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Stabilization of dimeric PYR/PYL/RCAR family members relieves abscisic acid-induced inhibition of seed germination

Author

Listed:
  • Zhi-Zheng Wang

    (Central China Normal University)

  • Min-Jie Cao

    (Southern University of Science and Technology)

  • Junjie Yan

    (Huazhong Agricultural University)

  • Jin Dong

    (Central China Normal University)

  • Mo-Xian Chen

    (Guizhou University)

  • Jing-Fang Yang

    (Central China Normal University)

  • Jian-Hong Li

    (Guizhou University)

  • Rui-Ning Ying

    (Central China Normal University)

  • Yang-Yang Gao

    (Guizhou University)

  • Li Li

    (Huazhong Agricultural University)

  • Ya-Nan Leng

    (Nanjing Forestry University)

  • Yuan Tian

    (Shandong Agricultural University)

  • Kamalani Achala H. Hewage

    (Central China Normal University)

  • Rong-Jie Pei

    (Central China Normal University)

  • Zhi-You Huang

    (Central China Normal University)

  • Ping Yin

    (Huazhong Agricultural University)

  • Jian-Kang Zhu

    (Southern University of Science and Technology)

  • Ge-Fei Hao

    (Central China Normal University
    Guizhou University)

  • Guang-Fu Yang

    (Central China Normal University)

Abstract

Abscisic acid (ABA) is the primary preventing factor of seed germination, which is crucial to plant survival and propagation. ABA-induced seed germination inhibition is mainly mediated by the dimeric PYR/PYL/RCAR (PYLs) family members. However, little is known about the relevance between dimeric stability of PYLs and seed germination. Here, we reveal that stabilization of PYL dimer can relieve ABA-induced inhibition of seed germination using chemical genetic approaches. Di-nitrobensulfamide (DBSA), a computationally designed chemical probe, yields around ten-fold improvement in receptor affinity relative to ABA. DBSA reverses ABA-induced inhibition of seed germination mainly through dimeric receptors and recovers the expression of ABA-responsive genes. DBSA maintains PYR1 in dimeric state during protein oligomeric state experiment. X-ray crystallography shows that DBSA targets a pocket in PYL dimer interface and may stabilize PYL dimer by forming hydrogen networks. Our results illustrate the potential of PYL dimer stabilization in preventing ABA-induced seed germination inhibition.

Suggested Citation

  • Zhi-Zheng Wang & Min-Jie Cao & Junjie Yan & Jin Dong & Mo-Xian Chen & Jing-Fang Yang & Jian-Hong Li & Rui-Ning Ying & Yang-Yang Gao & Li Li & Ya-Nan Leng & Yuan Tian & Kamalani Achala H. Hewage & Rong, 2024. "Stabilization of dimeric PYR/PYL/RCAR family members relieves abscisic acid-induced inhibition of seed germination," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52426-y
    DOI: 10.1038/s41467-024-52426-y
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    References listed on IDEAS

    as
    1. Min-Jie Cao & Yu-Lu Zhang & Xue Liu & Huan Huang & X. Edward Zhou & Wen-Long Wang & Ai Zeng & Chun-Zhao Zhao & Tong Si & Jiamu Du & Wen-Wu Wu & Fu-Xing Wang & H. Eric Xu & Jian-Kang Zhu, 2017. "Combining chemical and genetic approaches to increase drought resistance in plants," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    2. Qibing Lin & Fuqing Wu & Peike Sheng & Zhe Zhang & Xin Zhang & Xiuping Guo & Jiulin Wang & Zhijun Cheng & Jie Wang & Haiyang Wang & Jianmin Wan, 2015. "The SnRK2-APC/CTE regulatory module mediates the antagonistic action of gibberellic acid and abscisic acid pathways," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    3. A. J. Challinor & A.-K. Koehler & J. Ramirez-Villegas & S. Whitfield & B. Das, 2016. "Current warming will reduce yields unless maize breeding and seed systems adapt immediately," Nature Climate Change, Nature, vol. 6(10), pages 954-958, October.
    4. Julia Santiago & Florine Dupeux & Adam Round & Regina Antoni & Sang-Youl Park & Marc Jamin & Sean R. Cutler & Pedro Luis Rodriguez & José Antonio Márquez, 2009. "The abscisic acid receptor PYR1 in complex with abscisic acid," Nature, Nature, vol. 462(7273), pages 665-668, December.
    5. Hiroaki Fujii & Viswanathan Chinnusamy & Americo Rodrigues & Silvia Rubio & Regina Antoni & Sang-Youl Park & Sean R. Cutler & Jen Sheen & Pedro L. Rodriguez & Jian-Kang Zhu, 2009. "In vitro reconstitution of an abscisic acid signalling pathway," Nature, Nature, vol. 462(7273), pages 660-664, December.
    6. Sang-Youl Park & Francis C. Peterson & Assaf Mosquna & Jin Yao & Brian F. Volkman & Sean R. Cutler, 2015. "Agrochemical control of plant water use using engineered abscisic acid receptors," Nature, Nature, vol. 520(7548), pages 545-548, April.
    7. Zhijuan Wang & Hongtao Ji & Bingjian Yuan & Shuangfeng Wang & Chao Su & Bin Yao & Hongtao Zhao & Xia Li, 2015. "ABA signalling is fine-tuned by antagonistic HAB1 variants," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
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