in the species composition of AM fungi in tropical montane forests [31], and habitat fragmentation could also cause changes in the community composition of mycorrhizal fungi [32]. ...
Global changes in nutrient deposition rates and habitat fragmentation are likely to have profound effects on plant communities, particularly in the nutrient-limited systems of the tropics and subtropics. However, it remains unclear how increased phosphorus (P) supply affects seedling growth in P-deficient subtropical fragmented forests. To explore this, we applied P to 11 islands in a subtropical Chinese archipelago and examined the results in combination with a contemporary greenhouse experiment to test the influence of P addition on seedling growth and survival. We measured the growth (i.e., base area) and mortality rate of seedlings for one arbuscular mycorrhizal (AM) and one ectomycorrhizal (EcM) tree species separately and calculated their relative growth rate and mortality when compared with P addition and control treatment on each island. We also measured three functional traits and the biomass of seedlings in the greenhouse experiment. Results showed that P addition significantly increased the mortality of AM and EcM seedlings and reduced the growth rate of EcM seedlings. The relative growth rate of AM seedlings, but not EcM seedlings, significantly decreased as the island area decreased, suggesting that P addition could promote the relative growth rate of AM seedlings on larger islands. The greenhouse experiment showed that P addition could reduce the specific root length of AM and EcM seedlings and reduce the aboveground and total biomass of seedlings, indicating that P addition may affect the resource acquisition of seedlings, thereby affecting their survival and growth. Our study reveals the synergistic influence of habitat fragmentation and P deposition, which may affect the regeneration of forest communities and biodiversity maintenance in fragmented habitats.
... We observed that the three grass species used here (i.e. A. odoratum, K. macrantha and F. ovina) systematically showed higher biomass when grown together with the Rhizoglomus isolate BEG-21, compared to the isolates DD-1 and DD-3. Other studies have shown that certain Rhizoglomus isolates can colonize plant roots to a greater degree and be more effective in promoting growth than other isolates (Munkvold et al., 2004;Paul Schreiner, 2007). However, roots of all plant species investigated here were equally colonized by the three AMF isolates tested, suggesting that no selectivity for colonization existed as found elsewhere (Helgason et al., 2002). ...
Plant colonization by arbuscular mycorrhizal fungi (AMF) is widespread and can offer considerable benefits in terms of growth, nutrient uptake and plant yield. However, it is still unresolved how different plant species and plant functional groups respond to AMF and to different AMF taxa.
Here we established 336 grassland microcosms to determine the response of 14 plant species displaying contrasting functional groups (grasses, legumes and non‐leguminous forbs) for the presence of three different AMF taxa. For each plant species, we calculated the degree to which plant growth depended on AMF colonization (i.e. mycorrhizal dependency [MD]). We also determined the degree to which each plant species relied on specific AMF taxa for optimal growth (i.e. mycorrhizal species sensitivity [MSS]). Additionally, we determined whether MD and MSS correlated to specific plant traits (i.e. specific root length [SRL], specific leaf area [SLA]).
The plant growth response to AMF ranged from −84.9% for a non‐mycorrhizal plant (Luzula campestris) to +94.0% for a legume (Trifolium arvensis). The MD was systematically higher in legumes (91.9% ± 2.4%), followed by non‐leguminous forbs (77.1% ± 11.06) and grasses (42.1% ± 15.73%). MSS was less variable (8.9%–37.7%); it was independent of plant functional group and did not correlate with MD. MD was linked to various mycorrhizal plant parameters, including AMF colonization (R² = +0.80) and total dry biomass (R² = +0.32). Moreover, among mycorrhizal plants (n = 12), MD negatively correlated with SRL (R² = −0.24) and positively with SLA (R² = +0.24).
Synthesis. This study shows that plants relying on AMF for biomass production also show higher root colonization, lower SRL, higher SLA and that different plant traits are interlinked with the way how plants respond to AMF. Overall, this study further demonstrates that different plant functional groups vary in their response to AMF.
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... However, an increase in AMF colonization does not necessarily translate directly into increased crop yields. Approximately 300 species of AMF have been identified [10], although different species have been reported to have different capacities to acquire P [11,12]. It has been reported that there exists variations in the capacity of different AMF species or community levels to assimilate P for plant growth in controlled and field conditions [13][14][15][16][17][18]. ...
This study investigated the effects of arbuscular mycorrhizal fungi (AMF) on the growth, phosphorus (P) uptake, and yield of maize in the presence or absence of tillage. The two-year field experiment was conducted in Kanagawa, Japan. Firstly, we investigated whether the presence of indigenous AMF communities in the roots, as determined by amplicon sequencing analysis, contributed to maize growth in Experiment 1, a 2-year field-based study. The findings revealed that the maize (Zea mays L.) in rotary tillage had higher P uptake, growth at the six-leaves collar stage, and yield, compared to no tillage. The AMF communities colonizing maize roots were altered by the presence or absence of tillage; specifically, tillage increased the dominance of the Gigasporaceae, whereas no tillage increased the dominance of the Acaulosporaceae. Based on these findings, we confirmed whether the inoculation of similar AMF strains, as analyzed in the field study of tillage practices on maize roots, produces growth-promoting effects for maize growth in a controlled pot experiment consistent with the results of the field experiment. For experiment 2, Dentiscutata cerradensis TK-1, Cetraspora pellucida SZ-3 (Gigasporaceae), Acaulospora morrowiae AP-5, and A. longula F-1 (Acaulosporaceae) were inoculated as AMF inocula for a pot experiment. The results showed that aboveground biomass did not change with any inoculum compared to the control. The P concentration in maize was higher for D. cerradensis TK-1 and C. pellucida SZ-3 inoculation than for the control. However, inoculation with A. morrowiae AP-5 and A. longula F-1 did not change P concentrations from the control. This indicates that D. cerradensis TK-1 and C. pellucida SZ-3 are more effective in promoting P uptake in maize than in A morrowiae AP-5 and A. longula F-1. Based on field and pot experiments, our findings suggest that tillage practices lead to alterations in the AMF communities that colonize the roots, and this shift may also contribute to changes in P uptake and crop growth.
... The behaviour of F. mosseae might be related to peculiar charateristics of this AM fungal species. Funneliformis mosseae is known to be ubiquitous in agricultural soils (Helgason et al. 1998;Pellegrino et al. 2020), quickly colonize plant roots (Chagnon et al. 2013) and facilitate shoot biomass and root length, as well as shoot and fungal P uptake respect to other species belonging to the same family (Avio et al. 2006;Munkvold et al. 2004). ...
Purpose
Plant microbial biostimulants, such as arbuscular mycorrhizal fungi (AMF), enhance nutrient concentration in fruits, including tomato. However, field studies on tomato AMF inoculation are scarce. AMF species belonging to Gigasporaceae and Glomeraceae families known to vary in life-history strategies may determine differential effects on plant nutrient benefits and residue decomposition. Despite this, the effect of different life-history strategies on nutrient acquisition of tomato fruits has not been investigated yet.
Methods
We studied the effect of inoculation of two tomato varieties with four AMF species belonging to Glomeraceae and Gigasporaceae. Fungal colonization, yield, fruit nutrient concentration, litter decomposition, and bacterial and fungal abundances in soil were assessed in the field under organic agriculture.
Results
Overall Gigasporaceae promoted the concentration of nutrients in tomato fruits compared to Glomeraceae. A variability in AM fungal colonization and fruit nutrient concentration was detected within Glomeraceae. Scutellospora pellucida increased the yield (+ 27%) of var. Rio Grande with respect to Gigaspora gigantea . In var. Rio Grande, inoculation with Funneliformis mosseae did not change litter decomposition as compared to non-inoculated controls, whereas it was lower than in Sclerocystis sinuosa and Gigasporaceae species, which showed the highest decomposition rates. AMF inoculation promoted soil total bacterial and fungal abundance and fungal:bacterial (F:B) ratio compared to controls, and members of Gigasporaceae had the highest F:B ratio.
Conclusion
These findings pointed at the inclusion of AM fungal life-history strategy within the selection criteria for the development of biofertilizers able to enhance the nutritional value of vegetables under organic farming systems.
... Functional diversifi cation among isolates in the same AM fungal species has recently been suggested from the different effects on plant growth (Munkvold et al. 2004). Under water-stressed conditions, some AM fungi adapt to such environmental conditions. ...
The community structure of arbuscular mycorrhizal (AM) fungi in the roots of drought-resistant trees, Moringa spp., was examined in semiarid regions in Madagascar and Uganda. Root samples were collected from 8 individuals of M. hildebrandtii and 2 individuals of M. drouhardii in Madagascar and from 21 individuals of M. oleifera in Uganda. Total DNA was extracted from the root samples, and partial nSSU rDNA of AM fungi was amplified using a universal eukaryotic primer NS31 and an AM fungalspecific primer AM1. The PCR products were cloned and divided by restriction fragment length polymorphism (RFLP) analysis with HinfI and RsaI. Some representatives in each RFLP types were sequenced, and a neighbor-joining phylogenetic analysis was conducted for the obtained sequences with analogous sequences of AM fungi. The RFLP and phylogenetic analyses showed that AM fungi closely related to Glomus intraradices or G. sinuosum were detected in many samples. The AM fungal groups frequently detected in the Moringa spp. might be widely distributed species in semiarid environments.
... For statistical details, see Table 2 and Supplementary Table 1. the benefits of AMF inoculation on mycorrhizal plants ability for interspecific competition with regard to biomass and nutrients. Another study has revealed that the AMF community might induce variable plant growth responses (Munkvold et al., 2004). Considering our study, in both harvests, V. faba is the stronger competitor than B. napus in terms of plant growth responses, which reveals that AMF inoculation contributes to reduce the growth rate in non-host plants (Jordan et al., 2000;Facelli et al., 2010). ...
In the Tibetan Plateau grassland ecosystems, nitrogen (N) availability is rising dramatically; however, the influence of higher N on the arbuscular mycorrhizal fungi (AMF) might impact on plant competitive interactions. Therefore, understanding the part played by AMF in the competition between Vicia faba and Brassica napus and its dependence on the N-addition status is necessary. To address this, a glasshouse experiment was conducted to examine whether the grassland AMF community’s inocula (AMF and NAMF) and N-addition levels (N-0 and N-15) alter plant competition between V. faba and B. napus. Two harvests took day 45 (1st harvest) and day 90 (2nd harvest), respectively. The findings showed that compared to B. napus, AMF inoculation significantly improved the competitive potential of the V. faba. In the occurrence of AMF, V. faba was the strongest competitor being facilitated by B. napus in both harvests. While under N-15, AMF significantly enhanced tissue N:P ratio in B. napus mixed-culture at 1st harvest, the opposite trend was observed in 2nd harvest. The mycorrhizal growth dependency slightly negatively affected mixed-culture compared to monoculture under both N-addition treatments. The aggressivity index of AMF plants was higher than NAMF plants with both N-addition and harvests. Our observation highlights that mycorrhizal associations might facilitate host plant species in mixed-culture with non-host plant species. Additionally, interacting with N-addition, AMF could impact the competitive ability of the host plant not only directly but also indirectly, thereby changing the growth and nutrient uptake of competing plant species.
... Differences in the impact of AMF species on nutrient uptake and growth of plant hosts have been documented, and species with a greater ability to access and transfer nutrients to host plants at lower C costs better benefit plant health. (Carrara & Heller, 2022;Cavagnaro et al., 2005;Feddermann et al., 2008;Hart & Reader, 2002;Lanfranco et al., 2018;Munkvold et al., 2004). Past work on mycorrhizal nitrogen (N) uptake and transfer to host plants has shown that direct mycorrhizal uptake of amino acids from soil is an important component of the plantmycorrhizal N economy (Talbot & Treseder, 2010;Whiteside et al., 2012). ...
Societal Impact Statement
Evidence has emerged that the antioxidant ergothioneine may be important in preventing many inflammatory diseases in humans. However, ergothioneine is not produced by humans or plants and is only made by fungi and some bacteria in soils. As such, humans get ergothioneine from eating fungi (mushrooms) or plants that take it up from the soil. In this study, we found that growing plants with beneficial fungi called arbuscular mycorrhizal fungi increased the amount of ergothioneine in plant tissues. This suggests that promoting agricultural practices that maintain healthy populations of beneficial soil fungi may improve the nutritional quality of crops.
Summary
The amino acid ergothioneine (ERGO) has recently gained attention as an antioxidant that benefits human health. ERGO is produced by fungi and mycobacteria in soils and is acquired only from diet. The mechanism by which ERGO is transferred from soil to plant is unknown. Recent work has shown that tillage reduces the amount of ERGO in crops. As tillage also reduces arbuscular mycorrhizal fungi (AMF) populations, we examined the relationship between AMF and plant ERGO uptake.
We grew asparagus, black beans, wheat, and oats with a variety of single and mixed species AMF inocula and compared ERGO levels of these plants to plants that were uninoculated.
Mycorrhizal inoculation enhanced ERGO content across all plants. There was a positive correlation between AMF colonization level and plant ERGO content.
AMF appear to be important mediators of plant ERGO uptake. Future research is needed to identify the mechanism that leads to higher ERGO in plants colonized by AMF in order to promote farming practices that enhance AMF populations and increase crop ERGO concentration in field settings.
... These organisms have been ideal for premium inoculum components due to their above described characteristics. "Several experiments have found that various isolates within the same species can induce broader differences in plant reaction rather than varying species [41,20,4]. This indicates that widespread use of single AM fungal organisms, such as R. intraradices, R. irregularis, and F. mosseae should not be considered a defect in inoculation trials because these organisms may possess substantial functional heterogeneity. ...
Arbuscular Mycorrhizal Fungi (AMF) are a group of soil-borne fungi that form symbiotic relationships with the roots of most plants, including crops. In this relationship, the fungus provides the plant with nutrients, such as phosphorous, in exchange for carbohydrates produced by the plant through photosynthesis. The use of AMF as a biofertilizer involves the application of these fungi to soil to enhance plant growth and improve nutrient uptake. Studies have shown that AMF can increase plant growth, drought tolerance, and nutrient uptake, leading to improved crop yields. The fungi form a network of hyphae in the soil, which helps to increase the soil's water-holding capacity, as well as its ability to retain nutrients. This can lead to improved plant growth and health, even in nutrient-poor soils. In addition, the use of AMF as a biofertilizer can help to reduce the dependence on synthetic fertilizers, which can have negative environmental impacts. AMF can help to improve soil fertility, increase plant nutrient uptake, and reduce soil erosion, leading to more sustainable agriculture practices. However, it is important to note that the effectiveness of AMF as a biofertilizer can vary depending on several factors, including the species of AMF used, the type of crop being grown, and the conditions of the soil. Additionally, the proper application and management of AMF is important to ensure its effectiveness. In conclusion, the use of AMF as a biofertilizer has the potential to enhance plant growth, improve nutrient uptake, and promote sustainable agriculture practices.
... This suggests that different AMF communities can have specific effects on grapevine rootstock uptake of different macro-and micro-nutrients. Previous studies have shown that genetically different AMF isolates, even from the same species, have different effects on their host plants with respect to nutrient uptake [46,47]. ...
Arbuscular mycorrhizal fungi (AMF) deliver potentially significant services in sustainable agricultural ecosystems, yet we still lack evidence showing how AMF abundance and/or community composition can benefit crops. In this study, we manipulated AMF communities in grapevine rootstock and measured plant growth and physiological responses. Glasshouse experiments were set up to determine the interaction between rootstock variety and different AMF communities, using AMF communities originating under their own (i.e., “home”) soil and other rootstocks’ (i.e., “away”) soil. The results revealed that specific AMF communities had differential effects on grapevine rootstock growth and nutrient uptake. It was demonstrated that a rootstock generally performed better in the presence of its own AMF community. This study also showed that AMF spore diversity and the relative abundance of certain species is an important factor as, when present in equal abundance, competition between species was indicated to occur, resulting in a reduction in the positive growth outcomes. Moreover, there was a significant difference between the communities with some AMF communities increasing plant growth and nutrient uptake compared with others. The outcomes also demonstrated that some AMF communities indirectly influenced the chlorophyll content in grapevine leaves through the increase of specific nutrients such as K, Mn, and Zn. The findings also indicated that some AMF species may deliver particular benefits to grapevine plants. This work has provided an improved understanding of community level AMF-grapevine interaction and delivered an increased knowledge of the ecosystem services they provide which will benefit the wine growers and the viticulture industry.
... Accordingly, Powell et al. (2009) found that evolution of increased soil colonization is positively correlated with total plant biomass. Thus, we can support that the agroecological relevance of the lifestrategies of the two AM fungal families in term of productivity may have been modulated in our study also by other site-speci c factors, such as soil disturbance, texture, pH, availabilities of mineral nutrients, plant genotype or the active microbiome shaped by the hyphal exudates (Hart and Reader 2004;Klironomos 2000Klironomos , 2003Lekberg et al. 2007; van der Heijden and Scheublin, 2007; Zhou et al. 2020), as well as by the intra-family AM fungal functional variability (Avio et al. 2006;Munkvold et al. 2004). The intra-family variability was supported by the higher total yield found in the var. ...
Purpose: In the scenario of an increased atmospheric CO2 concentration, nutrients are reduced in all vegetables. In this context, arbuscular mycorrhizal fungi (AMF) could enhance nutrient concentration in edible portions of plants, including tomato. However, field studies on tomato AMF inoculation are scarse. AMF species belonging to Gigasporaceae and Glomeraceae families known to vary in life-history strategies may determine differential effects on plant nutrient benefits and residue decomposition. Despite this, the effect of different life-history strategies on nutrient acquisition of tomato fruits has not yet been investigated.
Methods: We studied the effect of inoculation of two tomato varieties with AMF belonging to Glomeraceae and Gigasporaceae. Fungal establishment, yield, fruit nutrient concentration, litter decomposition, and bacterial and fungal abundances in soil were assessed in a two-year field trial under organic agriculture.
Results: Overall Gigasporaceae promoted the concentration of nutrients in tomato fruits compared to Glomeraceae. A variability in AM fungal colonization and fruit nutrient concentration occurred within Glomeraceae. Scutellospora pellucida increased the yield (+27%) of var. Rio Grande respect to Gigaspora gigantea. In var. Rio Grande, Funneliformis mosseae determined a litter degradation similar to controls and lower than Sclerocystis sinuosa and Gigasporaceae species, which showed the highest decomposition rates. AMF inoculation promoted soil total bacterial and fungal abundance and fungal:bacterial (F:B) ratio compared to controls, and members of Gigasporaceae had the highest F:B ratio.
Conclusion: These findings strongly support that AM fungal life-history strategy should be considered in biofertilizer development to enhance the nutritional value of vegetables under organic farming systems.
... Arbuscular mycorrhizae (AM), originally named vesicular-arbuscular mycorrhizae, are symbiotic mutualistic relationships among most vascular plant roots and a few species of fungi of the novel phylum Glomeromycota (Schüßler et al. 2001) More than 80% of land plant communities form mutualistic relationships with AM species, playing a major role in the performance of the plants (Munkvold et al. 2004). There are two main types of AM: The Paris type and the Arum type (Smith and Read 1997;Peterson et al. 2004;Matsuda et al. 2021). ...
Plant-microbe associations contribute significantly to the nutrient supply of their host plant and may assist the plant in resolving a number of abiotic and biotic stresses. Plant-microbe interactions can be beneficial, harmful or neutral and they have a direct impact on ecological processes such as nutrient availability and plant health. Understanding how this association ensures a healthy balance in nature with the help of secondary metabolites is crucial for the maintenance of soil ecosystems. Secondary metabolites generated by plant microbes and the mechanisms that underpin plant-microbe interactions in symbiotic relationships and biocontrol activities are poorly understood. The summarization of such information is needed at this time. Therefore, this chapter mainly focuses on different compounds or metabolites that influence the communication of plant-microbes in the rhizosphere soil and how these associations are important for maintaining nutrient availability, fertility of soil and plant productivity in healthy as well as stressed plants through release of exudates in the rhizosphere.
... VTX00112 was abundant under the NT-based systems and was rare under CT systems, whereas Glomus VTX00132 showed the opposite behaviour. These results support the high functional variability within the family Glomeraceae, as previously reported in some studies (Avio et al. 2006;Munkvold et al. 2004). In contrast to previous studies that found Gigasporaceae propagating from intact mycelia to be abundant under NT systems but Fig. 3 Principal coordinates analysis (PCoA) based on Bray-Curtis distance dissimilarity of fourth-root transformed AMF community relative abundances. ...
Weeds are responsible for major crop losses worldwide but can provide beneficial agroecosystem services. This study aimed to elucidate how arbuscular mycorrhizal fungi (AMF) in weeds respond to host identity and conservation agricultural practices. The study was carried out at two locations in Southern Africa during off-season and in-season maize cultivation. Off-season AMF root colonisation, diversity indices and community composition significantly differed among weed species at both locations. Glomus sp. VTX00280 explains most of the AMF community differences. In-season, implementation of conventional tillage with mulching alone (CT + M) or together with crop rotation (CT + M + R) resulted in a 20% increase in AMF colonisation of the constantly occurring weed species, Bidens pilosa (BIDPI) and Richardia scabra (RCHSC), compared with conventional tillage plus rotations (CT + R). The diversity of AMF was highest under no-tillage plus mulching (NT + M). Off-season and in-season AMF structures of both BIDPI and RCHSC were not related, but 39% of the taxa were shared. Structural equation modelling showed a significant effect of the cropping system on weed AMF diversity parameters and weed and maize root colonisation, but no significant influence of weed root AMF traits and maize colonisation was detected on maize yield. This may be explained by the improvement in weed competitive ability, which may have offset the AMF-mediated benefits on yield. Our findings highlight that implementing M and CR to CT and NT positively affected weed AMF colonisation and diversity. The similarity between the off-season and in-season AMF composition of weeds supports the fact that weeds functionally host AMF during the non-crop period.
... Meanwhile, the long-term objective for mycorrhizal ecophysiologists should still be to isolate and culture strains, and make these permanent resources for them and other research groups to measure traits in future studies. Intraspecific trait variation appears so important, at least for arbuscular mycorrhizal fungi (e.g., Munkvold et al., 2004;Antunes et al., 2011), that strain identity will be just as important as species identity in building trait databases. And as mycorrhizal ecophysiology matures, new traits will gain interest and have to be measured on those strains for which we have already measured a number of other traits. ...
... High levels of intra-specific genomic and phenotypic variation have been reported for AM fungi, including examples from the genus Funneliformis (Munkvold et al. 2004). Based on genetic markers, variation also has been observed within morpho-species assigned to Funneliformis, collected from fallow and cultivated soils (Rosendahl and Matzen 2008). ...
Arbuscular mycorrhizal (AM) fungi are ubiquitous mutualistic symbionts of most terrestrial plants and many complete their lifecycles underground. Whole genome analysis of AM fungi has long been restricted to species and strains that can be maintained under controlled conditions that facilitate collection of biological samples. There is some evidence suggesting that AM fungi can adapt to culture resulting in phenotypic and possibly also genotypic changes in the fungi. In this study, we used field isolated spores of AM fungi and identified them as Funneliformis geosporum based on morphology and phylogenetic analyses. We separately assembled the genomes of two representative spores using DNA sequences of 19 and 22 individually amplified nuclei. The genomes were compared with previously published data from other members of Glomeraceae including two strains of F. mosseae . No significant differences were observed among the species in terms of gene content, while the single nucleotide polymorphism density was higher in the strains of F. geosporum than in the strains of F. mosseae . In this study, we demonstrate that it is possible to sequence and assemble genomes from AM fungal spores sampled in the field, which opens up the possibility to include uncultured AM fungi in phylogenomic and comparative genomic analysis and to study genomic variation in natural populations of these important plant symbionts.
... This is likely because root colonisation of mycorrhizal fungi is not the sole determinant of the functionality of the mutualistic interaction. Instead of the expected increase in mycorrhizal root colonisation, mycorrhizal spore addition may have resulted in more soil hyphae, higher nutrient mobilisation capacity of the fungus and/or more nutrient exchange structures (Munkvold et al. 2004;Smith et al. 2004;Jansa et al. 2005;Feddermann et al. 2010). This may arise from an earlier developing plant-mycorrhizae association and result in the observed positive plant-soil feedback effects. ...
... and in turn reduce agricultural dependence on synthetic agro-chemicals, thereby promoting a more sustainable approach to food production (Thirkell et al., 2017). However, crop-mycorrhizal outcomes are context specific, being driven by plant genotype or cultivar (Ellouze et al., 2016;Hetrick et al., 1992;Thirkell et al., 2021) as well as by which AM fungi are involved (Munkvold et al., 2004), as is also the case in unmanaged ecosystems (Hoeksema et al., 2010;Klironomos, 2003). Abiotic factors, like soil nutrient status (Li et al., 2005), shading (Johnson et al., 2015) and atmospheric CO 2 (Johnson et al., 2005), may intensify this variability. ...
Societal Impact Statement
The Earth's population is projected to rise to 9.7 billion by 2050 resulting in mounting pressure to increase agricultural yields in a sustainable manner. Arbuscular mycorrhizal (AM) fungi may be important players in this agricultural transition given their capacity to improve soil and plant health. Benefits gained by crops hosting AM fungi can be cultivar‐specific and also affected by insect herbivory, although the combined effect of these factors remains unclear. Here, we show that, in an economically and socially significant tri‐partite system, there is interplay between crop cultivar, AM colonisation and aphid herbivory on plant growth and nutritional status.
Summary
Arbuscular mycorrhizal (AM) fungi are critical components of the rhizosphere across nearly all terrestrial biomes. AM fungi associate with most plants, including major crops, usually increasing plant access to soil nutrients and enhancing defence against pests and pathogens in return for photosynthetic carbon (C). However, plant growth responses to AM fungi vary according to species and genotype, an issue pertinent in agro‐ecosystems where crop cultivar can play an important role in AM function. Evidence suggests other biotic interactions, including with sap‐feeding aphids, impact the function of AM symbioses in plants. Nonetheless, whether these biotic factors alter genotype (or cultivar)‐specific plant growth and nutritional responses to colonisation by AM fungi remains unclear.
Here, we investigated whether mycorrhizal responsiveness of three cultivars of wheat (Triticum eastivum L.) to colonisation by a ubiquitously occurring AM fungus (Rhizophagus irregularis) differ in the presence or absence of bird cherry‐oat aphids (Rhopalosiphum padi), a major pest of cereals.
Our findings show that although AM fungal colonisation and AM‐mediated plant growth responses were not affected by aphid feeding, there was variation between cultivars in the benefits gained by host plants in terms of nutrient acquisition and root growth, while aphid abundances also differed between wheat varieties.
Understanding what causes cultivar‐specific outcomes and how they ultimately impact plant growth promotion, crop yields and food production represent key future research goals in agroecology.
... The availability of P is thought to be one of the important factors affecting many biological processes in lowland tropical forests [61], which is a limiting nutrient in these forests [62,63]. The role of arbuscular mycorrhizal fungi (AMF) in P acquisition is well known [64], and there is evidence that different AMF differs in their ability to acquire and transport P to the plant host [65]. The shift in phosphorus acquisition strategies of AMF may cause the segregation of ecological niches [66]. ...
Forests acting as carbon storage and sequestration play an essential role in the global nutrient cycle, in which fungi are active participants. The forests cover almost all regions from the boreal, temperate to the subtropical and tropical forests. The relative proportion of carbon sequestrated in forest soil varies from approximately 85% of the terrestrial carbon pool in boreal forests to 60% in temperate forests and to 50% in tropical rainforests. Fungi as decomposers of organic matter and root-associated mediators of belowground carbon transport and respiration are the key drivers of the carbon cycle in forests. For example, saprophytic fungi can degrade soil organic matter to release carbon into the soil, whereas symbiotic fungi could form symbiosis with plants, through which plant and fungi can benefit each other with nutrient flow. Given the importance of fungi in the ecological environment, this paper summarizes the importance of soil fungi in terms of fungal diversity and function in forest ecosystems.
Differences in functioning among various genotypes of arbuscular mycorrhizal (AM) fungi can determine their fitness under specific environmental conditions, although knowledge of the underlying mechanisms still is very fragmented. Here we compared seven homokaryotic isolates (genotypes) of Rhizophagus irregularis, aiming to characterize the range of intraspecific variability with respect to hyphal exploration of organic nitrogen (N) resources, and N supply to plants. To this end we established two experiments (one in vitro and one in open pots) and used ¹⁵N-chitin as the isotopically labeled organic N source. In Experiment 1 (in vitro), mycelium of all AM fungal genotypes transferred a higher amount of ¹⁵N to the plants than the passive transfer of ¹⁵N measured in the non-mycorrhizal (NM) controls. Noticeably, certain genotypes (e.g., LPA9) showed higher extraradical mycelium biomass production but not necessarily greater ¹⁵N acquisition than the others. Experiment 2 (in pots) highlighted that some of the AM fungal genotypes (e.g., MA2, STSI) exhibited higher rates of targeted hyphal exploration of chitin-enriched zones, indicative of distinct N exploration patterns from the other genotypes. Importantly, there was a high congruence of hyphal exploration patterns between the two experiments (isolate STSI always showing highest efficiency of hyphal exploration and isolate L23/1 being consistently the lowest), despite very different (micro) environmental conditions in the two experiments. This study suggests possible strategies that AM fungal genotypes employ for efficient N acquisition, and how to measure them. Implications of such traits for local mycorrhizal community assembly still need to be understood.
This study aimed to explore the community of arbuscular mycorrhizal fungi (AMF) in the rhizosphere soil with different generations of the hybridized progeny of wild Erianthus arundinaceus and sugarcane. Rhizosphere soils were collected from E. arundinaceus (P), and the F1, F3, and F5 progeny of its hybrid with sugarcane, and community of AMF in the rhizosphere soil was analyzed using Illumina Miseq high-throughput sequencing. The results showed that a total of 159 AMF fungal OTUs were obtained from the sequencing analysis, belonging to 1 phylum, 4 classes, 6 orders, 11 families, 14 genera, and 42 species. Alpha diversity analysis showed that the Chao1 and ACE indices decreased with increasing of the generations, that is, the highest species abundance was in parent P, and significant differences were observed between P and F1, F3, and F5 (P < 0.05). The Shannon index in P was the highest, with significant differences between P and F3, and F5. The dominant genus in P was Acaulospora, while that in F1 was Glomus, that in F3 was Claroideoglomus, and that in F5 was Glomus. Diversispora and Dentiscutata were the dominant genera unique to P. Glomus, Claroideoglomus, Acaulospora, Rhizophagus, and Gigaspora were present in the rhizosphere soil of different generations. PCoA analysis showed significant differences in the distribution of AMF communities in the rhizosphere soils of different generations. Significant differences were observed between the inter-group comparisons of the AMF community at the genus level, with significant differences in the relative abundance of Glomus and Acaulospora in different generations on the levels P < 0.05 and P < 0.01, respectively. These findings indicate that the community of AMF in the rhizosphere soils with different generations of the hybridized progeny of E. arundinaceus with sugarcane is different, but some AMF groups do not change with addition of the generations. Further research is needed to determine whether these characteristics are related to the agronomic traits of the crops.
Arbuscular mycorrhizal fungi (AMF) can form mycorrhizal relationships with a large majority of the plant species on Earth. However, the actual symbiosis can be complex, with the mutual relationships being affected by the mycorrhizal partner(s) involved, the functionalities they bring to the relationship, the available nutrient resources, and the environment. It has been suggested that the use of indigenous AMF may be superior to commercial AMF products in the long term, especially with respect to improved nutrient uptake and their adaptation to local biotic or abiotic stresses. However, such a strategy would require the identification of the AMF involved, the determination of their respective contributions in the face of local biotic and abiotic factors and the subsequent introduction and management of their relationships. This chapter will focus on how the various aspects of traditional, molecular, and next generation AMF identification may be used to help in the field application of AMF, especially when used in conjunction with an understanding of AMF biology. In this context, AMF contributions to nutrient and water uptake in plants are also described.
Soil characteristics, land management practices, and plant genotypes influence arbuscular mycorrhizal fungi (AMF) communities, leading to the proliferation of AMF taxa with different growth and nutritional outcomes in their hosts. However, the specific patterns driving these relationships are still not well understood. This study aimed to (1) evaluate the influence of soil characteristics, land use, and rootstock on AMF diversity and community structure and (2) assess the effect of those AMF communities on grapevine growth and nutrition. Soil samples were collected from vineyard and non-agricultural areas in Lisbon and Pegões, Portugal, and trap cultures established using Richter 110 and 1103 Paulsen rootstocks. After 3.5 months growth under greenhouse conditions, root-associated AMF communities were assessed by amplicon metagenomic sequencing using AMF-specific primers. Alpha diversity was only influenced by the soil type, while in β-diversity, an interaction was found between the soil type and land use. Both diversity measures were positively correlated with foliar K and negatively with leaf Mn and Mg. Notably, the concentrations of these nutrients were highly correlated with the relative abundance of operational taxonomic units (OTUs) within the genera Glomus, Rhizophagus, and Claroideoglomus. These results are valuable for supporting AMF selection for improved plant nutrition based on varying soil types and land uses.
Arbuscular mycorrhizal (AM) fungi could mitigate individual drought and heat stress in host plants. However, there are still major gaps in our understanding of AM symbiosis response to the combined stresses. Here, we compared seven AM fungi, Rhizophagus irregularis, Funneliformis mosseae, Funneliformis geosporum, Funneliformis verruculosum, Funneliformis coronatum, Septoglomus deserticola, Septoglomus constrictum, distributed to many world regions in terms of their impacts on tomato endurance to combined drought and chronic heat as well as combined drought and heat shock. A multidisciplinary approach including morphometric, ecophysiological, biochemical, targeted metabolic (by ultrahigh-performance LC-MS), and molecular analyses was applied. The variation among AM fungi isolates in the enhancement in leaf water potential, stomatal conductance, photosynthetic activity, and maximal PSII photochemical efficiency, proline accumulation, antioxidant enzymes (POD, SOD, CAT), and lowered ROS markers (H2O2, MDA) in host plants under combined stresses were observed. S. constrictum inoculation could better enhanced the host plant physiology and biochemical parameters, while F. geosporum colonization less positively influenced the host plants than other treatments under both combined stresses. F. mosseae- and S. constrictum-associated plants showed the common AM-induced modifications and AM species-specific alterations in phytohormones (ABA, SA, JA, IAA), aquaporin (SlSIP1-2; SlTIP2-3; SlNIP2-1; SlPIP2-1) and abiotic stress-responsive genes (SlAREB1, SlLEA, SlHSP70, SlHSP90) in host plants under combined stresses. Altogether, mycorrhizal mitigation of the negative impacts of drought + prolonged heat and drought + acute heat, with the variation among different AM fungi isolates, depending on the specific combined stress and stress duration.
Grasslands represent an essential part of terrestrial ecosystems. In particular, coastal grasslands are dominated by the influence of environmental factors resulting from sea-land interaction. Therefore, coastal grasslands are extremely heterogeneous both spatially and temporally. In this review, recent knowledge in the field of biotic interactions in coastal grassland soil is summarized. A detailed analysis of arbuscular mycorrhiza symbiosis, rhizobial symbiosis, plant-parasitic plant interactions, and plant-plant interactions is performed. The role of particular biotic interactions in the functioning of a coastal grassland ecosystem is characterized. Special emphasis is placed on future directions and development of practical applications for sustainable agriculture and environmental restoration. It is concluded that plant biotic interactions in soil are omnipresent and important constituents in different ecosystem services provided by coastal grasslands.
Food production is heavily dependent on soil phosphorus (P), a non-renewable mineral resource essential for plant growth and development. Alas, about 80% is unavailable for plant uptake. Arbuscular mycorrhizal fungi may promote soil P efficient use, although the mechanistic aspects are yet to be completely understood. In this study, plant and fungal variables involved in P acquisition were investigated in maize inbred lines, differing for mycorrhizal responsiveness and low-P tolerance, when inoculated with the symbiont Rhizoglomus irregulare (synonym Rhizophagus irregularis). The expression patterns of phosphate transporter (PT) genes in extraradical and intraradical mycelium (ERM/IRM) and in mycorrhizal and control maize roots were assessed, together with plant growth responses and ERM extent and structure. The diverse maize lines differed in plant and fungal accumulation patterns of PT transcripts, ERM phenotypic traits and plant performance. Mycorrhizal plants of the low-P tolerant maize line Mo17 displayed increased expression of roots and ERM PT genes, compared with the low-P susceptible line B73, which revealed larger ERM hyphal densities and interconnectedness. ERM structural traits showed significant correlations with plant/fungal expression levels of PT genes and mycorrhizal host benefit, suggesting that both structural and functional traits are differentially involved in the regulation of P foraging capacity in mycorrhizal networks.
Arbuscular mycorrhizal fungi (AMF) of the Glomeromycotina subphylum are one of the oldest fungal lineages for which the mechanistic underpinning of genetic diversity is unknown. They are present in all terrestrial ecosystems and interact with the majority of land plants, significantly impacting global nutrient cycling. The study of genomes of AMF is of fundamental importance for understanding their evolutionary history and the molecular bases of symbiosis. Here we summarize the current knowledge of AMF genome organization, regulation, and transmission. We discuss the implications of recent findings in our understanding of AMF biodiversity, adaptation, and evolution.
Traits are the intermediate by which species respond to environmental filters and influence ecosystem functions. With the myriad of biogeochemical processes controlled by fungi, the past decade has witnessed a rising interest in applying trait-based approaches, core to the toolkit of plant and animal ecophysiologists, to fungi. One of the first challenges to tackle when working on fungal ecophysiology is to circumscribe the very definition of what we consider a fungal trait. Traits are characteristics/features possessed by an individual that can influence how it interacts with its environment. Here, the individual scale is both important, and problematic. Important because the very goal of comparative ecology is to measure traits on individuals belonging to known species. This allows us to populate trait databases, and syntheses of such databases can reveal key trade-offs and trait syndromes that govern species' life-histories. The scale of the individual is problematic, however, because it is hard to define for soil fungi, and because a rare minority of fungi can be sampled at the individual scale in the environment (e.g., macroscopic sporocarps, ectomycorrhizal root tips, lichen thalli). Beyond this minority, the individual organisms can only be accessed/sampled through establishing fungal cultures, which probably represents one of the main bottlenecks in the development of fungal trait databases. In this issue of Molecular Ecology, Zhang et al. (2022) show how interesting insights in fungal trait-based ecology can be gained by working at the community level.
Aims
Afforestation of trace-element contaminated soils, notably with fast growing trees, has been demonstrated to be an attractive option for bioremediation due to the lower costs and dispersion of contaminants than conventional cleanup methods. Mycorrhizal fungi form symbiotic associations with plants, contributing to their tolerance towards toxic elements and actively participating to the biorestoration processes. The aim of this study was to deepen our understanding on the effects of mycorrhizal inoculation on plant development and fungal community at two trace-element contaminated sites (Pierrelaye and Fresnes-sur-Escaut, France) planted with poplar (Populus trichocarpa x Populus maximowiczii).
Methods
The 2 sites were divided into 4 replicated field blocks with a final plant density of 2200 tree h⁻¹. Half of the trees were inoculated with a commercial inoculum made of a mix of mycorrhizal species. The sites presented different physico-chemical characteristics (e.g., texture: sandy soil versus silty-loam soil and organic matter: 5.7% versus 3.4% for Pierrelaye and Fresnes-sur-Escaut, respectively) and various trace element contamination levels.
Results
After 7 years of plantation, inoculation showed a significant positive effect on poplar biomass production at the two sites. Fungal composition study demonstrated a predominance of the phylum Ascomycota at both sites, with a dominance of Geopora Arenicola and Mortierella elongata, and a higher proportion of ectomycorrhizal and endophytic fungi (with the highest values observed in Fresnes-sur-Escaut: 45% and 28% for ECM and endophytic fungi, respectively), well known for their capacity to have positive effects on plant development in stressful conditions. Furthermore, Pierrelaye site showed higher frequency (%) of mycorrhizal tips for ectomycorrhizal fungi (ECM) and higher intensity (%) of mycorrhizal root cortex colonization for arbuscular mycorrhizal fungi (AMF) than Fresnes-sur-Escaut site, which translates in a higher level of diversity.
Conclusions
Finally, this study demonstrated that this biofertilization approach could be recommended as an appropriate phytomanagement strategy, due to its capacity to significantly improve poplar productivity without any perturbations in soil mycobiomes.
Sorghum is an important worldwide source of food, feed and fibers. Like most plants, it forms mutualistic symbioses with arbuscular mycorrhizal fungi (AMF), but the nutritional basis of mycorrhiza-responsiveness is largely unknown. Here, we investigated the transcriptional and physiological responses of sorghum to two different AMF species, Rhizophagus irregularis and Funneliformis mosseae, under sixteen different conditions of nitrogen (N) and phosphorus (P) supply. Our experiment reveals fine-scale differences between two AMF species in the nutritional interactions with sorghum plants. Physiological and gene expression patterns (ammonium transporters: AMT; phosphate transporters: PHT) indicate the existence of generalist or specialist mycorrhizal pathway: While R. irregularis switched on the mycorrhizal pathway independently of the plant nutritional status, F. mosseae influenced the mycorrhizal pathway depending on the N-to-P plant ratio and soil supply. The differences between both AMF species suggest some AMT and PHT as ideal candidates to develop markers for improving efficiency of nutrient acquisition in sorghum under P and N limitation, and for the selection of plant genotypes. This article is protected by copyright. All rights reserved.
Olive ( Olea europaea L.) is a highly mycotrophic species that has been introduced and cultivated in China for half a century. The arbuscular mycorrhizal fungi (AMF) is extremely valuable as a kind of biofertilizer to promote the health and vigor of olive plants. However, it is still unclear how native AMF impact growth and mineral nutrients, especially phosphorus absorption in the area where olive trees were introduced in China. In the present study, through a pot experiment, the effects of native AMF on the growth, phosphorus uptake and expression levels of four phosphate transporter genes ( Pht ) of olive plantlets were characterized. We found that (1) typical AMF colonization was observed within the roots of inoculated olive plantlets, and the growth of plantlets was significantly promoted; (2) some indigenous consortia (AMF1 and AMF2) notably promoted the absorption of phosphorus, fertilizers significantly increased the foliar content of nitrogen, and both AMF inoculation and fertilization had no significant effect on the uptake of potassium; and (3) AMF inoculation enhanced the expression of phosphate transporter genes in inoculated olive roots. This work demonstrates the effectiveness of native AMF on the cultivation of robust olive plantlets and highlights the role of AMF in increasing phosphorus uptake. There is great potential in using native AMF consortia as inoculants for the production of healthy and robust olive plantlets.
PCR amplification of a region of the large subunit ribosomal DNA sequence with Glomus specific primers was used to detect arbuscular mycorrhizal fungi in root tissue of four plant species. The primers were specific
to Glomus mosseae, Glomus caledonium, Glomus geosporum, Glomus coronatum, Glomus fragilistratum and Glomus constrictum, and did not recognise sequences from Glomus claroideum. Sequence differences between isolates were detected by Single Stranded Conformation Polymorphisms (SSCPs) in polyacrylamide
gels under non-denaturing conditions. Isolates of G. mosseae, G. caledonium and G. coronatum could be separated by their SSCP patterns, while three isolates of G. geosporumshowed no variation. Specific SSCP patterns from isolates of G. mosseae and G. caledonium allowed detection of both fungi in the same root segment. Sequence differences leading to variations in SSCP patterns were
confirmed by direct sequencing.
The population ecology of clonal plants depends on the number and distribution of ramets formed during growth. Variation in clonal reproduction has previously been explained by variation in effects of abiotic resource heterogeneity and by plant genotypic variation. Different co-occurring species of the mutualistic arbuscular mycorrhizal fungi (AMF) have been shown to differentially alter growth traits of Prunella vulgaris, which we hypothesize would lead to changes in clonal reproduction. Two experiments were carried out to test whether different co-occurring mycorrhizal fungi significantly influence clonal reproduction of P. vulgaris, whether this effect also occurs when P. vulgaris is growing in an artificial plant community, and how the effects compare with plant genotype effects on clonal growth of P. vulgaris.
In the first experiment, the number of ramets of P. vulgaris, growing in a plant community of simulated calcareous grassland, was significantly affected by inoculation with different mycorrhizal fungi. The number of ramets produced by P. vulgaris differed by a factor of up to 1.8 with different mycorrhizal fungi. The fungal effects on the number of new ramets were independent of their effects on the biomass of P. vulgaris.
In a second experiment, 17 different genotypes of P. vulgaris were inoculated with different mycorrhizal fungi. There were significant main effects of genotypes and mycorrhizal fungi on clonal reproduction of P. vulgaris. The effect of different mycorrhizal fungi contributed more than the effect of plant genotype to variation in size and ramet production. However, mean stolon length and spacer length, which determine the spatial arrangement of ramets, were only significantly affected by plant genotype. There were no mycorrhizal fungal × plant genotype interactions on clonal growth of P. vulgaris indicating that there is no obvious evidence that selection pressures would favor further coevolution between P. vulgaris and mycorrhizal fungal species.
In natural communities plants can be colonized by several different AMF at the same time. The effect of the mixed AMF treatment on the growth and clonal reproduction of P. vulgaris could not be predicted from the responses of the plants to the single AMF. To what extent, however, the patterns of colonization by different AMF differ among plants in a natural community is unknown.
Since the effects of AMF on growth and clonal reproduction occur on a population of P. vulgaris in a microcosm plant community and because the effects are also as great as those caused by plant genotypic variation, we conclude that the effects are strong enough to potentially affect population size and variation of clonal plants in communities.
The program MRBAYES performs Bayesian inference of
phylogeny using a variant of Markov chain Monte Carlo.
Availability: MRBAYES, including the source code, documentation,
sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
Contact: johnh{at}brahms.biology.rochester.edu
We have used molecular techniques to investigate the diversity and distribution of the arbuscular mycorrhizal (AM) fungi colonizing tree seedling roots in the tropical forest on Barro Colorado Island (BCI), Republic of Panama. In the first year, we sampled newly emergent seedlings of the understory treelet Faramea occidentalis and the canopy emergent Tetragastris panamensis, from mixed seedling carpets at each of two sites. The following year we sampled surviving seedlings from these cohorts. The roots of 48 plants were analysed using AM fungal-specific primers to amplify and clone partial small subunit (SSU) ribosomal RNA gene sequences. Over 1300 clones were screened for random fragment length polymorphism (RFLP) variation and 7% of these were sequenced. Compared with AM fungal communities sampled from temperate habitats using the same method, the overall diversity was high, with a total of 30 AM fungal types identified. Seventeen of these types have not been recorded previously, with the remainder being similar to types reported from temperate habitats. The tropical mycorrhizal population showed significant spatial heterogeneity and nonrandom associations with the different hosts. Moreover there was a strong shift in the mycorrhizal communities over time. AM fungal types that were dominant in the newly germinated seedlings were almost entirely replaced by previously rare types in the surviving seedlings the following year. The high diversity and huge variation detected across time points, sites and hosts, implies that the AM fungal types are ecologically distinct and thus may have the potential to influence recruitment and host composition in tropical forests.
Isolates of Glomus mosseae from international collections were compared using two molecular techniques: PCR-fingerprinting of genomic DNA with direct amplification of microsatellite regions, and sequencing of the small subunit (SSU) rDNA. Numerical analyses of these data using parsimony models were used to calculate phylogenetic topologies. The phylogenetic tree from SSU rDNA sequences was similar to the phylogenetic trees obtained from genomic fingerprinting using the amplification of microsatellite regions, except for one G. mosseae isolate, DAOM221475. Another isolate was not grouped with the other G. mosseae isolates by either method and was found to be Glomus sp. a posteriori. Both analyses showed considerable genetic variation within the species G. mosseae. We suggest that molecular data such as SSU rDNA sequences be used in the description of Glomales species, and PCR-fingerprinting could be used to study diversity within species of Glomales.
A single solution reagent is described for the determination of phosphorus in sea water. It consists of an acidified solution of ammonium molybdate containing ascorbic acid and a small amount of antimony. This reagent reacts rapidly with phosphate ion yielding a blue-purple compound which contains antimony and phosphorus in a 1:1 atomic ratio. The complex is very stable and obeys Beer's law up to a phosphate concentration of at least 2 μg/ml.The sensitivity of the procedure is comparable with that of the stannous chloride method. The salt error is less than 1 %.
The roots are laid out on a flat surface, and a count is made of the number of intersections between the roots and random straight lines. Then the total root length = πNA/2H, where N is the number of intersections, A the area within which the roots lie, and H the total length of the straight lines. Details are given of a technique in which a microscope hair-line provides the straight lines. In practical tests the method was compared with direct measurement, and with direct measurement of a sub-sample followed by weighing of the sub-sample and the remainder. The results from the different methods agreed well. The line intersection method was much quicker than direct measurement, and in a given time achieved higher precision than measurement of a sub-sample and weighing.
Isolates of Glomus mosseae from international collections were compared using two molecular techniques: PCR-fingerprinting of genomic DNA with direct amplification of microsatellite regions, and sequencing of the small subunit (SSU) rDNA. Numerical analyses of these data using parsimony models were used to calculate phylogenetic topologies. The phylogenetic tree from SSU rDNA sequences was similar to the phylogenetic trees obtained from genomic fingerprinting using the amplification of microsatellite regions, except for one G. mosseae isolate, DAOM221475. Another isolate was not grouped with the other G. mosseae isolates by either method and was found to be Glomus sp. a posteriori. Both analyses showed considerable genetic variation within the species G. mosseae. We suggest that molecular data such as SSU rDNA sequences be used in the description of Glomales species, and PCR-fingerprinting could be used to study diversity within species of Glomales.
The growth and yield response of greenhouse‐grown soybean plants to colonization by 19 isolates (including 6 Glomus and 3 Gigaspora species) of vesicular‐arbuscular mycorrhizal fungi is reported. Each isolate was evaluated in a high (169 kg/ha Bray‐I P 2 O 5 ) and a low (50 kg/ha Bray‐I P 2 O 5 ) fertility soil. Colonization by most Glomus isolates significantly increased plant top dry weight and seed yields, and of these isolates most produced larger increases in dry weight in the low fertility soil. Colonization by five of the Gigaspora isolates did not significantly affect top dry weight and seed yield in the high or Iow fertility soil. The value of comparative testing of species is discussed.
Phosphorus transport by hyphae of the three VA mycorrhizal fungi, Acaulospora laevis Gerdemann & Trappe, Glomus sp. and Scutellospora calospora (Nicol. & Gerd.) Walker & Sanders, associated with Trifolium subterraneum L. was investigated by means of radiotracer techniques. Plants with roots heavily colonized by each mycorrhizal fungus were transplanted to two-compartment systems, where a hyphal compartment was separated from the main compartment by a fine mesh preventing root penetration. The hyphal compartment contained layers of 32P-labelled soil, which were placed at 0, 1, 2.5, 4.5 or 7 cm from the root compartment.
A time-course study over 37 d showed that Glomus sp. transported most 32P to shoots over soil-root distances shorter than 1 cm. In contrast, A. laevis transported most 32P to shoots over soil–root distances longer than 1 cm. This ability of A. laevis to transport phosphorus over longer distances than Glomus sp. parallels previous observations that hyphae of A. laevis spread faster and further in soil than hyphae of the Glomus sp.
Scutellospora calospora transported much less 32P to plants, but accumulated more 32P in its hyphae, than the two other fungi. The higher specific radioactivity in the hyphae of S. calospora than of A. laevis and Glomus sp. indicated a retarded translocation of 32P in its hyphae or retarded transfer of 32P across its interface with the host. However, the poor phosphorus transport by S. calospora might also have resulted from its reaction to root trimming at transplanting; percentage root colonization by S. calospora decreased markedly after transplanting to the labelling system.
Cucumber ( Cucumis sativus L.) was grown in an irradiated soil:sand mixture in PVC tubes containing a root compartment, a hyphal compartment and a hyphal ³² P‐labelling compartment. The soil was inoculated with either Scutellospora calospora (Nicol. & Gerd.) Walker & Sanders, Glomus sp. or Glomus caledonium (Nicol. & Gerd.) Trappe & Gerdemann or left uninoculated.
At 23 d from sowing 20 μCi of an aqueous solution of carrier‐free ³² P was pipetted into the hyphal labelling compartment. Just 24 h later the plants were labelled with ¹⁴ CO 2 for 16 h. At harvest the plants were analysed for mycorrhizal colonization and distribution of ¹⁴ C and ³² P.
Hyphae of G. caledonium proved to have the most rapid ³² P uptake and transfer system of the three fungi studied. The host was provided with an order of magnitude more ³² P than supplied by either Glomus sp. or S. calospora. The S. calospora ‐colonized plants contained the least ³² P counts of the three mycorrhizal treatments. 75% of the total ³² P in the plant was present in the shoots of the plants colonized by G. caledonium ; the corresponding figures for the shoots of S. calospora and Glomus sp. were 45 and 25%, respectively.
The proportion of assimilated ¹⁴ C allocated to below‐ground events was 35, 32 and 25 with S. calospora, Glomus sp. and G. caledonium , respectively. The specific incorporation of ¹⁴ C into roots colonized by Glomus sp. was 1.8 and 3.1 times as high as into roots colonized by G. caledonium and S. calospora , respectively.
In contrast, the specific root respiration (Bq mg ⁻¹ d. wt) was similar in the mycorrhizal treatments. The ¹⁴ C flow into external hyphae was approximately 0.8% of the total assimilated ¹⁴ C for all three fungi.
Based on these results, mycorrhizal efficiency was calculated as hyphal ¹⁴ C use per unit ³² P transported, below‐ground ¹⁴ C use per unit ³² P transported, ³² P transported per metre of hyphae and hyphal ¹⁴ C use per metre of hyphae.
Summary • High levels of variation are reported in the large subunit (LSU) rRNA gene, D2 region of Glomus coronatum, a well characterized species of arbuscular mycorrhizal fungus (AMF). • Clones (435) containing the D2 regions from 7 isolates of G. coronatum were investigated for intra- and inter-isolate sequence variation using PCR-single-strand conformational polymorphism (PCR-SSCP) as a prescreen before sequencing. Isolates of G. mosseae, G. constrictum and G. geosporum, three species of AMF with similar spore ontogeny and morphology, were also analysed. • Analysis of 138 representative sequences indicated that most were unique; this variation could not be attributed to DNA polymerase or cloning artefacts. Only 13 sequences were found in more than one isolate. Neighbour-joining analysis showed that most sequences from G. coronatum formed a main group although several sequences from G. mosseae and G. constrictum clustered with G. coronatum. • There was greater than expected variation in the LSU D2 region sequences from G. coronatum. The four Glomus species, closely related by spore morphology, might represent part of a genetic continuum. Implications for the concept of species in AMF, the use of rRNA sequences to estimate biodiversity and in situ detection in field ecology are discussed.
Summary • We investigated structural and functional diversity in arbuscular mycorrhizal (AM) symbioses involving three plant species and three AM fungi and measured contributions of the fungi to P uptake using compartmented pots and 33P. The plant/fungus combinations varied in growth and P responses. Flax (Linum usitatissimum) responded positively to all fungi, and medic (Medicago truncatula) to Glomus caledonium and G. intraradices, but not Gigaspora rosea. Tomato (Lycopersicon esculentum) showed no positive responses. • Hyphal growth in soil was very low for Gi. rosea and high for both Glomus spp. Hyphal lengths in root + hyphal compartment (RHC) and hyphal compartment (HC) were similar for G. intraradices, but much higher in HC for G. caledonium. • Specific activities of 33P in plants and soil indicated that fungal P uptake made substantial contributions to five plant/fungus combinations and significant contributions to a further two. G. intraradices delivered close to 100% of the P in all three plants. G. caledonium and Gi. rosea delivered less P. The amount was not related to colonisation or to growth or P responses. • We conclude that: AM colonisation can result in complete inactivation of the direct P uptake pathway via root hairs and epidermis; calculations of AM contributions to P uptake from total plant P will often be highly inaccurate; and lack of plant responsiveness does not mean that an AM fungus makes no contribution to P uptake.
Summary • It is often thought that the coexistence of plants and plant diversity is determined by resource heterogeneity of the abiotic environment. However, the presence and heterogeneity of biotic plant resources, such as arbuscular mycorrhizal fungi (AMF), could also affect plant species coexistence. • In this study, Brachypodium pinnatum and Prunella vulgaris were grown together in pots and biotic resource heterogeneity was simulated by inoculating these pots with one of three different AMF taxa, with a mixture of these three taxa, or pots remained uninoculated. • The AMF acted as biotic plant resources since the biomass of plants in pots inoculated with AMF was on average 11.8 times higher than uninoculated pots. The way in which the two plant species coexisted, and the distribution of phosphorus and nitrogen between the plant species, varied strongly depending on which AMF were present. The results showed that the composition of AMF communities determines how plant species coexist and to which plant species nutrients are allocated. • Biotic plant resources such as AMF should therefore be considered as one of the factors that determine how plant species coexist and how soil resources are distributed among co-occurring plant species.
Responses of Medicago truncatula to colonization by two arbuscular mycorrhizal fungi, Scutellospora calospora isolate WUM 12(2) and Glomus caledonium isolate RIS 42, were compared in the light of previous findings that the former fungus can be ineffective as a beneficial microsymbiont with some host plants. The plants were grown individually in two-compartment systems in which a lateral side arm containing soil labelled with 33P was separated from the main soil compartment by a nylon mesh that prevented penetration by roots but not fungal hyphae. Fungal inoculum was applied as a root–soil mixture in a band opposite the side arm. Nonmycorrhizal controls were set up similarly, without inoculum. There were harvests at 28, 35, 42 and 49 d. Both sets of mycorrhizal plants grew better than nonmycorrhizal plants and initially had higher concentrations of P in shoots and roots. Plants grown with S. calospora grew better than plants grown with G. caledonium, and this was associated with somewhat greater fungal colonization in terms of intraradical hyphae and numbers of arbuscules. Scutellospora calospora formed denser hyphae at root surfaces than G. caledonium. By 28 d there were extensive hyphae of both fungi in the side arms, and after 35 d S. calospora produced denser hyphae there than G. caledonium. Nevertheless, there was very little transfer of 33P via S. calospora to the plant at 28 d, and thereafter its transfer increased at a rate only c. 33% of that via G. caledonium. The results showed that plants colonized by S. calospora preferentially obtained P from sites in the main soil chamber relatively close to the roots, compared with plants colonized by G. caledonium. Hence formation of a highly beneficial arbuscular mycorrhizal symbiosis does not necessarily depend on development of hyphae at a distance from the roots or on large-scale translocation of P from distant sites. The results are discussed in relation to previous studies with compartmented systems that have involved the same fungi. Possible causes of the variable effects of S. calospora in symbiosis with different host plants are briefly assessed. Differences in spatial abilities of individual arbuscular mycorrhizal fungi to acquire P might have strong ecological implications for plant growth in soils low in P.
Summary •W e studied the relationships of plant and AMF (arbuscular mycorrhizal fungi) species richness and community composition to each other and gradients in soil texture, nutrient content, and light availability in three oak savannas in southern Wisconsin, USA. • Sixty-three samples were analysed for plant and AMF composition along sun-shade and sand-loam gradients. Samples consisted of plant community composition at quadrat and point scales, point-scale AMF community composition, canopy trans- mittance, soil Kjeldahl nitrogen (N) content, available phosphorus (P), and texture. • Numbers of AMF and plant species at the point scale were positively correlated with each other and increased with soil texture/N content. The compositions of plant and AMF communities were also significantly correlated with each other and the soils gradient. The paradoxical increase in AMF richness on the most fertile soils may reflect their small soil pores or low P : N ratios. • Plant and AMF communities appear to respond to underlying environmental gradients in similar ways, perhaps reflecting similar responses to soil conditions by both groups, effects of one group on the other or both.
Research on nutrient acquisition by symbiotic arbuscular mycorrhizal (AM) fungi has mainly focused on the root–fungus interface and less attention has been given to the growth and functioning of external hyphae in the bulk soil. The growth and function of external hyphae may be affected by unfavourable soil environments, such as compacted soils in which pores may be narrow. The effects of pore size on the growth of two AM fungi (Glomus intraradices and G. mosseae) and their ability to transport 33P from the bulk soil to the host were investigated. Trifolium subterraneum L. plants were grown individually in `single arm cross-pots' with and without AM fungi. The side arm was separated from the main compartment by nylon mesh to prevent root penetration. It contained three zones: 5 mm of soil:sand mix (HC1); 25 mm of media treatment (HC2); and 20 mm of 33P-labelled soil (HC3). There were four media treatments; soil and three types of quartz sand with most common continuous pore diameters of 100, 38 and 26 m. AM plants had similar growth and total P uptake in all treatments. However, plants grown with G. intraradices contained almost three times more 33P than those grown with G. mosseae, indicating G. intraradices obtained a greater proportion of P at a distance from the host roots. Differences in P acquisition were not correlated with production of external hyphae in the four media zones and changes in sand pore size did not affect the ability of the fungi studied to acquire P at a distance from the host roots. Production of external hyphae in HC2 was influenced by fungal species and media treatment. Both fungi produced maximum amounts of external hyphae in the soil medium. Sand pore size affected growth of G. intraradices (but not G. mosseae) and hyphal diameter distributions of both fungi. The results suggest that not only are G. mosseae and G. intraradices functionally complementary in terms of spatial phosphorus acquisition, they are also capable of altering their morphology in response to the soil environment.
A single solution reagent is described for the determination of phosphorus in sea water. It consists of an acidified solution of ammonium molybdate containing ascorbic acid and a small amount of antimony. This reagent reacts rapidly with phosphate ion yielding a blue-purple compound which contains antimony and phosphorus in a 1:1 atomic ratio. The complex is very stable and obeys Beer's law up to a phosphate concentration of at least 2 μg/ml.The sensitivity of the procedure is comparable with that of the stannous chloride method. The salt error is less than 1 %.RésuméUne méthode spectrophotométrique est décrite pour le dosage du phosphate dans l'eau de mer, an moyen de molybdate d'ammonium, en présence d'acide ascorbique et d'antimoinc. Il se forme rapidement un composé violet bleu, renfermant antimoine et phosphore dans un rapport atomique de 1:1.ZusammenfassungBeschreibung einer Methode zur Bestimmung von Phosphat in Mecrwasser mit Hilfe von Ammoniummolybdat in Gegenwart von Ascorbinsäure und Antimon. Der gebildete blau-violette Komplex wird spektrophotometrisch gemessen.
A series of experiments was conducted in the field, greenhouse, and laboratory to investigate population variation among three geographic isolates of the widely distributed vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Uniform garden experiments were used to determine whether these populations from dissimilar environments are physiologically different ecotypes or phenotypic variants. Using Melilotus officinalis as host, comparisons were made of the mycorrhizas formed, spore production, spore germination, propagule density, and the influence of the endophytes on host growth and physiology. Large disparities were observed in the responses of the three fungal populations and in their effects under uniform environmental conditions. Analysis of variance indicated highly significant differences among the G. mosseae populations in terms of amounts of mycorrhizas formed, spore production and their effect on biomass production, shoot phosphorus concentration and water relations of M. officinalis. These results support the hypothesis that populations of G. mosseae from dissimilar environments are genetically different races or ecotypes and suggest that there may be significant genetic and physiological diversity within this morphologically defined taxon.
1 The arbuscular mycorrhizal (AM) fungi colonizing plants at a woodland site in North Yorkshire (UK) have been characterized from the roots of five plant species (Rubus fruticosus agg. L., Epilobium angustifolium L., Acer pseudoplatanus L., Ajuga reptans L. and Glechoma hederacea L.), and identified using small-subunit rRNA (SSUrRNA) gene amplification and sequencing.
2 Interactions between five plant species from the site and four co-occurring glomalean fungi were investigated in artificial one-to-one AM symbioses. Three of the fungi were isolated from the site; the fourth was a culture genetically similar to a taxon found at the site. Phosphorus uptake and growth responses were compared with non-mycorrhizal controls.
3 Individual fungi colonized each plant with different spatial distribution and intensity. Some did not colonize at all, indicating incompatibility under the conditions used in the experiments.
4Glomus hoi consistently occupied a large proportion of root systems and out-performed the other fungi, improving P uptake and enhancing the growth of four out of the five plant species. Only G. hoi colonized and increased P uptake in Acer pseudoplatanus, the host plant with which it associates almost exclusively under field conditions. Colonization of all plant species by Scutellospora dipurpurescens was sparse, and beneficial to only one of the host plants (Teucrium scorodonia). Archaeospora trappei and Glomus sp. UY1225 had variable effects on the host plants, conferring a range of P uptake and growth benefits on Lysimachia nummularia and T. scorodonia, increasing P uptake whilst not affecting biomass in Ajuga reptans and Glechoma hederacea, and failing to form mycorrhizas with A. pseudoplatanus.
5 These experimental mycorrhizas show that root colonization, symbiont compatibility and plant performance vary with each fungus–plant combination, even when the plants and fungi naturally co-exist.
6 We provide evidence of physical and functional selectivity in AM. The small number of described AM fungal species (154) has been ascribed to their supposed lack of host specificity, but if the selectivity we have observed is the general rule, then we may predict that many more, probably hard-to-culture glomalean species await discovery, or that members of species as currently perceived may be physiologically or functionally distinct.
The aim of the present work was to study colonization patterns in roots by different arbuscular mycorrhizal fungi developing from a mixed community in soil. As different fungi cannot be distinguished with certainty in planta on the basis of fungal structures, taxon-discriminating molecular probes were developed. The 5' end of the large ribosomal subunit containing the variable domains D1 and D2 was amplified by PCR from Glomus mosseae (BEG12), G. intraradices (LPA8), Gigaspora rosea (BEG9) and Scutellospora castanea (BEG1) using newly designed eukaryote-specific primers. Sequences of the amplification products showed high interspecies variability and PCR taxon-discriminating primers were designed to distinguish between each of these four fungi. A nested PCR, using universal eukaryotic primers for the first amplification and taxon-discriminating primers for the second, was performed on individual trypan blue-stained mycorrhizal root fragments of onion and leek, and root colonization by four fungi inoculated together in a microcosm experiment was estimated. More than one fungus was detected in the majority of root fragments and all four fungi frequently co-existed within the same root fragment. Root colonization by G. mosseae and G. intraradices was similar from individual mixed inoculum, whilst the frequency of S. castanea and Gig. rosea increased in the presence of the two Glomus species, suggesting that synergistic interactions may exist between some arbuscular mycorrhizal fungi.
Key species groups that affect major ecological processes are vital
components of community diversity. Many such key groups are found in the
soil, including the mycorrhizal fungi that may connect plants into a
functional ``wood-wide web''. Arbuscular mycorrhizal associations are
formed by fungi of the order Glomales with 90% of land plant families,
and many arbuscular mycorrhizal fungi are thought to have a broad host
range. Here we show that, despite this broad host range, the diversity
of arbuscular mycorrhizal fungi is strikingly low in arable sites
compared with a woodland.
Fossilized fungal hyphae and spores from the Ordovician of Wisconsin (with an age of about 460 million years) strongly resemble
modern arbuscular mycorrhizal fungi (Glomales, Zygomycetes). These fossils indicate that Glomales-like fungi were present
at a time when the land flora most likely only consisted of plants on the bryophytic level. Thus, these fungi may have played
a crucial role in facilitating the colonization of land by plants, and the fossils support molecular estimates of fungal phylogeny
that place the origin of the major groups of terrestrial fungi (Ascomycota, Basidiomycota, and Glomales) around 600 million
years ago.
We used differences in small subunit ribosomal RNA genes to identify groups of arbuscular mycorrhizal fungi that are active in the colonisation of plant roots growing in arable fields around North Yorkshire, UK. Root samples were collected from four arable fields and four crop species, fungal sequences were amplified from individual plants by the polymerase chain reaction using primers NS31 and AM1. The products were cloned and 303 clones were classified by their restriction pattern with HinfI or RsaI; 72 were subsequently sequenced. Colonisation was dominated by Glomus species with a preponderance of only two sequence types, which are closely related. There is evidence for seasonal variation in colonisation in terms of both level of colonisation and sequence types present. Fungal diversity was much lower than that previously reported for a nearby woodland.
Arbuscular mycorrhizal (AM) fungi are biotrophic symbionts colonizing about two-thirds of land plant species and found in all ecosystems. They are of major importance in plant nutrient supply and their diversity is suggested to be an important determinant of plant community composition. The diversity of the AM fungal community composition in the roots of two plant species (Agrostis capillaris and Trifolium repens) that co-occurred in the same grassland ecosystem was characterized using molecular techniques. We analysed the small subunit (SSU) ribosomal RNA gene amplified from a total root DNA extract using AM fungal-specific primers. A total of 2001 cloned fragments from 47 root samples obtained on four dates were analysed by restriction fragment length polymorphism, and 121 of them were sequenced. The diversity found was high: a total of 24 different phylotypes (groups of phylogenetically related sequences) colonized the roots of the two host species. Phylogenetic analyses demonstrate that 19 of these phylotypes belonged to the Glomaceae, three to the Acaulosporaceae and two to the Gigasporaceae. Our study reveals clearly that the AM fungal community colonizing T. repens differed from that colonizing A. capillaris, providing evidence for AM fungal host preference. In addition, our results reveal dynamic changes in the AM fungal community through time.
Arbuscular mycorrhizal fungi (AMF) are ecologically important root symbionts of most terrestrial plants. Ecological studies of AMF have concentrated on differences between species; largely assuming little variability within AMF species. Although AMF are clonal, they have evolved to contain a surprisingly high within-species genetic variability, and genetically different nuclei can coexist within individual spores. These traits could potentially lead to within-population genetic variation, causing differences in physiology and symbiotic function in AMF populations, a consequence that has been largely neglected. We found highly significant genetic and phenotypic variation among isolates of a population of Glomus intraradices but relatively low total observed genetic diversity. Because we maintained the isolated population in a constant environment, phenotypic variation can be considered as variation in quantitative genetic traits. In view of the large genetic differences among isolates by randomly sampling two individual spores, <50% of the total observed population genetic diversity is represented. Adding an isolate from a distant population did not increase total observed genetic diversity. Genetic variation exceeded variation in quantitative genetic traits, indicating that selection acted on the population to retain similar traits, which might be because of the multigenomic nature of AMF, where considerable genetic redundancy could buffer the effects of changes in the genetic content of phenotypic traits. These results have direct implications for ecological research and for studying AMF genes, improving commercial AMF inoculum, and understanding evolutionary mechanisms in multigenomic organisms.
High genetic variability and low local diversity in an arbuscular mycorrhizal fungal population
- Kocham Kuhng Fontanillasp Fumagallil Goudetj Sandersir
Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR.
2004. High genetic variability and low local diversity in an arbuscular
mycorrhizal fungal population. Proceedings of the National Academy of
Sciences, USA 101: 2369-2371.
Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops
- Daniell