Laser capture microdissection‐based spatiotemporal transcriptomes uncover regulatory networks during seed abortion in seedless Ponkan (Citrus reticulata)
SUMMARY Seed abortion is an important process in the formation of seedless characteristics in citrus fruits. However, the molecular regulatory mechanism underlying citrus seed abortion is poorly understood. Laser capture microdissection‐based RNA‐seq combined with Pacbio‐seq was used to profile seed...
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| Veröffentlicht in: | The Plant journal : for cell and molecular biology 2023-08, Vol.115 (3), p.642-661 |
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| container_title | The Plant journal : for cell and molecular biology |
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| creator | Lu, Liqing Yang, Haijian Xu, Yanhui Zhang, Li Wu, Juxun Yi, Hualin |
| description | SUMMARY
Seed abortion is an important process in the formation of seedless characteristics in citrus fruits. However, the molecular regulatory mechanism underlying citrus seed abortion is poorly understood. Laser capture microdissection‐based RNA‐seq combined with Pacbio‐seq was used to profile seed development in the Ponkan cultivars ‘Huagan No. 4’ (seedless Ponkan) (Citrus reticulata) and ‘E'gan No. 1’ (seeded Ponkan) (C. reticulata) in two types of seed tissue across three developmental stages. Through comparative transcriptome and dynamic phytohormone analyses, plant hormone signal, cell division and nutrient metabolism‐related processes were revealed to play critical roles in the seed abortion of ‘Huagan No. 4’. Moreover, several genes may play indispensable roles in seed abortion of ‘Huagan No. 4’, such as CrWRKY74, CrWRKY48 and CrMYB3R4. Overexpression of CrWRKY74 in Arabidopsis resulted in severe seed abortion. By analyzing the downstream regulatory network, we further determined that CrWRKY74 participated in seed abortion regulation by inducing abnormal programmed cell death. Of particular importance is that a preliminary model was proposed to depict the regulatory networks underlying seed abortion in citrus. The results of this study provide novel insights into the molecular mechanism across citrus seed development, and reveal the master role of CrWRKY74 in seed abortion of ‘Huagan No. 4’.
Significance Statement
The seedless character of citrus has important economic value and is favored by consumers, but the formation process of its internal mechanism still lacks understanding. In this study, the molecular mechanism of seed abortion in seedless Ponkan caused by abnormal programmed cell death was preliminarily analyzed by functional genomics, cytological morphological observation, physiological and biochemical assays, as well as stable genetic transformation. |
| doi_str_mv | 10.1111/tpj.16251 |
| format | Article |
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Seed abortion is an important process in the formation of seedless characteristics in citrus fruits. However, the molecular regulatory mechanism underlying citrus seed abortion is poorly understood. Laser capture microdissection‐based RNA‐seq combined with Pacbio‐seq was used to profile seed development in the Ponkan cultivars ‘Huagan No. 4’ (seedless Ponkan) (Citrus reticulata) and ‘E'gan No. 1’ (seeded Ponkan) (C. reticulata) in two types of seed tissue across three developmental stages. Through comparative transcriptome and dynamic phytohormone analyses, plant hormone signal, cell division and nutrient metabolism‐related processes were revealed to play critical roles in the seed abortion of ‘Huagan No. 4’. Moreover, several genes may play indispensable roles in seed abortion of ‘Huagan No. 4’, such as CrWRKY74, CrWRKY48 and CrMYB3R4. Overexpression of CrWRKY74 in Arabidopsis resulted in severe seed abortion. By analyzing the downstream regulatory network, we further determined that CrWRKY74 participated in seed abortion regulation by inducing abnormal programmed cell death. Of particular importance is that a preliminary model was proposed to depict the regulatory networks underlying seed abortion in citrus. The results of this study provide novel insights into the molecular mechanism across citrus seed development, and reveal the master role of CrWRKY74 in seed abortion of ‘Huagan No. 4’.
Significance Statement
The seedless character of citrus has important economic value and is favored by consumers, but the formation process of its internal mechanism still lacks understanding. In this study, the molecular mechanism of seed abortion in seedless Ponkan caused by abnormal programmed cell death was preliminarily analyzed by functional genomics, cytological morphological observation, physiological and biochemical assays, as well as stable genetic transformation.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16251</identifier><identifier>PMID: 37077034</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Abortion ; Apoptosis ; Cell death ; Cell division ; Citrus - metabolism ; Citrus fruits ; Citrus reticulata ; CrWRKY74 ; Cultivars ; Developmental stages ; Fruit - metabolism ; Fruits ; Gene Expression Regulation, Plant ; Gene Regulatory Networks ; Laser Capture Microdissection ; Molecular modelling ; Phytochrome - genetics ; Phytochrome - metabolism ; Phytohormones ; Plant hormones ; programmed cell death ; Regulatory mechanisms (biology) ; seed abortion ; seedless citrus ; Seeds - metabolism ; Transcriptome ; Transcriptomes</subject><ispartof>The Plant journal : for cell and molecular biology, 2023-08, Vol.115 (3), p.642-661</ispartof><rights>2023 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2023 Society for Experimental Biology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3531-2cc53a64b0243df5a35a0b3b48b85dffc052be08ca4bec0cc391273e0e7f8db43</citedby><cites>FETCH-LOGICAL-c3531-2cc53a64b0243df5a35a0b3b48b85dffc052be08ca4bec0cc391273e0e7f8db43</cites><orcidid>0000-0001-7420-0548 ; 0000-0003-0785-1927</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.16251$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.16251$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27903,27904,45553,45554,46388,46812</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37077034$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lu, Liqing</creatorcontrib><creatorcontrib>Yang, Haijian</creatorcontrib><creatorcontrib>Xu, Yanhui</creatorcontrib><creatorcontrib>Zhang, Li</creatorcontrib><creatorcontrib>Wu, Juxun</creatorcontrib><creatorcontrib>Yi, Hualin</creatorcontrib><title>Laser capture microdissection‐based spatiotemporal transcriptomes uncover regulatory networks during seed abortion in seedless Ponkan (Citrus reticulata)</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Seed abortion is an important process in the formation of seedless characteristics in citrus fruits. However, the molecular regulatory mechanism underlying citrus seed abortion is poorly understood. Laser capture microdissection‐based RNA‐seq combined with Pacbio‐seq was used to profile seed development in the Ponkan cultivars ‘Huagan No. 4’ (seedless Ponkan) (Citrus reticulata) and ‘E'gan No. 1’ (seeded Ponkan) (C. reticulata) in two types of seed tissue across three developmental stages. Through comparative transcriptome and dynamic phytohormone analyses, plant hormone signal, cell division and nutrient metabolism‐related processes were revealed to play critical roles in the seed abortion of ‘Huagan No. 4’. Moreover, several genes may play indispensable roles in seed abortion of ‘Huagan No. 4’, such as CrWRKY74, CrWRKY48 and CrMYB3R4. Overexpression of CrWRKY74 in Arabidopsis resulted in severe seed abortion. By analyzing the downstream regulatory network, we further determined that CrWRKY74 participated in seed abortion regulation by inducing abnormal programmed cell death. Of particular importance is that a preliminary model was proposed to depict the regulatory networks underlying seed abortion in citrus. The results of this study provide novel insights into the molecular mechanism across citrus seed development, and reveal the master role of CrWRKY74 in seed abortion of ‘Huagan No. 4’.
Significance Statement
The seedless character of citrus has important economic value and is favored by consumers, but the formation process of its internal mechanism still lacks understanding. In this study, the molecular mechanism of seed abortion in seedless Ponkan caused by abnormal programmed cell death was preliminarily analyzed by functional genomics, cytological morphological observation, physiological and biochemical assays, as well as stable genetic transformation.</description><subject>Abortion</subject><subject>Apoptosis</subject><subject>Cell death</subject><subject>Cell division</subject><subject>Citrus - metabolism</subject><subject>Citrus fruits</subject><subject>Citrus reticulata</subject><subject>CrWRKY74</subject><subject>Cultivars</subject><subject>Developmental stages</subject><subject>Fruit - metabolism</subject><subject>Fruits</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Regulatory Networks</subject><subject>Laser Capture Microdissection</subject><subject>Molecular modelling</subject><subject>Phytochrome - genetics</subject><subject>Phytochrome - metabolism</subject><subject>Phytohormones</subject><subject>Plant hormones</subject><subject>programmed cell death</subject><subject>Regulatory mechanisms (biology)</subject><subject>seed abortion</subject><subject>seedless citrus</subject><subject>Seeds - metabolism</subject><subject>Transcriptome</subject><subject>Transcriptomes</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kbtuFDEUhi0EIptAwQsgSzRJMYk99txKtOKqlUgRJLqR7TkTeTNjDz52ou14BHreLk-CNxsokHBj-fjTp6P_J-QVZ-c8n4u4bM95XVb8CVlxUVeF4OLbU7JiXc2KRvLyiBwjbhnjjajlc3IkGtY0TMgV-bVRCIEatcQUgM7WBD9YRDDRenf_46fO_wPFReV3hHnxQU00BuXQBLtEPwPS5Iy_zZYA12lS0YcddRDvfLhBOqRg3TVFyBalfdhrqXUPgwkQ6aV3N8rR07WNIWF2RGv2FnX2gjwb1YTw8vE-IV_fv7tafyw2Xz58Wr_dFEZUghelMZVQtdSslGIYKyUqxbTQstVtNYyjYVWpgbVGSQ2GGSM6XjYCGDRjO2gpTsjpwbsE_z0Bxn62aGCalAOfsC9bJrocby0y-uYfdOtTcHm7TEnedV1Zt5k6O1A5TMQAY78EO6uw6znr9431ubH-obHMvn40Jj3D8Jf8U1EGLg7AnZ1g939Tf3X5-aD8Dag4peI</recordid><startdate>202308</startdate><enddate>202308</enddate><creator>Lu, Liqing</creator><creator>Yang, Haijian</creator><creator>Xu, Yanhui</creator><creator>Zhang, Li</creator><creator>Wu, Juxun</creator><creator>Yi, Hualin</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7420-0548</orcidid><orcidid>https://orcid.org/0000-0003-0785-1927</orcidid></search><sort><creationdate>202308</creationdate><title>Laser capture microdissection‐based spatiotemporal transcriptomes uncover regulatory networks during seed abortion in seedless Ponkan (Citrus reticulata)</title><author>Lu, Liqing ; Yang, Haijian ; Xu, Yanhui ; Zhang, Li ; Wu, Juxun ; Yi, Hualin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3531-2cc53a64b0243df5a35a0b3b48b85dffc052be08ca4bec0cc391273e0e7f8db43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Abortion</topic><topic>Apoptosis</topic><topic>Cell death</topic><topic>Cell division</topic><topic>Citrus - metabolism</topic><topic>Citrus fruits</topic><topic>Citrus reticulata</topic><topic>CrWRKY74</topic><topic>Cultivars</topic><topic>Developmental stages</topic><topic>Fruit - metabolism</topic><topic>Fruits</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Regulatory Networks</topic><topic>Laser Capture Microdissection</topic><topic>Molecular modelling</topic><topic>Phytochrome - genetics</topic><topic>Phytochrome - metabolism</topic><topic>Phytohormones</topic><topic>Plant hormones</topic><topic>programmed cell death</topic><topic>Regulatory mechanisms (biology)</topic><topic>seed abortion</topic><topic>seedless citrus</topic><topic>Seeds - metabolism</topic><topic>Transcriptome</topic><topic>Transcriptomes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lu, Liqing</creatorcontrib><creatorcontrib>Yang, Haijian</creatorcontrib><creatorcontrib>Xu, Yanhui</creatorcontrib><creatorcontrib>Zhang, Li</creatorcontrib><creatorcontrib>Wu, Juxun</creatorcontrib><creatorcontrib>Yi, Hualin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lu, Liqing</au><au>Yang, Haijian</au><au>Xu, Yanhui</au><au>Zhang, Li</au><au>Wu, Juxun</au><au>Yi, Hualin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Laser capture microdissection‐based spatiotemporal transcriptomes uncover regulatory networks during seed abortion in seedless Ponkan (Citrus reticulata)</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2023-08</date><risdate>2023</risdate><volume>115</volume><issue>3</issue><spage>642</spage><epage>661</epage><pages>642-661</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Seed abortion is an important process in the formation of seedless characteristics in citrus fruits. However, the molecular regulatory mechanism underlying citrus seed abortion is poorly understood. Laser capture microdissection‐based RNA‐seq combined with Pacbio‐seq was used to profile seed development in the Ponkan cultivars ‘Huagan No. 4’ (seedless Ponkan) (Citrus reticulata) and ‘E'gan No. 1’ (seeded Ponkan) (C. reticulata) in two types of seed tissue across three developmental stages. Through comparative transcriptome and dynamic phytohormone analyses, plant hormone signal, cell division and nutrient metabolism‐related processes were revealed to play critical roles in the seed abortion of ‘Huagan No. 4’. Moreover, several genes may play indispensable roles in seed abortion of ‘Huagan No. 4’, such as CrWRKY74, CrWRKY48 and CrMYB3R4. Overexpression of CrWRKY74 in Arabidopsis resulted in severe seed abortion. By analyzing the downstream regulatory network, we further determined that CrWRKY74 participated in seed abortion regulation by inducing abnormal programmed cell death. Of particular importance is that a preliminary model was proposed to depict the regulatory networks underlying seed abortion in citrus. The results of this study provide novel insights into the molecular mechanism across citrus seed development, and reveal the master role of CrWRKY74 in seed abortion of ‘Huagan No. 4’.
Significance Statement
The seedless character of citrus has important economic value and is favored by consumers, but the formation process of its internal mechanism still lacks understanding. In this study, the molecular mechanism of seed abortion in seedless Ponkan caused by abnormal programmed cell death was preliminarily analyzed by functional genomics, cytological morphological observation, physiological and biochemical assays, as well as stable genetic transformation.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>37077034</pmid><doi>10.1111/tpj.16251</doi><tpages>661</tpages><orcidid>https://orcid.org/0000-0001-7420-0548</orcidid><orcidid>https://orcid.org/0000-0003-0785-1927</orcidid></addata></record> |
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| source | MEDLINE; IngentaConnect Open Access Journals; Wiley Online Library Journals Frontfile Complete; EZB-FREE-00999 freely available EZB journals; Wiley Open Access |
| subjects | Abortion Apoptosis Cell death Cell division Citrus - metabolism Citrus fruits Citrus reticulata CrWRKY74 Cultivars Developmental stages Fruit - metabolism Fruits Gene Expression Regulation, Plant Gene Regulatory Networks Laser Capture Microdissection Molecular modelling Phytochrome - genetics Phytochrome - metabolism Phytohormones Plant hormones programmed cell death Regulatory mechanisms (biology) seed abortion seedless citrus Seeds - metabolism Transcriptome Transcriptomes |
| title | Laser capture microdissection‐based spatiotemporal transcriptomes uncover regulatory networks during seed abortion in seedless Ponkan (Citrus reticulata) |
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