Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING-kinase-WD40 protein

Front Plant Sci. 2023 Jun 8:14:1180899. doi: 10.3389/fpls.2023.1180899. eCollection 2023.

Abstract

In moth-pollinated petunias, production of floral volatiles initiates when the flower opens and occurs rhythmically during the day, for optimal flower-pollinator interaction. To characterize the developmental transcriptomic response to time of day, we generated RNA-Seq databases for corollas of floral buds and mature flowers in the morning and in the evening. Around 70% of transcripts accumulating in petals demonstrated significant changes in expression levels in response to the flowers' transition from a 4.5-cm bud to a flower 1 day postanthesis (1DPA). Overall, 44% of the petal transcripts were differentially expressed in the morning vs. evening. Morning/evening changes were affected by flower developmental stage, with a 2.5-fold larger transcriptomic response to daytime in 1DPA flowers compared to buds. Analyzed genes known to encode enzymes in volatile organic compound biosynthesis were upregulated in 1DPA flowers vs. buds-in parallel with the activation of scent production. Based on analysis of global changes in the petal transcriptome, PhWD2 was identified as a putative scent-related factor. PhWD2 is a protein that is uniquely present in plants and has a three-domain structure: RING-kinase-WD40. Suppression of PhWD2 (termed UPPER - Unique Plant PhEnylpropanoid Regulator) resulted in a significant increase in the levels of volatiles emitted from and accumulated in internal pools, suggesting that it is a negative regulator of petunia floral scent production.

Keywords: daytime; flower development; petunia scent; regulation; transcriptome.

Grants and funding

AV is an incumbent of the Wolfson Chair in Floriculture. This work was supported by the Israel Science Foundation (grant no. 2511/16). EKS was supported by the Lady Davis Fellowship Trust. Work in AV’s laboratory is supported by the Chief Scientist of the Israeli Ministry of Agriculture and Rural Development (no. 20-01-0209) as part of the National Center for Genome Editing in Agriculture.