Research Article: An Oomycete CRN Effector Reprograms Expression of Plant HSP Genes by Targeting their Promoters

Date Published: December 29, 2015

Publisher: Public Library of Science

Author(s): Tianqiao Song, Zhenchuan Ma, Danyu Shen, Qi Li, Wanlin Li, Liming Su, Tingyue Ye, Meixiang Zhang, Yuanchao Wang, Daolong Dou, Paul Birch.


Oomycete pathogens produce a large number of CRN effectors to manipulate plant immune responses and promote infection. However, their functional mechanisms are largely unknown. Here, we identified a Phytophthora sojae CRN effector PsCRN108 which contains a putative DNA-binding helix-hairpin-helix (HhH) motif and acts in the plant cell nucleus. Silencing of the PsCRN108 gene reduced P. sojae virulence to soybean, while expression of the gene in Nicotiana benthamiana and Arabidopsis thaliana enhanced plant susceptibility to P. capsici. Moreover, PsCRN108 could inhibit expression of HSP genes in A. thaliana, N. benthamiana and soybean. Both the HhH motif and nuclear localization signal of this effector were required for its contribution to virulence and its suppression of HSP gene expression. Furthermore, we found that PsCRN108 targeted HSP promoters in an HSE- and HhH motif-dependent manner. PsCRN108 could inhibit the association of the HSE with the plant heat shock transcription factor AtHsfA1a, which initializes HSP gene expression in response to stress. Therefore, our data support a role for PsCRN108 as a nucleomodulin in down-regulating the expression of plant defense-related genes by directly targeting specific plant promoters.

Partial Text

Filamentous pathogens produce a large number of host intracellular effectors to suppress host immune responses and facilitate colonization [1–3]. In oomycete pathogens, two groups of intracellular effectors (RxLR, Arg, any amino acid, Leu, Arg; CRN, Crinkler or crinkling- and necrosis-inducing protein) have been identified [3–6]. However, their biochemical activities and molecular mechanisms are incompletely understood. By identifying host targets, some oomycete effectors have been shown to target important intracellular processes controlling disease resistance. For example, P. infestans PiAVR3a manipulates plant programmed cell death (PCD) by interacting with and stabilizing the host E3 ligase CMPG1 [7], and P. infestans PITG_03192 targets plant NAC transcriptional factors to prevent their accumulation in the host nucleus [8]. In addition, we recently found that two effectors (PsIsc1 and PsAvr3b) in P. sojae act as enzymes to suppress accumulation of the essential defense compounds salicylic acid and H2O2 [9,10].

The CRN (Crinkler) and RxLR effectors are two major groups of intracellular effector proteins produced by oomycete pathogens. CRN effectors exhibit several important features. First, they represent an ancient effector family that is widely distributed in oomycete pathogens [6], and CRN-like proteins are found even in Batrachochytrium dendrobatidis (a fungal chytrid pathogen of amphibians) [48] and arbuscular mycorrhizal fungi [49]. In contrast, RxLR effectors have been identified only in plant pathogens of the Peronosporaceae lineage [6]. Second, most CRN effectors are highly expressed. For example, ~50% of CRN-encoding genes are among the top 10% of most highly expressed genes in P. infestans [25], and the average expression levels of CRN genes in P. sojae were higher than those of RXLR genes and many housekeeping genes [24]. Third, the CRN effectors are more conserved than the RXLR effectors, and most of those characterized appear to function within the nucleus of host cells [6,22]. These features together suggest that this effector family plays important roles during pathogen—host interactions. The mechanisms by which they act are however largely unknown. Here, we have demonstrated that PsCRN108, a CRN effector from P. sojae, targets specific host promoters to manipulate plant defense responses.




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