An integral insight into pollen wall development: involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach
Summary We aimed to understand the underlying mechanisms of development in the sporopollenin‐containing part of the pollen wall, the exine, one of the most complex cell walls in plants. Our hypothesis is that distinct physical processes, phase separation and micellar self‐assembly, underpinexine dev...
Gespeichert in:
Veröffentlicht in: | The Plant journal : for cell and molecular biology 2021-02, Vol.105 (3), p.736-753 |
---|---|
Hauptverfasser: | , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 753 |
---|---|
container_issue | 3 |
container_start_page | 736 |
container_title | The Plant journal : for cell and molecular biology |
container_volume | 105 |
creator | Gabarayeva, Nina I. Grigorjeva, Valentina V. |
description | Summary
We aimed to understand the underlying mechanisms of development in the sporopollenin‐containing part of the pollen wall, the exine, one of the most complex cell walls in plants. Our hypothesis is that distinct physical processes, phase separation and micellar self‐assembly, underpinexine development by taking the molecular building blocks, determined and synthesised by the genome, through several phase transitions. To test this hypothesis, we traced each stage of microspore development in Calycanthus floridus with transmission electron microscopy and then generated in vitro experimental simulations corresponding to every developmental stage. The sequence of structures observed within the periplasmic space around developing microspores starts with spherical units, which are rearranged into columns to then form rod‐like units (the young columellae) and, finally, white line centred endexine lamellae. Phase separation precedes each developmental stage. The set of experimental simulations, obtained as self‐assembled micellar mesophases formed at the interface between lipid and water compartments, was the same: spherical micelles; columns of spherical micelles; cylindrical micelles; and laminate micelles, separated by gaps, resembling white‐lined lamellae. Thus, patterns simulating structures observed at the main stages of exine development in C. floridus were obtained from in vitro experiments, and hence purely physicochemical processes can construct exine‐like patterns. This highlights the important part played by physical processes that are not under direct genomic control and share influence on the emerging ultrastructure with the genome during exine development. These findings suggest that a new approach to ontogenetic studies, including a consideration of physical factors, is required for a better understanding of developmental processes.
Significance Statement
Interdisciplinary research summarizing morphology, ultrastructure, and biological, chemical and physical processes facilitate deeper insights into the mechanisms of development, including pollen wall ontogeny. |
doi_str_mv | 10.1111/tpj.15070 |
format | Article |
fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2458039117</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2488464341</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3880-e13f301a15145f1d5692aece435238a8a1036431945231754046779f12c1e07a3</originalsourceid><addsrcrecordid>eNp1kU2P0zAQhi0EYkvhwB9AlriARLqe2M4Ht1XF16rSclgkbpFJJ40r1w5x0pJfw1_dCV04IK0v9oyfecfjl7GXIFZA63Lo9ivQIheP2AJkphMJ8vtjthBlJpJcQXrBnsW4FwJymamn7EJK0FpqsWC_rzy3fsBdbxwdot21w5wIvAvOoecn4xzf4hFd6A7oh_d0ewzuiHPAQ8O7doq2puquDzXGiJEIjr-sRx5IaId-mjNr46ba-KEdI29c6O2WDpvVO36yQ8vNXNJhb2dZEjMdyZm6fc6eNMZFfHG_L9m3jx9u15-Tzc2nL-urTVLLohAJgmykAAMalG5gq7MyNVijkjqVhSkMCJpcQqkohlwrobI8LxtIa0CRG7lkb8661PbniHGoDjbW6JzxGMZYpUoXQpZAP7hkr_9D92HsPb2OqKJQ1EcBUW_PVN2HGHtsqo6GM_1Ugahm1ypyrfrjGrGv7hXHHwfc_iP_2kTA5Rk4WYfTw0rV7dfrs-Qd9AaiJw</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2488464341</pqid></control><display><type>article</type><title>An integral insight into pollen wall development: involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach</title><source>Access via Wiley Online Library</source><source>IngentaConnect Free/Open Access Journals</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Wiley Online Library (Open Access Collection)</source><creator>Gabarayeva, Nina I. ; Grigorjeva, Valentina V.</creator><creatorcontrib>Gabarayeva, Nina I. ; Grigorjeva, Valentina V.</creatorcontrib><description>Summary
We aimed to understand the underlying mechanisms of development in the sporopollenin‐containing part of the pollen wall, the exine, one of the most complex cell walls in plants. Our hypothesis is that distinct physical processes, phase separation and micellar self‐assembly, underpinexine development by taking the molecular building blocks, determined and synthesised by the genome, through several phase transitions. To test this hypothesis, we traced each stage of microspore development in Calycanthus floridus with transmission electron microscopy and then generated in vitro experimental simulations corresponding to every developmental stage. The sequence of structures observed within the periplasmic space around developing microspores starts with spherical units, which are rearranged into columns to then form rod‐like units (the young columellae) and, finally, white line centred endexine lamellae. Phase separation precedes each developmental stage. The set of experimental simulations, obtained as self‐assembled micellar mesophases formed at the interface between lipid and water compartments, was the same: spherical micelles; columns of spherical micelles; cylindrical micelles; and laminate micelles, separated by gaps, resembling white‐lined lamellae. Thus, patterns simulating structures observed at the main stages of exine development in C. floridus were obtained from in vitro experiments, and hence purely physicochemical processes can construct exine‐like patterns. This highlights the important part played by physical processes that are not under direct genomic control and share influence on the emerging ultrastructure with the genome during exine development. These findings suggest that a new approach to ontogenetic studies, including a consideration of physical factors, is required for a better understanding of developmental processes.
Significance Statement
Interdisciplinary research summarizing morphology, ultrastructure, and biological, chemical and physical processes facilitate deeper insights into the mechanisms of development, including pollen wall ontogeny.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.15070</identifier><identifier>PMID: 33155350</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Calycanthus floridus ; Cell walls ; Columns (structural) ; Developmental stages ; Genomes ; Hypotheses ; Lamellae ; Lamellar structure ; Lipids ; Micelles ; Microspores ; Ontogeny ; Periplasmic space ; Phase separation ; Phase transitions ; Physical factors ; Pollen ; pollen wall development ; self‐assembly ; Simulation ; simulation of pollen walls ; Transmission electron microscopy ; Ultrastructure ; underlying biophysical mechanisms</subject><ispartof>The Plant journal : for cell and molecular biology, 2021-02, Vol.105 (3), p.736-753</ispartof><rights>2020 Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>2020 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2021 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3880-e13f301a15145f1d5692aece435238a8a1036431945231754046779f12c1e07a3</citedby><cites>FETCH-LOGICAL-c3880-e13f301a15145f1d5692aece435238a8a1036431945231754046779f12c1e07a3</cites><orcidid>0000-0001-8193-8831 ; 0000-0002-4340-1416</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.15070$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.15070$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33155350$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gabarayeva, Nina I.</creatorcontrib><creatorcontrib>Grigorjeva, Valentina V.</creatorcontrib><title>An integral insight into pollen wall development: involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
We aimed to understand the underlying mechanisms of development in the sporopollenin‐containing part of the pollen wall, the exine, one of the most complex cell walls in plants. Our hypothesis is that distinct physical processes, phase separation and micellar self‐assembly, underpinexine development by taking the molecular building blocks, determined and synthesised by the genome, through several phase transitions. To test this hypothesis, we traced each stage of microspore development in Calycanthus floridus with transmission electron microscopy and then generated in vitro experimental simulations corresponding to every developmental stage. The sequence of structures observed within the periplasmic space around developing microspores starts with spherical units, which are rearranged into columns to then form rod‐like units (the young columellae) and, finally, white line centred endexine lamellae. Phase separation precedes each developmental stage. The set of experimental simulations, obtained as self‐assembled micellar mesophases formed at the interface between lipid and water compartments, was the same: spherical micelles; columns of spherical micelles; cylindrical micelles; and laminate micelles, separated by gaps, resembling white‐lined lamellae. Thus, patterns simulating structures observed at the main stages of exine development in C. floridus were obtained from in vitro experiments, and hence purely physicochemical processes can construct exine‐like patterns. This highlights the important part played by physical processes that are not under direct genomic control and share influence on the emerging ultrastructure with the genome during exine development. These findings suggest that a new approach to ontogenetic studies, including a consideration of physical factors, is required for a better understanding of developmental processes.
Significance Statement
Interdisciplinary research summarizing morphology, ultrastructure, and biological, chemical and physical processes facilitate deeper insights into the mechanisms of development, including pollen wall ontogeny.</description><subject>Calycanthus floridus</subject><subject>Cell walls</subject><subject>Columns (structural)</subject><subject>Developmental stages</subject><subject>Genomes</subject><subject>Hypotheses</subject><subject>Lamellae</subject><subject>Lamellar structure</subject><subject>Lipids</subject><subject>Micelles</subject><subject>Microspores</subject><subject>Ontogeny</subject><subject>Periplasmic space</subject><subject>Phase separation</subject><subject>Phase transitions</subject><subject>Physical factors</subject><subject>Pollen</subject><subject>pollen wall development</subject><subject>self‐assembly</subject><subject>Simulation</subject><subject>simulation of pollen walls</subject><subject>Transmission electron microscopy</subject><subject>Ultrastructure</subject><subject>underlying biophysical mechanisms</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp1kU2P0zAQhi0EYkvhwB9AlriARLqe2M4Ht1XF16rSclgkbpFJJ40r1w5x0pJfw1_dCV04IK0v9oyfecfjl7GXIFZA63Lo9ivQIheP2AJkphMJ8vtjthBlJpJcQXrBnsW4FwJymamn7EJK0FpqsWC_rzy3fsBdbxwdot21w5wIvAvOoecn4xzf4hFd6A7oh_d0ewzuiHPAQ8O7doq2puquDzXGiJEIjr-sRx5IaId-mjNr46ba-KEdI29c6O2WDpvVO36yQ8vNXNJhb2dZEjMdyZm6fc6eNMZFfHG_L9m3jx9u15-Tzc2nL-urTVLLohAJgmykAAMalG5gq7MyNVijkjqVhSkMCJpcQqkohlwrobI8LxtIa0CRG7lkb8661PbniHGoDjbW6JzxGMZYpUoXQpZAP7hkr_9D92HsPb2OqKJQ1EcBUW_PVN2HGHtsqo6GM_1Ugahm1ypyrfrjGrGv7hXHHwfc_iP_2kTA5Rk4WYfTw0rV7dfrs-Qd9AaiJw</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Gabarayeva, Nina I.</creator><creator>Grigorjeva, Valentina V.</creator><general>Blackwell Publishing Ltd</general><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/0000-0001-8193-8831</orcidid><orcidid>https://orcid.org/0000-0002-4340-1416</orcidid></search><sort><creationdate>202102</creationdate><title>An integral insight into pollen wall development: involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach</title><author>Gabarayeva, Nina I. ; Grigorjeva, Valentina V.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3880-e13f301a15145f1d5692aece435238a8a1036431945231754046779f12c1e07a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Calycanthus floridus</topic><topic>Cell walls</topic><topic>Columns (structural)</topic><topic>Developmental stages</topic><topic>Genomes</topic><topic>Hypotheses</topic><topic>Lamellae</topic><topic>Lamellar structure</topic><topic>Lipids</topic><topic>Micelles</topic><topic>Microspores</topic><topic>Ontogeny</topic><topic>Periplasmic space</topic><topic>Phase separation</topic><topic>Phase transitions</topic><topic>Physical factors</topic><topic>Pollen</topic><topic>pollen wall development</topic><topic>self‐assembly</topic><topic>Simulation</topic><topic>simulation of pollen walls</topic><topic>Transmission electron microscopy</topic><topic>Ultrastructure</topic><topic>underlying biophysical mechanisms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gabarayeva, Nina I.</creatorcontrib><creatorcontrib>Grigorjeva, Valentina V.</creatorcontrib><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>Gabarayeva, Nina I.</au><au>Grigorjeva, Valentina V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An integral insight into pollen wall development: involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2021-02</date><risdate>2021</risdate><volume>105</volume><issue>3</issue><spage>736</spage><epage>753</epage><pages>736-753</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
We aimed to understand the underlying mechanisms of development in the sporopollenin‐containing part of the pollen wall, the exine, one of the most complex cell walls in plants. Our hypothesis is that distinct physical processes, phase separation and micellar self‐assembly, underpinexine development by taking the molecular building blocks, determined and synthesised by the genome, through several phase transitions. To test this hypothesis, we traced each stage of microspore development in Calycanthus floridus with transmission electron microscopy and then generated in vitro experimental simulations corresponding to every developmental stage. The sequence of structures observed within the periplasmic space around developing microspores starts with spherical units, which are rearranged into columns to then form rod‐like units (the young columellae) and, finally, white line centred endexine lamellae. Phase separation precedes each developmental stage. The set of experimental simulations, obtained as self‐assembled micellar mesophases formed at the interface between lipid and water compartments, was the same: spherical micelles; columns of spherical micelles; cylindrical micelles; and laminate micelles, separated by gaps, resembling white‐lined lamellae. Thus, patterns simulating structures observed at the main stages of exine development in C. floridus were obtained from in vitro experiments, and hence purely physicochemical processes can construct exine‐like patterns. This highlights the important part played by physical processes that are not under direct genomic control and share influence on the emerging ultrastructure with the genome during exine development. These findings suggest that a new approach to ontogenetic studies, including a consideration of physical factors, is required for a better understanding of developmental processes.
Significance Statement
Interdisciplinary research summarizing morphology, ultrastructure, and biological, chemical and physical processes facilitate deeper insights into the mechanisms of development, including pollen wall ontogeny.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>33155350</pmid><doi>10.1111/tpj.15070</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0001-8193-8831</orcidid><orcidid>https://orcid.org/0000-0002-4340-1416</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0960-7412 |
ispartof | The Plant journal : for cell and molecular biology, 2021-02, Vol.105 (3), p.736-753 |
issn | 0960-7412 1365-313X |
language | eng |
recordid | cdi_proquest_miscellaneous_2458039117 |
source | Access via Wiley Online Library; IngentaConnect Free/Open Access Journals; EZB-FREE-00999 freely available EZB journals; Wiley Online Library (Open Access Collection) |
subjects | Calycanthus floridus Cell walls Columns (structural) Developmental stages Genomes Hypotheses Lamellae Lamellar structure Lipids Micelles Microspores Ontogeny Periplasmic space Phase separation Phase transitions Physical factors Pollen pollen wall development self‐assembly Simulation simulation of pollen walls Transmission electron microscopy Ultrastructure underlying biophysical mechanisms |
title | An integral insight into pollen wall development: involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T07%3A33%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=An%20integral%20insight%20into%20pollen%20wall%20development:%20involvement%20of%20physical%20processes%20in%20exine%20ontogeny%20in%20Calycanthus%20floridus%20L.,%20with%20an%20experimental%20approach&rft.jtitle=The%20Plant%20journal%20:%20for%20cell%20and%20molecular%20biology&rft.au=Gabarayeva,%20Nina%20I.&rft.date=2021-02&rft.volume=105&rft.issue=3&rft.spage=736&rft.epage=753&rft.pages=736-753&rft.issn=0960-7412&rft.eissn=1365-313X&rft_id=info:doi/10.1111/tpj.15070&rft_dat=%3Cproquest_cross%3E2488464341%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2488464341&rft_id=info:pmid/33155350&rfr_iscdi=true |