IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32770-7.html
   My bibliography  Save this article

Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis

Author

Listed:
  • Wen Shi

    (Shandong University)

  • Lingyan Wang

    (Shandong University)

  • Lianmei Yao

    (Shandong University)

  • Wei Hao

    (Shandong University)

  • Chao Han

    (Shandong University)

  • Min Fan

    (Shandong University)

  • Wenfei Wang

    (Fujian Agriculture and Forestry University)

  • Ming-Yi Bai

    (Shandong University)

Abstract

Stomatal pores allow gas exchange between plant and atmosphere. Stomatal development is regulated by multiple intrinsic developmental and environmental signals. Here, we show that spatially patterned hydrogen peroxide (H2O2) plays an essential role in stomatal development. H2O2 is remarkably enriched in meristemoids, which is established by spatial expression patterns of H2O2-scavenging enzyme CAT2 and APX1. SPEECHLESS (SPCH), a master regulator of stomatal development, directly binds to the promoters of CAT2 and APX1 to repress their expression in meristemoid cells. Mutations in CAT2 or APX1 result in an increased stomatal index. Ectopic expression of CAT2 driven by SPCH promoter significantly inhibits the stomatal development. Furthermore, H2O2 activates the energy sensor SnRK1 by inducing the nuclear localization of the catalytic α-subunit KIN10, which stabilizes SPCH to promote stomatal development. Overall, these results demonstrate that the spatial pattern of H2O2 in epidermal leaves is critical for the optimal stomatal development in Arabidopsis.

Suggested Citation

  • Wen Shi & Lingyan Wang & Lianmei Yao & Wei Hao & Chao Han & Min Fan & Wenfei Wang & Ming-Yi Bai, 2022. "Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32770-7
    DOI: 10.1038/s41467-022-32770-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32770-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-32770-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Lynn Jo Pillitteri & Daniel B. Sloan & Naomi L. Bogenschutz & Keiko U. Torii, 2007. "Termination of asymmetric cell division and differentiation of stomata," Nature, Nature, vol. 445(7127), pages 501-505, February.
    2. Cora A. MacAlister & Kyoko Ohashi-Ito & Dominique C. Bergmann, 2007. "Transcription factor control of asymmetric cell divisions that establish the stomatal lineage," Nature, Nature, vol. 445(7127), pages 537-540, February.
    3. Chao Han & Yue Liu & Wen Shi & Yan Qiao & Lingyan Wang & Yanchen Tian & Min Fan & Zhiping Deng & On Sun Lau & Geert De Jaeger & Ming-Yi Bai, 2020. "KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. Edward Owusu-Ansah & Utpal Banerjee, 2009. "Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation," Nature, Nature, vol. 461(7263), pages 537-541, September.
    5. Tae-Wuk Kim & Marta Michniewicz & Dominique C. Bergmann & Zhi-Yong Wang, 2012. "Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway," Nature, Nature, vol. 482(7385), pages 419-422, February.
    6. Elena Baena-González & Filip Rolland & Johan M. Thevelein & Jen Sheen, 2007. "A central integrator of transcription networks in plant stress and energy signalling," Nature, Nature, vol. 448(7156), pages 938-942, August.
    7. Jie Le & Xu-Guang Liu & Ke-Zhen Yang & Xiao-Lan Chen & Jun-Jie Zou & Hong-Zhe Wang & Ming Wang & Steffen Vanneste & Miyo Morita & Masao Tasaka & Zhao-Jun Ding & Jiří Friml & Tom Beeckman & Fred Sack, 2014. "Auxin transport and activity regulate stomatal patterning and development," Nature Communications, Nature, vol. 5(1), pages 1-8, May.
    8. Yanchen Tian & Min Fan & Zhaoxia Qin & Hongjun Lv & Minmin Wang & Zhe Zhang & Wenying Zhou & Na Zhao & Xiaohui Li & Chao Han & Zhaojun Ding & Wenfei Wang & Zhi-Yong Wang & Ming-Yi Bai, 2018. "Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    9. Masashi Yamada & Xinwei Han & Philip N. Benfey, 2020. "RGF1 controls root meristem size through ROS signalling," Nature, Nature, vol. 577(7788), pages 85-88, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Wen Shi & Yue Liu & Na Zhao & Lianmei Yao & Jinge Li & Min Fan & Bojian Zhong & Ming-Yi Bai & Chao Han, 2024. "Hydrogen peroxide is required for light-induced stomatal opening across different plant species," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Ayami Nakagawa & Krishna Mohan Sepuru & Shu Jan Yip & Hyemin Seo & Calvin M. Coffin & Kota Hashimoto & Zixuan Li & Yasutomo Segawa & Rie Iwasaki & Hiroe Kato & Daisuke Kurihara & Yusuke Aihara & Steph, 2024. "Chemical inhibition of stomatal differentiation by perturbation of the master-regulatory bHLH heterodimer via an ACT-Like domain," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Xiaoyu Guo & Xue Ding & Juan Dong, 2022. "Dichotomy of the BSL phosphatase signaling spatially regulates MAPK components in stomatal fate determination," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Linsan Liu & Sarah B. Jose & Chiara Campoli & Micha M. Bayer & Miguel A. Sánchez-Diaz & Trisha McAllister & Yichun Zhou & Mhmoud Eskan & Linda Milne & Miriam Schreiber & Thomas Batstone & Ian D. Bull , 2022. "Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Gilad Gabay & Hanchao Wang & Junli Zhang & Jorge I. Moriconi & German F. Burguener & Leonardo D. Gualano & Tyson Howell & Adam Lukaszewski & Brian Staskawicz & Myeong-Je Cho & Jaclyn Tanaka & Tzion Fa, 2023. "Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Tao Zhang & Sarah E. Noll & Jesus T. Peng & Amman Klair & Abigail Tripka & Nathan Stutzman & Casey Cheng & Richard N. Zare & Alexandra J. Dickinson, 2023. "Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Yonglun Zeng & Baiying Li & Shuxian Huang & Hongbo Li & Wenhan Cao & Yixuan Chen & Guoyong Liu & Zhenping Li & Chao Yang & Lei Feng & Jiayang Gao & Sze Wan Lo & Jierui Zhao & Jinbo Shen & Yan Guo & Ca, 2023. "The plant unique ESCRT component FREE1 regulates autophagosome closure," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Gabriel Krouk & Daniel Tranchina & Laurence Lejay & Alexis A Cruikshank & Dennis Shasha & Gloria M Coruzzi & Rodrigo A Gutiérrez, 2009. "A Systems Approach Uncovers Restrictions for Signal Interactions Regulating Genome-wide Responses to Nutritional Cues in Arabidopsis," PLOS Computational Biology, Public Library of Science, vol. 5(3), pages 1-12, March.
    9. Chuanzhong Zhang & Hongru Wang & Xiaojie Tian & Xinyan Lin & Yunfei Han & Zhongmin Han & Hanjing Sha & Jia Liu & Jianfeng Liu & Jian Zhang & Qingyun Bu & Jun Fang, 2024. "A transposon insertion in the promoter of OsUBC12 enhances cold tolerance during japonica rice germination," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Ping Li & Nana Xu & Yang Shui & Jie Zhang & Wuzhong Yin & Min Tian & Faping Guo & Dasong Bai & Pan Qi & Qingxiong Huang & Biluo Li & Yuanyuan Li & Yungao Hu & Youlin Peng, 2023. "Phenotypic Analysis and Gene Cloning of a New Allelic Mutant of SPL5 in Rice," Agriculture, MDPI, vol. 13(10), pages 1-16, September.
    11. Miaomiao Li & Tao Yao & Wanru Lin & Will E. Hinckley & Mary Galli & Wellington Muchero & Andrea Gallavotti & Jin-Gui Chen & Shao-shan Carol Huang, 2023. "Double DAP-seq uncovered synergistic DNA binding of interacting bZIP transcription factors," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32770-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.