Luciano Avio's research while affiliated with Università di Pisa and other places

Lettuce (Lactuca sativa L.) is an annual autogamous diploid plant belonging to Asteraceae and is among the top ten most profitable crops worldwide due to its nutritional value. Nevertheless, lettuce is an intensive crop with high input demand, especially fertilisers, both in soil-bound and soilless culture, with negative impact on the environment and production costs. In this context, arbuscular mycorrhizal symbioses could help to reduce the impact of fertilisers, improving plant nutrition, particularly regarding phosphorus, and contributing to growing healthier plants for human consumption. In our work, we compared lettuce plants (cv. Salinas) grown in soilless culture with optimal phosphorus concentration in the nutrient solution, with sub-optimal phosphorus nutrition and with plants grown with sub-optimal phosphorus concentration and inoculated with the fungus Funneliformis mosseae before transplanting. Higher levels of primary and secondary metabolites along with increased biomass were observed for mycorrhizal plants compared to lettuces grown with optimal and sub-optimal concentrations of phosphate. Gene expression profile was analysed in both roots and leaves, and transcriptomic values were associated with growth and biochemical parameters. Three-thousand and fifty-seven genes were differentially regulated by mycorrhizal symbiosis and 2,606 genes by optimal phosphate nutrition. Different genes related to photosynthesis, solute transport, metabolism of phytohormones, redox homeostasis, and transcriptional regulation resulted differentially regulated between culture conditions. Mycorrhizal plants also boosted the activation of genes involved in phenylpropanoids and carotenoids metabolism. In conclusion, growth, biochemical, and transcriptomic data show that symbiotic plants benefit both plant growth and leaf content of health promoting phytochemicals through genetic pathways that largely differed those activated in plants grown with optimal phosphorus supply.

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.

In intercropping systems, crop species select host-adapted microorganisms and influence the associated plant-microbial interactions like in the case of arbuscular mycorrhizal fungi (AMF). Attempts to assess the impact of intercropping on the activity, diversity, and community composition of AMF remain inconclusive, more so in intercropping systems involving traditional Mediterranean crops such as durum wheat and lentils. We carried out field experiments in Central Italy to assess the impact of relay intercropping durum wheat (Triticum durum Desf. cv. Minosse) and lentil (Lens culinaris Medik. cv. Elsa) on soil mycorrhizal inoculum potential (MIP) (2019 and 2020), AMF root colonization (2019, 2020, and 2021), and root AMF diversity and community composition (2020 and 2021), compared to the respective sole crops. Results showed that relay intercropping enhanced lentil grain yield and durum wheat grain protein concentration but marginally reduced durum wheat grain yield and lentil grain protein concentration. In addition, relay intercropping enhanced soil mycorrhizal activity but differentially influenced mycorrhizal root colonization compared to sole cropping. Sequencing analyses generated a total of 234 amplicon sequence variants belonging to Glomeromycota, which were assigned to 31 virtual taxa using the MaarjAM reference database. Glomeraceae and Claroideoglomeraceae were the most abundant taxa but had contrasting abundances in 2020 and 2021. The overall changes in AMF species diversity and community structure were affected by the interaction between crop species and year, and not by intercropping. Claroideoglomus and Septoglomus showed a strong association with lentil roots while Rhizophagus and Paraglomus were associated with durum wheat roots in 2020, affirming host genotype-AMF preferences. The principal component analysis showed that grain protein concentration was associated with selected mycorrhizal parameters such as community richness and AMF root colonization. Further studies on the functional analysis of the different AMF communities selected by the crop genotype and year may reveal the importance of intercropping in maintaining soil functionality and productivity under low-input systems.

Background and aims One of the most promising strategies for sustainable intensification of crop production involves the utilization of beneficial root-associated microorganisms, such as plant growth-promoting bacteria and arbuscular mycorrhizal fungi (AMF). The aim of this study was to investigate whether a seed-applied biostimulant, based on the bacterial strain Bacillus amyloliquefaciens IT-45 and a plant polysaccharide extract, and crop enhancement tools, such as hybrids with contrasting early vigor and nitrogen (N) plus phosphorus (P) starter fertilization, and their interactions, shape the communities of native root-colonizing AMF symbionts in maize. Methods A factorial growth chamber experiment was set up with two maize genotypes in natural soil. Mycorrhizal colonization was evaluated after root staining. The diversity and composition of AMF communities were assessed by PCR-DGGE of the 18S rRNA gene and amplicon sequencing. Results N and P fertilization determined a consistent reduction of AMF root colonization and, in combination of biostimulant, a reduction of AMF richness. The biostimulant alone generally did not affect AMF colonization or the community biodiversity. In addition the effect of the two factors were modulated by maize genotype. In all treatments, predominant AMF were represented by Glomus sp. and Funneliformis mosseae, while populations of the genus Rhizoglomus were rarely detected in biostimulant and NP fertilization treatments. Conclusion The results of this study increase our understanding of how the biostimulant seed treatment may affect native AMF communities, depending on NP fertilization and maize genotype and may improve the implementation of innovative tools in sustainable and resilient agroecosystems.

The increased ultraviolet radiation (UV) due to the altered stratospheric ozone leads to multiple plant physiological and biochemical adaptations, likely affecting their interaction with other organisms, such as pests and pathogens. Arbuscular mycorrhizal fungi (AMF) and UV-B treatment can be used as eco-friendly techniques to protect crops from pests by activating plant mechanisms of resistance. In this study, we investigated plant (Lactuca sativa) response to UV-B exposure and Funneliformis mosseae (IMA1) inoculation as well as the role of a major insect pest, Spodoptera littoralis. Lettuce plants exposed to UV-B were heavier and taller than non-irradiated ones. A considerable enrichment in phenolic, flavonoid, anthocyanin, and carotenoid contents and antioxidant capacity, along with redder and more homogenous leaf color, were also observed in UV-B-treated but not in AMF-inoculated plants. Biometric and biochemical data did not differ between AMF and non-AMF plants. AMF-inoculated plants showed hyphae, arbuscules, vesicles, and spores in their roots. AMF colonization levels were not affected by UV-B irradiation. No changes in S. littoralis-feeding behavior towards treated and untreated plants were observed, suggesting the ability of this generalist herbivore to overcome the plant chemical defenses boosted by UV-B exposure. The results of this multi-factorial study shed light on how polyphagous insect pests can cope with multiple plant physiological and biochemical adaptations following biotic and abiotic preconditioning.

Arbuscular mycorrhizal fungi (AMF) and ultraviolet-B radiation (UV-B) play important roles in plant–insect interactions by altering plant physiology and histology. We hypothesized that UV-B-induced oxidative stress was mitigated by AMF symbiosis. In this study, we conducted a multifactorial experiment to explore lettuce plant response to AMF inoculation and UV-B exposure (0.4 W m−2; 16 h d−1; 2 weeks), either together or individually, as well as the interaction with the polyphagous insect pest Myzus persicae (Sulzer). Lettuce plants subjected to UV-B radiation showed an increase in callose and oxidative stress indicators, as well as a decrease in stomatal density. Mycorrhizal colonization cancelled out the effect of UV-B on stomatal density, while the symbiosis was not affected by UV-B treatment. The plant volatile emission was significantly altered by UV-B treatment. Specifically, the non-terpene 1-undecene abundance (+M/+UVB: 48.0 ± 7.78%; −M/+UVB: 56.6 ± 14.90%) was increased, whereas the content of the non-terpene aldehydes decanal (+M/+UVB: 8.50 ± 3.90%; −M/+UVB: 8.0 ± 4.87%) and undecanal (+M/+UVB: 2.1 ± 0.65%; −M/+UVB: 1.20 ± 1.18%) and the sesquiterpene hydrocarbons (+M/+UVB: 18.0 ± 9.62 %; −M/+UVB: 19.2 ± 5.90%) was decreased. Mycorrhization, on the other hand, had no significant effect on the plant volatilome, regardless of UV-B treatment. Aphid population was unaffected by any of the treatments, implying a neutral plant response. Overall, this study provides new insights about the interactions among plants, UV-B, and AMF, outlining their limited impact on a polyphagous insect pest.

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.

Purpose Commercial production and the use of liquid vermicompost extract (LVE) is gaining attention as a technique that supports integrated soil-microbial-crop management for sustainable agriculture. However, the interaction effects of LVE, arbuscular mycorrhizal fungi (AMF), and host plants on the delivery of agroecosystem services in alkaline soil have been less studied. Methods We carried out a 3-year field experiment in Central Italy, to investigate the short-term effect of LVE on soil mycorrhizal inoculum potential (MIP), AMF root colonization, and productivity of berseem clover, lentil, and sunflower. LVE produced in different years were screened for microbial properties using Illumina Miseq sequencing. LVE was applied at seeding, crop stem elongation and flowering stages. Control crops received water as a placebo. Results LVE bacterial communities were more diverse and showed a higher turnover between 2019 and 2020 than fungal communities. Diverse microbial groups, the majority of which belonged to phyla Proteobacteria, Bacteroidetes, Firmicutes, and Mucoromycota, were detected, including N-fixers (Flavobacterium, Malikia, and Citrobacter), P-solubilizers (Pseudomonas), and C-degraders (Tolumonas, Arcobacter, and Mucor). Notably, LVE treatment enhanced soil MIP and AMF root colonization in most crops, but selectively improved shoot biomass of berseem clover (+ 32%) and sunflower (+ 34%), and grain yield (+ 37%) and oil concentration (+ 5%) in sunflower, compared to the corresponding non-treated controls. Conclusions LVE had diverse groups of bacteria and a few fungal taxa, and its application enhanced mycorrhizal properties and selected growth- and yield-related variables in lentil, berseem clover, and sunflower. This could be due to LVE’s biostimulating effect arising from the vermicompost-associated microbiome and biomolecules.