Phytotoxicity and Innate Immune Responses Induced by Nep1-Like Proteins

Qutob, Dinah; Kemmerling, Birgit; Brunner, Frédéric; Küfner, Isabell; Engelhardt, Stefan; Gust, Andrea A.; Luberacki, Borries; Seitz, Hanns Ulrich; Stahl, Dietmar J.; Rauhut, Thomas; Glawischnig, Erich; Schween, Gabriele; Lacombe, Benoı̂t; Watanabe, Naohide; Lam, Eric; Schlichting, Rita; Scheel, Dierk; Nau, Katja; Dodt, Gabriele; Hubert, David A.; Gijzen, Mark; Nürnberger, Thorsten

doi:10.1105/tpc.106.044180

Cited by 305 publications

(332 citation statements)

References 96 publications

(189 reference statements)

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“…S3C). Another of the top genes (At1g61420) has been implicated in Arabidopsis innate immunity (Qutob et al, 2006), consistent with a function in stress response similar to RCD1 and SRO1.…”

Section: Rcd1mentioning

confidence: 92%

The Paralogous GenesRADICAL-INDUCED CELL DEATH1andSIMILAR TO RCD ONE1Have Partially Redundant Functions during Arabidopsis Development

2009

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RADICAL-INDUCED CELL DEATH1 (RCD1) and SIMILAR TO RCD ONE1 (SRO1) are the only two proteins encoded in the Arabidopsis (Arabidopsis thaliana) genome containing both a putative poly(ADP-ribose) polymerase catalytic domain and a WWE protein-protein interaction domain, although similar proteins have been found in other eukaryotes. Poly(ADP-ribose) polymerases mediate the attachment of ADP-ribose units from donor NAD + molecules to target proteins and have been implicated in a number of processes, including DNA repair, apoptosis, transcription, and chromatin remodeling. We have isolated mutants in both RCD1 and SRO1, rcd1-3 and sro1-1, respectively. rcd1-3 plants display phenotypic defects as reported for previously isolated alleles, most notably reduced stature. In addition, rcd1-3 mutants display a number of additional developmental defects in root architecture and maintenance of reproductive development. While single mutant sro1-1 plants are relatively normal, loss of a single dose of SRO1 in the rcd1-3 background increases the severity of several developmental defects, implying that these genes do share some functions. However, rcd1-3 and sro1-1 mutants behave differently in several developmental events and abiotic stress responses, suggesting that they also have distinct functions. Remarkably, rcd1-3; sro1-1 double mutants display severe defects in embryogenesis and postembryonic development. This study shows that RCD1 and SRO1 are at least partially redundant and that they are essential genes for plant development.

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“…S3C). Another of the top genes (At1g61420) has been implicated in Arabidopsis innate immunity (Qutob et al, 2006), consistent with a function in stress response similar to RCD1 and SRO1.…”

Section: Rcd1mentioning

confidence: 92%

The Paralogous GenesRADICAL-INDUCED CELL DEATH1andSIMILAR TO RCD ONE1Have Partially Redundant Functions during Arabidopsis Development

2009

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“…Considering its expression patterns during infection, we suggest that PsCRN63-induced PCD by association with CATs may contribute to a hemibiotrophic lifestyle. By contrast, PsCRN115 also exhibits the ability to suppress PCD induced by P. sojae necrosis-inducing protein (Liu et al, 2011), which transcribes during the transition from biotrophy to necrotrophy and is highly expressed during late stages of a compatible interaction (Qutob et al, 2006). Silencing of CAT genes in N. benthamiana compromises the PCD-suppressing activity of PsCRN115, suggesting that catalases are required for the biological function of PsCRN115 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Two Cytoplasmic Effectors of Phytophthora sojae Regulate Plant Cell Death via Interactions with Plant Catalases

et al. 2014

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Plant pathogenic oomycetes, such as Phytophthora sojae, secrete an arsenal of host cytoplasmic effectors to promote infection. We have shown previously that P. sojae PsCRN63 (for crinkling- and necrosis-inducing proteins) induces programmed cell death (PCD) while PsCRN115 blocks PCD in planta; however, they are jointly required for full pathogenesis. Here, we find that PsCRN63 alone or PsCRN63 and PsCRN115 together might suppress the immune responses of Nicotiana benthamiana and demonstrate that these two cytoplasmic effectors interact with catalases from N. benthamiana and soybean (Glycine max). Transient expression of PsCRN63 increases hydrogen peroxide (H2O2) accumulation, whereas PsCRN115 suppresses this process. Transient overexpression of NbCAT1 (for N. benthamiana CATALASE1) or GmCAT1 specifically alleviates PsCRN63-induced PCD. Suppression of the PsCRN63-induced PCD by PsCRN115 is compromised when catalases are silenced in N. benthamiana. Interestingly, the NbCAT1 is recruited into the plant nucleus in the presence of PsCRN63 or PsCRN115; NbCAT1 and GmCAT1 are destabilized when PsCRN63 is coexpressed, and PsCRN115 inhibits the processes. Thus, PsCRN63/115 manipulates plant PCD through interfering with catalases and perturbing H2O2 homeostasis. Furthermore, silencing of catalase genes enhances susceptibility to Phytophthora capsici, indicating that catalases are essential for plant resistance. Taken together, we suggest that P. sojae secretes these two effectors to regulate plant PCD and H2O2 homeostasis through direct interaction with catalases and, therefore, overcome host immune responses.

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“…In Cladosporium fulvum, the causal agent of leaf mold of tomato, implicated in suppression of chitin-triggered plant immunity (35). Second, there is an example of a necrosis-inducing protein or (Nep1)-like protein (NLP) that is a candidate fungi-to-oomycete HGT (36). Infiltration of NPP1 protein into leaves of Arabidopsis thaliana results in transcript accumulation of plant defense-related genes, production of reactive oxygen species and ethylene, callose apposition, and localized cell death (36).…”

Section: Distribution Of Hgts Relative To Evolution Of Parasitic Traimentioning

confidence: 99%

Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes

Richards

Soanes

Jones

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

227

196

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Horizontal gene transfer (HGT) can radically alter the genomes of microorganisms, providing the capacity to adapt to new lifestyles, environments, and hosts. However, the extent of HGT between eukaryotes is unclear. Using whole-genome, gene-by-gene phylogenetic analysis we demonstrate an extensive pattern of cross-kingdom HGT between fungi and oomycetes. Comparative genomics, including the de novo genome sequence of Hyphochytrium catenoides , a free-living sister of the oomycetes, shows that these transfers largely converge within the radiation of oomycetes that colonize plant tissues. The repertoire of HGTs includes a large number of putatively secreted proteins; for example, 7.6% of the secreted proteome of the sudden oak death parasite Phytophthora ramorum has been acquired from fungi by HGT. Transfers include gene products with the capacity to break down plant cell walls and acquire sugars, nucleic acids, nitrogen, and phosphate sources from the environment. Predicted HGTs also include proteins implicated in resisting plant defense mechanisms and effector proteins for attacking plant cells. These data are consistent with the hypothesis that some oomycetes became successful plant parasites by multiple acquisitions of genes from fungi.

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Phytotoxicity and Innate Immune Responses Induced by Nep1-Like Proteins

Cited by 305 publications

References 96 publications

The Paralogous GenesRADICAL-INDUCED CELL DEATH1andSIMILAR TO RCD ONE1Have Partially Redundant Functions during Arabidopsis Development

The Paralogous GenesRADICAL-INDUCED CELL DEATH1andSIMILAR TO RCD ONE1Have Partially Redundant Functions during Arabidopsis Development

Two Cytoplasmic Effectors of Phytophthora sojae Regulate Plant Cell Death via Interactions with Plant Catalases

Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes

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