A Phytophthora effector hijacks host StKNOX3-StHUB1/2 complex to reprogram defense gene expression via histone monoubiquitination

Abstract

KNOX (KNOTTED1-like HOMEOBOX) transcription factors regulate the expression of genes involved in plant growth, development, and immunity by specifically binding to DNA elements. Previously, we found that the Phytophthora infestans RxLR effector Pi22798 targets the potato transcription factor StKNOX3 to promote colonization. We show here that StKNOX3 interacts with StHUB1 and StHUB2, two E3 ubiquitin ligases that monoubiquitinate histone 2B to form H2Bub1. StKNOX3 stabilizes StHUB1 and StHUB2 in the nucleus, and the StKNOX3-StHUB1/2 complex acts to enhance P. infestans infection. The effector Pi22798 promotes the formation of the StKNOX3-StHUB1/2 complex, facilitating the nuclear accumulation of StHUB1/2, thereby elevating H2Bub1 levels and increasing plant susceptibility. Combined ChIP-Seq and RNA-Seq analyses demonstrate that StKNOX3 modulates transcriptome reprogramming governing cell wall composition, phytohormone responses, and stress responses. StKNOX3 directly binds to the core motifs TGAC or TGTCA in promoter regions of target genes and represses the expression of multiple defense-related genes. Expression of Pi22798 results in reinforced regulation of the StKNOX3-targeted genes by affecting the binding affinity of StKNOX3 to their promoters and increasing H2Bub1 levels. Our data support a model in which the host StKNOX3-StHUB1/2 complex is hijacked by Pi22798 to induce epigenetic modifications that ultimately enhance potato susceptibility to P. infestans.