Pathogen-Responsive MPK3 and MPK6 Reprogram the Biosynthesis of Indole Glucosinolates and Their Derivatives in Arabidopsis Immunity

Abstract

ORCID IDs: 0000-0001-6683-6415 (J.X.); 0000-0002-9910-3119 (J.M.); 0000-0002-4265-7399 (J.L.); 0000-0002-0757-5208 (Q.W.); 0000-0003-2959-6461 (S.Z.)Antimicrobial compounds have critical roles in plant immunity; for example, Arabidopsis thaliana and other crucifers deploy phytoalexins and glucosinolate derivatives in defense against pathogens. The pathogen-responsive MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3) and MPK6 have essential functions in the induction of camalexin, the major phytoalexin in Arabidopsis. In search of cyanide, a coproduct of ethylene and camalexin biosynthesis, we found that MPK3 and MPK6 also affect the accumulation of extracellular thiocyanate ion derived from the indole glucosinolate (IGS) pathway. Botrytis cinerea infection activates MPK3/MPK6, which promote indole-3-yl-methylglucosinolate (I3G) biosynthesis and its conversion to 4-methoxyindole-3-yl-methylglucosinolate (4MI3G). Gain-and loss-of-function analyses demonstrated that MPK3/MPK6 regulate the expression of MYB51 and MYB122, two key regulators of IGS biosynthesis, as well as CYP81F2 and IGMT1/ IGMT2, which encode enzymes in the conversion of I3G to 4MI3G, through ETHYLENE RESPONSE FACTOR6 (ERF6), a substrate of MPK3/MPK6. Under the action of PENETRATION2 (PEN2), an atypical myrosinase, and PEN3, an ATP binding cassette transporter, 4MI3G is converted to extracellular unstable antimicrobial compounds, possibly isothiocyanates that can react with nucleophiles and release the stable thiocyanate ion. Recent studies demonstrated the importance of PEN2/ PEN3-dependent IGS derivatives in plant immunity. Here, we report that MPK3/MPK6 and their substrate ERF6 promote the biosynthesis of IGSs and the conversion of I3G to 4MI3G, a target of PEN2/PEN3-dependent chemical defenses in plant immunity.

PP2A‐B′γ modulates foliar trans‐methylation capacity and the formation of 4‐methoxy‐indol‐3‐yl‐methyl glucosinolate in Arabidopsis leaves

“…Recently, Xu et al . () showed that infection by the necrotrophic fungal pathogen Botrytis cinerea promotes the biosynthesis of indole GSLs and their conversion to methoxylated intermediates, which are further metabolized to unstable antimicrobial compounds by PEN2. The beta‐thioglucoside glucosidases TGG1 and TGG2 have also recently been implicated in the degradation of indole GSLs and shown to attenuate cell death caused by the detrimental fungal toxin fumonisin B1 (Zhao et al ., ).…”

Phenotypic and seed structural comparison in hybrids of different Brassica rapa and B. oleracea

“…This indicates that cross between BoZ and BrK would be helpful in creating B. napus with higher glucosinolate content. As reported, the glucosinolates in Arabidopsis and Brassica crops were transported from maternal tissues (e.g., leaves; Nour‐Eldin & Halkier, ; Nour‐Eldin et al, ), and glucosinolates in leaves have been proved with functions in improving stress tolerance, insect and pathogen resistance (Davila Olivas et al, ; Mao et al, ; Xu et al, ). The linoleic acid was greatly increased in all the hybrids but in diploid parents, indicating better oil composition in resynthesized B. napus .…”

Cooperative Regulatory Functions of miR858 and MYB83 during Cyst Nematode Parasitism

“…7A). This included ERF6, ERF9, and ERF72, which play key regulatory functions in biotic stress responses (Ogawa et al, 2005;Camehl and Oelmüller, 2010;Moffat et al, 2012;Maruyama et al, 2013;Meng et al, 2013;Chen et al, 2014;Xu et al, 2016), as well as ERF109, which regulates the accumulation of reactive oxygen species following biotic and abiotic stresses stimuli (Matsuo et al, 2015). Remarkably, a substantial number of genes associated with gibberellin, jasmonic acid, and abscisic acid signal transduction networks were directly or indirectly regulated by MYB83 in the syncytium (Fig.…”