Novel stripe rust effector boosts the transcription of a host susceptibility factor through affecting histone modification to promote infection in wheat

Abstract

Summary Regulation of host gene expression to promote disease is a common strategy for plant pathogens. However, it remains unclear whether or not fungal pathogens manipulate host gene expression directly through secreted effectors with transcriptional activity. Here, we identified a fungal effector PstGTA1 from Puccinia striiformis f. sp. tritici (Pst), which has partial homology to the subunit of global transcriptional activator SNF2 from oyster. The transcriptional activating activity of PstGTA1 was validated in yeast, and the potential role of PstGTA1 in pathogenicity was assessed using gene silenced and overexpression transgenic wheat plants. Candidate targets regulated by PstGTA1 were screened by transcriptomic analysis, and the specific promoter region binding to PstGTA1 was further determined. PstGTA1 can be delivered to the wheat cell nucleus and contributes to the full virulence of Pst by targeting the promoter of TaSIG, a gene negatively regulating wheat immunity, and possibly activates its transcription by affecting the histone H3K4 acetylation level. Our study provides the first direct evidence for a fungal effector with transactivation activity modulating the transcription of a host specific susceptibility gene through promoter binding and histone acetylation.

Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility

“…The Pst effector PstGSRE1 is rich in glycine and serine and regulates host gene transcription by stopping transcription factor TaLOL2 from entering into the nucleus [ 27 ]. The nuclear localized effectors Pst_A23 and PstGTA regulate host gene expression via post-transcription modification, by modulating host pre-mRNA alternative splicing or the H3K4 acetylation level of TaSIG to promote fungal infection [ 12 , 30 ]. Pst18363 and Pst27791 enhance the activity of the negative immune regulatory factor Nudix hydrolase23 (TaNUDX23) and the stability of TaRaf46, while PsSpg1 inhibits host disease resistance by increasing the kinase activity of the susceptible gene TaPsIPK1 [ 31 , 44 , 45 ].…”

“…Pst_A23 enters the wheat splicesome to directly bind the splicing sites of wheat pre-mRNAs and reprogram wheat pre-mRNA alternative splicing [ 12 ]. PstGTA1 can locate in the wheat cell nucleus, which binds to the promoter region of the wheat susceptibility gene TaSIG to activate its transcription by regulating the acetylation level of H3K4 [ 30 ]. The unconventional effector PsSpg1 enhances the phosphorylation of the wheat susceptibility gene TaPsIPK1 to promote the nuclear entrance of TaPsIPK1, where it modulates the transcription activity of TaCBF1 and promotes wheat susceptibility [ 31 ].…”