Advance of DAM-like genes in bud dormancy of deciduous fruit trees in Rosaceae family

Dormancy is a biological characteristic that adapts to seasonal changes during the long-term evolution of plants, which is of great significance for the safe overwintering of fruit trees and the exploration of the cultivation mode for facility fruit trees. Under the background of the rapid change of global climate, the study on bud dormancy of perennial deciduous fruit trees has been carried out to further deepen the understanding of the regulation mechanism of dormancy process. Dormancy is highly dependent on external environment, and seasonal variations in bud break and flowering time have been reported in the context of global warming. Notably, advances in bud break and blooming dates in spring have been observed for tree species, like Malus domestica and Prunus mume. In the northern hemisphere, as the risk of late frost damages increases, the insufficient cold accumulation during winter may lead to incomplete dormancy release, which frequently results in bud break delay and low bud break rate. Phenological change response to climate warming (ST, expressed in days advance of leaf unfolding per ℃ warming) has significantly decreased beyond 30 years in all monitored tree species, and these phenological changes can directly affect the production of fruit crops, leading to large potential economic losses. Consequently, it is urgent to acquire a better understanding of bud responses to temperature stimuli for tackling fruit losses and anticipating future production changes. Several bud dormancy-related transcription factors have been proposed, among which the SHORT VEGETATIVE PHASE/AGAMOUS LIKE 24 (SVP/AGL24)-clade MADS-box genes in diverse woody perennials have been widely studied. These in-clude DORMANCY- ASSOCIATED MADS- box (DAM) in Rosaceae fruit trees and SVP- like (SVL) in Populus. Recently, the peach [P. persica (L.) Batsch] evergrowing (evg) mutant is found with a dormancy impaired genotype identified in Mexico, which can still grow when exposed to shortened days and low temperatures, and six arranged in tandem dormancy- associated MADS- box (DAM) genes were identified. Transgenic poplar and apple suggested the growth inhibitory functions of DAM6. The expression profile of these genes during the dormancy period indicated that DAMs served as dose-dependent inhibitors of bud break. DAM-like genes have been studied in many perennial species in relation to bud dormancy, including Japanese apricot, apple, plum, cherry, peach and pear, which suggested that DAMs controlled bud dormancy of perennial plants in a similar manner. DAM-likes were up-regulated during dormancy set and down-regulated when dormancy release in Rosaceae deciduous fruit trees. Under controlled environmental conditions, the expressions of PpDAM5/6 were up-regulated in autumn under the influence of environmental low temperature, while they were down-regulated in winter under the influence of long-term low temperature, and their expression levels were negatively correlated with germination rate. Early germination of lateral buds was induced with the PpDAM5/6 down- regulated expressions, which indicated that they may regulate CR by inhibiting lateral bud growth. The homologous dimers of PpTCP20 (Teosinte branched1 Cycloidea/Proliferating cell factors) negatively regulates PpDAM5 and PpDAM6 expression, and the dimers can interact with PpABF2 (ABRE-Binding FACTOR2) to regulate the dormancy of peach buds. In poplar, SVL can directly regulate the expression of FT1, NCED3 and TCP18, while TCP18 can inhibit the growth of axillary buds. However, we can’t prove that whether the direct involvement of DAMs in bud dormancy through its growth inhibitory effects. Furthermore, DAM- likes directly regulate ABA biosynthesis (forming a DAM- like- ABA feedforward loop) and up- regulate the expression of GIBBERELLIN 2- OXIDASE (GA2ox; GA catabolism) during dormancy. After an exposure to low temperatures, the inhibition of the DAM- like- ABA feedforward loop leads to the up- regulated expression of EARLY BUD BREAK3 (EBB3), which encodes an AP2/ ERF transcription factor that subsequently activates CYCLIN D3.1 expression and cell division, ultimately leading to bud break. DAM gene can modulate abscisic acid accumulation in apple dormant buds, the content of ABA increased first at initial dormancy stage and then decreased when the dormancy release. ABA can inhibit cell proliferation and shoot growth, and that dormancy can be induced by ABA biosynthesis, catabolism, signaling promotion of terminal bud set, and induction of dormancy. The content of GA must be restricted during initial activation of the dormant bud meristem, but after that, the level of GA increased to enhance primordia regrowth in grape. In addition, lipid accumulation can resist to low temperature, the changes of lipid accumulation in different metabolic processes create conditions for bud break under optimal conditions. Several studies have indicated the specific role of α-linolenic and linoleic acids in dormancy regulation. α-linolenic acid, a precursor of JA, synthesis along with DAM genes also has a crucial role in pear bud dormancy phase transitions. Differentially expressed genes (DEGs) and metabolites work during various dormancy stage, involving sugars, phytohormone, fatty acids, protein kinases and dehydrins. KEGG analysis revealed that secondary metabolites biosynthesis and phytohormone signaling were found most enriched in the grape dormancy bud; redox activity process was abundant in GO biological process category. GA and ABA pathways were found to be the most enriched. GID1 family transcripts (GA pathway) were up- regulated while DELLA family transcripts were down-regulated during different dormancy stages. Accordingly, histone methylation levels in DAM genes have been intensively studied. Most of the relevant researches indicated H3K4me3 and H3K27me3 levels are respectively positively and negatively correlated with down- regulated DAM ex-pression during dormancy release. PpBPCs interact with two GA- repeat motifs present in the H3K27me3-enriched region in peach DAM6, which further supports that down-regulation of DAM expression could be regulated by H3K27me3 marks. However, not all studies supported the correlation between the accumulation of H3K27me3 at DAM loci and an exposure to low temperatures. Increases in the H3K27me3 level at DAM loci were revealed to be linked with an exposure to cold stress, but not in the study completed, suggestive of a difference in the mechanisms controlling the transcription of Arabidopsis FLC and Rosaceae DAM genes. Therefore, the deposition of H3K27me3 at peach DAM loci may be controlled in a cultivar- dependent manner and/or considerably influenced by environmental conditions. The significance of the direct effect of H3K27me3 on the down-regulation of DAM transcription during chilling-induced bud dormancy release will need to be verified. In contrast to Rosaceae DAM genes, down- regulated SVPa and SVPb expression levels are reportedly not associated with histone methylations. In kiwifruit, the down- regulated gene SVP2, which encodes a bud break repressor, contains H3K4me3 modification, but lacks H3K27me3. Similarly, poplar SVL also lacks H3K27me3 marks. In this paper, the identification and function of DAM-like gene in the regulation of bud dormancy process, the relationship between DAM-like gene and hormones, the influence of epigenetic regulation on DAM-like gene, and the relationship between pollen color change and dormancy process were reviewed, in order to lay the foundation for the analysis of bud dormancy regulation mechanism and dormancy-related molecular breeding in fruit crops.