Editing of the rice importin gene IMPα1b results in sequestration of TAL effectors from plant cell nuclei

Abstract

Transcription activator-like effectors (TALEs) produced by plant pathogenic bacteria mainly belonging to the genus Xanthomonas cause plant diseases through activation of host susceptibility genes in plant cell nuclei. How TALEs enter plant cell nuclei was not clear until recent studies about PthXo1 and TALI, two TALEs produced by Xanthomonas oryzae pv. oryzae (Xoo) and X. oryzae pv. oryzicola (Xoc), the rice (Oryza sativa) pathogens that cause bacterial blight and bacterial leaf streak, respectively. Here, we report that rice importin IMPα1b serves as a nuclear transport receptor in rice plants to facilitate the nuclear import of PthXo1 and TALI from Xoo and Xoc, respectively. While wild-type (WT) rice plants support the nuclear import of PthXo1 and TALI, nuclear trafficking is defective in OsIMPα1b loss-of-function mutants generated by clustered regularly interspaced short palindromic repeats (CRISPR)–CRISPR-associated 9 (Cas9)-based gene editing. In the edited plants infected by Xoo, OsIMPα1b sequesters PthXo1 from the nucleus, the PthXo1-targeted rice susceptibility gene is no longer activated, and bacterial virulence and blight disease are alleviated as a result. In the edited plants infected by Xoc, OsIMPα1b sequesters TALI from the nucleus, the role of TALI in suppressing rice defense responses is nullified, and rice defense responses are in turn activated to inhibit bacterial virulence and alleviate bacterial leaf streak severity.