Effector rewiring of host transcription

Xanthomonas XopD Effector Biology

We discovered that XopD is the only non-TAL (transcription activator-like) T3SE localized to host sub-nuclear foci that directly represses host transcription during Xe infection. XopD encodes a small ubiquitin-like modifier (SUMO) protease that suppresses ethylene (ET) and salicylic acid (SA) production to interfere with host immunity. Notably, XopD proteolysis in tomato leaves correlates with plant tolerance – the ability of the host to cope with bacterial colonization. This striking observation suggested that XopD-mediated desumoylation of host nuclear factors is critical for promoting Xe multiplication while suppressing leaf symptom development. Indeed, we demonstrated that XopD represses ET-stimulated transcription by cleaving SUMO from lysine 53 of the tomato transcription factor (TF) SlERF4. SlERF4 is required for both anti-Xe immunity and symptom development. XopD-mediated desumoylation of SlERF leads to the destabilization of SlERF4 and repression of SlERF4-mediated transcription in planta, providing mechanistic insight to how immunity is suppressed and tolerance is established. Our research also highlights that pathogen-dependent manipulation of host TFs is a key virulence strategy to dampen hormone-mediated immune signaling during infection. Our data provide the first example of mimicry of SUMO proteases by pathogenic bacteria.

Nothing is known about how plants recognize XopD and activate defense. We noticed however that XopD triggers defense responses in some Xe-tomato interactions. Given that XopD manipulates transcription, we hypothesize that host transcription triggered but not repressed by XopD may define defense pathways effective for anti-Xcv immunity. Indeed, we found a group of tomato basic helix-loop-helix (bHLH) TFs that are differentially expressed by XopD, in a SUMO protease-dependent manner. These data suggest that XopD may target one or more TF-modules that control bHLH transcription or that XopD virulence activity is guarded by a TF-module that activates bHLH transcription. Notably, we discovered that one bHLH is required for immunity and growth, and a second is required for the suppression of anti-Xe defense in tomato. We now hypothesize that Xe regulates tomato bHLH transcription circuits to dynamically alter growth and/or immunity during infection. How growth-defense tradeoffs are regulated at the molecular level is largely unknown and a central question in plant biology. Future research will focus on the role of bHLH-containing TF modules in tomato to contribute mechanistic insight to the machinery that regulates growth-defense trade-offs in important crop plants.