Arbuscular Mycorrhizal Symbiosis Leads to Differential Regulation of Drought-Responsive Genes in Tissue-Specific Root Cells of Common Bean

Abstract

Arbuscular mycorrhizal fungi (AMF) colonization in plants promotes both local and systemic changes in the gene expression profiles of the host that might be relevant for drought-stress perception and response. Drought-tolerant common bean plants (cv. BAT 477), colonized by a mixture of AMF (Glomus clarum, Acaulospora scrobiculata, and Gigaspora rosea), were exposed to a water deprivation regime of 96 h during pre-flowering. Root transcriptomes were accessed through RNA-Seq revealing a set of 9,965 transcripts with significant differential regulation in inoculated plants during a water deficit event, and 10,569 in non-inoculated. These data include 1,589 transcripts that are exclusively regulated by AMF-inoculation, and 2,313 under non-inoculation conditions. Relative gene expression analyses of nine aquaporin-related transcripts were performed in roots and leaves of plants harvested at initial stages of treatment. Significant shifts in gene expression were detected in AM water deficit-treated roots, in relation to non-inoculated, between 48 and 72 h. Leaves also showed significant mycorrhizal influence in gene expression, especially after 96 h. Root cortical cells, harboring or not arbuscules, were collected from both inoculation treatments through a laser microdissection-based technique. This allowed the identification of transcripts, such as the aquaporin PvPIP2;3 and Glucan 1,3 β-Glucosidase, that are unique to arbuscule-containing cells. During the water deficit treatment, AMF colonization exerted a fine-tune regulation in the expression of genes in the host. That seemed to initiate in arbuscule-containing cells and, as the stressful condition persisted, propagated to the whole-plant through secondary signaling events. Collectively, these results demonstrate that arbuscular mycorrhization leads to shifts in common bean’s transcriptome that could potentially impact its adaptation capacity during water deficit events.

Benefits of Arbuscular Mycorrhizal Fungi Application to Crop Production under Water Scarcity

“…Downregulation of genes TIP1;1, TIP2;3, PIP1;1, PIP1;3, PIP1;4, PIP1;6, PIP2;2, and PIP2;4 whereas only upregulation of TIP4;1 were observed in drought-sensitive cultivar colonized by Rhizophagus irregularis, supporting the decrease in water loss in host plants subjected to drought stress [71]. Recent research also revealed a significant shift in the transcriptional regulation profiles with AQP genes as potential targets in mycorrhizal roots, in comparison to non-AM ones during a water stress event, which may influence some key metabolic pathways linked with drought response [76]. In parallel, it has been proposed that during drought stress a controlled mechanism mediated by the presence of arbuscules at cortical cells in roots fine-tuned the gene expression regulation in the host plant [76].…”

“…Recent research also revealed a significant shift in the transcriptional regulation profiles with AQP genes as potential targets in mycorrhizal roots, in comparison to non-AM ones during a water stress event, which may influence some key metabolic pathways linked with drought response [76]. In parallel, it has been proposed that during drought stress a controlled mechanism mediated by the presence of arbuscules at cortical cells in roots fine-tuned the gene expression regulation in the host plant [76].…”

Flowering plant immune repertoires expand under mycorrhizal symbiosis

“…(). Similarly, transcriptomic studies of genes up‐regulated in response to AM colonization find some MycEx genes, but no family is over‐represented (Sugimura & Saito, ; Recchia et al., ; Vangelisti et al., ; and Supporting Information Table ). Transcriptomic studies do report up‐regulation of defense‐related genes following AM colonization, but these genes are mostly downstream of the signaling pathways represented by the MycEx familes (Calabrese et al., ; Hohnjec, Vieweg, Puhler, Becker, & Kuster, ).…”

“…They found 744 genes up‐regulated in the AM‐treated plants. Recchia, Konzen, Cassieri, Caldas, and Tsai () used RNA‐seq to compare root transcriptomes of Phaseolus vulgaris plants grown with or without AM fungal inoculum. They found 714 genes up‐regulated in the plants grown with AM.…”

“…A search among gene lists related to arbuscular mycorrhization finds some MycEx genes, but they are not over-represented in any set we examined (Bravo et al, 2016;Delaux et al, 2014;Recchia et al, 2018;Sugimura & Saito, 2017;Vangelisti et al, 2018) (Supporting Information Table S8).…”