Dataset Information

The chromatin-remodeling protein BAF60/SWP73A regulates the plant immune receptor NLRs.

ABSTRACT: In both plant and animal innate immune responses, surveillance of pathogen infection is mediated by membrane-associated receptors and intracellular nucleotide-binding domain and leucine-rich-repeat receptors (NLRs). Homeostasis of NLRs is under tight multilayered regulation to avoid over-accumulation or over-activation, which often leads to autoimmune responses that have detrimental effects on growth and development. How NLRs are regulated epigenetically at the chromatin level remains unclear. Here, we report that SWP73A, an ortholog of the mammalian switch/sucrose nonfermentable (SWI/SNF) chromatin-remodeling protein BAF60, suppresses the expression of NLRs either directly by binding to the NLR promoters or indirectly by affecting the alternative splicing of some NLRs through the suppression of cell division cycle 5 (CDC5), a key regulator of RNA splicing. Upon infection, bacteria-induced small RNAs silence SWP73A to activate a group of NLRs and trigger robust immune responses. SWP73A may function as a H3K9me2 reader to enhance transcription suppression.

SUBMITTER: Huang CY

PROVIDER: S-EPMC7987208 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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The chromatin-remodeling protein BAF60/SWP73A regulates the plant immune receptor NLRs.

Huang Chien-Yu CY Rangel Diana Sánchez DS Qin Xiaobo X Bui Christine C Li Ruidong R Jia Zhenyu Z Cui Xinping X Jin Hailing H

Cell host & microbe 20210205 3

In both plant and animal innate immune responses, surveillance of pathogen infection is mediated by membrane-associated receptors and intracellular nucleotide-binding domain and leucine-rich-repeat receptors (NLRs). Homeostasis of NLRs is under tight multilayered regulation to avoid over-accumulation or over-activation, which often leads to autoimmune responses that have detrimental effects on growth and development. How NLRs are regulated epigenetically at the chromatin level remains unclear. H ...[more]

PMID: 33548199

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Project description:Nitrate is the main source of nitrogen for plants and an essential component of fertilizers. Rapid transcriptional activation of genes encoding the high-affinity nitrate transport system (HATS) is an important strategy that plants use to cope with nitrogen deficiency. However, the specific transcriptional machineries involved in this process and the detailed transcriptional regulatory mechanism of the core HATS remain poorly understood. ZmCHB101 is the core subunit of the SWI/SNF-type ATP-dependent chromatin remodeling complex in maize. RNA-interference transgenic plants (ZmCHB101-RNAi) display abaxially curling leaves and impaired tassel and cob development. Here, we demonstrate that ZmCHB101 plays a pivotal regulatory role in nitrate-responsive gene expression. ZmCHB101-RNAi lines showed accelerated root growth and increased biomass under low nitrate conditions. An RNA sequencing analysis revealed that ZmCHB101 regulates the expression of genes involved in nitrate transport, including ZmNRT2.1 and ZmNRT2.2. The NIN-like protein (NLP) of maize, ZmNLP3.1, recognized the consensus nitrate-responsive cis-elements (NREs) in the promoter regions of ZmNRT2.1 and ZmNRT2.2, and activated the transcription of these genes in response to nitrate. Intriguingly, well-positioned nucleosomes were detected at NREs in the ZmNRT2.1 and ZmNRT2.2 gene promoters, and nucleosome densities were lower in ZmCHB101-RNAi lines than in wild-type plants, both in the absence and presence of nitrate. The ZmCHB101 protein bound to NREs and was involved in the maintenance of nucleosome occupancies at these sites, which may impact the binding of ZmNLP3.1 to NREs in the absence of nitrate. However, in the presence of nitrate, the binding affinity of ZmCHB101 for NREs decreased dramatically, leading to reduced nucleosome density at NREs and consequently increased ZmNLP3.1 binding. Our results provide novel insights into the role of chromatin remodeling proteins in the regulation of nitrate-responsive gene expression in plants.

Project description:BackgroundThe plant immune system employs intracellular NLRs (nucleotide binding [NB], leucine-rich repeat [LRR]/nucleotide-binding oligomerization domain [NOD]-like receptors) to detect effector proteins secreted into the plant cell by potential pathogens. Activated plant NLRs trigger a range of immune responses, collectively known as the hypersensitive response (HR), which culminates in death of the infected cell. Plant NLRs show structural and functional resemblance to animal NLRs involved in inflammatory and innate immune responses. Therefore, knowledge of the activation and regulation of animal NLRs can help us understand the mechanism of action of plant NLRs, and vice versa.ScopeThis review provides an overview of the innate immune pathways in plants and animals, focusing on the available structural and biochemical information available for both plant and animal NLRs. We highlight the gap in knowledge between the animal and plant systems, in particular the lack of structural information for plant NLRs, with crystal structures only available for the N-terminal domains of plant NLRs and an integrated decoy domain, in contrast to the more complete structures available for animal NLRs. We assess the similarities and differences between plant and animal NLRs, and use the structural information on the animal NLR pair NAIP/NLRC4 to derive a plausible model for plant NLR activation.ConclusionsSignalling by cooperative assembly formation (SCAF) appears to operate in most innate immunity pathways, including plant and animal NLRs. Our proposed model of plant NLR activation includes three key steps: (1) initially, the NLR exists in an inactive auto-inhibited state; (2) a combination of binding by activating elicitor and ATP leads to a structural rearrangement of the NLR; and (3) signalling occurs through cooperative assembly of the resistosome. Further studies, structural and biochemical in particular, will be required to provide additional evidence for the different features of this model and shed light on the many existing variations, e.g. helper NLRs and NLRs containing integrated decoys.

Dataset Information

The chromatin-remodeling protein BAF60/SWP73A regulates the plant immune receptor NLRs.

Publications

The chromatin-remodeling protein BAF60/SWP73A regulates the plant immune receptor NLRs.

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