Abstract

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.

Highlights

  • Viruses are ubiquitous obligate intracellular parasites able to cause severe diseases worldwide [1,2,3,4].Virus infections dramatically impair host plant performances by hampering photosynthetic carbon assimilation [5] and alter a number of processes within plants, such as cell cycle, transport, protein modifications, secondary metabolism, hormone regulation, and biosynthesis of volatile and nonvolatile isoprenoids, weakening plant defenses and promoting virus transmission and replication [6].Viruses 2020, 12, 675; doi:10.3390/v12060675 www.mdpi.com/journal/virusesTo date, genetic resistance and control of vectors are the most widespread strategies against viral infection

  • We evaluated the arbuscular mycorrhizal fungi (AMF) colonization of the roots, in order to be sure that all the plants were successfully colonized by the AMF and to evaluate a possible impact of viral infection on AMF intraradical growth (Table S3)

  • Concerning the induction of more robust defense responses, we observed that the development of cucumber mosaic virus (CMV) infection was influenced by the AMF, that exerted an initial (14 dpi) protective role against viral symptoms development; this phenomenon disappeared over time, possibly as a consequence of a recovery occurred in the virus-infected plants [48]

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Summary

Introduction

Genetic resistance and control of vectors (insect/fungi and others) are the most widespread strategies against viral infection. Due to the viral high mutation and recombination rates [7,8,9], only a limited number of effective plant resistance genes are available and the acquisition of genetic resistance through crossing is not always obtainable [10]. Physical or chemical methods aimed to limit viral vector populations, such as physical barriers and chemical insecticides, are useful but not decisive in contrasting virus infection and may have negative consequences on nontarget organisms, public health, and environment [11,12,13]. Cucumber mosaic virus (CMV, type species of the genus Cucumovirus, family Bromoviridae) is an economically important RNA virus belonging to the top 10 list of plant viral pathogens [2,14] and has major agricultural impact worldwide. CMV is characterized by a wide host range including about

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