Transcriptome features of stone cell development in weevil‐resistant and susceptible Sitka spruce
Summary Stone cells are a specialized, highly lignified cell type found in both angiosperms and gymnosperms. In conifers, abundance of stone cells in the cortex provides a robust constitutive physical defense against stem feeding insects. Stone cells are a major insect‐resistance trait in Sitka spru...
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Veröffentlicht in: | The New phytologist 2023-09, Vol.239 (6), p.2138-2152 |
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creator | Whitehill, Justin G. A. Yuen, Macaire M. S. Chiang, Angela Ritland, Carol E. Bohlmann, Jörg |
description | Summary
Stone cells are a specialized, highly lignified cell type found in both angiosperms and gymnosperms. In conifers, abundance of stone cells in the cortex provides a robust constitutive physical defense against stem feeding insects. Stone cells are a major insect‐resistance trait in Sitka spruce (Picea sitchensis), occurring in dense clusters in apical shoots of trees resistant (R) to spruce weevil (Pissodes strobi) but being rare in susceptible (S) trees.
To learn more about molecular mechanisms of stone cell formation in conifers, we used laser microdissection and RNA sequencing to develop cell‐type‐specific transcriptomes of developing stone cells from R and S trees. Using light, immunohistochemical, and fluorescence microscopy, we also visualized the deposition of cellulose, xylan, and lignin associated with stone cell development.
A total of 1293 genes were differentially expressed at higher levels in developing stone cells relative to cortical parenchyma. Genes with potential roles in stone cell secondary cell wall formation (SCW) were identified and their expression evaluated over a time course of stone cell formation in R and S trees.
The expression of several transcriptional regulators was associated with stone cell formation, including a NAC family transcription factor and several genes annotated as MYB transcription factors with known roles in SCW formation. |
doi_str_mv | 10.1111/nph.19103 |
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Stone cells are a specialized, highly lignified cell type found in both angiosperms and gymnosperms. In conifers, abundance of stone cells in the cortex provides a robust constitutive physical defense against stem feeding insects. Stone cells are a major insect‐resistance trait in Sitka spruce (Picea sitchensis), occurring in dense clusters in apical shoots of trees resistant (R) to spruce weevil (Pissodes strobi) but being rare in susceptible (S) trees.
To learn more about molecular mechanisms of stone cell formation in conifers, we used laser microdissection and RNA sequencing to develop cell‐type‐specific transcriptomes of developing stone cells from R and S trees. Using light, immunohistochemical, and fluorescence microscopy, we also visualized the deposition of cellulose, xylan, and lignin associated with stone cell development.
A total of 1293 genes were differentially expressed at higher levels in developing stone cells relative to cortical parenchyma. Genes with potential roles in stone cell secondary cell wall formation (SCW) were identified and their expression evaluated over a time course of stone cell formation in R and S trees.
The expression of several transcriptional regulators was associated with stone cell formation, including a NAC family transcription factor and several genes annotated as MYB transcription factors with known roles in SCW formation.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19103</identifier><identifier>PMID: 37403300</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Angiosperms ; Cell walls ; Cells ; Cellulose ; conifer ; Conifers ; Fluorescence ; Fluorescence microscopy ; Gene sequencing ; Genes ; Gymnosperms ; Insects ; laser‐capture microdissection ; lignin ; Molecular modelling ; Parenchyma ; Pest resistance ; Picea sitchensis ; plant resistance ; plant–insect interaction ; RNA sequencing ; secondary cell wall ; Shoots ; spruce ; Stone ; Transcription ; Transcription factors ; Transcriptomes ; Trees ; weevil ; Xylan</subject><ispartof>The New phytologist, 2023-09, Vol.239 (6), p.2138-2152</ispartof><rights>2023 The Authors © 2023 New Phytologist Foundation</rights><rights>2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3483-a24c9d27d6368e06ff8394fccc23c346652829fab5425f8d691e47e7f003fa663</cites><orcidid>0000-0003-1765-6228 ; 0000-0002-3637-7956 ; 0000-0003-2578-9522 ; 0000-0003-3179-6956 ; 0000-0001-9732-8229</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%2Fnph.19103$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19103$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,1427,27903,27904,45553,45554,46387,46811</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37403300$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Whitehill, Justin G. A.</creatorcontrib><creatorcontrib>Yuen, Macaire M. S.</creatorcontrib><creatorcontrib>Chiang, Angela</creatorcontrib><creatorcontrib>Ritland, Carol E.</creatorcontrib><creatorcontrib>Bohlmann, Jörg</creatorcontrib><title>Transcriptome features of stone cell development in weevil‐resistant and susceptible Sitka spruce</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Stone cells are a specialized, highly lignified cell type found in both angiosperms and gymnosperms. In conifers, abundance of stone cells in the cortex provides a robust constitutive physical defense against stem feeding insects. Stone cells are a major insect‐resistance trait in Sitka spruce (Picea sitchensis), occurring in dense clusters in apical shoots of trees resistant (R) to spruce weevil (Pissodes strobi) but being rare in susceptible (S) trees.
To learn more about molecular mechanisms of stone cell formation in conifers, we used laser microdissection and RNA sequencing to develop cell‐type‐specific transcriptomes of developing stone cells from R and S trees. Using light, immunohistochemical, and fluorescence microscopy, we also visualized the deposition of cellulose, xylan, and lignin associated with stone cell development.
A total of 1293 genes were differentially expressed at higher levels in developing stone cells relative to cortical parenchyma. Genes with potential roles in stone cell secondary cell wall formation (SCW) were identified and their expression evaluated over a time course of stone cell formation in R and S trees.
The expression of several transcriptional regulators was associated with stone cell formation, including a NAC family transcription factor and several genes annotated as MYB transcription factors with known roles in SCW formation.</description><subject>Angiosperms</subject><subject>Cell walls</subject><subject>Cells</subject><subject>Cellulose</subject><subject>conifer</subject><subject>Conifers</subject><subject>Fluorescence</subject><subject>Fluorescence microscopy</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Gymnosperms</subject><subject>Insects</subject><subject>laser‐capture microdissection</subject><subject>lignin</subject><subject>Molecular modelling</subject><subject>Parenchyma</subject><subject>Pest resistance</subject><subject>Picea sitchensis</subject><subject>plant resistance</subject><subject>plant–insect interaction</subject><subject>RNA sequencing</subject><subject>secondary cell wall</subject><subject>Shoots</subject><subject>spruce</subject><subject>Stone</subject><subject>Transcription</subject><subject>Transcription factors</subject><subject>Transcriptomes</subject><subject>Trees</subject><subject>weevil</subject><subject>Xylan</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp10M9KxDAQBvAgiq6rB19AAl70UM2_pu1RFnUFUUEFbyWbTjDaNjVplb35CD6jT2LWVQ-CcxkYfnwMH0I7lBzSOEdt93BIC0r4ChpRIYskpzxbRSNCWJ5IIe830GYIj4SQIpVsHW3wTBDOCRkhfetVG7S3Xe8awAZUP3gI2BkcetcC1lDXuIIXqF3XQNtj2-JXgBdbf7y9R2lDr-JVtRUOQ9DQ9XZWA76x_ZPCofODhi20ZlQdYPt7j9Hd6cntZJpcXJ2dT44vEs1FzhPFhC4qllWSyxyINCbnhTBaa8ajkDJlOSuMmqWCpSavZEFBZJAZQrhRUvIx2l_mdt49DxD6srFh8b9qwQ2hZDnnUhSEZZHu_aGPbvBt_C6qlKZp7EpEdbBU2rsQPJiy87ZRfl5SUi6aL2Pz5Vfz0e5-Jw6zBqpf-VN1BEdL8GprmP-fVF5eT5eRn2F1jnY</recordid><startdate>202309</startdate><enddate>202309</enddate><creator>Whitehill, Justin G. A.</creator><creator>Yuen, Macaire M. S.</creator><creator>Chiang, Angela</creator><creator>Ritland, Carol E.</creator><creator>Bohlmann, Jörg</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1765-6228</orcidid><orcidid>https://orcid.org/0000-0002-3637-7956</orcidid><orcidid>https://orcid.org/0000-0003-2578-9522</orcidid><orcidid>https://orcid.org/0000-0003-3179-6956</orcidid><orcidid>https://orcid.org/0000-0001-9732-8229</orcidid></search><sort><creationdate>202309</creationdate><title>Transcriptome features of stone cell development in weevil‐resistant and susceptible Sitka spruce</title><author>Whitehill, Justin G. A. ; Yuen, Macaire M. S. ; Chiang, Angela ; Ritland, Carol E. ; Bohlmann, Jörg</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3483-a24c9d27d6368e06ff8394fccc23c346652829fab5425f8d691e47e7f003fa663</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Angiosperms</topic><topic>Cell walls</topic><topic>Cells</topic><topic>Cellulose</topic><topic>conifer</topic><topic>Conifers</topic><topic>Fluorescence</topic><topic>Fluorescence microscopy</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Gymnosperms</topic><topic>Insects</topic><topic>laser‐capture microdissection</topic><topic>lignin</topic><topic>Molecular modelling</topic><topic>Parenchyma</topic><topic>Pest resistance</topic><topic>Picea sitchensis</topic><topic>plant resistance</topic><topic>plant–insect interaction</topic><topic>RNA sequencing</topic><topic>secondary cell wall</topic><topic>Shoots</topic><topic>spruce</topic><topic>Stone</topic><topic>Transcription</topic><topic>Transcription factors</topic><topic>Transcriptomes</topic><topic>Trees</topic><topic>weevil</topic><topic>Xylan</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Whitehill, Justin G. A.</creatorcontrib><creatorcontrib>Yuen, Macaire M. S.</creatorcontrib><creatorcontrib>Chiang, Angela</creatorcontrib><creatorcontrib>Ritland, Carol E.</creatorcontrib><creatorcontrib>Bohlmann, Jörg</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</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 New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Whitehill, Justin G. A.</au><au>Yuen, Macaire M. S.</au><au>Chiang, Angela</au><au>Ritland, Carol E.</au><au>Bohlmann, Jörg</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptome features of stone cell development in weevil‐resistant and susceptible Sitka spruce</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2023-09</date><risdate>2023</risdate><volume>239</volume><issue>6</issue><spage>2138</spage><epage>2152</epage><pages>2138-2152</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
Stone cells are a specialized, highly lignified cell type found in both angiosperms and gymnosperms. In conifers, abundance of stone cells in the cortex provides a robust constitutive physical defense against stem feeding insects. Stone cells are a major insect‐resistance trait in Sitka spruce (Picea sitchensis), occurring in dense clusters in apical shoots of trees resistant (R) to spruce weevil (Pissodes strobi) but being rare in susceptible (S) trees.
To learn more about molecular mechanisms of stone cell formation in conifers, we used laser microdissection and RNA sequencing to develop cell‐type‐specific transcriptomes of developing stone cells from R and S trees. Using light, immunohistochemical, and fluorescence microscopy, we also visualized the deposition of cellulose, xylan, and lignin associated with stone cell development.
A total of 1293 genes were differentially expressed at higher levels in developing stone cells relative to cortical parenchyma. Genes with potential roles in stone cell secondary cell wall formation (SCW) were identified and their expression evaluated over a time course of stone cell formation in R and S trees.
The expression of several transcriptional regulators was associated with stone cell formation, including a NAC family transcription factor and several genes annotated as MYB transcription factors with known roles in SCW formation.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37403300</pmid><doi>10.1111/nph.19103</doi><tpages>2152</tpages><orcidid>https://orcid.org/0000-0003-1765-6228</orcidid><orcidid>https://orcid.org/0000-0002-3637-7956</orcidid><orcidid>https://orcid.org/0000-0003-2578-9522</orcidid><orcidid>https://orcid.org/0000-0003-3179-6956</orcidid><orcidid>https://orcid.org/0000-0001-9732-8229</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Angiosperms Cell walls Cells Cellulose conifer Conifers Fluorescence Fluorescence microscopy Gene sequencing Genes Gymnosperms Insects laser‐capture microdissection lignin Molecular modelling Parenchyma Pest resistance Picea sitchensis plant resistance plant–insect interaction RNA sequencing secondary cell wall Shoots spruce Stone Transcription Transcription factors Transcriptomes Trees weevil Xylan |
title | Transcriptome features of stone cell development in weevil‐resistant and susceptible Sitka spruce |
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