J Integr Plant Biol ›› 2024, Vol. 66 ›› Issue (8): 1752-1768.DOI: 10.1111/jipb.13719

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  • 收稿日期:2024-01-05 接受日期:2024-05-13 出版日期:2024-08-01 发布日期:2024-08-19

A transcriptional cascade involving BBX22 and HY5 finely regulates both plant height and fruit pigmentation in citrus

Jialing Fu1,2†, Li Liao1,2†, Jiajing Jin1, Zhihao Lu1, Juan Sun1, Lizhi Song1, Yue Huang1, Shengjun Liu1, Ding Huang1, Yuantao Xu1, Jiaxian He1, Bin Hu1, Yiqun Zhu1, Fangfang Wu3, Xia Wang1,2, Xiuxin Deng1,2 and Qiang Xu1,2*   

  1. 1. National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, P. R. China
    2. Hubei Hongshan Laboratory, Wuhan 430070, P. R. China
    3. Science and Technology Innovation Research Center of Majia Pomelo, Shangrao 334000, China
    †Jialing Fu and Li Liao contributed equally to this work.
    *Correspondence: Qiang Xu (xuqiang@mail.hzau.edu.cn)
  • Received:2024-01-05 Accepted:2024-05-13 Online:2024-08-01 Published:2024-08-19
  • Supported by:
    This research was supported by funding from the National Natural Science Foundation of China granted to Q.X. (number 31925034), the National Key Research and Development Program of China granted to Q.X. (number 2022YFFF1003100), Major Special Projects and Key R&D Projects in Yunnan Province granted to Q.X. (202102AE090054), the Key Research and Development Program of Hubei granted to X.W. (number 2022BBA155), the Foundation of Hubei Hongshan Laboratory granted to Q.X. (number 2021hszd016), and Key Project of Hubei Provincial Natural Science Foundation granted to Q.X. (number 2021CFA017). We are grateful to Dr. Qi Xie from the Institute of Genetics and Development, Chinese Academy of Sciences, for providing the YAO promoter driven CRISPR/Cas9 vector.

Abstract: Dwarfing is a pivotal agronomic trait affecting both yield and quality. Citrus species exhibit substantial variation in plant height, among which internode length is a core element. However, the molecular mechanism governing internode elongation remains unclear. Here, we unveiled that the transcriptional cascade consisting of B-BOX DOMAIN PROTEIN 22 (BBX22) and ELONGATED HYPOCOTYL 5 (HY5) finely tunes plant height and internode elongation in citrus. Loss-of-function mutations of BBX22 in an early-flowering citrus (Citrus hindsii “SJG”) promoted internode elongation and reduced pigment accumulation, whereas ectopic expression of BBX22 in SJG, sweet orange (C. sinensis), pomelo (C. maxima) or heterologous expression of BBX22 in tomato (Solanum lycopersicum) significantly decreased internode length. Furthermore, exogenous application of gibberellin A3 (GA3) rescued the shortened internode and dwarf phenotype caused by BBX22 overexpression. Additional experiments revealed that BBX22 played a dual role in regulation internode elongation and pigmentation in citrus. On the one hand, it directly bound to and activated the expression of HY5, GA metabolism gene (GA2 OXIDASE 8, GA2ox8), carotenoid biosynthesis gene (PHYTOENE SYNTHASE 1, PSY1) and anthocyanin regulatory gene (Ruby1, a MYB DOMAIN PROTEIN). On the other hand, it acted as a cofactor of HY5, enhancing the ability of HY5 to regulate target genes expression. Together, our results reveal the critical role of the transcriptional cascade consisting of BBX22 and HY5 in controlling internode elongation and pigment accumulation in citrus. Unraveling the crosstalk regulatory mechanism between internode elongation and fruit pigmentation provides key genes for breeding of novel types with both dwarf and health-beneficial fortification in citrus.

Key words: anthocyanins, BBX22, carotenoids, citrus, HY5, internode elongation, plant height

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