Phytophthora pathogens secrete a large arsenal of effectors that manipulate host processes to create an environment conducive to pathogen colonization. However, the underlying mechanisms by which Phytophthora effectors manipulate host plant cells still remain largely unclear. In this study, we report that PcAvr3a12, a Phytophthora capsici RXLR effector and a member of the Avr3a effector family, suppresses plant immunity by targeting and inhibiting host plant peptidyl-prolyl cis-trans isomerase (PPIase). Overexpression of PcAvr3a12 in Arabidopsis thaliana enhanced plant susceptibility to P. capsici. FKBP15-2, an endoplasmic reticulum (ER)-localized protein, was identified as a host target of PcAvr3a12 during early P. capsici infection. Analyses of A. thaliana T-DNA insertion mutant (fkbp15-2), RNAi, and overexpression lines consistently showed that FKBP15-2 positively regulates plant immunity in response to Phytophthora infection. FKBP15-2 possesses PPIase activity essential for its contribution to immunity but is directly suppressed by PcAvr3a12. Interestingly, we found that FKBP15-2 is involved in ER stress sensing and is required for ER stress-mediated plant immunity. Taken together, these results suggest that P. capsici deploys an RXLR effector, PcAvr3a12, to facilitate infection by targeting and suppressing a novel ER-localized PPIase, FKBP15-2, which is required for ER stress-mediated plant immunity.
Along with the well-studied microRNA (miRNA) and small interfering RNA (siRNA) is a new class of transfer RNA-derived small RNA (tsRNA), which has recently been detected in multiple organisms and is implicated in gene regulation. However, while miRNAs and siRNAs are known to repress gene expression through sequence-specific RNA cleavage or translational repression, how tsRNAs regulate gene expression remains unclear. Here we report the identification and functional characterization of tsRNAs in the oomycete pathogen Phytophthora sojae. We show that multiple tRNAs are processed into abundant tsRNAs, which accumulate in a similar developmental stage-specific manner and are negatively correlated with the expression of predicted target genes. Degradome sequencing and 5′ RLM RACE experiments indicate tsRNAs can trigger degradation of target transcripts. Transient expression assays using GUS sensor constructs confirmed the requirement of sequence complementarity in tsRNA-mediated RNA degradation in P. sojae. Our results show that the tsRNA are a class of functional endogenous sRNAs and suggest that tsRNA regulate gene expression through inducing sequence-specific degradation of target RNAs in oomycetes.
Summary
RXLR effectors encoded by
Phytophthora
species play a central role in pathogen–plant interactions. An understanding of the biological functions of RXLR effectors is conducive to the illumination of the pathogenic mechanisms and the development of disease control strategies. However, the virulence function of
Phytophthora parasitica
RXLR effectors is poorly understood. Here, we describe the identification of a
P. parasitica
RXLR effector gene,
PPTG00121
(
PpE4
), which is highly transcribed during the early stages of infection. Live cell imaging of
P. parasitica
transformants expressing a full‐length PpE4 (E4FL)‐mCherry protein indicated that PpE4 is secreted and accumulates around haustoria during plant infection. Silencing of
PpE4
in
P. parasitica
resulted in significantly reduced virulence on
Nicotiana benthamiana
. Transient expression of
PpE4
in
N. benthamiana
in turn restored the pathogenicity of the
PpE4
‐silenced lines. Furthermore, the expression of
PpE4
in both
N. benthamiana
and
Arabidopsis thaliana
consistently enhanced plant susceptibility to
P. parasitica
. These results indicate that
PpE4
contributes to pathogen infection. Finally, heterologous expression experiments showed that
PpE4
triggers non‐specific cell death in a variety of plants, including tobacco, tomato, potato and
A. thaliana
. Virus‐induced gene silencing assays revealed that
PpE4
‐induced cell death is dependent on
HSP90
,
NPK
and
SGT1
, suggesting that PpE4 is recognized by the plant immune system. In conclusion, PpE4 is an important virulence RXLR effector of
P. parasitica
and recognized by a wide range of host plants.
Summary
Oomycete pathogens secrete numerous effectors to manipulate host immunity. While some effectors share a conserved structural fold, it remains unclear if any have conserved host targets. Avr3a‐like family effectors, which are related to Phytophthora infestans effector PiAvr3a and are widely distributed across diverse clades of Phytophthora species, were used to study this question.
By using yeast‐two‐hybrid, bimolecular fluorescence complementation and co‐immunoprecipitation assays, we identified members of the plant cinnamyl alcohol dehydrogenase 7 (CAD7) subfamily as targets of multiple Avr3a‐like effectors from Phytophthora pathogens.
The CAD7 subfamily has expanded in plant genomes but lost the lignin biosynthetic activity of canonical CAD subfamilies. In turn, we identified CAD7s as negative regulators of plant immunity that are induced by Phytophthora infection. Moreover, AtCAD7 was stabilized by Avr3a‐like effectors and involved in suppression of pathogen‐associated molecular pattern‐triggered immunity, including callose deposition, reactive oxygen species burst and WRKY33 expression.
Our results reveal CAD7 subfamily proteins as negative regulators of plant immunity that are exploited by multiple Avr3a‐like effectors to promote infection in different host plants.
Plant NDR1/HIN1-like (NHL) genes play an important role in triggering plant defenses in response to biotic stresses. In this study, we performed a genome-wide identification of the NHL genes in pepper (Capsicum annuum L.) and characterized the functional roles of these CaNHL genes in response to abiotic stresses and infection by different pathogens. Phylogenetic analysis revealed that CaNHLs can be classified into five distinct subgroups, with each group containing generic and specific motifs. Regulatory element analysis showed that the majority of the promoter regions of the identified CaNHLs contain jasmonic acid (JA)-responsive and salicylic acid (SA)-responsive elements, and transcriptomic analysis revealed that CaNHL genes are expressed in all the examined tissues of pepper. The CaNHL1, CaNHL4, CaNHL6, CaNHL10, CaNHL11, and CaNHL12 genes were significantly upregulated under abiotic stress as well as in response to different pathogens, such as TMV, Phytophthora capsici and Pseudomonas syringae. In addition, we found that CaNHL4 localizes to the plasma membrane. CaNHL4-silenced pepper plants display significantly increased susceptibility to TMV, Phytophthora capsici and Pseudomonas syringae, exhibiting reduced expression of JA-related and SA-related genes and reduced ROS production. However, transient overexpression of CaNHL4 in pepper increases the expression of JArelated and SA-related genes, enhances the accumulation of ROS, and inhibits the infection of these three pathogens. Collectively, for the first time, we identified the NHL genes in pepper and demonstrated that CaNHL4 is involved in the production of ROS and that it also regulates the expression of JA-related and SA-related genes in response to different pathogens, suggesting that members of the CaNHL family play an essential role in the disease resistance of pepper.
At present, the management of Phytophthora capsici (P. capsici) mainly relies on chemical pesticides. However, along with the resistance generated by P. capsici to these chemical pesticides, the toxicity and non-degradability of this chemical molecule may also cause serious environmental problems. Herein, a new bio-based nano-antifungal material (CNC@CTAB) was made with coating hexadecyl trimethyl ammonium bromide (CTAB) on the surface of a cellulose nanocrystal (CNC). This material was then applied to the prevention of P. capcisi. This particle was facilely fabricated by mixing CTAB and sulfuric group modified CNC in an aqueous solvent. Compared to pure CTAB, the enrichment of CTAB on the CNC surface showed a better anti-oomycete activity both in vitro and in vivo. When CNC@CTAB was applied on P. capsici in vitro, the inhibition rate reached as high as 100%, while on the pepper leaf, the particle could also efficiently prevent the infection of P. capsici, and achieve a disease index as low as zero Thus, considering the high safety of CNC@CTAB in agricultural applications, and its high anti-oomycete activity against P. capsici, we believe that this CNC@CTAB has great application potential as a new green nano-fungicide in P. capsici management during the production of peppers or other vegetables.
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