CONSTITUTIVE EXPRESSER OF PATHOGENESIS-RELATED GENES 5 is an RNA-binding protein controlling plant immunity via an RNA processing complex

Peng, Shun; Guo, Dongbei; Guo, Yuan; Zhao, Huixian; Mei, Jun; Han, Yanling; Guan, Rui; Wang, Tianhua; Song, Tianze; Sun, Keke; Liu, Yunhan; Ting, Mao; Chang, Huan Cheng; Xue, Jing-Shi; Cai, Yingfan; Dong, Chen; Wang, Shui

doi:10.1093/plcell/koac037

Cited by 30 publications

(23 citation statements)

References 74 publications

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“…It was reported that the Arabidopsis ORC nucleoporin Nup85 physically interacts with a key Mediator component MED18, which is required for the expression of abscisic acid- and salt stress-responsive genes [ 66 ]. Recently, the plant-specific transmembrane nucleoporin CPR5 was identified as a novel RNA-binding protein and may work in the pre-mRNA splicing and polyadenylation complex to regulate plant immune induction [ 67 ]. We showed that the NB component GBPL3 recruits chromatin modifiers, core transcription apparatus, and various TFs in vivo.…”

Section: Discussionmentioning

confidence: 99%

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

Tang

Ho²,

Kang³

et al. 2022

PLoS Biol

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The nuclear basket (NB) is an essential structure of the nuclear pore complex (NPC) and serves as a dynamic and multifunctional platform that participates in various critical nuclear processes, including cargo transport, molecular docking, and gene expression regulation. However, the underlying molecular mechanisms are not completely understood, particularly in plants. Here, we identified a guanylate-binding protein (GBP)-like GTPase (GBPL3) as a novel NPC basket component in Arabidopsis. Using fluorescence and immunoelectron microscopy, we found that GBPL3 localizes to the nuclear rim and is enriched in the nuclear pore. Proximity labeling proteomics and protein-protein interaction assays revealed that GBPL3 is predominantly distributed at the NPC basket, where it physically associates with NB nucleoporins and recruits chromatin remodelers, transcription apparatus and regulators, and the RNA splicing and processing machinery, suggesting a conserved function of the NB in transcription regulation as reported in yeasts and animals. Moreover, we found that GBPL3 physically interacts with the nucleoskeleton via disordered coiled-coil regions. Simultaneous loss of GBPL3 and 1 of the 4 Arabidopsis nucleoskeleton genes CRWNs led to distinct development- and stress-related phenotypes, ranging from seedling lethality to lesion development, and aberrant transcription of stress-related genes. Our results indicate that GBPL3 is a bona fide component of the plant NPC and physically and functionally connects the NB with the nucleoskeleton, which is required for the coordination of gene expression during plant development and stress responses.

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Section: Discussionmentioning

confidence: 99%

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

Tang

Ho²,

Kang³

et al. 2022

PLoS Biol

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“…Upon ETI, CPR5 releases SIM and SMR1, which activate E2F TFs to induce PCD [ 103 ]. Finally, CPR5 regulates alternative splicing (AS; Figure 1 L) via its RNA-binding activity [ 105 ]. Interestingly, the mRNA of the gene-silencing-related AGO1 and several AS regulators are among its targets, suggesting that apart from its own role in AS, it also indirectly affects gene silencing and AS [ 105 ].…”

Section: Regulation Of the Plant Immune Transcriptome Occurs At Multi...mentioning

confidence: 99%

“…Finally, CPR5 regulates alternative splicing (AS; Figure 1 L) via its RNA-binding activity [ 105 ]. Interestingly, the mRNA of the gene-silencing-related AGO1 and several AS regulators are among its targets, suggesting that apart from its own role in AS, it also indirectly affects gene silencing and AS [ 105 ]. In addition, Exportin-4 (XPO4) mediates nuclear export of TOPLESS-RELATED1 (TPR1), counteracting the translocation of TPR1 into the nucleus during ETI in the presence of high SA levels, as was studied in the cpr5 background [ 106 ].…”

Section: Regulation Of the Plant Immune Transcriptome Occurs At Multi...mentioning

confidence: 99%

Transcriptional regulation of plant innate immunity

Aerts

Chhillar

Ding

et al. 2022

Essays in Biochemistry

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Transcriptional reprogramming is an integral part of plant immunity. Tight regulation of the immune transcriptome is essential for a proper response of plants to different types of pathogens. Consequently, transcriptional regulators are proven targets of pathogens to enhance their virulence. The plant immune transcriptome is regulated by many different, interconnected mechanisms that can determine the rate at which genes are transcribed. These include intracellular calcium signaling, modulation of the redox state, post-translational modifications of transcriptional regulators, histone modifications, DNA methylation, modulation of RNA polymerases, alternative transcription inititation, the Mediator complex and regulation by non-coding RNAs. In addition, on their journey from transcription to translation, mRNAs are further modulated through mechanisms such as nuclear RNA retention, storage of mRNA in stress granules and P-bodies, and post-transcriptional gene silencing. In this review, we highlight the latest insights into these mechanisms. Furthermore, we discuss some emerging technologies that promise to greatly enhance our understanding of the regulation of the plant immune transcriptome in the future.

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“…Meanwhile, data from the cpr5 RNA-sequencing indicate that CPR5 participates in the regulation of alternative splicing (AS). Hence, CPR5 may act as a component of LLPS [ 68 ] which is involved in the plant immune response [ 69 ]. Collaboratively, NUP54, NUP58, NUP88, and XPO4 cooperate with CPR5 to regulate the disease resistance, highlighting that the integrity of the NPC plays pivotal roles in immune signals.…”

Section: Defensive Roles Of Npc In Plantsmentioning

confidence: 99%

Function of Nuclear Pore Complexes in Regulation of Plant Defense Signaling

Wang

Han

Guo

2022

IJMS

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In eukaryotes, the nucleus is the regulatory center of cytogenetics and metabolism, and it is critical for fundamental biological processes, including DNA replication and transcription, protein synthesis, and biological macromolecule transportation. The eukaryotic nucleus is surrounded by a lipid bilayer called the nuclear envelope (NE), which creates a microenvironment for sophisticated cellular processes. The NE is perforated by the nuclear pore complex (NPC), which is the channel for biological macromolecule bi-directional transport between the nucleus and cytoplasm. It is well known that NPC is the spatial designer of the genome and the manager of genomic function. Moreover, the NPC is considered to be a platform for the continual adaptation and evolution of eukaryotes. So far, a number of nucleoporins required for plant-defense processes have been identified. Here, we first provide an overview of NPC organization in plants, and then discuss recent findings in the plant NPC to elaborate on and dissect the distinct defensive functions of different NPC subcomponents in plant immune defense, growth and development, hormone signaling, and temperature response. Nucleoporins located in different components of NPC have their unique functions, and the link between the NPC and nucleocytoplasmic trafficking promotes crosstalk of different defense signals in plants. It is necessary to explore appropriate components of the NPC as potential targets for the breeding of high-quality and broad spectrum resistance crop varieties.

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CONSTITUTIVE EXPRESSER OF PATHOGENESIS-RELATED GENES 5 is an RNA-binding protein controlling plant immunity via an RNA processing complex

Cited by 30 publications

References 74 publications

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

Transcriptional regulation of plant innate immunity

Function of Nuclear Pore Complexes in Regulation of Plant Defense Signaling

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