Abscisic acid-induced transcription factor PsMYB306 negatively regulates tree peony bud dormancy release

Authors: YUAN, YANPING - Northwest Agriculture And Forestry University; ZENG, LINGLING - Northwest Agriculture And Forestry University; KONG, DERONG - Northwest Agriculture And Forestry University; MAO, YANXIANG - Northwest Agriculture And Forestry University; XU, YINGRU - Northwest Agriculture And Forestry University; WANG, MEILING - Northwest Agriculture And Forestry University; ZHAO, YIKE - Northwest Agriculture And Forestry University; Jiang, Cai-Zhong; ZHANG, YANLONG - Northwest Agriculture And Forestry University; SUN, DAOYANG - Northwest Agriculture And Forestry University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/2/2023
Publication Date: 1/11/2024
Citation: Yuan, Y., Zeng, L., Kong, D., Mao, Y., Xu, Y., Wang, M., Zhao, Y., Jiang, C., Zhang, Y., Sun, D. 2024. Abscisic acid-induced transcription factor PsMYB306 negatively regulates tree peony bud dormancy release. Plant Physiology. 194(4):2449-2471. https://doi.org/10.1093/plphys/kiae014.
DOI: https://doi.org/10.1093/plphys/kiae014

Interpretive Summary: During the annual growth cycle of perennial plants, bud dormancy can be considered as the inability of the meristems to resume growth under favorable conditions. It is an effective strategy to adapt to the harsh winter environments, such as cold and drought, for the plant survival and growth. It is also a crucial step to improve the quality of bud sprouting, plant growth, and flowering after winter. Bud dormancy can be classified into the endo-, para-, and eco-dormancy. Of them, the state of bud formation and meristem quiescence is called endo-dormancy, and low temperature is one of the main signals that induce growth arrest. Meanwhile, endo-dormant buds can recover their growth after exposure to low temperature for a certain period of time. Thus, the release of endo-dormancy is the prerequisite for the bud break under favorable climatic conditions. It is well recognized that bud dormancy is regulated by various phytohormone signals, especially abscisic acid (ABA) and gibberellins (GAs). It has been known that ABA content varies during dormancy establishment, maintenance, and release by modifying a series of metabolic processes. For example, ABA levels increased at the initial stage of dormancy and then gradually decreased as the dormancy was relieved in grapevine buds. The treatment with ABA on apple and grapevine plants has been shown to be effective for inducing deeper dormancy and facilitating the occurrence of dormancy-associated physiological events. GAs also play a critical role in the modulation of bud dormancy, as a significant change in bioactive GA levels during dormancy release has been reported. In general, endogenous GA levels can be reduced during dormancy induction and increased during dormancy release. However, the GA-promoting effect on primordial growth and bud break was inhibited after meristem activation, suggesting a complex role of GAs in the dormancy regulation. It has been demonstrated that the dormancy was maintained by ABA-mediated repression of bud meristem activity, and the removal of this repression triggered the dormancy release in grapevine buds. A previous report has revealed that GA3 had the most obvious effect on bud promotion in tree peony, indicating that GA3 may be the key bioactive GA in promoting dormancy release. However, the crosstalk between ABA and GAs during bud dormancy release is still not well understood. In addition, a massive transcriptional reprogramming occurs during developmental or forced bud burst. MYB proteins constitute the largest transcription factor (TF) family in plants. They are well known for the important roles in the accumulation of anthocyanins in plants. However, there are few reports on MYB TFs regulating the bud dormancy in perennial plants. Previous studies have demonstrated that three MYB genes showed higher expression levels during dormancy transition in tea plants. To date, the detailed regulatory mechanism of bud dormancy by MYB TFs is still unknown. Tree peony (Paeonia section Moutan DC.) is one of the most famous traditional flowers originating in China with higher ornamental values. Like many perennial plants, tree peony must undergo a prolonged chilling or freezing period in winter before bud sprouting, and its bud dormancy belongs to the endo-dormancy. The off-season flowering will largely improve the commercial application of tree peonies. In the past decade, several studies have found that bud dormancy release depends on nutrient substance, membrane lipid peroxidation, and dynamic changes of endogenous hormones during the chilling requirement fulfillment. GAs might be the primary signal to initiate the bud dormancy break in tree peony. When tree peony endured insufficient chilling accumulation, exogenous GA3 and GA4 treatments accelerated bud dormancy release and subsequent growth. PsMYB1 was reported to be down-regulated at the later stage of chill

Technical Abstract: Bud dormancy is a crucial strategy for perennial plants to withstand the adverse winter conditions. However, the regulatory mechanism of bud dormancy in tree peony remains largely unknown. Here, we observed dramatically reduced and increased accumulation of abscisic acid (ABA) and bioactive gibberellins (GAs) GA1 and GA3, respectively, during bud dormancy release of tree peony under prolonged chilling treatment. An Illumina RNA sequencing study was performed to identify potential genes involved in the bud dormancy regulation in tree peony. Combined with correlation matrix, principal component, and interaction network analyses, a down-regulated MYB transcription factor, PsMYB306, was found to be positively correlated with the expression of an ABA biosynthesis gene, PsNCED3. Protein modeling analysis revealed four residues within the R2R3 domain of PsMYB306 to possess DNA binding capability. Transcription of PsMYB306 was increased by ABA rather than GA3 treatment. Overexpression of PsMYB306 in petunia inhibited seed germination and plant growth, concomitant with elevated ABA and decreased GA contents. Silencing of PsMYB306 accelerated cold-triggered tree peony bud burst, and influenced the production of ABA and GAs as well as the expression of their biosynthetic genes. ABA application alleviated the promoted bud dormancy release and transcription of PsKAO1, PsGA20ox1, and PsGA3ox1 associated with GA biosynthesis in PsMYB306-silenced buds. In vivo and in vitro binding assays confirmed that PsMYB306 specifically transactivated the promoter of PsNCED3. Silencing of PsNCED3 also resulted in promoted bud break and growth. Altogether, our findings suggest that PsMYB306 negatively modulates cold-induced bud dormancy release by regulating the antagonism of ABA to GAs.