Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton

Abstract

ABSTRACTXanthomonasspp. employ transcription activator-like effectors (TALEs) to promote pathogenicity by activating host susceptibility (S) genes. CottonGhSWEET10is anSgene targeted by a TALE in an early isolate ofXanthomonas citripv.malvacearum(Xcm), but not by recent fieldXcmisolates. To understand the pathogenicity shift inXcmand its adaptation to cotton, we assembled the whole genome and the TALE repertoire of three recentXcmTexas field isolates. A newly evolved TALE, Tal7b, activated differentGhSWEETgenes,GhSWEET14aandGhSWEET14b. Simultaneous activation ofGhSWEET14aandGhSWEET14bresulted in pronounced water-soaked lesions. Transcriptome profiling coupled with TALE-binding element prediction identified a pectin lyase as an additional Tal7b target, quantitatively contributing toXcmvirulence alongsideGhSWEET14a/b. CRISPR-Cas9-based gene editing supported the function ofGhSWEETsasSgenes in cotton bacterial blight and the promise of disrupting the TALE-binding site in these genes to control the disease. Collectively, our findings elucidate the rapid evolution of TALEs inXanthomonasfield isolates and highlight the virulence mechanism wherein TALEs induce multipleSgenes simultaneously to promote pathogenicity.