Amur grape VaMYB4a mediates grapevine cold tolerance via dual regulation of CBF-COR and ABA pathways

doi:10.1016/j.jia.2025.09.005

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Amur grape VaMYB4a mediates grapevine cold tolerance via dual regulation of CBF-COR and ABA pathways

Qinhan Yu^1*, Yue Sun^2*, Yaping Xie², Jiaxin Li², Rong Wang², Qiaoling Zheng¹, Chang Liu¹, Ningbo Zhang^{2, 3, 4, 5, 6}, Weirong Xu^{1, 2, 3, 4, 5, 6#}

¹School of Life Sciences, Ningxia University, Yinchuan 750021, China

²College of Enology and Horticulture, Ningxia University, Yinchuan 750021, Ningxia, China

³Engineering Research Center of Grape and Wine, Ministry of Education, Ningxia University, Yinchuan 750021, China

⁴Ningxia Grape and Wine Research Institute, Ningxia University, Yinchuan 750021, China

⁵Key Laboratory of Modern Molecular Breeding for Dominant and Special Crops in Ningxia, Yinchuan 750021, China

⁶State Key Laboratory of Efficient Production of Forest Resources, Ningxia, Yinchuan 750021, China

Highlights

1. VaMYB4a integrates CBF-COR and ABA signaling to enhance cold tolerance in grapevines.

2. CRISPR/Cas9 knockout and overexpression studies reveal VaMYB4a’s dual regulatory mechanisms.

3. ABA exerts a dual role, dynamically modulating VaMYB4a-mediated cold tolerance.

Abstract
References

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摘要

低温胁迫是限制作物产量的关键因素，尤其在温带气候条件下尤为突出。尽管脱落酸在寒冷胁迫响应中的作用已被广泛认可，但转录因子如何介导ABA依赖的耐寒机制仍不明确。本研究从山葡萄（Vitis amurensis Rupr.）中鉴定出MYB转录因子VaMYB4a，其通过整合ABA信号与CBF-COR通路协同调控低温适应性。通过构建拟南芥、葡萄愈伤组织及欧洲葡萄（Vitis vinifera L.）幼苗中进行过表达和CRISPR/Cas9基因编辑株系，我们发现VaMYB4a通过促进渗透调节、活性氧清除及气孔关闭来增强植株抗冻性。该蛋白以同源二聚体形式发挥作用，其C端结构域对转录激活至关重要。在分子机制上，VaMYB4a可直接上调CBF和COR基因表达，并精细调控ABA信号通路关键因子ABI1和ABF4。值得注意的是，ABA呈现双重调控效应：在短期胁迫下增强VaMYB4a介导的抗冻性，而在长期冷暴露中削弱其功能，揭示低温与激素通路间复杂的级联调控网络。本研究不仅深化了对植物冷适应机制的认知，更为培育气候韧性葡萄品种提供了关键遗传靶标。

Abstract

Cold stress represents a critical constraint on crop productivity, particularly in temperate climates. Despite the established role of abscisic acid (ABA) in cold stress responses, the precise mechanisms through which transcription factors mediate ABA-dependent cold tolerance remain elusive. Here, we identify VaMYB4a, a MYB transcription factor from Vitis amurensis Rupr. (Amur grape), as a key regulator of cold tolerance. It integrates ABA signaling with the CBF (C-repeat binding factors)-COR (cold-regulated) pathway to orchestrate cold stress adaptation. Through a combination of overexpression and CRISPR/Cas9-mediated knockout lines in Arabidopsis thaliana, grape callus, and Vitis vinifera.L seedlings, we demonstrate that VaMYB4a enhances freezing tolerance by promoting osmotic regulation, ROS (Reactive oxygen species) scavenging, and stomatal closure. VaMYB4a functions as a homo-dimer, with its C-terminal domain being essential for transcriptional activation. Mechanistically, VaMYB4a directly upregulates CBF and COR genes while fine-tuning ABA signaling components such as ABI1 and ABF4. Notably, ABA exhibits a dual role: enhancing VaMYB4a-mediated freezing tolerance under short-term stress but attenuating its effects during prolonged cold exposure, revealing an intricate regulatory crosstalk between cold and hormonal pathways. Our work not only advances the molecular understanding of cold adaptation but also provides a promising genetic target for developing stress-resilient grape varieties to mitigate the impacts of climate change.

Keywords: Vitis amurensis Rupr. VaMYB4a CRISPR/Cas9 ABA signaling CBF-COR pathway cold tolerance

Online: 12 September 2025

Fund:

This work was supported by Ningxia Hui Autonomous Region Key R&D Program (2023BCF01003), the National Natural Science Foundation of China (32472711 and 32060672) and the Agricultural Breeding Project of Ningxia Hui Autonomous Region (NXNYYZ202101).

About author: #Correspondence Weirong Xu, E-mail: xuwr@nxu.edu.cn * These authors contributed equally to this study.

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Qinhan Yu, Yue Sun, Yaping Xie, Jiaxin Li, Rong Wang, Qiaoling Zheng, Chang Liu, Ningbo Zhang, Weirong Xu. 2025. Amur grape VaMYB4a mediates grapevine cold tolerance via dual regulation of CBF-COR and ABA pathways. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.005

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