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

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 flor...

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Main Authors: Ekaterina Shor, Oded Skaliter, Elad Sharon, Yaarit Kitsberg, Dominika Bednarczyk, Shane Kerzner, Danny Vainstein, Yuval Tabach, Alexander Vainstein
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1180899/full
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author Ekaterina Shor
Oded Skaliter
Elad Sharon
Elad Sharon
Yaarit Kitsberg
Dominika Bednarczyk
Shane Kerzner
Danny Vainstein
Yuval Tabach
Alexander Vainstein
author_facet Ekaterina Shor
Oded Skaliter
Elad Sharon
Elad Sharon
Yaarit Kitsberg
Dominika Bednarczyk
Shane Kerzner
Danny Vainstein
Yuval Tabach
Alexander Vainstein
author_sort Ekaterina Shor
collection DOAJ
description 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.
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spelling doaj.art-d6849bc691f14e4e8cb49dc83cbde9862023-06-08T11:47:08ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-06-011410.3389/fpls.2023.11808991180899Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 proteinEkaterina Shor0Oded Skaliter1Elad Sharon2Elad Sharon3Yaarit Kitsberg4Dominika Bednarczyk5Shane Kerzner6Danny Vainstein7Yuval Tabach8Alexander Vainstein9The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelThe Institute for Medical Research, Israel-Canada, Hadassah Medical School, The Hebrew University of Jerusalem, Jerusalem, IsraelThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelSchool of Computer Science, Tel Aviv University, Tel Aviv, IsraelThe Institute for Medical Research, Israel-Canada, Hadassah Medical School, The Hebrew University of Jerusalem, Jerusalem, IsraelThe Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelIn 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.https://www.frontiersin.org/articles/10.3389/fpls.2023.1180899/fulltranscriptomedaytimeflower developmentregulationpetunia scent
spellingShingle Ekaterina Shor
Oded Skaliter
Elad Sharon
Elad Sharon
Yaarit Kitsberg
Dominika Bednarczyk
Shane Kerzner
Danny Vainstein
Yuval Tabach
Alexander Vainstein
Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 protein
Frontiers in Plant Science
transcriptome
daytime
flower development
regulation
petunia scent
title Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 protein
title_full Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 protein
title_fullStr Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 protein
title_full_unstemmed Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 protein
title_short Developmental and temporal changes in petunia petal transcriptome reveal scent-repressing plant-specific RING–kinase–WD40 protein
title_sort developmental and temporal changes in petunia petal transcriptome reveal scent repressing plant specific ring kinase wd40 protein
topic transcriptome
daytime
flower development
regulation
petunia scent
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1180899/full
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