RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity

Abstract

An emerging area in plant research focuses on antagonism between regulatory systems governing growth and immunity. Such cross talk represents a point of vulnerability for pathogens to exploit. AVR2, an RXLR effector secreted by the potato blight pathogen Phytophthora infestans, interacts with potato BSL1, a putative phosphatase implicated in growthpromoting brassinosteroid (BR) hormone signaling. Transgenic potato (Solanum tuberosum) plants expressing the effector exhibit transcriptional and phenotypic hallmarks of overactive BR signaling and show enhanced susceptibility to P. infestans. Microarray analysis was used to identify a set of BR-responsive marker genes in potato, all of which are constitutively expressed to BR-induced levels in AVR2 transgenic lines. One of these genes was a bHLH transcription factor, designated StCHL1, homologous to AtCIB1 and AtHBI1, which are known to facilitate antagonism between BR and immune responses. Transient expression of either AVR2 or CHL1 enhanced leaf colonization by P. infestans and compromised immune cell death activated by perception of the elicitin Infestin1 (INF1). Knockdown of CHL1 transcript using Virus-Induced Gene Silencing (VIGS) reduced colonization of P. infestans on Nicotiana benthamiana. Moreover, the ability of AVR2 to suppress INF1-triggered cell death was attenuated in NbCHL1-silenced plants, indicating that NbCHL1 was important for this effector activity. Thus, AVR2 exploits cross talk between BR signaling and innate immunity in Solanum species, representing a novel, indirect mode of innate immune suppression by a filamentous pathogen effector.

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“…For example, effectors can represses host transcription of the flagellin receptor FLS2 (Han et al, 2014) or target MAMP-induced proteins/ signals (Shan et al, 2008). The pathogenic bacteria Pseudomonas syringae produces at least three effectors that activate JA signaling (Cui et al, 2010;Jiang et al, 2013;Gimenez-Ibanez et al, 2014;Zhou et al, 2015), whereas Hyaloperonospora arabidopsidis use effectors to shift the balance from SA signaling to ET/JA signaling (Caillaud et al, 2013), and Phytophthora infestans use effectors to induce brassinosteroid signaling (Turnbull et al, 2017). With respect to nutrient transport, certain pathogens have evolved effector proteins that can alter either gene expression or transporter function Cox et al, 2017).…”

Plasmopara viticola effector PvRXLR131 suppresses plant immunity by targeting plant receptor‐like kinase inhibitor BKI1

“…Suppression of plant innate immunity is thought to be the primary function of most pathogen effectors, including RXLR effectors (Anderson et al ., ). In some cases, ectopic expression of an effector results in an increased susceptibility to pathogens (Anderson et al ., ; Li et al ., ; Turnbull et al ., ). For example, Fabro et al .…”

“…BR activates the expression of several immunity‐related genes and triggers defence responses against diverse pathogens in plant (Divi et al ., ; Nakashita et al ., ). On the other hand, BR signalling also negatively regulates disease resistance (Turnbull et al ., ; De Vleeschauwer et al ., ). A recent study revealed that treatment of grapevine leaves with BL significantly reduced the development of P. viticola sporangiophores, suggesting that grapevine BR signalling positively regulates disease resistance against P. viticola (Liu et al ., ).…”

“…The Phytophthora parasitica effector PSE1 interferes with plant auxin accumulation to promote infection (Evangelisti et al ., ). The P. infestans effector Avr2 up‐regulates a brassinosteroid (BR)‐responsive bHLH transcription factor through antagonistic crosstalk between BR signalling and innate immunity to suppress immunity indirectly (Turnbull et al ., ).…”

An unreported NB‐LRR protein SUT1 is required for the autoimmune response mediated by type one protein phosphatase 4 mutation (topp4‐1) in Arabidopsis

“…At the same time, it is involved in temperature‐dependent and R protein CHS3‐mediated defense responses in Arabidopsis (Liu et al ., ). In addition, recent research has shown that potato phosphatase BSL1 is implicated in growth‐promoting BR hormone signaling and the AVR 2 effector recognition, which is monitored by the host resistance protein R2 in plant immunity (Saunders et al ., ; Turnbull et al ., ). To sum up, PP1 likely plays multiple functions in plant development and defense responses.…”