Unraveling the role of MADS transcription factor complexes in apple tree dormancy

Abstract

 A group of MADS transcription factors (TFs) are believed to control temperature-mediated bud dormancy. These TFs are encoded by genes similar to SHORT VEGETATIVE PHASE (SVP) from Arabidopsis and called DORMANCY-ASSOCIATED MADS-BOX (DAM). MADS proteins form transcriptional complexes whose combinatory composition define their molecular function. However, how MADS multimeric complexes control the dormancy cycle in trees is unclear.  Apple MdDAM and other dormancy-related MADS proteins form complexes with MdSVPa, which is essential for the transcriptional complexes ability to bind to DNA. Sequential DNA-affinity purification sequencing (seq-DAP-seq) was performed to define the genome-wide binding sites of apple MADS TF complexes. Target genes associated with the binding sites were identified by combining seq-DAP-seq data with transcriptomics datasets obtained by the glucocorticoid receptor system, and RNA-seq data related to apple dormancy.  We have determined a gene regulatory network (GRN) formed by MdSVPa-containing complexes, which regulate the dormancy cycle in response to environmental cues and hormonal signaling pathways. Moreover, novel molecular evidence on the evolutionary functional segregation between DAM and SVP proteins in the Rosaceae is presented. MdSVPa sequentially forms complexes with the MADS TFs that predominate at each dormancy phase, altering its DNA-binding specificity and, therefore, the transcriptional regulation of its target genes.

The Identification of Small RNAs Differentially Expressed in Apple Buds Reveals a Potential Role of the Mir159-MYB Regulatory Module during Dormancy

“…The miR164-CUC module seems conserved in other plant species and in cotton (Gossypium hirsutum) gh-miR164 and gh-CUC2 form a regulatory gene network with BRANCHED 1 (BRC1) that is believed to control branching. BRC1 encodes a TF that controls branching in several plant species [60,61] and it is part of a GRN controlling dormancy and budbreak in apple [5]. Therefore, the downregulation of mdm-miR164c that we observed at ecodormancy (stage 4) (Table 2 and Figure 2C) could be involved in a BRC1-mediated mechanism of budbreak control in apple.…”

“…The transition from endodormancy to ecodormancy and the activation of budbreak is believed to be controlled by complex GRNs that integrate endogenous and environmental signals [3,5,43]. TFs are key players in these GRNs, and a timed and coordinated control of their gene expression seems essential to orchestrate dormancy phase transitions [3,5]. This tight regulation is likely to occur not only at the transcriptional level but also posttranscriptionally.…”

“…However, despite the importance of a well-adjusted dormancy cycle for flowering timing and fruit production, the understanding on how this process is controlled in Rosaceous species and other significant crops is still in its infancy. A group of genes encoding MADS transcription factors (TF) are believed to be major regulators of the dormancy cycle in many Rosaceous fruit trees [3,[5][6][7]. Some of these MADS TF are named as DORMANCY-ASSOCIATED MADS-BOX (DAM) because of their genetic association with the non-dormant phenotype of the evg mutant of peach [6].…”

“…DAM genes belong to the MIKC C type of MADS TF genes and are similar to SHORT VEGETATIVE PHASE (SVP) from Arabidopsis thaliana [8]. They associate in transcriptional complexes that act in an intricate gene regulatory network (GRN) that control the transition between dormancy phases [3,5,9]. This GRN seems to be regulated, at least in part, by the hormonal and environment-mediated transcriptional modulation of its key components [5,7,10].…”

“…They associate in transcriptional complexes that act in an intricate gene regulatory network (GRN) that control the transition between dormancy phases [3,5,9]. This GRN seems to be regulated, at least in part, by the hormonal and environment-mediated transcriptional modulation of its key components [5,7,10]. For example, the plant hormone abscisic acid (ABA) is a positive regulator of dormancy induction in several tree species [11][12][13].…”