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Occurrence and role of Gliocladium roseum in field-grown soybeans in Illinois

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Abstract

Gliodadium roseum was isolated from roots, stems, pods and seeds of soybeans without symptoms in Illinois. It did not cause symptoms but was isolated from roots and stems of soybeans either inoculated or grown in soil infested with G. roseum. Isolation increased with increasing age of plant, but decreased with increasing distance up the stem. G. roseum appears to be a non-pathogenic systemic parasite of soybeans.

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... Strains of C. rosea have been isolated from all continents except Antarctica and from a wide range of habitats (Sun et al., 2020a;Sutton et al., 1997), indicating a cosmopolitan distribution. Strains are typically isolated from soil, fungi, plant debris and from plant parts including roots, leaves and flowers (Walker and Maude, 1975;Nobre et al., 2005;Mueller and Sinclair, 1986;García et al., 2003), but isolations from nematodes and insects are also reported (Verdejo-Lucas et al., 2002;Haarith et al., 2020). Strains of C. rosea are even present as endophytes in several halophyte plant species in coastal areas (You et al., 2017). ...
... There is clear evidence that many Clonostachys spp. strains, including C. rosea, can live as endophytes in plants (Maillard et al., 2020;Saraiva et al., 2015;Sutton et al., 2002;Chatterton and Punja, 2010;Mueller and Sinclair, 1986). This fact alone is significant for biocontrol as the BCA can be present at the sites of infection of plant pathogens. ...
... This discrepancy between plant-beneficial and plant-detrimental properties of different strains of C. rosea is intriguing but not easily explained. The intimate association between C. rosea and plants, sometimes even involving systemic, asymptomatic colonisation Mueller and Sinclair, 1986), indicate a delicate balance between the colonisation of C. rosea and the immune responses by the plant host. It is plausible that poor physiological status of the plant, a high inoculum of C. rosea, as well as certain genotype-bygenotype (C. ...
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The fungus Clonostachys rosea was recognized as an aggressive parasite on other fungi already in the late 1950s. Research into its potential use in biological control of plant diseases soon followed. Today, there are several commercial products based on C. rosea available for biocontrol applications worldwide. Although its mycoparasitic ability has attracted a lot of interest, C. rosea is now viewed as an ecological generalist whose lifestyle also includes plant endophytism, rhizosphere competence and polyphagous ability. Protocols for producing high amounts of C. rosea spores are available for both solid state and liquid fermentation. Low temperature and low moisture content are key factors that influence the shelf life of C. rosea propagules. Products based on C. rosea can be delivered to flowers using bumble bees, applied by spraying or as seed dressing or by incorporation into the soil. Clonostachys rosea is today an established factor in sustainable plant protection strategies.
... Nordström [65] reported variable colonization of tomato and Arabidopsis thaliana by a C. rosea f. catenula strain. Sutton et al. [20] also reported that C. rosea is a plant endophyte on different plant species and was isolated from roots and stems of soya beans (Glycine max), which were either inoculated with, or were grown in, soil infested with C. rosea [66]. Nordström [65] suggested that the rhizosphere can affect the establishment of C. rosea. ...
... Moloinyane and Nchu [68] did not observe a reduction of grapevine mealy bug infestations by the endophyte Beauveria bassiana, and they argued that factors such as host species, fungal strain, and insect species may influence the efficacy of endophytic entomopathogens on both the plant and the insect pest. However, inoculation method and the effect of endophytic colonization can be influenced by biotic and abiotic factors, such as growth substrate, plant species and age, fungal species and inoculum density [59,66,69]. For instance, Tefera and Vidal [59] demonstrated that despite the inoculation method used, B. bassiana colonized the entire parts of sorghum plants. ...
... Nordström [65] reported variable colonization of tomato and Arabidopsis thaliana by a C. rosea f. catenula strain. Sutton et al. [20] also reported that C. rosea is a plant endophyte on different plant species and was isolated from roots and stems of soya beans (Glycine max), which were either inoculated with, or were grown in, soil infested with C. rosea [66]. Nordström [65] suggested that the rhizosphere can affect the establishment of C. rosea. ...
... Moloinyane and Nchu [68] did not observe a reduction of grapevine mealy bug infestations by the endophyte Beauveria bassiana, and they argued that factors such as host species, fungal strain, and insect species may influence the efficacy of endophytic entomopathogens on both the plant and the insect pest. However, inoculation method and the effect of endophytic colonization can be influenced by biotic and abiotic factors, such as growth substrate, plant species and age, fungal species and inoculum density [59,66,69]. For instance, Tefera and Vidal [59] demonstrated that despite the inoculation method used, B. bassiana colonized the entire parts of sorghum plants. ...
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Citation: Ntsobi, N.; Fanadzo, M.; Le Roes-Hill, M.; Nchu, F. Effects of Clonostachys rosea f. catenula Inoculum on the Composting of Cabbage Wastes and the Endophytic Activities of the Composted Material on Tomatoes and Red Spider Mite Infestation. Microorganisms 2021, 9, 1184. https://doi.
... Reports point to an abundance of G. roseum within senescent and dead roots and foliage of a wide variety of plants and in plants weakened by stress factors such as herbicides and disease (5,9,11,12,13,16). Intriguingly, G. roseum is known to colonize, without symptom production, apparently healthy roots, stems, pods, and seeds of soybean (34,46), roots of red clover (50), and leaves of strawberry (55) and raspberry (63). In these instances, the fungus apparently colonized the host as a nonpathogenic parasite, and in soybean at least, the association is systemic. ...
... The antagonist progressively colonized senescent leaves and flowers of strawberry, begonia, cyclamen, and geranium, and frequently sporulated within a couple days after the tissues died (38,56; D-W Li and G. Peng, unpublished). While senescence and stress apparently favor progressive colonization of host tissues by G. roseum, the antagonist also is known to colonize vascular elements of vigorous soybean and red clover plants (34,46,50). In our experience and in almost all other reports, host tissues infected by G. roseum remained symptomless. ...
... Reports point to an abundance of G. roseum within senescent and dead roots and foliage of a wide variety of plants and in plants weakened by stress factors such as herbicides and disease (5,9,11,12,13,16). Intriguingly, G. roseum is known to colonize, without symptom production, apparently healthy roots, stems, pods, and seeds of soybean (34,46), roots of red clover (50), and leaves of strawberry (55) and raspberry (63). In these instances, the fungus apparently colonized the host as a nonpathogenic parasite, and in soybean at least, the association is systemic. ...
... The antagonist progressively colonized senescent leaves and flowers of strawberry, begonia, cyclamen, and geranium, and frequently sporulated within a couple days after the tissues died (38,56; D-W Li and G. Peng, unpublished). While senescence and stress apparently favor progressive colonization of host tissues by G. roseum, the antagonist also is known to colonize vascular elements of vigorous soybean and red clover plants (34,46,50). In our experience and in almost all other reports, host tissues infected by G. roseum remained symptomless. ...
... Reports point to an abundance of G. roseum within senescent and dead roots and foliage of a wide variety of plants and in plants weakened by stress factors such as herbicides and disease (5,9,11,12,13,16). Intriguingly, G. roseum is known to colonize, without symptom production, apparently healthy roots, stems, pods, and seeds of soybean (34,46), roots of red clover (50), and leaves of strawberry (55) and raspberry (63). In these instances, the fungus apparently colonized the host as a nonpathogenic parasite, and in soybean at least, the association is systemic. ...
... The antagonist progressively colonized senescent leaves and flowers of strawberry, begonia, cyclamen, and geranium, and frequently sporulated within a couple days after the tissues died (38,56; D-W Li and G. Peng, unpublished). While senescence and stress apparently favor progressive colonization of host tissues by G. roseum, the antagonist also is known to colonize vascular elements of vigorous soybean and red clover plants (34,46,50). In our experience and in almost all other reports, host tissues infected by G. roseum remained symptomless. ...
... Therefore, we focused our research on C. rosea. According to the literature reports, strains of this species, which are considered to be cosmopolitan, have been isolated from a wide range of soils, fungi, plant remains and plant parts (roots, leaves and even flowers), freshwater, forests, heaths, etc. (Walker and Maude, 1975;Mueller and Sinclair, 1986;Sutton et al. 1997;García et al. 2003;Nobre et al. 2005;Sun et al. 2020;Yu et al. 2020). The fungus is characterized by a variety of lifestyles, from saprobic to endophytic to parasitic, with a wide range of target organisms, including fungi, nematodes and insects (Shigo, 1958;Li et al. 2002;Verdejo-Lucas et al. 2002;Chatterton and Punja, 2012;Saraiva et al. 2015;Haarith et al. 2020;Maillard et al. 2020). ...
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The unfavorable phenomenon of activated sludge bulking that occurs in sewage treatment plants (WWTPs) is caused by the over-proliferation of filamentous bacteria that should be limited by the Lecane rotifers that feed on them; however, predatory, rotiferovorous fungi that often inhabit WWTPs pose a real threat to these organisms. To solve this problem, we investigated the interaction of the fungus Clonostachys rosea, which is a known Biological Control Agent (BCA) and the predacious Zoophagus sp. in simplified laboratory culture conditions. The presence of C. rosea in the cultures reduced the number of active traps, thus translating into a much smaller number of rotifers being caught. The mycelium of C. rosea was labeled with a red fluorescent protein (RFP). The life cycle of C. rosea that were attacking Zoophagus sp. (hunting for rotifers) is described. C. rosea spores germinate into single-celled forms and penetrate the interior of the Zoophagus mycelium where they feed on the cytoplasm. Then is the mycelium produced abundantly and forms conidiophores. This type of life strategy has not been known before. The obtained results demonstrated the potential of C. rosea as a BCA that can be used to protect rotifers in the event of an infection of activated sludge by the predatory fungi that threaten the rotifer population.
... The highest presence of C. rosea has been recorded from soil, followed by different parts of plants including roots, stems, leaves, fruits, and seeds. This fungal species normally occurs on plant organ surfaces, such as the phylloplane of strawberry, and the mycorrhizoplane of European silver fir (Abies alba) (McLean and Sutton 1992;Mosca and Marchisio 1985), but is also known to exhibit endophytic ability in different tissues, colonizing roots, stems, pods, and seeds of soybean (Glycine max (L.) Merr.), leaves, stems, roots and seeds of onion (Allium cepa L.), foliage of Geranium cultivars and red clover (Trifolium pratense L.), and leaves of strawberry (Fragaria x ananassa Duch.) and raspberry (Rubus corchorifolius L.f.) (Mueller and Sinclair 1986;Skipp and Christensen 1990;Sutton and Peng 1993;Muvea et al. 2014;Yu 1996). ...
Article
Clonostachys rosea is an ascomycetous fungal species commonly found in tropical and subtropical regions as soil saprotroph, plant decomposer, and endophyte. This fungus is also well-known as a mycoparasite, exhibiting strong biological control ability against numerous fungal plant pathogens, nematode and insect parasite. In this study, we isolated for the first time C. rosea as entomopathogen of the Coleoptera species Ophrida xanthospilota (Chrysomelidae) in China. This finding increases our knowledge of the ecology and distribution of C. rosea. Full-text available at: https://www.tandfonline.com/eprint/AJUWMMKIS5BKWGHSI38U/full?target=10.1080/11263504.2021.2013339
... It also has been isolated as a saprotrophic species from soil and various plant materials such as senescence roots, dead trees, decaying leaves and litter samples (Domsch et al. 1980). There is a report of endophytic infection of soybean plants with this species without causing disease symptoms (Mueller and Sinclair 1986). Theron and Holz (1991) reported a dry rot of potato tubers caused by C. rosea. ...
Article
During a field survey in faba bean cultivating areas in 2015, in Tarom county, north-west of Iran, a fungal species was frequently isolated from faba bean plants showing wilt and crown rot symptoms. Identification using morphological characteristics as well as molecular data based on the sequence of internal transcribed spacer region, revealed the fungal species as Clonostachys rosea. Greenhouse pathogenicity experiment, demonstrated this species as the causal agent of the disease. This is the first report of the occurrence as well as pathogenicity of C. rosea on faba bean in the world.
... The fungus is primarily known as a versatile biological control agent (BCA) that can control seed-and soil-borne diseases (Jensen et al., 2007) as well as stem, leaf and fruit diseases primarily caused by Botrytis cinerea (Sutton et al., 1997;Reeh & Cutler, 2013). However, it has also been reported as a plant endophyte on various plant species (Sutton et al., 1997) and from, e.g., soybean, Mueller & Sinclair (1986) isolated C. rosea from roots and stems of plants that were either inoculated with or were grown in soil infested with C. rosea. ...
... It may well be that these fungi could enter cut surfaces of plant residues and use them as a food source after harvest, particularly if normal resistance mechanisms were impaired by senescence in the residue. Of note here is the recent report that G. roseum has been found as a non-pathogenic systemic parasite of soybeans, particularly of roots and older parts of the stem (Mueller & Sinclair, 1986), but the method of entry into the soybean is not known. ...
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To assess the ability of fungi antagonistic to Sclerotinia sclerotiorum to inhibit the formation of sclerotia and to grow through plant tissue from cut surfaces, a plant-tissue-based system has been developed using celery, lettuce and tomato segments. Pythium oligandrum consistently showed no ability to grow through plant tissue or prevent sclerotium formation whereas Gliocladium roseum and three isolates of Trichoderma harzianum showed significant ability to grow through plant tissue and significantly decreased the production of sclerotia. Treatment of the plant tissue with G. roseum or T. harzianum 24 h before, or at the same time as, application of S. sclerotiorum gave significantly greater inhibition of sclerotium formation than did treatment 24 h after application of S. sclerotiorum. Of the fungi tested, G. roseum had the greatest ability to grow through the tissue and T. harzianum WT6 the greatest ability to inhibit sclerotium formation.
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The black timber bark beetle ( Xylosandrus germanus ) is a strongly invasive ambrosia beetle and an important forest pest in Slovakia. This pest is closely associated with symbiotic fungi used as its food source. We investigated the fungi associated with X. germanus adults in Slovakia. In this study, Beauveria bassiana , B. pseudobassiana , Clonostachys rosea , Fusarium oxysporum , Ophiostoma quercus , Phaeoacremonium scolyti , and Talaromyces amestolkiae were isolated and identified by morphological and molecular analyses. The fungus Ophiostoma quercus was most frequently isolated from living beetles, while the entomopathogenic Beauveria bassiana was the most commonly isolated from dead beetles. The morphological descriptions of fungi based on isolates from the surface of X. germanus adults are provided.
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Clonostachys rosea, an ascomycetous, omnipresent, cellulose-decaying soil fungus, has been reported to be a well-known mycoparasitic biological control agent. In this study, we isolated C. rosea, a mycoparasitic fungus for the first time in India from sclerotia of the notorious plant pathogen Sclerotinia sclerotiorum, causing head rot disease in cabbage. A total of five mycoparasitic fungi were isolated from the sclerotial bodies of S. sclerotiorum (TNAU-CR 01, 02, 03, 04 and 05). All the isolates were tested under morpho-molecular characterization. Among them, TNAU-CR 02 showed the greatest mycelial inhibition of 79.63% over the control. Similarly, the SEM imaging of effective C. rosea isolates indicated the presence of numerous conidia destroying the outer cortex layers of sclerotia. Metabolite fingerprinting of C. rosea TNAU-CR 02 identified 18 chemical compounds using GC-MS analysis. The crude antibiotics of C. rosea TNAU-CR 02 were verified for their antifungal activity against S. sclerotiorum and the results revealed 97.17% mycelial inhibition compared with the control. Similarly, foliar application of TNAU-CR 02 at 5 mL/litre on 30, 45 and 60 days after transplanting showed the lowest disease incidence of 15.1 PDI compared to the control. This discovery expands our understanding of the biology and the dissemination of C. rosea, providing a way for the exploitation of C. rosea against cabbage head rot pathogens.
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The rhizosphere competence on barley of the antagonist, Gliocladium roseum (isolate IK 726), was investigated in semi-sterile sand and field soil. Following application of the antagonist to the seeds it was shown by the dilution plating method, that G. roseum was present on the roots. In sand colonization occurred most on proximal compared to distal parts of the roots. In field soil, 4 month after sowing, G. roseum was recovered from roots of plants derived both from seed inoculated with G. roseum and non inoculated with the antagonist. However, the population of G. roseum was significantly higher on roots derived from inoculated seeds.
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Morphological development and interactions of Glioclodium roseum and Botrytis cinerea on leaves, stems, and stemens of Taspberry were examined by light microscopy. Tissues were inoculated with conidial suspensions of the antagonist, the pathogen, or both, and kept in continuous high humidity at 21-23°C. In the absence of B. cinerea, G. roseum produced germ tubes and superficial hyphae with short side branches that penetrated the host. No symptoms developed, but numerous conidiophores and conidia of G. roseum were observed on tissues at 40-72 h after inoculation. In the absence of G. roseum, B. cinerea germinated slowly on leaves but rapidly on stems and stamens. The pathogen produced a few single-lobed appressoria on leaves, various kinds of appressoria on stems, and a range of appressoria and infection cushions on stamens. After coinoculation, G. roseum strongly suppressed germination and germ tube growth of B. cinerea on leaf surfaces. On stems the antagonist moderately suppressed germ tube growth and intensely parasitized the pathogen. Hyphae of G. roseum grew on, coiled around, penetrated, and developed within hyphae and conidia of B. cinerea. On stamens, G. roseum reduced colonization incidence of the tissues but did not suppress germination, growth, or formation of appressoria and infection cushions by B. cinerea, or intensely parasitize the pathogen. Available nutrients are postulated to determine the mode of antagonism on the various organs. G. roseum suppressed sporulation and, by inference, infection and colonization of B. cinerea in raspberry tissues more effectively when applied before or at the same time as the pathogen than after the pathogen. It is concluded that G. roseum is a nonpathogenic parasite of raspberry with flexible modes of antagonism towards B. cinerea in this host.
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Colonies of Aspergillus glaucus arising from single asexual spores or hyphal tips of the same or different homokaryon clones often vary in their adaptability to new environments. This shows itself as differences in the percentage survival and mean lag period of inocula taken from colonies growing on a normal medium when transferred to one containing a poison such as mercuric chloride, or unfamiliar sugar sources, e.g. arabinose, galactose, lactose and xylose. The differences in adaptability to these new media between homokaryon clones are characteristically nuclear in origin, while those between colonies of the same clone are characteristically cytoplasmic. The nuclear system might be formally regarded as epistatic to the cytoplasmic system involved in these adaptive changes. Selection for the cytoplasmic differences can produce marked changes in the adaptability of the asexual spores of single colonies, even though the selection technique is such that colonies in the direct line of selected descent are at no time exposed to the new media. The changes in adaptability to mercuric chloride are independent of those for adaptability to the new sugars and only the latter shows any correlation with changes in rate of growth. There is therefore evidence of two or possibly three cytoplasmic systems with much the same properties of variation but independent in action and transmission.
The Genus Aspergillus
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