Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms

Palma, Kristoffer; Zhao, Qingguo; Cheng, Yi-Qiang; Bi, Dongling; Monaghan, Jacqueline; Wei, Cheng; Zhang, Yuelin; Li, Xin

doi:10.1101/gad.1559607

Cited by 150 publications

(217 citation statements)

References 48 publications

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“…On the basis of studies of CDC5 homologs in other organisms, the roles of plant CDC5 in transcription have been speculated (31,32). This study provides direct evidence to support the theory that CDC5 is a positive transcription factor.…”

Section: Discussionsupporting

confidence: 64%

“…causes both immunity and pleiotropic development defects, which agrees with the crucial roles of miRNAs in regulating multiple biological processes (31,32). However, it is possible that the regulation of genes other than small RNAs by CDC5 also contributes to the observed phenotypes in cdc5-1.…”

Section: Discussionmentioning

confidence: 66%

“…In cdc5-1, a T-DNA insertion disrupts the expression of CDC5, resulting in multiple developmental defects such as smaller plant size, altered leaf shape, late flowering, and sterility (31,32). We reasoned that cdc5-1 might impair miRNA accumulation, as the alteration in miRNA levels often causes pleiotropic developmental defects (33,34).…”

Section: Cdc5 Ismentioning

confidence: 99%

“…In human and yeast, CDC5 has been shown to act as a component of spliceosome to participate in mRNA splicing (29,30). In Arabidopsis, CDC5 binds DNA and is required for development and immunity to bacteria infection (31,32). However, how CDC5 functions in Arabidopsis is unclear.…”

mentioning

confidence: 99%

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CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts

Zhang

Xie

Ren

et al. 2013

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

134

160

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CDC5 is a MYB-related protein that exists in plants, animals, and fungi. In Arabidopsis, CDC5 regulates both growth and immunity through unknown mechanisms. Here, we show that CDC5 from Arabidopsis positively regulates the accumulation of microRNAs (miRNAs), which control many biological processes including development and adaptations to environments in plants. CDC5 interacts with both the promoters of genes encoding miRNAs (MIR) and the DNA-dependent RNA polymerase II. As a consequence, lack of CDC5 reduces the occupancy of polymerase II at MIR promoters, as well as MIR promoter activities. In addition, CDC5 is associated with the DICER-LIKE1 complex, which generates miRNAs from their primary transcripts and is required for efficient miRNA production. These results suggest that CDC5 may have dual roles in miRNA biogenesis: functioning as a positive transcription factor of MIR and/or acting as a component of the DICER-LIKE1 complex to enhance primary miRNA processing.M icroRNAs (miRNAs) and small interfering RNAs (siRNAs) are ∼22-nucleotide (nt) noncoding RNAs that regulate various biological processes including development, metabolism, and immunity in plants and animals (1-3). miRNAs are generated from primary miRNA transcripts (pri-miRNAs) containing stem-loop structure, whereas siRNAs are derived from long, perfect, doublestranded RNAs (dsRNAs) (1-3). They are associated with members of the Argonaute protein family to repress gene expression at posttranscriptional and/or transcriptional levels (1-3). In addition to miRNAs, plants encode two major classes of siRNAs: siRNAs derived from repeated DNAs (ra-siRNAs) and transacting siRNAs (ta-siRNAs) (4-6).Studies in Arabidopsis have established the framework of miRNA biogenesis in plants (1-3). In Arabidopsis, pri-miRNAs are primarily transcribed by DNA-dependent RNA polymerase II (Pol II), with assistance from the mediator complex and the transcription factor Negative on TATA less2 (NOT2) (7,8). After transcription, pri-miRNAs are processed by an RNase III enzyme called DICER-LIKE1 (DCL1) to miRNA precursors and then to mature miRNAs (9, 10). The efficient processing of pri-miRNA requires SERRATE (SE; a zinc finger protein), TOUGH (an RNA-binding protein), and a dephosphorylated HYPONASTIC LEAVES1 (HYL1; a double-stranded RNA binding protein) that form a complex with DCL1 (11-18). SE and HYL1 also promote the processing accuracy of pri-miRNAs (19). Four other proteins, DAWDLE (DDL; an RNA binding protein), Cap-binding protein 20, Cap-binding protein 80, and NOT2, which are associated with the DCL1 complex (8,(20)(21)(22), also function in miRNA biogenesis. Recent studies also reveal that the correct localization of DCL1 requires NOT2 and MODIFIER OF SNC1, 2 (an RNA binding protein) (8,23). In addition, the accumulation of a subset of miRNAs requires a proline-rich protein named SICKLE (24).The cell division cycle 5 (CDC5) protein is a conserved protein in animals, plants, and fungi (25). It was first isolated from Schizosaccharomyces pombe as a cell cycle regulat...

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Section: Discussionsupporting

confidence: 64%

Section: Discussionmentioning

confidence: 66%

Section: Cdc5 Ismentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts

Zhang

Xie

Ren

et al. 2013

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

134

160

View full text Add to dashboard Cite

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“…Both MOS4 and MOS2 were identified as important positive regulators from the screens. MOS4 is a component of the nuclear spliceosome-associated MOS4-associated complex, which functions in regulating the proper splicing of R genes 7,8 . MOS2 contains one G-patch domain and two KOW motifs and is predicted to be involved in RNA processing pathways to regulate plant immunity 9 .…”

mentioning

confidence: 99%

Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity

et al. 2013

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Proteins containing nucleotide-binding and leucine-rich repeat domains (NB-LRRs) serve as immune receptors in plants and animals. Negative regulation of immunity mediated by NB-LRR proteins is crucial, as their overactivation often leads to autoimmunity. Here we describe a new mutant, snc1-enhancing (muse) forward genetic screen, targeting unknown negative regulators of NB-LRR-mediated resistance in Arabidopsis. From the screen, we identify MUSE5, which is renamed as AtPAM16 because it encodes the ortholog of yeast PAM16, part of the mitochondrial inner membrane protein import motor. Consistently, AtPAM16-GFP localizes to the mitochondrial inner membrane. AtPAM16L is a paralog of AtPAM16. Double mutant Atpam16-1 Atpam16l is lethal, indicating that AtPAM16 function is essential. Single mutant Atpam16 plants exhibit a smaller size and enhanced resistance against virulent pathogens. They also display elevated reactive oxygen species (ROS) accumulation. Therefore, AtPAM16 seems to be involved in importing a negative regulator of plant immunity into mitochondria, thus protecting plants from over-accumulation of ROS and preventing autoimmunity.

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Potato leafroll virus structural proteins manipulate overlapping, yet distinct protein interaction networks during infection

et al. 2015

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Potato leafroll virus (PLRV) produces a readthrough protein (RTP) via translational readthrough of the coat protein amber stop codon. The RTP functions as a structural component of the virion and as a nonincorporated protein in concert with numerous insect and plant proteins to regulate virus movement/transmission and tissue tropism. Affinity purification coupled to quantitative MS was used to generate protein interaction networks for a PLRV mutant that is unable to produce the read through domain (RTD) and compared to the known wild-type PLRV protein interaction network. By quantifying differences in the protein interaction networks, we identified four distinct classes of PLRV-plant interactions: those plant and nonstructural viral proteins interacting with assembled coat protein (category I); plant proteins in complex with both coat protein and RTD (category II); plant proteins in complex with the RTD (category III); and plant proteins that had higher affinity for virions lacking the RTD (category IV). Proteins identified as interacting with the RTD are potential candidates for regulating viral processes that are mediated by the RTP such as phloem retention and systemic movement and can potentially be useful targets for the development of strategies to prevent infection and/or viral transmission of Luteoviridae species that infect important crop species.

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Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms

Cited by 150 publications

References 48 publications

CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts

CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts

Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity

Potato leafroll virus structural proteins manipulate overlapping, yet distinct protein interaction networks during infection

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