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MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis

Author

Listed:
  • Qing Sang

    (Shenzhen University
    Shenzhen University
    University of California)

  • Lusheng Fan

    (University of California)

  • Tianxiang Liu

    (University of California)

  • Yongjian Qiu

    (University of California
    University of Mississippi)

  • Juan Du

    (University of California)

  • Beixin Mo

    (Shenzhen University
    Shenzhen University)

  • Meng Chen

    (University of California)

  • Xuemei Chen

    (University of California
    Peking University)

Abstract

MicroRNAs (miRNAs) play diverse roles in plant development, but whether and how miRNAs participate in thermomorphogenesis remain ambiguous. Here we show that HYPONASTIC LEAVES 1 (HYL1)—a key component of miRNA biogenesis—acts downstream of the thermal regulator PHYTOCHROME INTERACTING FACTOR 4 in the temperature-dependent plasticity of hypocotyl growth in Arabidopsis. A hyl1-2 suppressor screen identified a dominant dicer-like1 allele that rescues hyl1-2’s defects in miRNA biogenesis and thermoresponsive hypocotyl elongation. Genome-wide miRNA and transcriptome analysis revealed microRNA156 (miR156) and its target SQUAMOSA PROMOTER-BINDING-PROTEIN-LIKE 9 (SPL9) to be critical regulators of thermomorphogenesis. Surprisingly, perturbation of the miR156/SPL9 module disengages seedling responsiveness to warm temperatures by impeding auxin sensitivity. Moreover, miR156-dependent auxin sensitivity also operates in the shade avoidance response at lower temperatures. Thus, these results unveil the miR156/SPL9 module as a previously uncharacterized genetic circuit that enables plant growth plasticity in response to environmental temperature and light changes.

Suggested Citation

  • Qing Sang & Lusheng Fan & Tianxiang Liu & Yongjian Qiu & Juan Du & Beixin Mo & Meng Chen & Xuemei Chen, 2023. "MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36774-9
    DOI: 10.1038/s41467-023-36774-9
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    References listed on IDEAS

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    1. Yurong Xie & Yang Liu & Hai Wang & Xiaojing Ma & Baobao Wang & Guangxia Wu & Haiyang Wang, 2017. "Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    2. Yongjian Qiu & Meina Li & Ruth Jean-Ae Kim & Carisha M. Moore & Meng Chen, 2019. "Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Yogev Burko & Björn Christopher Willige & Adam Seluzicki & Ondřej Novák & Karin Ljung & Joanne Chory, 2022. "PIF7 is a master regulator of thermomorphogenesis in shade," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Patrick May & Will Liao & Yijin Wu & Bin Shuai & W. Richard McCombie & Michael Q. Zhang & Qiong A. Liu, 2013. "The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    5. Xu Tan & Luz Irina A. Calderon-Villalobos & Michal Sharon & Changxue Zheng & Carol V. Robinson & Mark Estelle & Ning Zheng, 2007. "Mechanism of auxin perception by the TIR1 ubiquitin ligase," Nature, Nature, vol. 446(7136), pages 640-645, April.
    6. Chan Yul Yoo & Jiangman He & Qing Sang & Yongjian Qiu & Lingyun Long & Ruth Jean-Ae Kim & Emily G. Chong & Joseph Hahm & Nicholas Morffy & Pei Zhou & Lucia C. Strader & Akira Nagatani & Beixin Mo & Xu, 2021. "Direct photoresponsive inhibition of a p53-like transcription activation domain in PIF3 by Arabidopsis phytochrome B," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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