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Journal of Integrative Agriculture
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EARLY BUD BREAK and SHORT VEGETATIVE PHASE 4 integrate ABA plant hormone signaling control of grape bud dormancy

Yang Dong1, Muhammad Khalil-Ur-Rehman3, Yi Zhang1, Liyuan Huang1, Haoran Li1, Lina Yang4, Huan Zheng1#, Jianmin Tao1, 2#

1 Sanya Institute of Nanjing Agricultural University, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China

2 Institute of Horticultural Crops, Xinjiang Academy of Agricultural Science, Urumqi 830001, Xinjiang, China

3 Department of Horticultural Sciences, The Islamia University of Bahawalpur 63100, Pakistan

4 Charles River Laboratories international, lnc. Mattawan, Michigan 49071, USA

 Highlights 

1. VvSVP4 promotes dormancy by activating VvPYL9 and enhancing ABA signaling.

2. VvEBB triggers bud break by repressing VvSAPK2 and activating IAA/CK pathways.

3. Transcriptome and hormone data reveal opposing roles of VvSVP4 and VvEBB in ABA-driven dormancy and IAA/CK-mediated bud break.

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摘要  

芽休眠是多年生果树的重要适应性特征,使其能够抵御不利的生长环境。该适应策略在植物的生存和繁殖过程中起着重要作用,但其分子机制尚不清楚。本研究鉴定并分析了葡萄中两个转录因子,EARLY BUD BREAKVvEBB)和SHORT VEGETATIVE PHASE 4VvSVP4)。研究结果表明,在杨树中过表达VvSVP4后,其作为萌芽负调控因子发挥作用,而VvEBB则作为正调控因子在芽萌发过程中发挥作用。转录组分析显示,与对照植株相比,植物激素信号通路,特别是涉及脱落酸(ABA)、吲哚乙酸(IAA)和细胞分裂素(CK)的信号通路,在VvSVP4VvSVP4oe)和VvEBBVvEBBoe)过表达植株中显著富集。此外,ABA、IAA和CK的内源激素水平变化与转录组数据呈正相关。在内休眠阶段,VvSVP4直接促进ABA受体基因VvPYL9的表达,从而维持芽的休眠状态。相反,在生态休眠阶段,VvEBB基因迅速上调表达,并负向调控与蔗糖非发酵-1-相关蛋白激酶亚家族2基因(VvSAPK2)的表达,促进芽休眠的解除。综上所述,本研究全面阐释了VvSVP4  VvEBB 基因在休眠和芽萌发中的作用,整合了细胞周期调控和多种激素信号通路的见解。



Abstract  

Bud dormancy is a crucial adaptation for perennial fruit plants, enabling them to withstand unfavorable growth conditions. This adaptive strategy plays a significant role in the survival and reproduction of these plants, yet its molecular basis is not fully understood. In the current study, two transcription factors in grapes, EARLY BUD BREAK (VvEBB) and SHORT VEGETATIVE PHASE 4 (VvSVP4), were identified and examined. The findings demonstrated that, following heterologous transformation in poplar, VvSVP4 functions as a negative regulator, whereas VvEBB acts as a positive regulator in the process of bud-break. Transcriptome analysis showed that plant hormone signaling pathways, specifically those involving abscisic acid (ABA), indole acetic acid (IAA), and cytokinin (CK), were significantly enriched in plants overexpressing VvSVP4 (VvSVP4oe) and VvEBB (VvEBBoe), compared to control plants. Additionally, changes in the endogenous levels of ABA, IAA, and CK were found to be positively correlated with the transcriptome data. During the endodormancy phase, VvSVP4 directly and positively influenced the expression of the ABA receptor gene VvPYL9, thereby maintaining the state of bud dormancy. Conversely, during ecodormancy, the VvEBB gene was rapidly upregulated and negatively impacted the expression of the sucrose nonfermenting 1-related protein kinase subfamily 2 gene (VvSAPK2), facilitating the release from dormancy. In summary, this study offers a comprehensive explanation of the roles of VvSVP4 and VvEBB genes in dormancy and bud break, integrating insights into cell cycle regulation and multiple hormones signaling pathways.

Keywords:  bud dormancy       cell cycle              grape              hormone              VvSVP4              VvEBB  
Online: 09 May 2025  
Fund: 

This work was supported by China Agriculture Research System of MOF and MARA (CARS-29), XinjiangUygur Autonomous Region Tianchi Talent Introduction Program, Key R&D Technology Commissioner Projects in Hainan Province, China (ZDYF2024KJTPY008).  

About author:  #Correspondence Huan Zheng, E-mail: huanzheng@njau.edu.cn; Jianmin Tao, E-mail: taojianmin@njau.edu.cn

Cite this article: 

Yang Dong, Muhammad Khalil-Ur-Rehman, Yi Zhang, Liyuan Huang, Haoran Li, Lina Yang, Huan Zheng, Jianmin Tao. 2025. EARLY BUD BREAK and SHORT VEGETATIVE PHASE 4 integrate ABA plant hormone signaling control of grape bud dormancy. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.05.003

Anh Tuan P, Bai S, Saito T, Imai T, Ito A, Moriguchi T. 2016. Involvement of EARLY BUD-BREAK, an AP2/ERF Transcription Factor Gene, in Bud Break in Japanese Pear (Pyrus pyrifolia Nakai) Lateral Flower Buds: Expression, Histone Modifications and Possible Target Genes. Plant & Cell Physiology, 57, 1038-1047.

Azeez A, Zhao Y C, Singh R K, Yordanov Y S, Dash M, Miskolczi P, Stojkovič K, Strauss S H, Bhalerao R P, Busov V B. 2021. EARLY BUD-BREAK 1 and EARLY BUD-BREAK 3 control resumption of poplar growth after winter dormancy. Nature Communications, 12, 1123.

Campoy J A, Ruiz D, Egea J. 2011. Dormancy in temperate fruit trees in a global warming context: A review. Scientia Horticulturae, 130, 357-372.

Danieli R, Assouline S, Salam B B, Vrobel O, Teper-Bamnolker P, Belausov E, Granot D, Tarkowski P.,Eshel D. 2023. Chilling induces sugar and ABA accumulation that antagonistically signals for symplastic connection of dormant potato buds. Plant, Cell & Environment, 46, 2097-2111.

Dewitte W, Scofield S, Alcasabas A A, Maughan S C, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray J A H. 2007. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proceedings of the National Academy of Sciences of the United States of America, 104, 14537-14542.

Dong Y, Khalil-Ur-Rehman M, Liu X, Wang X, Yang L, Tao J, Zheng H. 2022. Functional characterisation of five SVP genes in grape bud dormancy and flowering. Plant Growth Regulation, 97, 511-522.

Dong Y, Liu J, Huang L, Yang L, Khalil-Ur-Rehman M, Zheng H, Tao J. 2023. SHORT VEGETATIVE PHASE 3 mediates hormonal signals control of bud dormancy in grape. Environmental and Experimental Botany, 211.

Feng C Z, Chen Y, Wang C, Kong Y H, Wu W H, Chen Y F. 2014. Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. The Plant Journal, 80, 654-668.

Hao X, Tang H, Wang B, Wang L, Cao H, Wang Y, Zeng J, Fang S, Chu J, Yang Y, Wang X. 2018. Gene characterization and expression analysis reveal the importance of auxin signaling in bud dormancy regulation in tea plant. Journal of Plant Growth Regulation, 38, 225-240.

Huang X, Hou L, Meng J, You H, Li Z, Gong Z, Yang S, Shi Y. 2018. The Antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Molecular Plant, 11, 970-982.

Li P, Zheng T, Zhang Z, Liu W, Qiu L, Wang J, Cheng T, Zhang Q. 2021. Integrative identification of crucial genes associated with plant hormone-mediated bud dormancy in prunus mume. Frontiers in Genetics, 12, 698598.

Liang D, Huang X, Shen Y, Shen T, Zhang H, Lin L, Wang J, Deng Q, Lyu X, Xia H. 2019. Hydrogen cyanamide induces grape bud endodormancy release through carbohydrate metabolism and plant hormone signaling. BMC Genomics, 20, 1034.

Liu Z, Wang N, Su Y, Long Q, Peng Y, Shangguan L, Zhang F, Cao S, Wang X, Ge M, Xue H, Ma Z, Liu W, Xu X, Li C, Cao X, Ahmad B, Su X, Liu Y, Huang G, et al., 2024. Grapevine pangenome facilitates trait genetics and genomic breeding. Nature Genetics, 56, 2804-2814.

Lloret A, Quesada-Traver C, Conejero A, Arbona V, Gómez-Mena C, Petri C, Sánchez-Navarro J A, Zuriaga E, Leida C, Badenes M L, Ríos G. 2021. Regulatory circuits involving bud dormancy factor PpeDAM6. Horticulture Research, 8, 261.

Luo L, Takahashi M, Kameoka H, Qin R, Shiga T, Kanno Y, Seo M, Ito M, Xu G, Kyozuka J. 2019. Developmental analysis of the early steps in strigolactone-mediated axillary bud dormancy in rice. The Plant Journal, 97, 1006-1021.

Moser M, Asquini E, Miolli G V, Weigl K, Hanke M V, Flachowsky H, Si-Ammour A. 2020. The MADS-Box gene MdDAM1 controls growth cessation and bud dormancy in apple. Frontiers in Plant Science, 11, 1003.

Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K. 2009. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant & Cell Physiology, 50, 1345-1363.

Roman H, Girault T, Barbier F, Péron T, Brouard N, Pěnčík A, Novák O, Vian A, Sakr S, Lothier J, Le Gourrierec J, Leduc N. 2016. Cytokinins are initial targets of light in the control of bud outgrowth. Plant Physiology, 172, 489-509.

Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao R P, Boerjan W, Rohde A. 2007. A molecular timetable for apical bud formation and dormancy induction in poplar. The Plant Cell, 19, 2370-2390.

Seeliger I, Frerichs A, Glowa D, Velo L, Comelli P, Chandler J W, Werr W. 2016. The AP2-type transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE promote G1/S transition. Molecular Genetics and Genomics, 291, 1835-1849.

Shi X, Cao S, Wang X, Huang S, Wang Y, Liu Z, Liu W, Leng X, Peng Y, Wang N, Wang Y, Ma Z, Xu X, Zhang F, Xue H, Zhong H, Wang Y, Zhang K, Velt A, Avia K, et al., 2023. The complete reference genome for grapevine (Vitis vinifera L.) genetics and breeding. Horticulture Research, 10, uhad061.

Shi Z, Halaly-Basha T, Zheng C, Weissberg M, Ophir R, Galbraith D W, Pang X, Or E, 2018. Transient induction of a subset of ethylene biosynthesis genes is potentially involved in regulation of grapevine bud dormancy release. Plant Molecular Biology, 98, 507-523.

Singh R K, Maurya J P, Azeez A, Miskolczi P, Tylewicz S, Stojkovič K, Delhomme N, Busov V, Bhalerao R P. 2018. A genetic network mediating the control of bud break in hybrid aspen. Nature Communications, 9, 4173.

Singh R K, Miskolczi P, Maurya J P, Bhalerao R P. 2019. A tree ortholog of SHORT VEGETATIVE PHASE floral repressor mediates photoperiodic control of bud dormancy. Current Biology, 29.

Singh R K, Svystun T, AlDahmash B, Jönsson A M, Bhalerao R P. 2017. Photoperiod and temperature mediated control of phenology in trees a molecular perspective. The New Phytologist, 213, 511-524.

Song J, Shang L, Wang X, Xing Y, Xu W, Zhang Y, Wang T, Li H, Zhang J, Ye Z. 2021. MAPK11 regulates seed germination and ABA signaling in tomato by phosphorylating SnRKs. Journal of Experimental Botany, 72, 1677-1690.

Tan W, Zhang D, Zhou H, Zheng T, Yin Y, Lin H. 2018. Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genetics, 14, e1007336.

Tuan P A, Bai S, Saito T, Ito A, Moriguchi T. 2017. Dormancy-associated MADS-Box (DAM) and the abscisic acid pathway regulate pear endodormancy through a feedback mechanism. Plant & Cell Physiology, 58, 1378-1390.

Tylewicz S, Petterle A, Marttila S, Miskolczi P, Azeez A, Singh R K, Immanen J, Mähler N, Hvidsten T R, Eklund D M, Bowman J L, Helariutta Y, Bhalerao R P. 2018. Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science, 360, 212-215.

Wang D, Gao Z, Du P, Xiao W, Tan Q, Chen X, Li L, Gao D. 2015. Expression of ABA metabolism-related genes suggests similarities and differences between seed dormancy and bud dormancy of peach (Prunus persica). Frontiers in Plant Science, 6, 1248.

Wang Q, Xu G, Zhao X, Zhang Z, Wang X, Liu X, Xiao W, Fu X, Chen X, Gao D, Li D, Li L. 2020. Transcription factor TCP20 regulates peach bud endodormancy by inhibiting DAM5/DAM6 and interacting with ABF2. Journal of Experimental Botany, 71, 1585-1597.

Wang X, Wei J, Wu J, Shi B, Wang P, Alabd A, Wang D, Gao Y, Ni J, Bai S, Teng Y. 2023. Transcription factors BZR2/MYC2 modulate brassinosteroid and jasmonic acid crosstalk during pear dormancy. Plant Physiology, 194(3), 1794–1814.

Wisniewski M, Norelli J, Artlip T, 2015. Overexpression of a peach CBF gene in apple: a model for understanding the integration of growth, dormancy, and cold hardiness in woody plants. Frontiers in Plant Science, 6, 85.

Wu R, Cooney J, Tomes S, Rebstock R, Karunairetnam S, Allan A C, Macknight R C, Varkonyi-Gasic E. 2021. RNAi-mediated repression of dormancy-related genes results in evergrowing apple trees. Tree Physiology, 41, 1510-1523.

Wu R, Tomes S, Karunairetnam S, Tustin S D, Hellens R P, Allan A C, Macknight R C, Varkonyi-Gasic E. 2017a. SVP-like MADS Box genes control dormancy and budbreak in apple. Frontiers in Plant Science, 8, 477.

Wu R, Wang T, Allan A C, Macknight R C, Varkonyi-Gasic E. 2018. Overexpression of both AcSVP1 and AcSVP4 delays budbreak in kiwifruit A. chinensis var. deliciosa, but only AcSVP1 delays flowering in model plants. Environmental and Experimental Botany, 153, 262-270.

Wu R, Wang T, Warren B A W, Allan A C, Macknight R C, Varkonyi-Gasic E. 2017b. Kiwifruit SVP2 gene prevents premature budbreak during dormancy. Journal of Experimental Botany, 68, 1071-1082.

Xiao H, Liu Z, Wang N, Long Q, Cao S, Huang G, Liu W, Peng Y, Riaz S, Walker A M, Gaut B S, Zhou Y. 2023. Adaptive and maladaptive introgression in grapevine domestication. Proceedings of the National Academy of Sciences of the United States of America, 120, e2222041120.

Yamane H, Wada M, Honda C, Matsuura T, Ikeda Y, Hirayama T, Osako Y, Gao-Takai M, Kojima M, Sakakibara H, Tao R. 2019. Overexpression of Prunus DAM6 inhibits growth, represses bud break competency of dormant buds and delays bud outgrowth in apple plants. PloS One, 14, e0214788.

Yang Q, Gao Y, Wu X, Moriguchi T, Bai S, Teng Y. 2021. Bud endodormancy in deciduous fruit trees: advances and prospects. Horticulture Research, 8, 139.

Yang Q, Niu Q, Li J, Zheng X, Ma Y, Bai S, Teng Y. 2018. PpHB22, a member of HD-Zip proteins, activates PpDAM1 to regulate bud dormancy transition in 'Suli' pear (Pyrus pyrifolia White Pear Group). Plant Physiology and Biochemistry, 127, 355-365.

Yang Q, Yang B, Li J, Wang Y, Tao R, Yang F, Wu X, Yan X, Ahmad M, Shen J, Bai S, Teng Y. 2020. ABA-responsive ABRE-BINDING FACTOR3 activates DAM3 expression to promote bud dormancy in Asian pear. Plant, Cell & Environment, 43, 1360-1375.

Yordanov Y S, Ma C, Strauss S H, Busov V B. 2014. EARLY BUD-BREAK 1 (EBB1) is a regulator of release from seasonal dormancy in poplar trees. Proceedings of the National Academy of Sciences of the United States of America, 111, 10001-10006.

Zhang K, Diederich L, John P C L. 2005. The cytokinin requirement for cell division in cultured Nicotiana plumbaginifolia cells can be satisfied by yeast Cdc25 protein tyrosine phosphatase: implications for mechanisms of cytokinin response and plant development. Plant Physiology, 137, 308-316.

Zhang J, Gao X, Cai G, Wang Y, Li J, Du H, Wang R, Zhang H, Huang J. 2021. An adenylate kinase OsAK3 involves brassinosteroid signaling and grain length in rice (Oryza sativa L.). Rice, 14, 105.

Zhang Y Z, Xu C, Lu W L, Wang X Z, Wang N, Meng X G, Fang Y H, Tan Q P, Chen X D, Fu X L, Li L. 2023. PpMAPK6 regulates peach bud endodormancy release through interactions with PpDAM6. Journal of Integrative Agriculture, 22, 139-148.

Zhao K, Zhou Y, Ahmad S, Xu Z, Li Y, Yang W, Cheng T, Wang J, Zhang Q. 2018. Comprehensive cloning of prunus mume dormancy associated MADS-Box genes and their response in flower bud development and dormancy. Frontiers in Plant Science, 9, 17.

Zhao X, Han X, Wang Q, Wang X, Chen X, Li L, Fu X, Gao D. 2020. EARLY BUD BREAK 1 triggers bud break in peach trees by regulating hormone metabolism, the cell cycle, and cell wall modifications. Journal of Experimental Botany, 71, 3512-3523.

Zhao X, Wen B, Li C, Liu L, Chen X, Li D, Li L, Fu X. 2021. PpEBB1 directly binds to the GCC box-like element of auxin biosynthesis related genes. Plant Science, 306, 110874.

Zhao X, Liu J, Fu X, Xiao L, Wang Q, Wang C, Chen Z, Li J, Lu C, Cao H, Li L. 2024. Whole-genome characterization of CKX genes in Prunus persica and their role in bud dormancy and regrowth. Journal of Integrative Agriculture, 23, 4058-4073.

Zheng C, Acheampong AK, Shi Z, Mugzech A, Halaly-Basha T, Shaya F, Sun Y, Colova V, Mosquna A, Ophir R, Galbraith DW, Or E. 2018. Abscisic acid catabolism enhances dormancy release of grapevine buds. Plant, Cell & Environment, 41, 2490-2503.

Zhou Y, Minio A, Massonnet M, Solares E, Lv Y, Beridze T, Cantu D, Gaut B S. 2019. The population genetics of structural variants in grapevine domestication. Nature Plants, 5, 965-979.

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