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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Published inFrontiers in plant science Vol. 13; p. 1082415
Main Authors Guo, Lili, Li, Yuying, Zhang, Chenjie, Wang, Zhanying, Carlson, John E., Yin, Weinlun, Zhang, Xiuxin, Hou, Xiaogai
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 14.12.2022
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Abstract 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.
AbstractList 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.
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.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.
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 'Fengdan', an early-flowering mutant line of 'Fengdan' and late-flowering variety 'Lianhe'. Transcriptome analysis revealed a transcript ( ) which was annotated as a xyloglucan endotransglycosylase/hydrolase precursor and found to be differentially expressed across flower developmental stages in 'Fengdan' and '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 -related, , , , and 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 ' ' and microRNA 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.
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.
Author Zhang, Chenjie
Wang, Zhanying
Li, Yuying
Zhang, Xiuxin
Yin, Weinlun
Guo, Lili
Hou, Xiaogai
Carlson, John E.
AuthorAffiliation 3 Department of Ecosystem Science and Management, Pennsylvania State University , University Park, PA , United States
4 College of Biological Sciences and Technology, Beijing Forestry University , Beijing , China
5 Center of Peony, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science , Beijing , China
1 College of Tree Peony, Henan University of Science and Technology , Luoyang, Henan , China
2 Department of Horticulture, Luoyang Academy of Agricultural and Forestry Sciences , Luoyang, Henan , China
AuthorAffiliation_xml – name: 2 Department of Horticulture, Luoyang Academy of Agricultural and Forestry Sciences , Luoyang, Henan , China
– name: 5 Center of Peony, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science , Beijing , China
– name: 3 Department of Ecosystem Science and Management, Pennsylvania State University , University Park, PA , United States
– name: 4 College of Biological Sciences and Technology, Beijing Forestry University , Beijing , China
– name: 1 College of Tree Peony, Henan University of Science and Technology , Luoyang, Henan , China
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Copyright Copyright © 2022 Guo, Li, Zhang, Wang, Carlson, Yin, Zhang and Hou.
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Keywords senescence
tree peony
floral development
miRNA-target modules
florescence
Language English
License Copyright © 2022 Guo, Li, Zhang, Wang, Carlson, Yin, Zhang and Hou.
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This article was submitted to Plant Bioinformatics, a section of the journal Frontiers in Plant Science
Reviewed by: Qianqian Shi, Northwest A&F University, China; Shiping Cheng, Pingdingshan University, China
Edited by: Hui Song, Qingdao Agricultural University, China
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Snippet As a candidate national flower of China, tree peony has extremely high ornamental, medicinal and oil value. However, the short florescence and rarity of...
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SubjectTerms floral development
florescence
miRNA-target modules
Plant Science
senescence
tree peony
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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
URI https://www.ncbi.nlm.nih.gov/pubmed/36589111
https://www.proquest.com/docview/2760171730
https://pubmed.ncbi.nlm.nih.gov/PMC9795019
https://doaj.org/article/aefd1928ddab4a0a81f66c6b881c6468
Volume 13
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