Integrated transcriptome, metabolome and phytohormone analysis reveals developmental differences between the first and secondary flowering in Castanea mollissima

Chestnut ( BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern China re-flower in the late summer. On the one hand, the second flowering consumes a lot of nutrients in the tree, weakening the tree and thus...

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Published in:	Frontiers in plant science Vol. 14; p. 1145418
Main Authors:	Qin, Cai, Du, Tingting, Zhang, Ruiyu, Wang, Qiujie, Liu, Yang, Wang, Tianyi, Cao, Hongyan, Bai, Qian, Zhang, Yu, Su, Shuchai
Format:	Journal Article
Language:	English
Published:	Switzerland Frontiers Media SA 16.03.2023 Frontiers Media S.A
Subjects:	Abscisic acid Autumn Biological clocks Biosynthesis Carotenoids Castanea mollissima Chestnut Circadian rhythm Circadian rhythms Crop yield Differentiation (biology) environment female flower Females Flavonoids Flowering Flowers Flowers & plants Fruits Gene expression Genes Hormones Lipid metabolism Lipids Males Metabolites Nutrients Phenolic acids Phenols phytohormone Phytohormones Plant hormones Plant Science Plants (botany) Proteins secondary flowering Sex Sex differentiation Signal transduction Summer Temperature Transcriptomes Trees environment chestnut metabolites secondary flowering female flower phytohormone
ISSN:	1664-462X, 1664-462X
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Abstract	Chestnut ( BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern China re-flower in the late summer. On the one hand, the second flowering consumes a lot of nutrients in the tree, weakening the tree and thus affecting flowering in the following year. On the other hand, the number of female flowers on a single bearing branch during the second flowering is significantly higher than that of the first flowering, which can bear fruit in bunches. Therefore, these can be used to study the sex differentiation of chestnut. In this study, the transcriptomes, metabolomes, and phytohormones of male and female chestnut flowers were determined during spring and late summer. We aimed to understand the developmental differences between the first and secondary flowering stages in chestnuts. We analysed the reasons why the number of female flowers is higher in the secondary flowering than in the first flowering and found ways to increase the number of female flowers or decrease the number of male flowers in chestnuts. Transcriptome analysis of male and female flowers in different developmental seasons revealed that EREBP-like mainly affected the development of secondary female flowers and HSP20 mainly affected the development of secondary male flowers. KEGG enrichment analysis showed that 147 common differentially-regulated genes were mainly enriched from circadian rhythm-plant, carotenoid biosynthesis, phenylpropanoid biosynthesis, and plant hormone signal transduction pathways. Metabolome analysis showed that the main differentially accumulated metabolites in female flowers were flavonoids and phenolic acids, whereas the main differentially accumulated metabolites in male flowers were lipids, flavonoids, and phenolic acids. These genes and their metabolites are positively correlated with secondary flower formation. Phytohormone analysis showed that abscisic and salicylic acids were negatively correlated with secondary flower formation. MYB305, a candidate gene for sex differentiation in chestnuts, promoted the synthesis of flavonoid substances and thus increased the number of female flowers. We constructed a regulatory network for secondary flower development in chestnuts, which provides a theoretical basis for the reproductive development mechanism of chestnuts. This study has important practical implications for improving chestnut yield and quality.
AbstractList	IntroductionChestnut ( Castanea mollissima BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern China re-flower in the late summer. On the one hand, the second flowering consumes a lot of nutrients in the tree, weakening the tree and thus affecting flowering in the following year. On the other hand, the number of female flowers on a single bearing branch during the second flowering is significantly higher than that of the first flowering, which can bear fruit in bunches. Therefore, these can be used to study the sex differentiation of chestnut.MethodsIn this study, the transcriptomes, metabolomes, and phytohormones of male and female chestnut flowers were determined during spring and late summer. We aimed to understand the developmental differences between the first and secondary flowering stages in chestnuts. We analysed the reasons why the number of female flowers is higher in the secondary flowering than in the first flowering and found ways to increase the number of female flowers or decrease the number of male flowers in chestnuts.ResultsTranscriptome analysis of male and female flowers in different developmental seasons revealed that EREBP-like mainly affected the development of secondary female flowers and HSP20 mainly affected the development of secondary male flowers. KEGG enrichment analysis showed that 147 common differentially-regulated genes were mainly enriched from circadian rhythm-plant, carotenoid biosynthesis, phenylpropanoid biosynthesis, and plant hormone signal transduction pathways. Metabolome analysis showed that the main differentially accumulated metabolites in female flowers were flavonoids and phenolic acids, whereas the main differentially accumulated metabolites in male flowers were lipids, flavonoids, and phenolic acids. These genes and their metabolites are positively correlated with secondary flower formation. Phytohormone analysis showed that abscisic and salicylic acids were negatively correlated with secondary flower formation. MYB305, a candidate gene for sex differentiation in chestnuts, promoted the synthesis of flavonoid substances and thus increased the number of female flowers.DiscussionWe constructed a regulatory network for secondary flower development in chestnuts, which provides a theoretical basis for the reproductive development mechanism of chestnuts. This study has important practical implications for improving chestnut yield and quality. Chestnut ( BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern China re-flower in the late summer. On the one hand, the second flowering consumes a lot of nutrients in the tree, weakening the tree and thus affecting flowering in the following year. On the other hand, the number of female flowers on a single bearing branch during the second flowering is significantly higher than that of the first flowering, which can bear fruit in bunches. Therefore, these can be used to study the sex differentiation of chestnut. In this study, the transcriptomes, metabolomes, and phytohormones of male and female chestnut flowers were determined during spring and late summer. We aimed to understand the developmental differences between the first and secondary flowering stages in chestnuts. We analysed the reasons why the number of female flowers is higher in the secondary flowering than in the first flowering and found ways to increase the number of female flowers or decrease the number of male flowers in chestnuts. Transcriptome analysis of male and female flowers in different developmental seasons revealed that EREBP-like mainly affected the development of secondary female flowers and HSP20 mainly affected the development of secondary male flowers. KEGG enrichment analysis showed that 147 common differentially-regulated genes were mainly enriched from circadian rhythm-plant, carotenoid biosynthesis, phenylpropanoid biosynthesis, and plant hormone signal transduction pathways. Metabolome analysis showed that the main differentially accumulated metabolites in female flowers were flavonoids and phenolic acids, whereas the main differentially accumulated metabolites in male flowers were lipids, flavonoids, and phenolic acids. These genes and their metabolites are positively correlated with secondary flower formation. Phytohormone analysis showed that abscisic and salicylic acids were negatively correlated with secondary flower formation. MYB305, a candidate gene for sex differentiation in chestnuts, promoted the synthesis of flavonoid substances and thus increased the number of female flowers. We constructed a regulatory network for secondary flower development in chestnuts, which provides a theoretical basis for the reproductive development mechanism of chestnuts. This study has important practical implications for improving chestnut yield and quality. Chestnut (Castanea mollissima BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern China re-flower in the late summer. On the one hand, the second flowering consumes a lot of nutrients in the tree, weakening the tree and thus affecting flowering in the following year. On the other hand, the number of female flowers on a single bearing branch during the second flowering is significantly higher than that of the first flowering, which can bear fruit in bunches. Therefore, these can be used to study the sex differentiation of chestnut.IntroductionChestnut (Castanea mollissima BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern China re-flower in the late summer. On the one hand, the second flowering consumes a lot of nutrients in the tree, weakening the tree and thus affecting flowering in the following year. On the other hand, the number of female flowers on a single bearing branch during the second flowering is significantly higher than that of the first flowering, which can bear fruit in bunches. Therefore, these can be used to study the sex differentiation of chestnut.In this study, the transcriptomes, metabolomes, and phytohormones of male and female chestnut flowers were determined during spring and late summer. We aimed to understand the developmental differences between the first and secondary flowering stages in chestnuts. We analysed the reasons why the number of female flowers is higher in the secondary flowering than in the first flowering and found ways to increase the number of female flowers or decrease the number of male flowers in chestnuts.MethodsIn this study, the transcriptomes, metabolomes, and phytohormones of male and female chestnut flowers were determined during spring and late summer. We aimed to understand the developmental differences between the first and secondary flowering stages in chestnuts. We analysed the reasons why the number of female flowers is higher in the secondary flowering than in the first flowering and found ways to increase the number of female flowers or decrease the number of male flowers in chestnuts.Transcriptome analysis of male and female flowers in different developmental seasons revealed that EREBP-like mainly affected the development of secondary female flowers and HSP20 mainly affected the development of secondary male flowers. KEGG enrichment analysis showed that 147 common differentially-regulated genes were mainly enriched from circadian rhythm-plant, carotenoid biosynthesis, phenylpropanoid biosynthesis, and plant hormone signal transduction pathways. Metabolome analysis showed that the main differentially accumulated metabolites in female flowers were flavonoids and phenolic acids, whereas the main differentially accumulated metabolites in male flowers were lipids, flavonoids, and phenolic acids. These genes and their metabolites are positively correlated with secondary flower formation. Phytohormone analysis showed that abscisic and salicylic acids were negatively correlated with secondary flower formation. MYB305, a candidate gene for sex differentiation in chestnuts, promoted the synthesis of flavonoid substances and thus increased the number of female flowers.ResultsTranscriptome analysis of male and female flowers in different developmental seasons revealed that EREBP-like mainly affected the development of secondary female flowers and HSP20 mainly affected the development of secondary male flowers. KEGG enrichment analysis showed that 147 common differentially-regulated genes were mainly enriched from circadian rhythm-plant, carotenoid biosynthesis, phenylpropanoid biosynthesis, and plant hormone signal transduction pathways. Metabolome analysis showed that the main differentially accumulated metabolites in female flowers were flavonoids and phenolic acids, whereas the main differentially accumulated metabolites in male flowers were lipids, flavonoids, and phenolic acids. These genes and their metabolites are positively correlated with secondary flower formation. Phytohormone analysis showed that abscisic and salicylic acids were negatively correlated with secondary flower formation. MYB305, a candidate gene for sex differentiation in chestnuts, promoted the synthesis of flavonoid substances and thus increased the number of female flowers.We constructed a regulatory network for secondary flower development in chestnuts, which provides a theoretical basis for the reproductive development mechanism of chestnuts. This study has important practical implications for improving chestnut yield and quality.DiscussionWe constructed a regulatory network for secondary flower development in chestnuts, which provides a theoretical basis for the reproductive development mechanism of chestnuts. This study has important practical implications for improving chestnut yield and quality.
Author	Wang, Qiujie Bai, Qian Cao, Hongyan Zhang, Yu Zhang, Ruiyu Liu, Yang Du, Tingting Wang, Tianyi Su, Shuchai Qin, Cai
AuthorAffiliation	Key Laboratory for Silviculture and Conservation, Ministry of Education, Beijing Forestry University , Beijing , China
AuthorAffiliation_xml	– name: Key Laboratory for Silviculture and Conservation, Ministry of Education, Beijing Forestry University , Beijing , China
Author_xml	– sequence: 1 givenname: Cai surname: Qin fullname: Qin, Cai – sequence: 2 givenname: Tingting surname: Du fullname: Du, Tingting – sequence: 3 givenname: Ruiyu surname: Zhang fullname: Zhang, Ruiyu – sequence: 4 givenname: Qiujie surname: Wang fullname: Wang, Qiujie – sequence: 5 givenname: Yang surname: Liu fullname: Liu, Yang – sequence: 6 givenname: Tianyi surname: Wang fullname: Wang, Tianyi – sequence: 7 givenname: Hongyan surname: Cao fullname: Cao, Hongyan – sequence: 8 givenname: Qian surname: Bai fullname: Bai, Qian – sequence: 9 givenname: Yu surname: Zhang fullname: Zhang, Yu – sequence: 10 givenname: Shuchai surname: Su fullname: Su, Shuchai
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/37008486$$D View this record in MEDLINE/PubMed
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Keywords	environment chestnut metabolites secondary flowering female flower phytohormone
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 This article was submitted to Plant Metabolism and Chemodiversity, a section of the journal Frontiers in Plant Science These authors have contributed equally to this work Reviewed by: Youchao Xin, Shandong Agricultural University, China; Deguo Han, Northeast Agricultural University, China Edited by: Chunlong Li, Huazhong Agricultural University, China
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Snippet	Chestnut ( BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut species in northern... IntroductionChestnut ( Castanea mollissima BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some... Chestnut (Castanea mollissima BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some chestnut... IntroductionChestnut (Castanea mollissima BL.) is an important woody grain, and its flower formation has a significant impact on fruit yield and quality. Some...
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SubjectTerms	Abscisic acid Autumn Biological clocks Biosynthesis Carotenoids Castanea mollissima Chestnut Circadian rhythm Circadian rhythms Crop yield Differentiation (biology) environment female flower Females Flavonoids Flowering Flowers Flowers & plants Fruits Gene expression Genes Hormones Lipid metabolism Lipids Males Metabolites Nutrients Phenolic acids Phenols phytohormone Phytohormones Plant hormones Plant Science Plants (botany) Proteins secondary flowering Sex Sex differentiation Signal transduction Summer Temperature Transcriptomes Trees
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Title	Integrated transcriptome, metabolome and phytohormone analysis reveals developmental differences between the first and secondary flowering in Castanea mollissima
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