Xanthomonas oryzaepv.oryzaetype-III effector TAL9b targets a broadly conserved disease susceptibility locus to promote pathogenesis in rice

Abstract

Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial blight of rice, translocates multiple Transcription Activator-Like Effectors (TALEs) into rice cells. The TALEs localize to the host cell nucleus, where they bind to the DNA in a sequence-specific manner and enhance gene expression to promote disease susceptibility. Xoo strain PXO99A encodes nineteen TALEs, but the host targets of all these TALEs have not been defined. A meta-analysis of rice transcriptome profiles revealed a gene annotated as flavonol synthase/flavanone-3 hydroxylase (henceforth OsS5H/FNS-03g) to be highly induced upon Xoo infection. Further analyses revealed that this gene is induced by PXO99A using TAL9b, a broadly conserved TALE of Xoo. Disruption of tal9b rendered PXO99A less virulent. OsS5H/FNS-03g functionally complemented its Arabidopsis homologue AtDMR6, a well-studied disease susceptibility locus. Biochemical analyses suggested that OsS5H/FNS-03g is a bifunctional protein with Salicylic Acid-5 Hydroxylase (S5H) and Flavone Synthase-I (FNS-I) activities. Further, an exogenous application of apigenin on rice leaves, the flavone that is enzymatically produced by OsS5H/FNS-03g, promoted virulence of PXO99A tal9b-. Overall, our study suggests that OsS5H/FNS-03g is a bifunctional enzyme and its product apigenin is potentially involved in promoting Xoo virulence.