Synergy between a pectate lyase gene and two SWEET genes all targeted by the same TAL effector in susceptibility to cotton bacterial blight

Xanthomonas spp. employ transcription activator-like (TAL) effectors to promote pathogenicity by activating host susceptibility (S) genes. Cotton GhSWEET10 is an S gene targeted by a TAL effector in an early isolate of Xanthomonas citri pv. malvacearum (Xcm), but not by recent field Xcm isolates. To understand the pathogenicity shift in Xcm and its adaptation to cotton, we assembled the whole genome and the TAL effector repertoire of three recent Xcm Texas field isolates. A newly evolved TAL effector, TAL7b, activated different GhSWEET genes, GhSWEET14a and GhSWEET14b. Simultaneous activation of GhSWEET14a and GhSWEET14b resulted in pronounced water-soaked lesions. Transcriptome profiling, coupled with TAL effector-binding element prediction, identified a pectin lyase as an additional TAL7b target, quantitatively contributing to Xcm virulence alongside GhSWEET14a/b. CRISPR-Cas9-based gene editing supported the function of GhSWEETs as S genes in cotton bacterial blight and the promise of disrupting the TAL effector binding site in these genes to control the disease. Collectively, our findings elucidate the rapid evolution of TAL effectors in Xanthomonas field isolates and highlight the virulence mechanism wherein TAL effectors induce multiple S genes simultaneously to promote pathogenicity.