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

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 (<i>Arabidopsis thaliana</i>) <i>dwarf at early stages1</i> (<i>dwe1</i>) mutant, which exhibits enhanced expression of defensin genes <i>PLANT DEFENSIN1.2a</i> (<i>PDF1.2a</i>) and <i>PDF1.2b</i> The <i>dwe1</i> mutant showed increased resistance to herbivory by beet armyworms (<i>Spodoptera exigua</i>) and infection by botrytis (<i>Botrytis cinerea</i>). <i>DWE1</i> encodes ROTUNDIFOLIA3, a cytochrome P450 protein essential for BR biosynthesis. The JA-inducible transcription of <i>PDF1.2a</i> and <i>PDF1.2b</i> was significantly reduced in the <i>BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1</i> (<i>BES1</i>) gain-of-function mutant <i>bes1- D</i>, which was highly susceptible to <i>S. exigua</i> and <i>B. cinerea</i> BES1 directly targeted the terminator regions of <i>PDF1.2a/PDF1.2b</i> and suppressed their expression. <i>PDF1.2a</i> overexpression diminished the enhanced susceptibility of <i>bes1- D</i> to <i>B. cinerea</i> but did not improve resistance of <i>bes1- D</i> to <i>S. exigua</i> In response to <i>S. exigua</i> 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.