Endosome-Associated CRT1 Functions Early in <i>Resistance</i> Gene–Mediated Defense Signaling in <i>Arabidopsis</i> and Tobacco

Kang, Hong Gu; Oh, Chang‐Sik; Sato, Mitsuru; Katagiri, Fumiaki; Glazebrook, Jane; Takahashi, Hideki; Kachroo, Pradeep; Martin, Gregory B.; Klessig, Daniel F.

doi:10.1105/tpc.109.071662

Cited by 56 publications

(80 citation statements)

References 113 publications

(141 reference statements)

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“…We next tested interaction of HRT with CIB1 and COP1 proteins, because both CIB1 and COP1 are known to interact with CRY2 (12,36). Consistent with earlier results (38), CRY2 interacted with COP1 in the nucleus (Fig. 4A).…”

Section: Mutation In Blue-light Photoreceptors Compromises Hrt-mediatedsupporting

confidence: 66%

Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase

Jeong

Chandra-Shekara

Barman

et al. 2010

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

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112

106

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Light harvested by plants is essential for the survival of most life forms. This light perception ability requires the activities of proteins termed photoreceptors. We report a function for photoreceptors in mediating resistance (R) protein-derived plant defense. The bluelight photoreceptors, cryptochrome (CRY) 2 and phototropin (PHOT) 2, are required for the stability of the R protein HRT, and thereby resistance to Turnip Crinkle virus (TCV). Exposure to darkness or blue-light induces degradation of CRY2, and in turn HRT, resulting in susceptibility. Overexpression of HRT can compensate for the absence of PHOT2 but not CRY2. HRT does not directly associate with either CRY2 or PHOT2 but does bind the CRY2-/PHOT2-interacting E3 ubiquitin ligase, COP1. Application of the proteasome inhibitor, MG132, prevents blue-light-dependent degradation of HRT, consequently these plants show resistance to TCV under blue-light. We propose that CRY2/PHOT2 negatively regulate the proteasomemediated degradation of HRT, likely via COP1, and blue-light relieves this repression resulting in HRT degradation.light | photoreceptors | plant defense | virus | resistance protein P lants are dependent on light for their survival. The light-absorbing ability of plants is derived from the activities of three known classes of photoreceptors. These include phytochromes (PHY) that detect light in the red/far-red (600-700 nm) range, and cryptochromes (CRY) and phototropins (PHOT) that detect light in the blue and UVA (320-500 nm) range (reviewed in refs. 1-6). Photon-absorption activates the PHY proteins from their physiologically inactive to active far-red absorbing forms. Light also modulates the phosphorylation and nucleocytoplasmic translocation of PHY proteins, which is essential for their function in mediating light-responsive physiological changes in plants. CRY photoreceptors are flavoproteins that share sequence similarity to DNA-repair enzymes called photolyases. However, CRY proteins have no DNA-repair activity (5, 7). CRY proteins were first characterized in Arabidopsis, but are also widely distributed in bacteria and eukaryotes. These proteins usually contain an amino terminal photolyase-related region and a carboxy domain of variable size. Both isoforms of CRY (CRY1 and CRY2) in Arabidopsis undergo blue-light-dependent phosphorylation (8, 9), and CRY2, but not CRY1, is degraded in response to blue light (10, 11). Both CRY1 and CRY2 interact with constitutively photomorphogenic 1 (COP1), an E3 ubiquitin ligase (12,13). It is thought that blue-light perception by CRY photoreceptors triggers the rapid inactivation of COP1 through their direct protein-protein interactions (12, 13), resulting in the abrogation of COP1-mediated degradation of the bZIP transcription factor HY5 and other COP1 substrates (14). Although CRY1 protein shuttles between the cytoplasm and nucleus, the CRY2 protein is mostly present in the nucleus (15). Because CRY2 also contributes to anion channel-mediated currents across the plasma membrane (16), it is possible ...

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Section: Mutation In Blue-light Photoreceptors Compromises Hrt-mediatedsupporting

confidence: 66%

Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase

Jeong

Chandra-Shekara

Barman

et al. 2010

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

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112

106

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“…CRT1 was subsequently shown to physically interact with HRT and ten other R proteins representing three different structural classes. This interaction appears to be dynamic as CRT1 bound inactive R proteins, but only poorly interacted with activated R proteins 13 . Analysis of the Arabidopsis genome revealed that CRT1 has two close (Z70% a.a. identity) and four distant (r50% a.a. identity) homologues.…”

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confidence: 99%

“…Cell death triggered by the R proteins ssi4 and RPS2 also was compromised by the crt1-1 mutation or silencing of CRT1 family members. Moreover, a double knockout (dKO) in the Col-0 background, crt1-2 crh1-1, which lacks CRT1 and its closest homologue, displayed compromised resistance to avirulent Pseudomonas syringae (Pst) and Hyaloperonospora arabidopsidis 13,14 . Construction of a triple KO was not possible as the CRH2 KO was lethal in the homozygous state.…”

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confidence: 99%

CRT1 is a nuclear-translocated MORC endonuclease that participates in multiple levels of plant immunity

et al. 2012

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Arabidopsis thaliana CRT1 (compromised for recognition of Turnip Crinkle Virus) was previously shown to be required for effector-triggered immunity. Sequence analyses previously revealed that CRT1 contains the ATPase and S5 domains characteristic of Microchidia (MORC) proteins; these proteins are associated with DNA modification and repair. Here we show that CRT1 and its closest homologue, CRH1, are also required for pathogen-associated molecular pattern (PAMP)-triggered immunity, basal resistance, nonhost resistance and systemic acquired resistance. Consistent with its role in PAMP-triggered immunity, CRT1 interacted with the PAMP recognition receptor FLS2. Subcellular fractionation and transmission electron microscopy detected a subpopulation of CRT1 in the nucleus, whose levels increased following PAMP treatment or infection with an avirulent pathogen. These results, combined with the demonstration that CRT1 binds DNA, exhibits endonuclease activity, and affects tolerance to the DNA-damaging agent mitomycin C, argue that this prototypic eukaryotic member of the MORC superfamily has important nuclear functions during immune response activation.

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“…1073/pnas.1406611111/-/DCSupplemental. CRH6; Defective in Meristem Silencing 11 (DMS11)], and AtMORC7 (NP_194227; AT4G24970; CRH3) (25,(29)(30)(31)(32). AtMORC1 and AtMORC2 are the most closely related homologs and share 80.9% amino acid sequence identity (29)(30)(31)(32) (Fig.…”

Section: Significancementioning

confidence: 99%

“…AtMORC6 has been identified in four independent forward genetic screens (24)(25)(26)31) as required for gene silencing and maintenance of heterochromatin integrity. AtMORC1 is also required for gene silencing (26), although it was originally described as a master regulator in plant disease resistance signaling (30)(31)(32)(33).…”

Section: Significancementioning

confidence: 99%

Transcriptional gene silencing by Arabidopsis microrchidia homologues involves the formation of heteromers

Moissiard¹,

Bischof²,

Husmann³

et al. 2014

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

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Epigenetic gene silencing is of central importance to maintain genome integrity and is mediated by an elaborate interplay between DNA methylation, histone posttranslational modifications, and chromatin remodeling complexes. DNA methylation and repressive histone marks usually correlate with transcriptionally silent heterochromatin, however there are exceptions to this relationship. In Arabidopsis, mutation of Morpheus Molecule 1 (MOM1) causes transcriptional derepression of heterochromatin independently of changes in DNA methylation. More recently, two Arabidopsis homologues of mouse microrchidia (MORC) genes have also been implicated in gene silencing and heterochromatin condensation without altering genome-wide DNA methylation patterns. In this study, we show that Arabidopsis microrchidia (AtMORC6) physically interacts with AtMORC1 and with its close homologue, AtMORC2, in two mutually exclusive protein complexes. RNA-sequencing analyses of high-order mutants indicate that AtMORC1 and AtMORC2 act redundantly to repress a common set of loci. We also examined genetic interactions between AtMORC6 and MOM1 pathways. Although AtMORC6 and MOM1 control the silencing of a very similar set of genomic loci, we observed synergistic transcriptional regulation in the mom1/atmorc6 double mutant, suggesting that these epigenetic regulators act mainly by different silencing mechanisms.epigenetics | plant biology

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Endosome-Associated CRT1 Functions Early in Resistance Gene–Mediated Defense Signaling in Arabidopsis and Tobacco

Cited by 56 publications

References 113 publications

Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase

Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase

CRT1 is a nuclear-translocated MORC endonuclease that participates in multiple levels of plant immunity

Transcriptional gene silencing by Arabidopsis microrchidia homologues involves the formation of heteromers

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