Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony

As a candidate national flower of China, tree peony has extremely high ornamental, medicinal and oil value. However, the short florescence and rarity of early-flowering and late-flowering varieties restrict further improvement of the economic value of tree peony. Specific miRNAs and their target gen...

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Main Authors: Lili Guo, Yuying Li, Chenjie Zhang, Zhanying Wang, John E. Carlson, Weinlun Yin, Xiuxin Zhang, Xiaogai Hou
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1082415/full
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author Lili Guo
Yuying Li
Chenjie Zhang
Zhanying Wang
John E. Carlson
Weinlun Yin
Xiuxin Zhang
Xiaogai Hou
author_facet Lili Guo
Yuying Li
Chenjie Zhang
Zhanying Wang
John E. Carlson
Weinlun Yin
Xiuxin Zhang
Xiaogai Hou
author_sort Lili Guo
collection DOAJ
description As a candidate national flower of China, tree peony has extremely high ornamental, medicinal and oil value. However, the short florescence and rarity of early-flowering and late-flowering varieties restrict further improvement of the economic value of tree peony. Specific miRNAs and their target genes engaged in tree peony floral florescence, development and senescence remain unknown. This report presents the integrated analysis of the miRNAome, transcriptome and degradome of tree peony petals collected from blooming, initial flowering, full blooming and decay stages in early-flowering variety Paeonia ostii ‘Fengdan’, an early-flowering mutant line of Paeonia ostii ‘Fengdan’ and late-flowering variety Paeonia suffruticosa ‘Lianhe’. Transcriptome analysis revealed a transcript (‘psu.G.00014095’) which was annotated as a xyloglucan endotransglycosylase/hydrolase precursor XTH-25 and found to be differentially expressed across flower developmental stages in Paeonia ostii ‘Fengdan’ and Paeonia suffruticosa ‘Lianhe’. The miRNA-mRNA modules were presented significant enrichment in various pathways such as plant hormone signal transduction, indole alkaloid biosynthesis, arachidonic acid metabolism, folate biosynthesis, fatty acid elongation, and the MAPK signaling pathway. Multiple miRNA-mRNA-TF modules demonstrated the potential functions of MYB-related, bHLH, Trihelix, NAC, GRAS and HD-ZIP TF families in floral florescence, development, and senescence of tree peony. Comparative spatio-temporal expression investigation of eight floral-favored miRNA-target modules suggested that transcript ‘psu.T.00024044’ and microRNA mtr-miR166g-5p are involved in the floral florescence, development and senescence associated agronomic traits of tree peony. The results might accelerate the understanding of the potential regulation mechanism in regards to floral florescence, development and abscission, and supply guidance for tree peony breeding of varieties with later and longer florescence characteristics.
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spelling doaj.art-aefd1928ddab4a0a81f66c6b881c64682022-12-22T03:52:40ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-12-011310.3389/fpls.2022.10824151082415Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peonyLili Guo0Yuying Li1Chenjie Zhang2Zhanying Wang3John E. Carlson4Weinlun Yin5Xiuxin Zhang6Xiaogai Hou7College of Tree Peony, Henan University of Science and Technology, Luoyang, Henan, ChinaCollege of Tree Peony, Henan University of Science and Technology, Luoyang, Henan, ChinaCollege of Tree Peony, Henan University of Science and Technology, Luoyang, Henan, ChinaDepartment of Horticulture, Luoyang Academy of Agricultural and Forestry Sciences, Luoyang, Henan, ChinaDepartment of Ecosystem Science and Management, Pennsylvania State University, University Park, PA, United StatesCollege of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaCenter of Peony, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, ChinaCenter of Peony, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, ChinaAs a candidate national flower of China, tree peony has extremely high ornamental, medicinal and oil value. However, the short florescence and rarity of early-flowering and late-flowering varieties restrict further improvement of the economic value of tree peony. Specific miRNAs and their target genes engaged in tree peony floral florescence, development and senescence remain unknown. This report presents the integrated analysis of the miRNAome, transcriptome and degradome of tree peony petals collected from blooming, initial flowering, full blooming and decay stages in early-flowering variety Paeonia ostii ‘Fengdan’, an early-flowering mutant line of Paeonia ostii ‘Fengdan’ and late-flowering variety Paeonia suffruticosa ‘Lianhe’. Transcriptome analysis revealed a transcript (‘psu.G.00014095’) which was annotated as a xyloglucan endotransglycosylase/hydrolase precursor XTH-25 and found to be differentially expressed across flower developmental stages in Paeonia ostii ‘Fengdan’ and Paeonia suffruticosa ‘Lianhe’. The miRNA-mRNA modules were presented significant enrichment in various pathways such as plant hormone signal transduction, indole alkaloid biosynthesis, arachidonic acid metabolism, folate biosynthesis, fatty acid elongation, and the MAPK signaling pathway. Multiple miRNA-mRNA-TF modules demonstrated the potential functions of MYB-related, bHLH, Trihelix, NAC, GRAS and HD-ZIP TF families in floral florescence, development, and senescence of tree peony. Comparative spatio-temporal expression investigation of eight floral-favored miRNA-target modules suggested that transcript ‘psu.T.00024044’ and microRNA mtr-miR166g-5p are involved in the floral florescence, development and senescence associated agronomic traits of tree peony. The results might accelerate the understanding of the potential regulation mechanism in regards to floral florescence, development and abscission, and supply guidance for tree peony breeding of varieties with later and longer florescence characteristics.https://www.frontiersin.org/articles/10.3389/fpls.2022.1082415/fulltree peonymiRNA-target modulesflorescencefloral developmentsenescence
spellingShingle Lili Guo
Yuying Li
Chenjie Zhang
Zhanying Wang
John E. Carlson
Weinlun Yin
Xiuxin Zhang
Xiaogai Hou
Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony
Frontiers in Plant Science
tree peony
miRNA-target modules
florescence
floral development
senescence
title Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony
title_full Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony
title_fullStr Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony
title_full_unstemmed Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony
title_short Integrated analysis of miRNAome transcriptome and degradome reveals miRNA-target modules governing floral florescence development and senescence across early- and late-flowering genotypes in tree peony
title_sort integrated analysis of mirnaome transcriptome and degradome reveals mirna target modules governing floral florescence development and senescence across early and late flowering genotypes in tree peony
topic tree peony
miRNA-target modules
florescence
floral development
senescence
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1082415/full
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