miR156b-targeted VvSBP8/13 functions downstream of the abscisic acid signal to regulate anthocyanins biosynthesis in grapevine fruit under drought

Shuihuan Guo; Meng Zhang; Mingxin Feng; Guipeng Liu; Laurent Torregrosa; Xiaoqing Tao; Ruihua Ren; Yulin Fang; Zhenwen Zhang; Jiangfei Meng; Tengfei Xu

doi:10.1093/hr/uhad293

miR156b-targeted VvSBP8/13 functions downstream of the abscisic acid signal to regulate anthocyanins biosynthesis in grapevine fruit under drought

Hortic Res. 2024 Jan 2;11(2):uhad293. doi: 10.1093/hr/uhad293. eCollection 2024 Feb.

Authors

Shuihuan Guo^{1

2}, Meng Zhang¹, Mingxin Feng¹, Guipeng Liu¹, Laurent Torregrosa³, Xiaoqing Tao¹, Ruihua Ren¹, Yulin Fang¹, Zhenwen Zhang¹, Jiangfei Meng¹, Tengfei Xu⁴

Affiliations

¹ College of Enology, Northwest A&F University, Yangling, Shaanxi 712100, China.
² College of Food Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450002, China.
³ UMR LEPSE, Université de Montpellier , CIRAD, INRAE, Institut Agro, 34060 Montpellier, France.
⁴ State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi 712100, China.

Abstract

Anthocyanins are the primary color components of grapevine berries and wines. In cultivation practices, a moderate water deficit can promote anthocyanin accumulation in red grape skins. Our previous study showed that abscisic acid (ABA) plays a key role in this process. Herein, we identified a microRNA, vv-miR156b, that is generated in grapevine berries in response to drought stress, along with increasing anthocyanin content and biosynthetic structural gene transcripts. In contrast, vv-miR156b short tandem target mimic (STTM) function-loss callus exhibits the opposite phenotype. Results from in vivo and in vitro experiments revealed that the ABA-signaling-regulated transcription factor VvAREB2 binds directly to the ABA-responsive element (ABRE) of the MIR156b promoter and activates miR156b expression. Furthermore, two miR156b downstream targets, VvSBP8 and VvSBP13, exhibited reduced grape anthocyanin content in their overexpressors but there was a contrary result in their CRISPR-edited lines, the decrease in anthocyanin content was rescued in miR156b and SBP8/13 double overexpressors. We further demonstrated that both VvSBP8 and VvSBP13, encoding transcriptional repressors, displayed sufficient ability to interact with VvMYC1 and VvMYBA1, thereby interfering with MYB-bHLH-WD (MBW) repeat transcriptional complex formation, resulting in the repression of anthocyanin biosynthesis. Our findings demonstrate a direct functional relationship between ABA signaling and the miR156-SBP-MBW complex regulatory module in driving drought-induced anthocyanin accumulation in grape berries.