BIG regulates stomatal immunity and jasmonate production in Arabidopsis

Abstract

Plants have evolved an array of responses that provide them with protection from attack by microorganisms and other predators. Many of these mechanisms depend upon interactions between the plant hormones jasmonate (JA) and ethylene (ET). However, the molecular basis of these interactions is insufficiently understood.Gene expression and physiological assays with mutants were performed to investigate the role of Arabidopsis BIG gene in stress responses.BIG transcription is downregulated by methyl JA (MeJA), necrotrophic infection or mechanical injury. BIG deficiency promotes JA-dependent gene induction, increases JA production but restricts the accumulation of both ET and salicylic acid. JA-induced anthocyanin accumulation and chlorophyll degradation are enhanced and stomatal immunity is impaired by BIG disruption. Bacteria-and lipopolysaccaride (LPS)-induced stomatal closure is reduced in BIG gene mutants, which are hyper-susceptible to microbial pathogens with different lifestyles, but these mutants are less attractive to phytophagous insects.Our results indicate that BIG negatively and positively regulate the MYC2 and ERF1 arms of the JA signalling pathway. BIG warrants recognition as a new and distinct regulator that regulates JA responses, the synergistic interactions of JA and ET, and other hormonal interactions that reconcile the growth and defense dilemma in Arabidopsis.

Involvement of Arabidopsis BIG protein in cell death mediated by Myo-inositol homeostasis

“…In the somi2 background, 76% of the DEGs displayed an increased expression compared to the wild type. As expected from previous characterization of big alleles 27 , genes involved in JA biosynthesis and signalling pathway, as respectively LOX2, JAZ1, JAZ5, JAZ7 and JAZ10 or in ethylene response were up-regulated. More generally, GO analysis of these genes showed a significant enrichment in response to stimulus, immune and defence response, anthocyanin production, response to ethylene, wounding and JA stimulus (Fig.…”

“…3b) which is consistent with the reported function of BIG in auxin signalling response 32 . Likewise, as described previously by 27 , ethylene biosynthesis genes (i.e. ACS5, ACS8, ACO3) displayed much lower expression levels in somi2 mutants than in the WT.…”

“…How BIG can control PCD mediated by the MIPS1 pathway is difficult to decipher because the molecular function of BIG is still unknown. Indeed, the BIG gene encodes a 5078-aa protein with several functional domains and has been implicated in numerous hormonal and light pathways [19][20][21]25,27,32,36 . One hypothesis could have been that the MI content was restored in the mips1 somi2 double mutant.…”

“…All these functions are in agreement with our results of transcriptome analysis showing an under-expression of genes involved in responses to auxin and auxin transport in somi2 background. According to 27 , the negative consequence on auxin transport broadly observed in big mutants, can be brought by the JA pathway, as JA negatively restrain the turnover and the intracellular trafficking of PIN proteins and thus the auxin transport 37,38 . Although no modification of global auxin content in somi2 background compared to WT plant has been detected, one can hypothesize that a local deregulation of auxin homeostasis or distribution can maybe suppress local cell death, as it has been recently demonstrated that DNA damage-triggered cell death in root stem cell could be largely inhibited by low levels of auxin 39 .…”

“…BIG has been also described for its involvement in the circadian clock control 25 and in elevated CO 2 -induced stomatal closure 26 . Recently 27 , demonstrated that BIG represents a new regulator of the Jasmonic Acid (JA) pathway and a point of convergence for the interactions of JA and others hormones. BIG deficiency promotes JA-dependent gene induction, increased JA production but restricts the accumulation of SA.…”