Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis

Feifei Wang, Zhong Hua Chen, Xiaohui Liu, Timothy D. Colmer, Lana Shabala, Anya Salih, Meixue Zhou, Sergey Shabala

    Research output: Contribution to journalArticle

    19 Citations (Scopus)

    Abstract

    Regulation of root cell K+ is essential for acclimation to low oxygen stress. The potential roles of GORK (depolarization-activated guard cell outward-rectifying potassium) channels and RBOHD (respiratory burst oxidase homologue D) in plant adaptive responses to hypoxia were investigated in the context of tissue specificity (epidermis versus stele; elongation versus mature zone) in roots of Arabidopsis. The expression of GORK and RBOHD was down-regulated by 2- to 3-fold within 1 h and 24 h of hypoxia treatment in Arabidopsis wild-type (WT) roots. Interestingly, a loss of the functional GORK channel resulted in a waterlogging-tolerant phenotype, while rbohD knockout was sensitive to waterlogging. To understand their functions under hypoxia stress, we studied K+, Ca2+, and reactive oxygen species (ROS) distribution in various root cell types. gork1-1 plants had better K+ retention ability in both the elongation and mature zone compared with the WT and rbohD under hypoxia. Hypoxia induced a Ca2+ increase in each cell type after 72 h, and the increase was much less pronounced in rbohD than in the WT. In most tissues except the elongation zone in rbohD, the H2O2 concentration had decreased after 1 h of hypoxia, but then increased significantly after 24 h of hypoxia in each zone and tissue, further suggesting that RBOHD may shape hypoxia-specific Ca2+ signatures via the modulation of apoplastic H2O2 production. Taken together, our data suggest that plants lacking functional GORK channels are more capable of retaining K+ for their better performance under hypoxia, and that RBOHD is crucial in hypoxia-induced Ca2+ signalling for stress sensing and acclimation mechanism.

    Original languageEnglish
    Pages (from-to)3191-3204
    Number of pages14
    JournalJournal of Experimental Botany
    Volume68
    Issue number12
    DOIs
    Publication statusPublished - 1 Jun 2017

    Fingerprint

    NADPH Oxidase
    Acclimatization
    Arabidopsis
    hypoxia
    acclimation
    flooded conditions
    calcium
    Hypoxia
    NAD(P)H oxidase (H2O2-forming)
    Organ Specificity
    stele
    Potassium Channels
    potassium channels
    guard cells
    cells
    epidermis (plant)
    Epidermis
    reactive oxygen species
    Reactive Oxygen Species
    rhizosphere

    Cite this

    Wang, Feifei ; Chen, Zhong Hua ; Liu, Xiaohui ; Colmer, Timothy D. ; Shabala, Lana ; Salih, Anya ; Zhou, Meixue ; Shabala, Sergey. / Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis. In: Journal of Experimental Botany. 2017 ; Vol. 68, No. 12. pp. 3191-3204.
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    title = "Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis",
    abstract = "Regulation of root cell K+ is essential for acclimation to low oxygen stress. The potential roles of GORK (depolarization-activated guard cell outward-rectifying potassium) channels and RBOHD (respiratory burst oxidase homologue D) in plant adaptive responses to hypoxia were investigated in the context of tissue specificity (epidermis versus stele; elongation versus mature zone) in roots of Arabidopsis. The expression of GORK and RBOHD was down-regulated by 2- to 3-fold within 1 h and 24 h of hypoxia treatment in Arabidopsis wild-type (WT) roots. Interestingly, a loss of the functional GORK channel resulted in a waterlogging-tolerant phenotype, while rbohD knockout was sensitive to waterlogging. To understand their functions under hypoxia stress, we studied K+, Ca2+, and reactive oxygen species (ROS) distribution in various root cell types. gork1-1 plants had better K+ retention ability in both the elongation and mature zone compared with the WT and rbohD under hypoxia. Hypoxia induced a Ca2+ increase in each cell type after 72 h, and the increase was much less pronounced in rbohD than in the WT. In most tissues except the elongation zone in rbohD, the H2O2 concentration had decreased after 1 h of hypoxia, but then increased significantly after 24 h of hypoxia in each zone and tissue, further suggesting that RBOHD may shape hypoxia-specific Ca2+ signatures via the modulation of apoplastic H2O2 production. Taken together, our data suggest that plants lacking functional GORK channels are more capable of retaining K+ for their better performance under hypoxia, and that RBOHD is crucial in hypoxia-induced Ca2+ signalling for stress sensing and acclimation mechanism.",
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    Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis. / Wang, Feifei; Chen, Zhong Hua; Liu, Xiaohui; Colmer, Timothy D.; Shabala, Lana; Salih, Anya; Zhou, Meixue; Shabala, Sergey.

    In: Journal of Experimental Botany, Vol. 68, No. 12, 01.06.2017, p. 3191-3204.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis

    AU - Wang, Feifei

    AU - Chen, Zhong Hua

    AU - Liu, Xiaohui

    AU - Colmer, Timothy D.

    AU - Shabala, Lana

    AU - Salih, Anya

    AU - Zhou, Meixue

    AU - Shabala, Sergey

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    N2 - Regulation of root cell K+ is essential for acclimation to low oxygen stress. The potential roles of GORK (depolarization-activated guard cell outward-rectifying potassium) channels and RBOHD (respiratory burst oxidase homologue D) in plant adaptive responses to hypoxia were investigated in the context of tissue specificity (epidermis versus stele; elongation versus mature zone) in roots of Arabidopsis. The expression of GORK and RBOHD was down-regulated by 2- to 3-fold within 1 h and 24 h of hypoxia treatment in Arabidopsis wild-type (WT) roots. Interestingly, a loss of the functional GORK channel resulted in a waterlogging-tolerant phenotype, while rbohD knockout was sensitive to waterlogging. To understand their functions under hypoxia stress, we studied K+, Ca2+, and reactive oxygen species (ROS) distribution in various root cell types. gork1-1 plants had better K+ retention ability in both the elongation and mature zone compared with the WT and rbohD under hypoxia. Hypoxia induced a Ca2+ increase in each cell type after 72 h, and the increase was much less pronounced in rbohD than in the WT. In most tissues except the elongation zone in rbohD, the H2O2 concentration had decreased after 1 h of hypoxia, but then increased significantly after 24 h of hypoxia in each zone and tissue, further suggesting that RBOHD may shape hypoxia-specific Ca2+ signatures via the modulation of apoplastic H2O2 production. Taken together, our data suggest that plants lacking functional GORK channels are more capable of retaining K+ for their better performance under hypoxia, and that RBOHD is crucial in hypoxia-induced Ca2+ signalling for stress sensing and acclimation mechanism.

    AB - Regulation of root cell K+ is essential for acclimation to low oxygen stress. The potential roles of GORK (depolarization-activated guard cell outward-rectifying potassium) channels and RBOHD (respiratory burst oxidase homologue D) in plant adaptive responses to hypoxia were investigated in the context of tissue specificity (epidermis versus stele; elongation versus mature zone) in roots of Arabidopsis. The expression of GORK and RBOHD was down-regulated by 2- to 3-fold within 1 h and 24 h of hypoxia treatment in Arabidopsis wild-type (WT) roots. Interestingly, a loss of the functional GORK channel resulted in a waterlogging-tolerant phenotype, while rbohD knockout was sensitive to waterlogging. To understand their functions under hypoxia stress, we studied K+, Ca2+, and reactive oxygen species (ROS) distribution in various root cell types. gork1-1 plants had better K+ retention ability in both the elongation and mature zone compared with the WT and rbohD under hypoxia. Hypoxia induced a Ca2+ increase in each cell type after 72 h, and the increase was much less pronounced in rbohD than in the WT. In most tissues except the elongation zone in rbohD, the H2O2 concentration had decreased after 1 h of hypoxia, but then increased significantly after 24 h of hypoxia in each zone and tissue, further suggesting that RBOHD may shape hypoxia-specific Ca2+ signatures via the modulation of apoplastic H2O2 production. Taken together, our data suggest that plants lacking functional GORK channels are more capable of retaining K+ for their better performance under hypoxia, and that RBOHD is crucial in hypoxia-induced Ca2+ signalling for stress sensing and acclimation mechanism.

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    KW - Fluorescence dyes

    KW - HO

    KW - Homeostasis

    KW - Potassium

    KW - Reactive oxygen species

    KW - Signalling

    KW - Stele

    KW - Superoxide

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    DO - 10.1093/jxb/erw378

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