Three-dimensional reconstruction and multiomics analysis reveal a unique pattern of embryogenesis in Ginkgo biloba
Abstract Ginkgo (Ginkgo biloba L.) is one of the earliest extant species in seed plant phylogeny. Embryo development patterns can provide fundamental evidence for the origin, evolution, and adaptation of seeds. However, the architectural and morphological dynamics during embryogenesis in G. biloba r...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2024-09, Vol.196 (1), p.95-111 |
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| creator | Ma, Lingyu Hu, Zijian Shen, Weiwei Zhang, Yingying Wang, Guangchao Chang, Bang Lu, Jinkai Cui, Yaning Xu, Huimin Feng, Yun Jin, Biao Zhang, Xi Wang, Li Lin, Jinxing |
| description | Abstract
Ginkgo (Ginkgo biloba L.) is one of the earliest extant species in seed plant phylogeny. Embryo development patterns can provide fundamental evidence for the origin, evolution, and adaptation of seeds. However, the architectural and morphological dynamics during embryogenesis in G. biloba remain elusive. Herein, we obtained over 2,200 visual slices from 3 stages of embryo development using micro-computed tomography imaging with improved staining methods. Based on 3-dimensional (3D) spatiotemporal pattern analysis, we found that a shoot apical meristem with 7 highly differentiated leaf primordia, including apical and axillary leaf buds, is present in mature Ginkgo embryos. 3D rendering from the front, top, and side views showed 2 separate transport systems of tracheids located in the hypocotyl and cotyledon, representing a unique pattern of embryogenesis. Furthermore, the morphological dynamic analysis of secretory cavities indicated their strong association with cotyledons during development. In addition, we identified genes GbLBD25a (lateral organ boundaries domain 25a), GbCESA2a (cellulose synthase 2a), GbMYB74c (myeloblastosis 74c), GbPIN2 (PIN-FORMED 2) associated with vascular development regulation, and GbWRKY1 (WRKYGOK 1), GbbHLH12a (basic helix–loop–helix 12a), and GbJAZ4 (jasmonate zim-domain 4) potentially involved in the formation of secretory cavities. Moreover, we found that flavonoid accumulation in mature embryos could enhance postgerminative growth and seedling establishment in harsh environments. Our 3D spatial reconstruction technique combined with multiomics analysis opens avenues for investigating developmental architecture and molecular mechanisms during embryogenesis and lays the foundation for evolutionary studies of embryo development and maturation.
Three-dimensional spatiotemporal pattern analysis reveals a unique pattern of morphogenesis and molecular dynamics of embryonic development states in Ginkgo biloba. |
| doi_str_mv | 10.1093/plphys/kiae219 |
| format | Article |
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Ginkgo (Ginkgo biloba L.) is one of the earliest extant species in seed plant phylogeny. Embryo development patterns can provide fundamental evidence for the origin, evolution, and adaptation of seeds. However, the architectural and morphological dynamics during embryogenesis in G. biloba remain elusive. Herein, we obtained over 2,200 visual slices from 3 stages of embryo development using micro-computed tomography imaging with improved staining methods. Based on 3-dimensional (3D) spatiotemporal pattern analysis, we found that a shoot apical meristem with 7 highly differentiated leaf primordia, including apical and axillary leaf buds, is present in mature Ginkgo embryos. 3D rendering from the front, top, and side views showed 2 separate transport systems of tracheids located in the hypocotyl and cotyledon, representing a unique pattern of embryogenesis. Furthermore, the morphological dynamic analysis of secretory cavities indicated their strong association with cotyledons during development. In addition, we identified genes GbLBD25a (lateral organ boundaries domain 25a), GbCESA2a (cellulose synthase 2a), GbMYB74c (myeloblastosis 74c), GbPIN2 (PIN-FORMED 2) associated with vascular development regulation, and GbWRKY1 (WRKYGOK 1), GbbHLH12a (basic helix–loop–helix 12a), and GbJAZ4 (jasmonate zim-domain 4) potentially involved in the formation of secretory cavities. Moreover, we found that flavonoid accumulation in mature embryos could enhance postgerminative growth and seedling establishment in harsh environments. Our 3D spatial reconstruction technique combined with multiomics analysis opens avenues for investigating developmental architecture and molecular mechanisms during embryogenesis and lays the foundation for evolutionary studies of embryo development and maturation.
Three-dimensional spatiotemporal pattern analysis reveals a unique pattern of morphogenesis and molecular dynamics of embryonic development states in Ginkgo biloba.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1093/plphys/kiae219</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><ispartof>Plant physiology (Bethesda), 2024-09, Vol.196 (1), p.95-111</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c236t-e750d2f80c8a9064bb32977507620b69b62988f780a9a9464af7395c43b48ad83</citedby><cites>FETCH-LOGICAL-c236t-e750d2f80c8a9064bb32977507620b69b62988f780a9a9464af7395c43b48ad83</cites><orcidid>0000-0001-5518-4220 ; 0009-0004-6134-1842 ; 0000-0002-9801-5010 ; 0000-0001-5920-5121 ; 0000-0002-0007-1306 ; 0000-0003-1688-064X ; 0000-0002-7330-334X ; 0000-0002-7615-1230 ; 0000-0001-9338-1356 ; 0000-0002-8711-948X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,1584,27924,27925</link.rule.ids></links><search><creatorcontrib>Ma, Lingyu</creatorcontrib><creatorcontrib>Hu, Zijian</creatorcontrib><creatorcontrib>Shen, Weiwei</creatorcontrib><creatorcontrib>Zhang, Yingying</creatorcontrib><creatorcontrib>Wang, Guangchao</creatorcontrib><creatorcontrib>Chang, Bang</creatorcontrib><creatorcontrib>Lu, Jinkai</creatorcontrib><creatorcontrib>Cui, Yaning</creatorcontrib><creatorcontrib>Xu, Huimin</creatorcontrib><creatorcontrib>Feng, Yun</creatorcontrib><creatorcontrib>Jin, Biao</creatorcontrib><creatorcontrib>Zhang, Xi</creatorcontrib><creatorcontrib>Wang, Li</creatorcontrib><creatorcontrib>Lin, Jinxing</creatorcontrib><title>Three-dimensional reconstruction and multiomics analysis reveal a unique pattern of embryogenesis in Ginkgo biloba</title><title>Plant physiology (Bethesda)</title><description>Abstract
Ginkgo (Ginkgo biloba L.) is one of the earliest extant species in seed plant phylogeny. Embryo development patterns can provide fundamental evidence for the origin, evolution, and adaptation of seeds. However, the architectural and morphological dynamics during embryogenesis in G. biloba remain elusive. Herein, we obtained over 2,200 visual slices from 3 stages of embryo development using micro-computed tomography imaging with improved staining methods. Based on 3-dimensional (3D) spatiotemporal pattern analysis, we found that a shoot apical meristem with 7 highly differentiated leaf primordia, including apical and axillary leaf buds, is present in mature Ginkgo embryos. 3D rendering from the front, top, and side views showed 2 separate transport systems of tracheids located in the hypocotyl and cotyledon, representing a unique pattern of embryogenesis. Furthermore, the morphological dynamic analysis of secretory cavities indicated their strong association with cotyledons during development. In addition, we identified genes GbLBD25a (lateral organ boundaries domain 25a), GbCESA2a (cellulose synthase 2a), GbMYB74c (myeloblastosis 74c), GbPIN2 (PIN-FORMED 2) associated with vascular development regulation, and GbWRKY1 (WRKYGOK 1), GbbHLH12a (basic helix–loop–helix 12a), and GbJAZ4 (jasmonate zim-domain 4) potentially involved in the formation of secretory cavities. Moreover, we found that flavonoid accumulation in mature embryos could enhance postgerminative growth and seedling establishment in harsh environments. Our 3D spatial reconstruction technique combined with multiomics analysis opens avenues for investigating developmental architecture and molecular mechanisms during embryogenesis and lays the foundation for evolutionary studies of embryo development and maturation.
Three-dimensional spatiotemporal pattern analysis reveals a unique pattern of morphogenesis and molecular dynamics of embryonic development states in Ginkgo biloba.</description><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkDtPwzAUhS0EEqWwMnuEIa0fedgjqqAgVWIpc2Q7Tmvq2MFOkPLvcZXuTPfco-9cXR0AHjFaYcTpurf9cYrrkxGaYH4FFrigJCNFzq7BAqGkEWP8FtzF-I0QwhTnCxD2x6B11phOu2i8ExYGrbyLQxjVkAwoXAO70SbdGRXTKuwUTUzYr060gKMzP6OGvRgGHRz0LdSdDJM_aKfPoHFwa9zp4KE01ktxD25aYaN-uMwl-Hp73W_es93n9mPzsssUoeWQ6apADWkZUkxwVOZSUsKrZFYlQbLksiScsbZiSHDB8zIXbUV5oXIqcyYaRpfgab7bB58ejEPdmai0tcJpP8aaohwTSoqCJHQ1oyr4GINu6z6YToSpxqg-l1vP5daXclPgeQ74sf-P_QOpSYAH</recordid><startdate>20240902</startdate><enddate>20240902</enddate><creator>Ma, Lingyu</creator><creator>Hu, Zijian</creator><creator>Shen, Weiwei</creator><creator>Zhang, Yingying</creator><creator>Wang, Guangchao</creator><creator>Chang, Bang</creator><creator>Lu, Jinkai</creator><creator>Cui, Yaning</creator><creator>Xu, Huimin</creator><creator>Feng, Yun</creator><creator>Jin, Biao</creator><creator>Zhang, Xi</creator><creator>Wang, Li</creator><creator>Lin, Jinxing</creator><general>Oxford University Press</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5518-4220</orcidid><orcidid>https://orcid.org/0009-0004-6134-1842</orcidid><orcidid>https://orcid.org/0000-0002-9801-5010</orcidid><orcidid>https://orcid.org/0000-0001-5920-5121</orcidid><orcidid>https://orcid.org/0000-0002-0007-1306</orcidid><orcidid>https://orcid.org/0000-0003-1688-064X</orcidid><orcidid>https://orcid.org/0000-0002-7330-334X</orcidid><orcidid>https://orcid.org/0000-0002-7615-1230</orcidid><orcidid>https://orcid.org/0000-0001-9338-1356</orcidid><orcidid>https://orcid.org/0000-0002-8711-948X</orcidid></search><sort><creationdate>20240902</creationdate><title>Three-dimensional reconstruction and multiomics analysis reveal a unique pattern of embryogenesis in Ginkgo biloba</title><author>Ma, Lingyu ; Hu, Zijian ; Shen, Weiwei ; Zhang, Yingying ; Wang, Guangchao ; Chang, Bang ; Lu, Jinkai ; Cui, Yaning ; Xu, Huimin ; Feng, Yun ; Jin, Biao ; Zhang, Xi ; Wang, Li ; Lin, Jinxing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c236t-e750d2f80c8a9064bb32977507620b69b62988f780a9a9464af7395c43b48ad83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ma, Lingyu</creatorcontrib><creatorcontrib>Hu, Zijian</creatorcontrib><creatorcontrib>Shen, Weiwei</creatorcontrib><creatorcontrib>Zhang, Yingying</creatorcontrib><creatorcontrib>Wang, Guangchao</creatorcontrib><creatorcontrib>Chang, Bang</creatorcontrib><creatorcontrib>Lu, Jinkai</creatorcontrib><creatorcontrib>Cui, Yaning</creatorcontrib><creatorcontrib>Xu, Huimin</creatorcontrib><creatorcontrib>Feng, Yun</creatorcontrib><creatorcontrib>Jin, Biao</creatorcontrib><creatorcontrib>Zhang, Xi</creatorcontrib><creatorcontrib>Wang, Li</creatorcontrib><creatorcontrib>Lin, Jinxing</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, Lingyu</au><au>Hu, Zijian</au><au>Shen, Weiwei</au><au>Zhang, Yingying</au><au>Wang, Guangchao</au><au>Chang, Bang</au><au>Lu, Jinkai</au><au>Cui, Yaning</au><au>Xu, Huimin</au><au>Feng, Yun</au><au>Jin, Biao</au><au>Zhang, Xi</au><au>Wang, Li</au><au>Lin, Jinxing</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Three-dimensional reconstruction and multiomics analysis reveal a unique pattern of embryogenesis in Ginkgo biloba</atitle><jtitle>Plant physiology (Bethesda)</jtitle><date>2024-09-02</date><risdate>2024</risdate><volume>196</volume><issue>1</issue><spage>95</spage><epage>111</epage><pages>95-111</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><abstract>Abstract
Ginkgo (Ginkgo biloba L.) is one of the earliest extant species in seed plant phylogeny. Embryo development patterns can provide fundamental evidence for the origin, evolution, and adaptation of seeds. However, the architectural and morphological dynamics during embryogenesis in G. biloba remain elusive. Herein, we obtained over 2,200 visual slices from 3 stages of embryo development using micro-computed tomography imaging with improved staining methods. Based on 3-dimensional (3D) spatiotemporal pattern analysis, we found that a shoot apical meristem with 7 highly differentiated leaf primordia, including apical and axillary leaf buds, is present in mature Ginkgo embryos. 3D rendering from the front, top, and side views showed 2 separate transport systems of tracheids located in the hypocotyl and cotyledon, representing a unique pattern of embryogenesis. Furthermore, the morphological dynamic analysis of secretory cavities indicated their strong association with cotyledons during development. In addition, we identified genes GbLBD25a (lateral organ boundaries domain 25a), GbCESA2a (cellulose synthase 2a), GbMYB74c (myeloblastosis 74c), GbPIN2 (PIN-FORMED 2) associated with vascular development regulation, and GbWRKY1 (WRKYGOK 1), GbbHLH12a (basic helix–loop–helix 12a), and GbJAZ4 (jasmonate zim-domain 4) potentially involved in the formation of secretory cavities. Moreover, we found that flavonoid accumulation in mature embryos could enhance postgerminative growth and seedling establishment in harsh environments. Our 3D spatial reconstruction technique combined with multiomics analysis opens avenues for investigating developmental architecture and molecular mechanisms during embryogenesis and lays the foundation for evolutionary studies of embryo development and maturation.
Three-dimensional spatiotemporal pattern analysis reveals a unique pattern of morphogenesis and molecular dynamics of embryonic development states in Ginkgo biloba.</abstract><cop>US</cop><pub>Oxford University Press</pub><doi>10.1093/plphys/kiae219</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-5518-4220</orcidid><orcidid>https://orcid.org/0009-0004-6134-1842</orcidid><orcidid>https://orcid.org/0000-0002-9801-5010</orcidid><orcidid>https://orcid.org/0000-0001-5920-5121</orcidid><orcidid>https://orcid.org/0000-0002-0007-1306</orcidid><orcidid>https://orcid.org/0000-0003-1688-064X</orcidid><orcidid>https://orcid.org/0000-0002-7330-334X</orcidid><orcidid>https://orcid.org/0000-0002-7615-1230</orcidid><orcidid>https://orcid.org/0000-0001-9338-1356</orcidid><orcidid>https://orcid.org/0000-0002-8711-948X</orcidid></addata></record> |
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| title | Three-dimensional reconstruction and multiomics analysis reveal a unique pattern of embryogenesis in Ginkgo biloba |
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