Arbuscular Mycorrhizal Symbiosis Limits Foliar Transcriptional Responses to Viral Infection and Favors Long-Term Virus Accumulation

Abstract

Tomato (Solanum lycopersicum) can establish symbiotic interactions with arbuscular mycorrhizal (AM) fungi, and can be infected by several pathogenic viruses. Here, we investigated the impact of mycorrhization by the fungus Glomus mosseae on the Tomato spotted wilt virus (TSWV) infection of tomato plants by transcriptomic and hormones level analyses. In TSWV-infected mycorrhizal plants, the AM fungus root colonization limited virus-induced changes in gene expression in the aerial parts. The virus-responsive upregulated genes, no longer induced in infected mycorrhizal plants, were mainly involved in defense responses and hormone signaling, while the virus-responsive downregulated genes, no longer repressed in mycorrhizal plants, were involved in primary metabolism. The presence of the AM fungus limits, in a salicylic acid-independent manner, the accumulation of abscissic acid observed in response to viral infection. At the time of the molecular analysis, no differences in virus concentration or symptom severity were detected between mycorrhizal and nonmycorrhizal plants. However, in a longer period, increase in virus titer and delay in the appearance of recovery were observed in mycorrhizal plants, thus indicating that the plant's reaction to TSWV infection is attenuated by mycorrhization.Arbuscular mycorrhiza (AM) is the term used to describe the mutualistic association between most land plants and fungi from the phylum Glomeromycota (Parniske 2008). The ability to form this association is widely distributed throughout the plant kingdom, and involves most agricultural, horticultural, and hardwood species (Bonfante and Genre 2010). The symbiosis develops in roots where the fungus colonizes the cortex and obtains carbon from the plant while facilitating the transfer of mineral nutrients to the root cells, through differentiated, highly branched intracellular fungal structures called arbuscules (Bonfante and Anca 2009). The benefits of the AM symbiosis on plant fitness are well described, including a better mineral nutrition and increased ability to overcome biotic and abiotic stresses (Aroca et al. 2008;Gernns et al. 2001;Hildebrandt et al. 2007; Pozo and Azcòn-Aguilar 2007;Pozo et al. 2010;van der Heijden and Sanders 2002).The AM symbiosis can have important impacts on plant interactions with pathogens. Alleviation of damage caused by soilborne pathogens has been widely reported in mycorrhizal plants. Most studies deal with the reduction of incidence or severity of soilborne disease. mainly root rot or wilting caused by fungi such as Rhizoctonia, Fusarium, or Verticillium spp., and root rot caused by oomycetes, including Phytophthora, Pythium, and Alphanomyces spp. Experimental evidence also supports the hypothesis that AM symbiosis preconditions plant tissues for a more effective activation of defense responses against stress. This phenomenon, which is also induced in plants by necrotizing pathogens, plant-growth-promoting fungi and rhizobacteria, or treatment with various natural and synthetic compounds, is know...

Interactive physiological response of potato (Solanum tuberosum L.) plants to fungal colonization and Potato virus Y (PVY) infection

“…The effect of mycorrhization of Solanum lycopersicum plants on the infection process with tomato spotted wilt virus (TSWV) suggests that mycorrhizae may cause suppression of plant response to viral infection [23]. Mycorrhizal symbiosis was shown to decrease expression of genes activated during viral infection and reduce visual symptoms in long-term [23]. Similarly, in our study growth promotion of virus-infected plants in mycorrhizal symbiosis was observed.…”

“…Since in our study the level of H 2 O 2 was tested 10 weeks after plant inoculation, any potential factors contributing to induction of resistance would have already acted. The effect of mycorrhization of Solanum lycopersicum plants on the infection process with tomato spotted wilt virus (TSWV) suggests that mycorrhizae may cause suppression of plant response to viral infection [23]. Mycorrhizal symbiosis was shown to decrease expression of genes activated during viral infection and reduce visual symptoms in long-term [23].…”

Transcriptomics of the Interaction between the Monopartite Phloem-Limited Geminivirus Tomato Yellow Leaf Curl Sardinia Virus and Solanum lycopersicum Highlights a Role for Plant Hormones, Autophagy and Plant Immune System Fine Tuning during Infection

“…Actually, in addition to playing a key role in developmental processes and in response to abiotic stresses, ABA has been shown to be involved in the interaction between RNA viruses and their host plants. ABA level was observed to increase in tomato shoots infected by Tomato spotted wilt virus [13], [51] and in tobacco leaves systemically infected by TMV [52]; interestingly, treatment with exogenous ABA improved resistance to TMV infection in tobacco [53]. A first relation between ABA and geminivirus infection was observed in Arabidopsis plants inoculated with the curtovirus, Beet severe curly top virus (BSCTV).…”

Arbuscular mycorrhiza‐mediated resistance in tomato against Cladosporium fulvum‐induced mould disease

“…Published articles have demonstrated that the systemic effect of pathogen infection on AM formation is quite variable depending on the tripartite pathogen—AM fungus—host plant interaction. For instance, Alternaria solani infection on leaves reduced the symbiosis rate between G. mosseae and tomato roots (Song et al., ), whereas the tomato spotted wilt virus infection on leaves enhanced the percentage of arbuscules within the G. mosseae ‐inoculated areas (Miozzi et al., ). The effect of AMF colonization on host growth also depends on the species‐specific plant–fungus interaction.…”