EARLY BUD-BREAK 1 and EARLY BUD-BREAK 3 control resumption of poplar growth after winter dormancy

Abstract

Bud-break is an economically and environmentally important process in trees and shrubs from boreal and temperate latitudes, but its molecular mechanisms are poorly understood. Here, we show that two previously reported transcription factors, EARLY BUD BREAK 1 (EBB1) and SHORT VEGETATIVE PHASE-Like (SVL) directly interact to control bud-break. EBB1 is a positive regulator of bud-break, whereas SVL is a negative regulator of bud-break. EBB1 directly and negatively regulates SVL expression. We further report the identification and characterization of the EBB3 gene. EBB3 is a temperature-responsive, epigenetically-regulated, positive regulator of bud-break that provides a direct link to activation of the cell cycle during bud-break. EBB3 is an AP2/ERF transcription factor that positively and directly regulates CYCLIND3.1 gene. Our results reveal the architecture of a putative regulatory module that links temperature-mediated control of bud-break with activation of cell cycle.

Bud endodormancy in deciduous fruit trees: advances and prospects

“…The decrease in ABA content during endodormancy release was related to the downregulation of ABA synthesis genes and the upregulation of genes for ABA catabolism in pear and grape buds 53 – 55 . Exogenous ABA treatment caused delayed endodormancy release, while treatment with fluridone, an ABA biosynthesis inhibitor, promoted endodormancy release in pear 40 , suggesting that ABA plays a crucial role in endodormancy maintenance, which is consistent with studies on poplar 19 , 22 . Overexpression of the ABA-responsive transcription factor PpyABF3 caused growth inhibition in pear calli with downregulation of CYCLIN-D and EXPANSIN A1 40 , indicating that ABA promotes endodormancy maintenance, possibly by inhibiting cell division and cell expansion.…”

“…Furthermore, the expression of DAM s can negatively regulate the expression of FT2 , a gene that promotes growth and flowering, during endodormancy 73 . In our recent study, overexpression of DAM3 in pear calli resulted in downregulation of Cyclin-D and EXPA1 , suggesting the potential regulation by DAMs of cell division and expansion 40 , which is similar to the role of SVL in poplar, indirectly inhibiting Cyclin-D3 via EBB3 22 . However, other target genes of DAMs in deciduous fruit trees remain obscure.…”

“…In peach, downregulation of DAM genes was closely related to the increased level of H3K4me3 and CHH DNA methylation during chilling accumulation and during warmer conditions after chilling exposure, while noncoding RNAs also participated in regulating epigenetic modification 76 , 96 . However, in poplar, SVL seems not to be a target for H3K27me3 histone modification, but the expression of the downstream gene EBB3 showed a negative correlation with H3K27me3 deposition after chilling exposure 19 , 22 . These studies indicate that DAM/SVP genes in deciduous fruit trees are potential target genes for epigenetic regulation during endodormancy maintenance and release, and that the changes in histone modification might be related to the chilling requirements of plants.…”

“…The functions of these proteins during the endodormancy process have been verified using transgenic plants in several species, such as poplar and kiwifruit 19 , 20 , 63 . In poplar, SVP-like (SVL) acts as a central transcription factor integrating ABA signaling, ABA synthesis, GA synthesis, GA catabolism, and cell division, hence maintaining bud endodormancy 19 , 20 , 22 . In rosaceous plants, these d ormancy- a ssociated M ADS-box proteins are named DAMs and are clustered separately from other SVPs.…”

“…EARLY BUD BREAK 1 (EBB1), which suppresses SVL expression, is positively regulated by low temperature, leading to the upregulation of EBB3 . EBB3 directly activates CYCD3.1 , promoting cell division and bud break 22 . In addition to transcriptional regulation, epigenetic regulation, including DNA methylation, is also reported to be involved in growth cessation and bud endodormancy processes in poplar.…”