Bud endodormancy in deciduous fruit trees: advances and prospects

Abstract

Bud endodormancy is a complex physiological process that is indispensable for the survival, growth, and development of deciduous perennial plants. The timely release of endodormancy is essential for flowering and fruit production of deciduous fruit trees. A better understanding of the mechanism of endodormancy will be of great help in the artificial regulation of endodormancy to cope with climate change and in creating new cultivars with different chilling requirements. Studies in poplar have clarified the mechanism of vegetative bud endodormancy, but the endodormancy of floral buds in fruit trees needs further study. In this review, we focus on the molecular regulation of endodormancy induction, maintenance and release in floral buds of deciduous fruit trees. We also describe recent advances in quantitative trait loci analysis of chilling requirements in fruit trees. We discuss phytohormones, epigenetic regulation, and the detailed molecular network controlling endodormancy, centered on SHORT VEGETATIVE PHASE (SVP) and Dormancy-associated MADS-box (DAM) genes during endodormancy maintenance and release. Combining previous studies and our observations, we propose a regulatory model for bud endodormancy and offer some perspectives for the future.

Fig. 1. Dormancy–growth cycle.

After growth cessation and bud set, low temperatures and/or the short-day photoperiod induces trees to enter endodormancy. When the chilling requirement is satisfied, endodormancy is released and trees enter the ecodormancy stage. Endodormancy is divided into three stages: induction (establishment), maintenance, and release

Fig. 2. A molecular model for growth cessation based on studies in poplar.

FT2 acts as a central regulator of active growth. Downregulation of FT2 causes growth cessation. Under long-day conditions, FT2 has a high expression level under the control of CO, GI, and other genes, thus promoting LAP1 and AIL1 expression and maintaining tree growth. When autumn approaches, the photoperiod is shortened, which promotes the expression of LHY2 and BRC1 and suppresses FT2 so that growth is inhibited. In addition, the ABA content increases, promoting ABI3 expression and bud development. Arrowheads denote positive effects; blocked arrows denote negative effects

Fig. 3. Daily temperature and bud break percentage of ‘Cuiguan' pear in Hangzhou.

Daily mean temperature in Hangzhou (a) and bud-break percentage indicating the dormancy status of ‘Cuiguan’ pear (b) in autumn and winter of 2019. The endodormancy stage is indicated between the vertical dashed red lines. Horizontal dashed red lines indicate temperatures as shown (a) and 50% bud breakage (b). Branches were sampled at the time points shown and were kept in floral foam in forcing conditions for 21 days for measuring the bud-break percentage. When the trees entered endodormancy (start of the period with the lowest bud-break percentage), the daily mean temperature was still ~14 °C, suggesting that the critical temperature to induce endodormancy of ‘Cuiguan’ pear is possibly not lower than 14 °C. When dormancy was released, the temperature was just approximately 7.2 °C, suggesting that the 7.2 °C model might not be suitable for calculating the chilling requirement of ‘Cuiguan’ pear in the Hangzhou area

Fig. 4. Phylogenetic analysis of DAMs/SVPs from several plant species.

Proteins used in the analysis are as follows: AtAGL24 (AT4G24540), AtFLC (AT5G10140), AtSVP (AT2G22540), AdSVP1 (AFA37963), AdSVP2 (AFA37964), AdSVP3 (AFA37965), AdSVP4 (AFA37966), EeDAM1 (ABY53594), EeDAM2 (ABY60423), MdDAM1 (AOA32865), MdDAM2 (AOA32866), MdDAM3 (XP_028963037.1), MdDAM4 (AOA32868), MdDAMb (ADL36743), MdSVPa (AOA32867), MdSVPb (BAR40332), PmDAM1 (BAK78921), PmDAM2 (BAK78922), PmDAM3 (BAK78923), PmDAM4 (BAK78924), PmDAM5 (BAK78920), PmDAM6 (BAH22477), PmSVP1 (AML81015), PmSVP2 (AML81016), PpeDAM1 (ABJ96361), PpeDAM2 (ABJ96363), PpeDAM3 (ABJ96364), PpeDAM4 (ABJ96358), PpeDAM5 (ABJ96359), PpeDAM6 (ABJ96360), PpeSVP1 (XP_020422316), PpeSVP2 (XP_020409383), as listed by Falavigna et al., VvSVP (GSVIVT01001701001) and PtSVL (Potri007G010800.1). Full-length protein sequences and the maximum likelihood method were used to perform the phylogenetic analysis. FLC in Arabidopsis was set as the outgroup of the phylogenetic tree

Fig. 5. Model for DAM/SVP-centered molecular regulation of bud endodormancy in deciduous fruit trees.

ABA is the primary hormone regulating DAM and SVP to maintain endodormancy. DAM and SVP proteins are transcription factors that integrate ABA signaling and GA biosynthesis and catabolism. Epigenetic regulation (such as H3ac, H3K4me3, H3K27me3, microRNAs, and DNA methylation) might be involved in the dormancy process during chilling exposure. CYP707A is a key enzyme in ABA catabolism, and the expression of CYP707A is upregulated with prolonged chilling. As CYP707A is regulated by epigenetic modification during seed dormancy and germination, the possibility that CYP707A is similarly regulated by epigenetic modification during bud endodormancy needs further study. Arrowheads denote positive effects; blocked arrows denote negative effects. Dashed lines indicate indirect regulation or uncertain pathways