Brassinosteroids Antagonize Jasmonate-Activated Plant Defense Responses through BRI1-EMS-SUPPRESSOR1 (BES1)

Plant Physiol. 2020 Feb;182(2):1066-1082. doi: 10.1104/pp.19.01220. Epub 2019 Nov 27.

Abstract

Brassinosteroids (BRs) and jasmonates (JAs) regulate plant growth, development, and defense responses, but how these phytohormones mediate the growth-defense tradeoff is unclear. Here, we identified the Arabidopsis (Arabidopsis thaliana) dwarf at early stages1 (dwe1) mutant, which exhibits enhanced expression of defensin genes PLANT DEFENSIN1.2a (PDF1.2a) and PDF1.2b The dwe1 mutant showed increased resistance to herbivory by beet armyworms (Spodoptera exigua) and infection by botrytis (Botrytis cinerea). DWE1 encodes ROTUNDIFOLIA3, a cytochrome P450 protein essential for BR biosynthesis. The JA-inducible transcription of PDF1.2a and PDF1.2b was significantly reduced in the BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 (BES1) gain-of-function mutant bes1- D, which was highly susceptible to S. exigua and B. cinerea BES1 directly targeted the terminator regions of PDF1.2a/PDF1.2b and suppressed their expression. PDF1.2a overexpression diminished the enhanced susceptibility of bes1- D to B. cinerea but did not improve resistance of bes1- D to S. exigua In response to S. exigua herbivory, BES1 inhibited biosynthesis of the JA-induced insect defense-related metabolite indolic glucosinolate by interacting with transcription factors MYB DOMAIN PROTEIN34 (MYB34), MYB51, and MYB122 and suppressing expression of genes encoding CYTOCHROME P450 FAMILY79 SUBFAMILY B POLYPEPTIDE3 (CYP79B3) and UDP-GLUCOSYL TRANSFERASE 74B1 (UGT74B1). Thus, BR contributes to the growth-defense tradeoff by suppressing expression of defensin and glucosinolate biosynthesis genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / genetics
  • Arabidopsis / immunology*
  • Arabidopsis / microbiology
  • Arabidopsis / parasitology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Botrytis / pathogenicity
  • Brassinosteroids / biosynthesis*
  • Brassinosteroids / metabolism
  • Cyclopentanes / metabolism*
  • Cyclopentanes / pharmacology
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Gene Expression Regulation, Plant / drug effects
  • Gene Expression Regulation, Plant / genetics*
  • Gene Knockout Techniques
  • Glucosinolates / biosynthesis
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Oxylipins / metabolism*
  • Oxylipins / pharmacology
  • Plant Diseases / genetics*
  • Plant Diseases / immunology
  • Plant Leaves / genetics
  • Plant Leaves / immunology
  • Plant Leaves / microbiology
  • Plant Leaves / parasitology
  • Plant Stomata / genetics
  • Plant Stomata / microbiology
  • Plant Stomata / parasitology
  • Plant Stomata / ultrastructure
  • Plants, Genetically Modified / metabolism
  • Spodoptera / pathogenicity
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • BES1 protein, Arabidopsis
  • Brassinosteroids
  • Cyclopentanes
  • DNA-Binding Proteins
  • Glucosinolates
  • MYB34 protein, Arabidopsis
  • MYB51 protein, Arabidopsis
  • Oxylipins
  • PDF1 protein, Arabidopsis
  • Transcription Factors
  • jasmonic acid
  • Cytochrome P-450 Enzyme System
  • ROT3 protein, Arabidopsis
  • cytochrome P-450 CYP79B3, Sinapis alba
  • Glucosyltransferases
  • UDP-glucose thiohydroximate S-glucosyltransferase UGT74B1, Arabidopsis

Supplementary concepts

  • Botrytis cinerea