I Want to (Bud) Break Free: The Potential Role of DAM and SVP-Like Genes in Regulating Dormancy Cycle in Temperate Fruit Trees

Abstract

Bud dormancy is an adaptive process that allows trees to survive the hard environmental conditions that they experience during the winter of temperate climates. Dormancy is characterized by the reduction in meristematic activity and the absence of visible growth. A prolonged exposure to cold temperatures is required to allow the bud resuming growth in response to warm temperatures. In fruit tree species, the dormancy cycle is believed to be regulated by a group of genes encoding MADS-box transcription factors. These genes are called DORMANCY-ASSOCIATED MADS-BOX (DAM) and are phylogenetically related to the Arabidopsis thaliana floral regulators SHORT VEGETATIVE PHASE (SVP) and AGAMOUS-LIKE 24. The interest in DAM and other orthologs of SVP (SVP-like) genes has notably increased due to the publication of several reports suggesting their role in the control of bud dormancy in numerous fruit species, including apple, pear, peach, Japanese apricot, and kiwifruit among others. In this review, we briefly describe the physiological bases of the dormancy cycle and how it is genetically regulated, with a particular emphasis on DAM and SVP-like genes. We also provide a detailed report of the most recent advances about the transcriptional regulation of these genes by seasonal cues, epigenetics and plant hormones. From this information, we propose a tentative classification of DAM and SVP-like genes based on their seasonal pattern of expression. Furthermore, we discuss the potential biological role of DAM and SVP-like genes in bud dormancy in antagonizing the function of FLOWERING LOCUS T-like genes. Finally, we draw a global picture of the possible role of DAM and SVP-like genes in the bud dormancy cycle and propose a model that integrates these genes in a molecular network of dormancy cycle regulation in temperate fruit trees.

Keywords: MADS-box family transcription factors; SVP-like genes; bud break; bud dormancy; phenology; seasonal; temperate tree species.

FIGURE 1

Representation of 1-year life cycle of a temperate fruit tree. Trees grow actively during the growing season, typically in spring and early summer. At the end of summer and beginning of autumn, they initiate growth cessation, presumably in response to short days. Toward autumn, trees increase their resistance to cold (hardiness) and buds enter in dormancy during autumn. Chilling temperatures during the winter periods triggers dormancy release. Then, ecodormant buds can respond to warm temperatures in the spring to promote budbreak, which is followed by active growth at the end of the spring and in the summer.

FIGURE 2

Phylogenetic analysis of DAM and SVP-like proteins from several plant species (Ade, Actinidia deliciosa; Ees, Euphorbia esula; Mdo, Malus × domestica; Pmu, Prunus mume; Ppe, Prunus persica; Pbr, Pyrus bretschneideri; Ppy, Pyrus pyrifolia). Arabidopsis AGL24, FLC and SVP were also used in the analysis. Sequences were aligned using MAFFT (Katoh et al., 2002). Poorly aligned positions and divergent regions were eliminated using Gblocks (Castresana, 2000). Maximum likelihood phylogeny was inferred using PhyML 3.0 (Guindon and Gascuel, 2003). The tree was drawn using FigTree v1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/). Arabidopsis FLC was used to root the tree. The scale bar unit represents branch lengths (0.2 substitutions/site). Accession codes (NCBI): AGL24 (AT4G24540), FLC (AT5G10140), SVP (AT2G22450), AdeSVP1 (AFA37963), AdeSVP2 (AFA37964), AdeSVP3 (AFA37965), AdeSVP4 (AFA37966), EesDAM1 (ABY53594), EesDAM2 (ABY60423), MdoDAM1 (AOA32865), MdoDAM2 (AOA32866), MdoDAM3 (XP_017186028), MdoDAM4 (AOA32868), MdoDAMb (ADL36743), MdoSVPa (AOA32867), MdoSVPb (BAR40332), PbrMADS47 (XP_009364259), PmuDAM1 (BAK78921), PmuDAM2 (BAK78922), PmuDAM3 (BAK78923), PmuDAM4 (BAK78924), PmuDAM5 (BAK78920), PmuDAM6 (BAH22477), PmuSVP1 (AML81015), PmuSVP2 (AML81016), PpeDAM1 (ABJ96361), PpeDAM2 (ABJ96363), PpeDAM3 (ABJ96364), PpeDAM4 (ABJ96358), PpeDAM5 (ABJ96359), PpeDAM6 (ABJ96360), PpeSVP1 (XP_020422316), PpeSVP2 (XP_020409383), PpyMADS13.1 (BAI48074), PpyMADS13.2 (BAI48075), PpyMADS13.3 (BAM74166), PpyDAM3 (AJW29049), PpySVP (AJW29050).

FIGURE 3

Tentative consensus of seasonal DAM and SVP-like gene expression dynamics. Data were gathered from studies marked with an asterisk in Table 1. Three different expression patterns (A) were identified for DAM and SVP-like genes (B). Additional information concerning the different dormancy cycle phases are present in Figure 1. AdeSVP3, MdoSVPa, MdoSVPb and PpySVP did not present a consistent seasonal transcript variation. Genes in bold were functionally characterized (see the sections “Functional Studies of DAM and SVP-Like Genes of Fruit Tree Species in Model Plants” and “DAM and SVP-Like Genes Might Act as Growth Inhibitors in Trees”).

FIGURE 4

A possible model of molecular control of bud dormancy in temperate fruit tree species mediated by DAM and SVP-like genes. It has been shown that DAM and SVP-like genes are regulated by photoperiod and temperature. This regulation is probably mediated by several transcription factors, miRNAs, plant hormones and chromatin modifiers. In turn, DAM and SVP-like transcription factors are involved in the repression of bud growth, probably by affecting the expression of FT-like genes and ABA levels. Black lines indicate molecular connections based on previous reports. Gray lines indicate expected genetic interactions that have not been proved yet.