Genome-wide changes of regulatory non-coding RNAs reveal pollen development initiated at ecodormancy in peach

Authors: YU, JIALI - University Of Tennessee; Bennett, Dennis; Dardick, Christopher - Chris; ZHEBENTYAYEVA, TATYANA - Pennsylvania State University; ABBOTT, ALBERT - University Of Kentucky; Liu, Zongrang; STATON, MARGARET - University Of Tennessee

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/15/2021
Publication Date: 4/9/2021
Citation: Yu, J., Bennett Jr, D.R., Dardick, C.D., Zhebentyayeva, T., Abbott, A., Liu, Z., Staton, M. 2021. Genome-wide changes of regulatory non-coding RNAs reveal pollen development initiated at ecodormancy in peach. Frontiers in Plant Science. https://doi.org/10.3389/fmolb.2021.612881.
DOI: https://doi.org/10.3389/fmolb.2021.612881

Interpretive Summary: Perennial woody plants in template zone evolved a winter dormancy to cope with and avoid freezing injury. In fall, both vegetative and floral buds cease development and enter a dormant state that is irreversible unless exposure to a certain period of chilling. This chilling requirement is obligatory. Dormancy/chilling period required for dormancy release is also related to flowering time in spring. How chilling regulates the dormancy release at genetic and epigenetic levels remains largely unknown. This work focused on analysis of small RNAs and non-coding RNAs -two types of regulatory RNAs during chilling treatment. This study identified two small RNAs and 72 non-coding RNAs that are regulated by chilling treatment in peach floral buds. The further analysis revealed that two non-coding RNAs interact with a small RNA and this intricate interaction suggests that these non-coding RNAs may regulate small RNA expression, which is implicated in pollen development, a key stage that dormancy may target and arrest. This result provides insight into understanding the molecular mechanism underlying the chilling-mediated regulation of dormancy exit and flower development, which will eventually lead to identification of key genes that may control not only dormancy exit and chilling requirement but also flowering time.

Technical Abstract: Perennial trees protect themselves from harsh winter conditions by entering endodormancy. To release from endodormancy, buds need to be exposed to a sufficient period of chill, after which they transit to ecodormancy and become capable of reactivating growth in favorable conditions. To study the function of regulatory non-coding RNAs in dormancy release, we analyzed the small RNA and long non-coding RNA (lncRNA) expression from peach floral buds in endodormancy (at 0 and 500 chill hours), ecodormancy (at 1000 chill hours) and bud break (incubated 3 and 7 days in a warm greenhouse after 1000 chill hours) stages. We identified ppe-miR6285 significantly upregulated at ecodormancy, with a target gene, an ASPARAGINE-RICH PROTEIN that is involved in the regulation of abscisic acid signaling, that is also differentially expressed. We also found ppe-miR2275 was significantly upregulated at ecodormancy. It is a homolog of rice miR2275, which is primarily expressed in rice anthers during pollen development, suggesting pollen development may be initiated at ecodormancy in peach. Of 791 predicted lncRNAs, 72 were significantly induced at ecodormancy and their co-localized genes are enriched in flavonoid biosynthesis. Two lncRNAs significantly upregulated at ecodormancy interact with ppe-miR2275, acting as a potential regulator of miRNA expression. Our findings of microRNA and lncRNA expression patterns over peach bud dormancy progression suggested that the pollen development may be a critical signal of endodormancy to ecodormancy transition.