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Title: Thermal-responsive genetic and epigenetic regulation of DAM cluster controlling dormancy and chilling requirement in peach floral buds

Author
item ZHU, HONG - Chinese Academy Of Sciences
item CHEN, PAO-YANG - University Of California
item ZHONG, SILIN - The Chinese University Of Hong Kong (CUHK)
item Dardick, Christopher - Chris
item Callahan, Ann
item An, Yong-Qiang - Charles
item VAN KNOCKER, STEVE - Michigan State University
item Yang, Yingzhen
item ZHONG, GAN-YUAN - US Department Of Agriculture (USDA)
item ABBOTT, ALBERT - University Of Kentucky
item Liu, Zongrang

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/10/2020
Publication Date: 8/1/2020
Citation: Zhu, H., Chen, P., Zhong, S., Dardick, C.D., Callahan, A.M., An, Y., Van Knocker, S., Yang, Y., Zhong, G., Abbott, A., Liu, Z. 2020. Thermal-responsive genetic and epigenetic regulation of DAM cluster controlling dormancy and chilling requirement in peach floral buds. Horticulture Research. 7:Article 114. https://doi.org/10.1038/s41438-020-0336-y.
DOI: https://doi.org/10.1038/s41438-020-0336-y

Interpretive Summary: Dormancy is an adaptation trait that enables perennial plants to survive unfavorable seasonal stresses. In the temperate zone where winter freezing is a major threat, plants enter the deep dormant state in late fall to avoid freezing injury. The dormant buds require exposure to a chilling period in order to exit dormancy in spring but how chilling releases plants from dormancy in fruit trees (e.g. peach) remains unclear. In this work, we treated the dormant peach floral buds with different chilling periods, and analyzed chemical modifications on genes controlling dormancy and chilling requirement. We found that chilling increases the chemical modifications on six genes that controlling dormancy release and the increased chemical modifications repress the gene expression, facilitating the release of the dormant floral buds from dormancy constraints. This finding helps us better understand the mechanism underlying the chilling-mediated facilitation of dormancy release and also provides information for breeding of new peach cultivars with proper chilling requirement and flowering time.

Technical Abstract: The DORMANCY-ASSOCIATED MADS-box (DAM) gene cluster in peach serves as a key regulatory hub on which the seasonal temperatures act and orchestrate dormancy onset and exit, chilling response and floral bud developmental pace. Yet, how different temperature regimes interact with and regulate the six linked DAM genes remains unclear. Here, we demonstrate that chilling down-regulates DAM1 and DAM3-6 in dormant floral buds with distinct patterns and identify DAM4 as the most abundantly expressed one. We reveal multiple epigenetic events, with tri-methyl histone H3 lysine 27 (H3K27me3) induced by chilling specifically in DAM1 and DAM5, a 21-nt sRNA in DAM3 and a ncRNA induced in DAM4. Such induction is inversely correlated with down-regulation of their cognate DAMs. We also show that the six DAMs were hypermethylated, associating with the production of 24-nt sRNAs. Hence, the chilling-responsive dynamic of the different epigenetic elements and their interactions likely define distinct expression abundance and down-regulation pattern of each DAM. We further show that the expression of the five DAMs remains steadily unchanged or continuously down-regulated at the ensuing warm temperature after chilling, and this state of regulation correlates with robust increase of sRNA expression, H3K27me3 and CHH methylation, which is particularly pronounced in DAM4. Such robust increase of repressive epigenetic marks may irreversibly reinforce the chilling-imposed repression of DAMs to ensure flower tissues developmental programming free from any residual DAM inhibition.