A host–pathogen interactome uncovers phytopathogenic strategies to manipulate plant ABA responses

Abstract

Summary The phytopathogen Pseudomonas syringae delivers into host cells type III secreted effectors (T3SEs) that promote virulence. One virulence mechanism employed by T3SEs is to target hormone signaling pathways to perturb hormone homeostasis. The phytohormone abscisic acid (ABA) influences interactions between various phytopathogens and their plant hosts, and has been shown to be a target of P. syringae T3SEs. In order to provide insight into how T3SEs manipulate ABA responses, we generated an ABA‐T3SE interactome network (ATIN) between P. syringae T3SEs and Arabidopsis proteins encoded by ABA‐regulated genes. ATIN consists of 476 yeast‐two‐hybrid interactions between 97 Arabidopsis ABA‐regulated proteins and 56 T3SEs from four pathovars of P. syringae. We demonstrate that T3SE interacting proteins are significantly enriched for proteins associated with transcription. In particular, the ETHYLENE RESPONSIVE FACTOR (ERF) family of transcription factors is highly represented. We show that ERF105 and ERF8 displayed a role in defense against P. syringae, supporting our overall observation that T3SEs of ATIN converge on proteins that influence plant immunity. In addition, we demonstrate that T3SEs that interact with a large number of ABA‐regulated proteins can influence ABA responses. One of these T3SEs, HopF3Pph6, inhibits the function of ERF8, which influences both ABA‐responses and plant immunity. These results provide a potential mechanism for how HopF3Pph6 manipulates ABA‐responses to promote P. syringae virulence, and also demonstrate the utility of ATIN as a resource to study the ABA‐T3SE interface.

Characterisation of the ERF102 to ERF105 genes of Arabidopsis thaliana and their role in the response to cold stress

“…Previously, we identified four phylogenetically closely related ERF genes with similar transcriptional responses to cytokinin (Brenner et al 2005). These genes, ERF102 (AT5G47230; known as ERF5), ERF103 (AT4G17490; identical to ERF6), ERF104 (AT5G61600) and ERF105 (AT5G51190) are members of group IXb of the ERF family (Nakano et al 2006).…”

“…ERF103, ERF104 and ERF105 are involved in the fast retrograde signalling response and the acclimation response to high light (Moore et al 2014a, b;Vogel et al 2014). Further studies have shown that ERF102 to ERF105 play a role in plant immunity (Bethke et al 2009;Moffat et al 2012;Son et al 2012;Mase et al 2013;Meng et al 2013;Cao et al 2019). Thus, ERF102 to ERF105 match the profile of other ERF transcription factors designated as a regulatory hub integrating hormone signalling in the plant response to abiotic stresses (Müller and Munné-Bosch 2015).…”

Characterisation of the ERF102 to ERF105 genes of Arabidopsis thaliana and their role in the response to cold stress

“…ERF103 , ERF104 and ERF105 are involved in the fast retrograde signalling response and the acclimation response to high light (Moore, Vogel & Dietz, 2014; Vogel et al ., 2014). Further studies have shown that ERF102 to ERF105 play a role in plant immunity (Bethke et al ., 2009; Cao et al ., 2019; Mase et al ., 2013; Meng et al ., 2013; Moffat et al ., 2012; Son et al ., 2012). Thus, ERF102 to ERF105 match the profile of other ERF transcription factors designated as a regulatory hub integrating hormone signalling in the plant response to abiotic stresses (Müller & Munné-Bosch, 2015).…”

Abscisic Acid Connects Phytohormone Signaling with RNA Metabolic Pathways and Promotes an Antiviral Response that Is Evaded by a Self-Controlled RNA Virus

“…In N. benthamiana compared with mock-treated or PPV-infected plants, P1Pro infection triggered HR that was accompanied by enhanced accumulation of the OZF1 homolog NbOZF1 and ABA ( p < 0.01; Figure 3A ). In A. thaliana , expression of the OZF1 zinc finger protein gene is activated by ABA in vegetative tissues ( Lee et al, 2012 ), and its protein was recently shown to be a preferential target of multiple secreted effectors from Pseudomonas syringae ( Cao et al, 2019 ). We asked whether the truncated P1 version encoded by the P1Pro clone and lacking the N-terminal autoinhibitory domain was sufficient to activate effector-triggered immunity (ETI), thereby causing HR.…”

“…The P1Pro infections showed HR accompanied by an increase in ABA levels and the expression of OZF1 , which encodes an ABA-responsive transcription factor thought to participate in PTI/ETI ( Lee et al, 2012 ; Cao et al, 2019 ). How can P1Pro infection trigger ABA-dependent responses?…”