WeiTsing, a pericycle-expressed ion channel, safeguards the stele to confer clubroot resistance

Wang, Wenxian; Qin, Li; Zhang, Wenjing; Tang, Ling-hui; Zhang, Chao; Xiao, Dong; Miao, Pei; Shen, Meng‐Ru; Du, Huilong; Cheng, Hangyuan; Wang, Ke; Zhang, Xiangyun; Su, Min; Lu, Hongwei; Li, Chang; Gao, Qiang; Zhang, Xiaojuan; Huang, Yun; Liang, Chengzhi; Zhou, Jian‐Min; Chen, Yuhang

doi:10.1016/j.cell.2023.05.023

Cited by 22 publications

(32 citation statements)

References 71 publications

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“…On the basis of these features, BI-1 emerges as a promising candidate for future investigations aimed at identifying the H + -sensitive ER Ca 2+ channel. Further, the recently identified ER-localized Ca 2+ channel WeiTsing (WTS) could also be a potential candidate ( 35 ), although its pH sensitivity has yet to be examined. We cannot rule out that Hc KCR2-mediated cytosolic pH changes may influence H + or cation Ca 2+ exchanger transport activity on the ER membrane ( 10 , 36 ).…”

Section: Discussionmentioning

confidence: 99%

Light-gated channelrhodopsin sparks proton-induced calcium release in guard cells

Huang,

Shen,

Roelfsema

et al. 2023

Science

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Although there has been long-standing recognition that stimuli-induced cytosolic pH alterations coincide with changes in calcium ion (Ca 2+ ) levels, the interdependence between protons (H + ) and Ca 2+ remains poorly understood. We addressed this topic using the light-gated channelrhodopsin Hc KCR2 from the pseudofungus Hyphochytrium catenoides , which operates as a H + conductive, Ca 2+ impermeable ion channel on the plasma membrane of plant cells. Light activation of Hc KCR2 in Arabidopsis guard cells evokes a transient cytoplasmic acidification that sparks Ca 2+ release from the endoplasmic reticulum. A H + -induced cytosolic Ca 2+ signal results in membrane depolarization through the activation of Ca 2+ -dependent SLAC1/SLAH3 anion channels, which enabled us to remotely control stomatal movement. Our study suggests a H + -induced Ca 2+ release mechanism in plant cells and establishes Hc KCR2 as a tool to dissect the molecular basis of plant intracellular pH and Ca 2+ signaling.

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Section: Discussionmentioning

confidence: 99%

Light-gated channelrhodopsin sparks proton-induced calcium release in guard cells

Huang,

Shen,

Roelfsema

et al. 2023

Science

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“…Of the candidate genes evaluated, RPB1 was found to be necessary for clubroot resistance though transformation of susceptible accession Col-0 revealed that it was not sufficient to confer full resistance. Following the completion and submission of this work for review, the same RPB1 gene has been characterised as WeiTsing (WTS) (Wang et al, 2023); we contrast our findings with respect to the ability of RPB1 to confer resistance to clubroot disease with those reported for WTS.…”

Section: Introductionmentioning

confidence: 91%

“…Ectopic expression of RPB1 in a susceptible background is not sufficient for resistance to clubroot RPB1 encodes a protein with no homology to previously characterised proteins, it is predicted to contain membrane-spanning regions (Figure S8); this prediction has been borne out by the cryo-electron microscopy characterisation of WTS/RPB1 as a pentameric membranebound protein (Wang et al, 2023). Orthologues of RPB1 can be found in the Brassicaceae and there is a homologue of RPB1 in the Col-0 genome-AT1G56270, however there is no information available regarding the role or function of these related genes (Figure S9).…”

Section: Deletion Of Rac1 Does Not Affect Clubroot Resistance Inmentioning

confidence: 99%

“…Of the loci implicated in resistance to P. brassicae that were tested through the generation of knock-out mutations only the gene RPB1-a locus initially identified by Fuchs and Sacristan (1996), sequenced by Rehn and Siemens, and now characterised as WTS by Wang et al (2023)-was confirmed to impact clubroot resistance. The deletions of RPB1 in accessions Est-1 and Uod-1 accumulated pathogen DNA titres that were comparable to the highly clubroot susceptible accession Col-0 19 dpi (Figure 3B).…”

Section: Rpb1 Is Essential For Clubroot Resistance In Est-1 and Uod-1mentioning

confidence: 99%

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Natural variation in Arabidopsis responses to Plasmodiophora brassicae reveals an essential role for Resistance to Plasmodiophora brasssicae 1 (RPB1)

Ochoa,

Mukhopadhyay,

Bieluszewski

et al. 2023

The Plant Journal

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SUMMARYDespite the identification of clubroot resistance genes in various Brassica crops our understanding of the genetic basis of immunity to Plasmodiophora brassicae infection in the model plant Arabidopsis thaliana remains limited. To address this issue, we performed a screen of 142 natural accessions and identified 11 clubroot‐resistant Arabidopsis lines. Genome‐wide association analysis identified several genetic loci significantly linked with resistance. Three genes from two of these loci were targeted for deletion by CRISPR/Cas9 mutation in resistant accessions Est‐1 and Uod‐1. Deletion of Resistance to Plasmodiophora brassicae 1 (RPB1) rendered both lines susceptible to the P. brassicae pathotype P1+. Further analysis of rpb1 knock‐out Est‐1 and Uod‐1 lines showed that the RPB1 protein is required for activation of downstream defence responses, such as the expression of phytoalexin biosynthesis gene CYP71A13. RPB1 has recently been shown to encode a cation channel localised in the endoplasmic reticulum. The clubroot susceptible Arabidopsis accession Col‐0 lacks a functional RPB1 gene; when Col‐0 is transformed with RPB1 expression driven by its native promoter it is capable of activating RPB1 transcription in response to infection, but this is not sufficient to confer resistance. Transient expression of RPB1 in Nicotiana tabacum induced programmed cell death in leaves. We conclude that RPB1 is a critical component of the defence response to P. brassicae infection in Arabidopsis, acting downstream of pathogen recognition but required for the elaboration of effective resistance.

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“…The activated EDS1‐PAD4 and EDS1‐SAG101 complexes interact with and activate ADR1 and NRG1.1 (Dongus & Parker, 2021; Ma et al, 2020). Recently, a novel endoplasmic reticulum (ER)‐localized Ca 2+ ‐permeable channel named WeiTsing (WTS) was identified essential for clubroot resistance; it acts in the pericycle to prevent Plasmodiophora brassicae colonization in the stele in Arabidopsis (Wang, Qin, et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

Calmodulin and calmodulin‐like protein‐mediated plant responses to biotic stresses

Zeng

Zhu

Yuan

et al. 2023

Plant Cell & Environment

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Plants have evolved a set of finely regulated mechanisms to respond to various biotic stresses. Transient changes in intracellular calcium (Ca2+) concentration have been well documented to act as cellular signals in coupling environmental stimuli to appropriate physiological responses with astonishing accuracy and specificity in plants. Calmodulins (CaMs) and calmodulin‐like proteins (CMLs) are extensively characterized as important classes of Ca2+ sensors. The spatial‐temporal coordination between Ca2+ transients, CaMs/CMLs and their target proteins is critical for plant responses to environmental stresses. Ca2+‐loaded CaMs/CMLs interact with and regulate a broad spectrum of target proteins, such as ion transporters (including channels, pumps, and antiporters), transcription factors, protein kinases, protein phosphatases, metabolic enzymes and proteins with unknown biological functions. This review focuses on mechanisms underlying how CaMs/CMLs are involved in the regulation of plant responses to diverse biotic stresses including pathogen infections and herbivore attacks. Recent discoveries of crucial functions of CaMs/CMLs and their target proteins in biotic stress resistance revealed through physiological, molecular, biochemical, and genetic analyses have been described, and intriguing insights into the CaM/CML‐mediated regulatory network are proposed. Perspectives for future directions in understanding CaM/CML‐mediated signalling pathways in plant responses to biotic stresses are discussed. The application of accumulated knowledge of CaM/CML‐mediated signalling in biotic stress responses into crop cultivation would improve crop resistance to various biotic stresses and safeguard our food production in the future.

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WeiTsing, a pericycle-expressed ion channel, safeguards the stele to confer clubroot resistance

Cited by 22 publications

References 71 publications

Light-gated channelrhodopsin sparks proton-induced calcium release in guard cells

Light-gated channelrhodopsin sparks proton-induced calcium release in guard cells

Natural variation in Arabidopsis responses to Plasmodiophora brassicae reveals an essential role for Resistance to Plasmodiophora brasssicae 1 (RPB1)

Calmodulin and calmodulin‐like protein‐mediated plant responses to biotic stresses

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