Host‐ and virus‐induced gene silencing of HOG1‐MAPK cascade genes in Rhizophagus irregularis inhibit arbuscule development and reduce resistance of plants to drought stress

Abstract

Summary Arbuscular mycorrhizal (AM) fungi can form beneficial associations with the most terrestrial vascular plant species. AM fungi not only facilitate plant nutrient acquisition but also enhance plant tolerance to various environmental stresses such as drought stress. However, the molecular mechanisms by which AM fungal mitogen‐activated protein kinase (MAPK) cascades mediate the host adaptation to drought stimulus remains to be investigated. Recently, many studies have shown that virus‐induced gene silencing (VIGS) and host‐induced gene silencing (HIGS) strategies are used for functional studies of AM fungi. Here, we identify the three HOG1 (High Osmolarity Glycerol 1)‐MAPK cascade genes RiSte11, RiPbs2 and RiHog1 from Rhizophagus irregularis. The expression levels of the three HOG1‐MAPK genes are significantly increased in mycorrhizal roots of the plant Astragalus sinicus under severe drought stress. RiHog1 protein was predominantly localized in the nucleus of yeast in response to 1 M sorbitol treatment, and RiPbs2 interacts with RiSte11 or RiHog1 directly by pull‐down assay. Importantly, VIGS or HIGS of RiSte11, RiPbs2 or RiHog1 hampers arbuscule development and decreases relative water content in plants during AM symbiosis. Moreover, silencing of HOG1‐MAPK cascade genes led to the decreased expression of drought‐resistant genes (RiAQPs, RiTPSs, RiNTH1 and Ri14‐3‐3) in the AM fungal symbiont in response to drought stress. Taken together, this study demonstrates that VIGS or HIGS of AM fungal HOG1‐MAPK cascade inhibits arbuscule development and expression of AM fungal drought‐resistant genes under drought stress.

Insights on the Impact of Arbuscular Mycorrhizal Symbiosis on Eucalyptus grandis Tolerance to Drought Stress

“…The Ri14-3-3 protein in R. irregularis is essential for arbuscule formation ( 71 ). We also analyzed the expression levels of RiAQP1 , RiAQP2 , RiTPS1 , RiTPS2 , RiNTH1 , and Ri14-3-3 from R. irregularis in mycorrhizal E. grandis , which were identified previously by Wang et al ( 52 ). We observed that the transcriptional levels of RiAQP1 , RiAQP2 , RiTPS1 , RiTPS2 , RiNTH1 , and Ri14-3-3 were increased significantly under ED conditions ( Fig.…”

“…According to the released genome of E. grandis ( 48 ), plasma-membrane-intrinsic proteins ( EgPIP1 and EgPIP2 ) and tonoplast-intrinsic proteins ( EgTIP1 and EgTIP2 ) were identified using related PIP and TIP genes in other plants ( 28 , 29 ). We also identified aquaporin ( RiAQP1 , - 2 , and - 3 ), trehalose-6-phosphate synthase (TPS) ( RiTPS1 and - 2 ), neutral trehalase (NTH) ( RiNTH1 ), and Ri14-3-3 genes in R. irregularis according to a previous study ( 52 ). There were no significant differences in the expression levels between AM and NM plants under WW conditions.…”

A module centered on the transcription factor Msn2 from arbuscular mycorrhizal fungus Rhizophagus irregularis regulates drought stress tolerance in the host plant

“…STRE is a stress response element (core consensus: AGGGG or CCCCT), which can be activated by various stress factors (Ruis & Schüller, 1995;Siderius & Mager, 1997). It has been reported that the mitogen-activated protein kinase (MAPK) cascade participates in the AM fungal and host plant symbionts in responses to drought stress (Liu et al, 2015;Huang et al, 2020;Wang et al, 2023). Very recently, Wang et al (2023) identified three Hog1-MAPK cascade genes from R. irregularis, RiSte11, RiPbs2, and RiHog1, the higher expression of three Hog1-MAPK genes increased the resistance of mycorrhizal plants to drought stress.…”

“…It has been reported that the mitogen-activated protein kinase (MAPK) cascade participates in the AM fungal and host plant symbionts in responses to drought stress (Liu et al, 2015;Huang et al, 2020;Wang et al, 2023). Very recently, Wang et al (2023) identified three Hog1-MAPK cascade genes from R. irregularis, RiSte11, RiPbs2, and RiHog1, the higher expression of three Hog1-MAPK genes increased the resistance of mycorrhizal plants to drought stress. It is a proven fact that the yeast protein kinase Hog1 (high osmolarity glycerol 1) regulates many target genes through the transcriptional activators Msn2/4, Hot1, and Sko1 (Capaldi et al, 2008;Azad et al, 2014).…”

“…STRE is a stress response element (core consensus: AGGGG or CCCCT), which can be activated by various stress factors (Ruis & Schüller, 1995; Siderius & Mager, 1997). It has been reported that the mitogen‐activated protein kinase (MAPK) cascade participates in the AM fungal and host plant symbionts in responses to drought stress (Liu et al ., 2015; Huang et al ., 2020; Wang et al ., 2023). Very recently, Wang et al .…”