Arbuscular Mycorrhizal Symbiosis: Plant Friend or Foe in the Fight Against Viruses?

Miozzi, Laura; Vaira, A. M.; Catoni, Marco; Fiorilli, Valentina; Accotto, G. P.; Lanfranco, Luisa

doi:10.3389/fmicb.2019.01238

Cited by 67 publications

(51 citation statements)

References 64 publications

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“…Our results are consistent with those of [ 37 ] showing a reduction in viral symptoms in mycorrhizal tomato plants infected by tomato yellow leaf curl Sardinia virus (a DNA virus) when compared with those infected but not mycorrhized. However, our results are in contrast with those reported by other studies, performed on different RNA viruses, highlighting that the AMF colonization may lead to a worsening of symptoms and to an increase of viral titer over time [ 34 , 35 , 52 , 53 ]. Overall, these data suggest that the mycorrhization interferes with dynamics of viral infection and symptomatology in a way that likely depends on the specific combination of virus and plant species involved.…”

Section: Discussioncontrasting

confidence: 99%

“…Although AMF colonization has been already shown to decrease the severity of diseases caused by several plant pathogens [ 24 ], the effects of AMF on plant–virus interaction have received limited consideration and are not yet fully understood. The final outcome of a plant–AMF–virus tripartite interaction relies on several factors, including viral pathogen lifestyle, nutritional status of the plant, and timing of interaction [ 35 ]. The term “mycorrhiza-induced susceptibility” (MIS) has been proposed for the cases where AMF colonization increases the susceptibility of plants to viruses [ 35 ].…”

Section: Introductionmentioning

confidence: 99%

“…The final outcome of a plant–AMF–virus tripartite interaction relies on several factors, including viral pathogen lifestyle, nutritional status of the plant, and timing of interaction [ 35 ]. The term “mycorrhiza-induced susceptibility” (MIS) has been proposed for the cases where AMF colonization increases the susceptibility of plants to viruses [ 35 ].…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Arbuscular Mycorrhizal Symbiosis Primes Tolerance to Cucumber Mosaic Virus in Tomato

Miozzi

Vaira

Brilli

et al. 2020

Viruses

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Tomato plants can establish symbiotic interactions with arbuscular mycorrhizal fungi (AMF) able to promote plant nutrition and prime systemic plant defenses against pathogens attack; the mechanism involved is known as mycorrhiza-induced resistance (MIR). However, studies on the effect of AMF on viral infection, still limited and not conclusive, indicate that AMF colonization may have a detrimental effect on plant defenses against viruses, so that the term “mycorrhiza-induced susceptibility” (MIS) has been proposed for these cases. To expand the case studies to a not yet tested viral family, that is, Bromoviridae, we investigated the effect of the colonization by the AMF Funneliformis mosseae on cucumber mosaic virus (CMV) infection in tomato by phenotypic, physiological, biochemical, and transcriptional analyses. Our results showed that the establishment of a functional AM symbiosis is able to limit symptoms development. Physiological and transcriptomic data highlighted that AMF mitigates the drastic downregulation of photosynthesis-related genes and the reduction of photosynthetic CO2 assimilation rate caused by CMV infection. In parallel, an increase of salicylic acid level and a modulation of reactive oxygen species (ROS)-related genes, toward a limitation of ROS accumulation, was specifically observed in CMV-infected mycorrhizal plants. Overall, our data indicate that the AM symbiosis influences the development of CMV infection in tomato plants and exerts a priming effect able to enhance tolerance to viral infection.

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Section: Discussioncontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Arbuscular Mycorrhizal Symbiosis Primes Tolerance to Cucumber Mosaic Virus in Tomato

Miozzi

Vaira

Brilli

et al. 2020

Viruses

Self Cite

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“…Finally, results from this study and other studies on the interaction of plant-virus and AM fungi [ 43 , 44 , 45 ] show a differential effect for AM fungi on plant virus disease development. We found that mycorrhizal symbiosis has a positive effect on tomato plant resistance to TBSV.…”

Section: Discussionsupporting

confidence: 67%

Differential Response of Mycorrhizal Plants to Tomato bushy stunt virus and Tomato mosaic virus Infection

et al. 2020

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Tomato bushy stunt virus (TBSV) and Tomato mosaic virus (ToMV) are important economic pathogens in tomato fields. Rhizoglomus irregulare is a species of arbuscular mycorrhizal (AM) fungus that provides nutrients to host plants. To understand the effect of R. irregulare on the infection by TBSV/ToMV in tomato plants, in a completely randomized design, five treatments, including uninfected control plants without AM fungi (C), uninfected control plants with AM fungi (M) TBSV/ToMV-infected plants without AM fungi (V), TBSV/ToMV-infected plants before mycorrhiza (VM) inoculation, and inoculated plants with mycorrhiza before TBSV/ToMV infection (MV), were studied. Factors including viral RNA accumulation and expression of Pathogenesis Related proteins (PR) coding genes including PR1, PR2, and PR3 in the young leaves were measured. For TBSV, a lower level of virus accumulation and a higher expression of PR genes in MV plants were observed compared to V and VM plants. In contrast, for ToMV, a higher level of virus accumulation and a lower expression of PR genes in MV plants were observed as compared to V and VM plants. These results indicated that mycorrhizal symbiosis reduces or increases the viral accumulation possibly via the regulation of PR genes in tomato plants.

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“…The benefits of AMF symbiosis to plants may arise from a combination of increased plant biomass and reprogrammed plant primary and secondary metabolome. However, studies have also found alternate results in which AMF association makes the plant vulnerable against pathogens [ 185 ] and decreases the biomass of the plants [ 35 ]. The outcome of the plant–AMF symbiosis is highly species-specific, where some AMF associations result in a positive outcome, while others exhibit neutral or negative outcomes (parasitism; [ 35 ]).…”

Section: Resultsmentioning

confidence: 99%

Unraveling Arbuscular Mycorrhiza-Induced Changes in Plant Primary and Secondary Metabolome

2020

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Arbuscular mycorrhizal fungi (AMF) is among the most ubiquitous plant mutualists that enhance plant growth and yield by facilitating the uptake of phosphorus and water. The countless interactions that occur in the rhizosphere between plants and its AMF symbionts are mediated through the plant and fungal metabolites that ensure partner recognition, colonization, and establishment of the symbiotic association. The colonization and establishment of AMF reprogram the metabolic pathways of plants, resulting in changes in the primary and secondary metabolites, which is the focus of this review. During initial colonization, plant–AMF interaction is facilitated through the regulation of signaling and carotenoid pathways. After the establishment, the AMF symbiotic association influences the primary metabolism of the plant, thus facilitating the sharing of photosynthates with the AMF. The carbon supply to AMF leads to the transport of a significant amount of sugars to the roots, and also alters the tricarboxylic acid cycle. Apart from the nutrient exchange, the AMF imparts abiotic stress tolerance in host plants by increasing the abundance of several primary metabolites. Although AMF initially suppresses the defense response of the host, it later primes the host for better defense against biotic and abiotic stresses by reprogramming the biosynthesis of secondary metabolites. Additionally, the influence of AMF on signaling pathways translates to enhanced phytochemical content through the upregulation of the phenylpropanoid pathway, which improves the quality of the plant products. These phytometabolome changes induced by plant–AMF interaction depends on the identity of both plant and AMF species, which could contribute to the differential outcome of this symbiotic association. A better understanding of the phytochemical landscape shaped by plant–AMF interactions would enable us to harness this symbiotic association to enhance plant performance, particularly under non-optimal growing conditions.

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Arbuscular Mycorrhizal Symbiosis: Plant Friend or Foe in the Fight Against Viruses?

Cited by 67 publications

References 64 publications

Arbuscular Mycorrhizal Symbiosis Primes Tolerance to Cucumber Mosaic Virus in Tomato

Arbuscular Mycorrhizal Symbiosis Primes Tolerance to Cucumber Mosaic Virus in Tomato

Differential Response of Mycorrhizal Plants to Tomato bushy stunt virus and Tomato mosaic virus Infection

Unraveling Arbuscular Mycorrhiza-Induced Changes in Plant Primary and Secondary Metabolome

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