Beyond dormancy: organ-specific gene regulatory networks control winter development in peach buds

Abstract

Bud dormancy in temperate perennials is often described as a stereotyped state of developmental repression triggered by environmental signals. Here, we investigate the development of vegetative buds in Prunus persica during the cold season to assess whether, like flower buds, they remain transcriptionally active. An integrated approach combining cytological analysis, hormone profiling, transcriptome sequencing, co-expression and gene regulatory network (GRN) inference, and in vivo interaction assays was used to compare bud types. Despite similar levels of abscisic acid and gibberellins during chilling accumulation, vegetative and flower buds displayed divergent transcriptional responses. Vegetative buds activated jasmonate- and photoperiod-responsive gene modules, while floral buds were marked by chilling-responsive modules regulated by SHORT VEGETATIVE PHASE 1 (SVP1). Bimolecular fluorescence complementation confirmed specific interactions between SVP1 and DORMANCY-ASSOCIATED MADS-box (DAM) proteins DAM3, DAM5, and DAM6. GRN analysis highlighted bud-specific combinations of DAM and SVP proteins, with DAM5 and DAM6 homodimers predominant in vegetative buds and DAM4 and SVP1/2 heterodimers dominant in flower buds. Our data revise the classical dormancy paradigm: flower and vegetative buds share hormonal trends yet deploy distinct MADS-box combinations to coordinate environment-dependent winter development. The organ-specific DAM/SVP circuitry uncovered here provides a new framework for mechanistic studies on cold mediated peach bud development.

Acknowledgements

This work was funded by BIRD 2019 and 2020-University of Padova with a grant to BC and SV.

Authors contributions

C.B. and S.V. conceived this study. M.C. and J.J. collected plant material and conducted cytological analysis and preparatory experiments and analyses for RNA-seq. C.B., M.M., and R.A.C. conducted the statistical analysis for RNA-seq WGCNA, and GNR. E.C. performed hormone quantification analysis. J.J., L.C., and G.P. performed the BIFC analysis. C.B. and S.V. wrote the original draft. All authors contributed to manuscript writing and editing.

Data availability

The data that support the findings of this study will be openly available in Gene Expression Omnibus at number GSE298924 for reference RNA-Seq data. Secure token for reviewer access: wjadiggqvfcrpez.

Conflicts of interest statement

The authors declare that they have no conflict of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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