Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis

IntroductionOrchids are renowned for their intricate floral structures, where sepals and petals contribute significantly to ornamental value and pollinator attraction. In Dendrobium Section Spatulata, the distinctive curvature of these floral organs enhances both aesthetic appeal and pollination eff...

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Main Authors: Xuefeng Qu, Na Li, Cong Xu, Zifeng Huang, Chunyan Li, Yang Jiang, Guizhao Zheng, Haiping Fu, Guangyan Zhang, Chuan Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1497230/full
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author Xuefeng Qu
Na Li
Cong Xu
Zifeng Huang
Chunyan Li
Yang Jiang
Guizhao Zheng
Haiping Fu
Guangyan Zhang
Chuan Liu
author_facet Xuefeng Qu
Na Li
Cong Xu
Zifeng Huang
Chunyan Li
Yang Jiang
Guizhao Zheng
Haiping Fu
Guangyan Zhang
Chuan Liu
author_sort Xuefeng Qu
collection DOAJ
description IntroductionOrchids are renowned for their intricate floral structures, where sepals and petals contribute significantly to ornamental value and pollinator attraction. In Dendrobium Section Spatulata, the distinctive curvature of these floral organs enhances both aesthetic appeal and pollination efficiency. However, the molecular and cellular mechanisms underlying this trait remain poorly understood.MethodsMorphological characteristics of five hybrids were analyzed, with a particular focus on hybrid H5, which exhibits pronounced sepal curling. Full-length transcriptomic sequencing was employed to assemble a reference transcriptome, while RNA-seq identified differentially expressed genes (DEGs) between sepals and petals. Gene ontology and pathway enrichment analyses were conducted to uncover biological processes associated with sepal curvature. Cytological microscopy was used to examine cell size and number, and quantitative real-time PCR (qRT-PCR) was performed to validate transcriptomic findings.ResultsThe reference transcriptome contained 94,258 non-redundant transcripts, and RNA-seq identified 821 DEGs between sepals and petals, with 72.8% of these upregulated in sepals. Enrichment analysis revealed the significant involvement of DEGs in cytokinesis, cytoskeletal organization, and energy metabolism. Notably, myosin II filament organization was implicated in generating the mechanical forces responsible for curling, while metabolic pathways provided the energy necessary for these developmental processes. Cytological observations showed that the upper cell layers of the sepal were smaller and more numerous than the lower layers, indicating that differential cell growth contributes to sepal curvature. qRT-PCR analysis validated the differential expression of selected genes, supporting the transcriptomic findings.DiscussionThe interplay of cellular mechanics, cytoskeletal dynamics, and metabolic regulation is crucial in shaping sepal morphology. Future studies involving gene knockdown or overexpression experiments are recommended to validate the roles of specific genes in processes such as actin organization and myosin activity. Such work would provide deeper insights into the contributions of cytoskeletal dynamics and mechanical force generation to sepal morphogenesis.
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spelling doaj-art-2079f575deba42e09a1fd8c4eabdbb0b2024-12-13T04:17:10ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-12-011510.3389/fpls.2024.14972301497230Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysisXuefeng Qu0Na Li1Cong Xu2Zifeng Huang3Chunyan Li4Yang Jiang5Guizhao Zheng6Haiping Fu7Guangyan Zhang8Chuan Liu9Dongguan Research Center of Agricultural Sciences, Dongguan, Guangdong, ChinaChongqing Key Laboratory of Big Data for Bio Intelligence, Chongqing University of Posts and Telecommunications, Chongqing, ChinaDongguan Research Center of Agricultural Sciences, Dongguan, Guangdong, ChinaDongguan Research Center of Agricultural Sciences, Dongguan, Guangdong, ChinaChongqing Key Laboratory of Big Data for Bio Intelligence, Chongqing University of Posts and Telecommunications, Chongqing, ChinaChongqing Key Laboratory of Big Data for Bio Intelligence, Chongqing University of Posts and Telecommunications, Chongqing, ChinaDongguan Research Center of Agricultural Sciences, Dongguan, Guangdong, ChinaDongguan Research Center of Agricultural Sciences, Dongguan, Guangdong, ChinaDongguan Research Center of Agricultural Sciences, Dongguan, Guangdong, ChinaChongqing Key Laboratory of Big Data for Bio Intelligence, Chongqing University of Posts and Telecommunications, Chongqing, ChinaIntroductionOrchids are renowned for their intricate floral structures, where sepals and petals contribute significantly to ornamental value and pollinator attraction. In Dendrobium Section Spatulata, the distinctive curvature of these floral organs enhances both aesthetic appeal and pollination efficiency. However, the molecular and cellular mechanisms underlying this trait remain poorly understood.MethodsMorphological characteristics of five hybrids were analyzed, with a particular focus on hybrid H5, which exhibits pronounced sepal curling. Full-length transcriptomic sequencing was employed to assemble a reference transcriptome, while RNA-seq identified differentially expressed genes (DEGs) between sepals and petals. Gene ontology and pathway enrichment analyses were conducted to uncover biological processes associated with sepal curvature. Cytological microscopy was used to examine cell size and number, and quantitative real-time PCR (qRT-PCR) was performed to validate transcriptomic findings.ResultsThe reference transcriptome contained 94,258 non-redundant transcripts, and RNA-seq identified 821 DEGs between sepals and petals, with 72.8% of these upregulated in sepals. Enrichment analysis revealed the significant involvement of DEGs in cytokinesis, cytoskeletal organization, and energy metabolism. Notably, myosin II filament organization was implicated in generating the mechanical forces responsible for curling, while metabolic pathways provided the energy necessary for these developmental processes. Cytological observations showed that the upper cell layers of the sepal were smaller and more numerous than the lower layers, indicating that differential cell growth contributes to sepal curvature. qRT-PCR analysis validated the differential expression of selected genes, supporting the transcriptomic findings.DiscussionThe interplay of cellular mechanics, cytoskeletal dynamics, and metabolic regulation is crucial in shaping sepal morphology. Future studies involving gene knockdown or overexpression experiments are recommended to validate the roles of specific genes in processes such as actin organization and myosin activity. Such work would provide deeper insights into the contributions of cytoskeletal dynamics and mechanical force generation to sepal morphogenesis.https://www.frontiersin.org/articles/10.3389/fpls.2024.1497230/fullDendrobiumfloral developmentsepal curvaturetranscriptomicscytokinesismyosin filament
spellingShingle Xuefeng Qu
Na Li
Cong Xu
Zifeng Huang
Chunyan Li
Yang Jiang
Guizhao Zheng
Haiping Fu
Guangyan Zhang
Chuan Liu
Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis
Frontiers in Plant Science
Dendrobium
floral development
sepal curvature
transcriptomics
cytokinesis
myosin filament
title Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis
title_full Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis
title_fullStr Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis
title_full_unstemmed Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis
title_short Unveiling the molecular mechanism of sepal curvature in Dendrobium Section Spatulata through full-length transcriptome and RNA-seq analysis
title_sort unveiling the molecular mechanism of sepal curvature in dendrobium section spatulata through full length transcriptome and rna seq analysis
topic Dendrobium
floral development
sepal curvature
transcriptomics
cytokinesis
myosin filament
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1497230/full
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