A WOX homolog disrupted by a transposon led to the loss of spines and contributed to the domestication of lettuce
Summary The loss of spines is one of the most important domestication traits for lettuce (Lactuca sativa). However, the genetics and regulation of spine development in lettuce remain unclear. We examined the genetics of spines in lettuce using a segregating population derived from a cross between cu...
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Veröffentlicht in: | The New phytologist 2024-06, Vol.242 (6), p.2857-2871 |
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creator | Sun, Peinan Yuan, Huanran Pan, Jiangpeng Wu, Zhihao Li, Weibo Wang, Xin Kuang, Hanhui Chen, Jiongjiong |
description | Summary
The loss of spines is one of the most important domestication traits for lettuce (Lactuca sativa). However, the genetics and regulation of spine development in lettuce remain unclear.
We examined the genetics of spines in lettuce using a segregating population derived from a cross between cultivated and wild lettuce (Lactuca serriola). A gene encoding WUSCHEL‐related homeobox transcription factor, named as WOX‐SPINE1 (WS1), was identified as the candidate gene controlling the spine development in lettuce, and its function on spines was verified. A CACTA transposon was found to be inserted into the first exon of the ws1 allele, knocking out its function and leading to the lack of spines in cultivated lettuce.
All lettuce cultivars investigated have the nonfunctional ws1 gene, and a selection sweep was found at the WS1 locus, suggesting its important role in lettuce domestication. The expression levels of WS1 were associated with the density of spines among different accessions of wild lettuce. At least two independent loss‐of‐function mutations in the ws1 gene caused the loss of spines in wild lettuce.
These findings provide new insights into the development of spines and facilitate the exploitation of wild genetic resources in future lettuce breeding programs. |
doi_str_mv | 10.1111/nph.19738 |
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The loss of spines is one of the most important domestication traits for lettuce (Lactuca sativa). However, the genetics and regulation of spine development in lettuce remain unclear.
We examined the genetics of spines in lettuce using a segregating population derived from a cross between cultivated and wild lettuce (Lactuca serriola). A gene encoding WUSCHEL‐related homeobox transcription factor, named as WOX‐SPINE1 (WS1), was identified as the candidate gene controlling the spine development in lettuce, and its function on spines was verified. A CACTA transposon was found to be inserted into the first exon of the ws1 allele, knocking out its function and leading to the lack of spines in cultivated lettuce.
All lettuce cultivars investigated have the nonfunctional ws1 gene, and a selection sweep was found at the WS1 locus, suggesting its important role in lettuce domestication. The expression levels of WS1 were associated with the density of spines among different accessions of wild lettuce. At least two independent loss‐of‐function mutations in the ws1 gene caused the loss of spines in wild lettuce.
These findings provide new insights into the development of spines and facilitate the exploitation of wild genetic resources in future lettuce breeding programs.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19738</identifier><identifier>PMID: 38584520</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>alleles ; CACTA transposon ; Cultivars ; Domestication ; exons ; Genetic resources ; Genetics ; Homeobox ; Lactuca sativa ; Lactuca serriola ; lettuce ; loci ; loss-of-function mutation ; Plant breeding ; Spine ; transcription factors ; Transposons ; Vegetables ; WS1</subject><ispartof>The New phytologist, 2024-06, Vol.242 (6), p.2857-2871</ispartof><rights>2024 The Authors © 2024 New Phytologist Foundation</rights><rights>2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><rights>2024 The Authors New Phytologist © 2024 New Phytologist Foundation.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3468-8b63d8f489c66e03fcdf6f27d2c4a20c29f483dcce9216ccea5b0b34307b5ed73</cites><orcidid>0000-0001-5620-6823 ; 0000-0003-4870-0578 ; 0000-0002-1690-8510</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.19738$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19738$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38584520$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sun, Peinan</creatorcontrib><creatorcontrib>Yuan, Huanran</creatorcontrib><creatorcontrib>Pan, Jiangpeng</creatorcontrib><creatorcontrib>Wu, Zhihao</creatorcontrib><creatorcontrib>Li, Weibo</creatorcontrib><creatorcontrib>Wang, Xin</creatorcontrib><creatorcontrib>Kuang, Hanhui</creatorcontrib><creatorcontrib>Chen, Jiongjiong</creatorcontrib><title>A WOX homolog disrupted by a transposon led to the loss of spines and contributed to the domestication of lettuce</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
The loss of spines is one of the most important domestication traits for lettuce (Lactuca sativa). However, the genetics and regulation of spine development in lettuce remain unclear.
We examined the genetics of spines in lettuce using a segregating population derived from a cross between cultivated and wild lettuce (Lactuca serriola). A gene encoding WUSCHEL‐related homeobox transcription factor, named as WOX‐SPINE1 (WS1), was identified as the candidate gene controlling the spine development in lettuce, and its function on spines was verified. A CACTA transposon was found to be inserted into the first exon of the ws1 allele, knocking out its function and leading to the lack of spines in cultivated lettuce.
All lettuce cultivars investigated have the nonfunctional ws1 gene, and a selection sweep was found at the WS1 locus, suggesting its important role in lettuce domestication. The expression levels of WS1 were associated with the density of spines among different accessions of wild lettuce. At least two independent loss‐of‐function mutations in the ws1 gene caused the loss of spines in wild lettuce.
These findings provide new insights into the development of spines and facilitate the exploitation of wild genetic resources in future lettuce breeding programs.</description><subject>alleles</subject><subject>CACTA transposon</subject><subject>Cultivars</subject><subject>Domestication</subject><subject>exons</subject><subject>Genetic resources</subject><subject>Genetics</subject><subject>Homeobox</subject><subject>Lactuca sativa</subject><subject>Lactuca serriola</subject><subject>lettuce</subject><subject>loci</subject><subject>loss-of-function mutation</subject><subject>Plant breeding</subject><subject>Spine</subject><subject>transcription factors</subject><subject>Transposons</subject><subject>Vegetables</subject><subject>WS1</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqF0UFPHCEYBmDStNGt9dA_YEh6qYdR4AOGOZpNqyYb9WDj3iYMMO6YmWEEJs3--2LXamJiyoUEHt4AL0JfKTmheZyO0-aEViWoD2hBuawKRaH8iBaEMFVILtf76HOMD4SQSki2h_ZBCcUFIwv0eIbvrtd44wff-3tsuxjmKTmLmy3WOAU9xslHP-I-ryWP08bh3seIfYvj1I0uYj1abPyYQtfM6VVZP7iYOqNTl49n3ruUZuO-oE-t7qM7fJ4P0K-fP26XF8Xq-vxyebYqDHCpCtVIsKrlqjJSOgKtsa1sWWmZ4ZoRw6q8B9YYVzEq86RFQxrgQMpGOFvCAfq-y52Cf5zzVeqhi8b1vR6dn2MNVIAQhAv1f0qAlyVARTP99oY--DmM-SFZ5SgFQFhWxztlQv6r4Np6Ct2gw7ampH6qrM6V1X8ry_boOXFuBmdf5L-OMjjdgd9d77bvJ9VXNxe7yD9vk6BT</recordid><startdate>202406</startdate><enddate>202406</enddate><creator>Sun, Peinan</creator><creator>Yuan, Huanran</creator><creator>Pan, Jiangpeng</creator><creator>Wu, Zhihao</creator><creator>Li, Weibo</creator><creator>Wang, Xin</creator><creator>Kuang, Hanhui</creator><creator>Chen, Jiongjiong</creator><general>Wiley Subscription Services, Inc</general><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><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0001-5620-6823</orcidid><orcidid>https://orcid.org/0000-0003-4870-0578</orcidid><orcidid>https://orcid.org/0000-0002-1690-8510</orcidid></search><sort><creationdate>202406</creationdate><title>A WOX homolog disrupted by a transposon led to the loss of spines and contributed to the domestication of lettuce</title><author>Sun, Peinan ; Yuan, Huanran ; Pan, Jiangpeng ; Wu, Zhihao ; Li, Weibo ; Wang, Xin ; Kuang, Hanhui ; Chen, Jiongjiong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3468-8b63d8f489c66e03fcdf6f27d2c4a20c29f483dcce9216ccea5b0b34307b5ed73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>alleles</topic><topic>CACTA transposon</topic><topic>Cultivars</topic><topic>Domestication</topic><topic>exons</topic><topic>Genetic resources</topic><topic>Genetics</topic><topic>Homeobox</topic><topic>Lactuca sativa</topic><topic>Lactuca serriola</topic><topic>lettuce</topic><topic>loci</topic><topic>loss-of-function mutation</topic><topic>Plant breeding</topic><topic>Spine</topic><topic>transcription factors</topic><topic>Transposons</topic><topic>Vegetables</topic><topic>WS1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sun, Peinan</creatorcontrib><creatorcontrib>Yuan, Huanran</creatorcontrib><creatorcontrib>Pan, Jiangpeng</creatorcontrib><creatorcontrib>Wu, Zhihao</creatorcontrib><creatorcontrib>Li, Weibo</creatorcontrib><creatorcontrib>Wang, Xin</creatorcontrib><creatorcontrib>Kuang, Hanhui</creatorcontrib><creatorcontrib>Chen, Jiongjiong</creatorcontrib><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><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sun, Peinan</au><au>Yuan, Huanran</au><au>Pan, Jiangpeng</au><au>Wu, Zhihao</au><au>Li, Weibo</au><au>Wang, Xin</au><au>Kuang, Hanhui</au><au>Chen, Jiongjiong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A WOX homolog disrupted by a transposon led to the loss of spines and contributed to the domestication of lettuce</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2024-06</date><risdate>2024</risdate><volume>242</volume><issue>6</issue><spage>2857</spage><epage>2871</epage><pages>2857-2871</pages><issn>0028-646X</issn><issn>1469-8137</issn><eissn>1469-8137</eissn><abstract>Summary
The loss of spines is one of the most important domestication traits for lettuce (Lactuca sativa). However, the genetics and regulation of spine development in lettuce remain unclear.
We examined the genetics of spines in lettuce using a segregating population derived from a cross between cultivated and wild lettuce (Lactuca serriola). A gene encoding WUSCHEL‐related homeobox transcription factor, named as WOX‐SPINE1 (WS1), was identified as the candidate gene controlling the spine development in lettuce, and its function on spines was verified. A CACTA transposon was found to be inserted into the first exon of the ws1 allele, knocking out its function and leading to the lack of spines in cultivated lettuce.
All lettuce cultivars investigated have the nonfunctional ws1 gene, and a selection sweep was found at the WS1 locus, suggesting its important role in lettuce domestication. The expression levels of WS1 were associated with the density of spines among different accessions of wild lettuce. At least two independent loss‐of‐function mutations in the ws1 gene caused the loss of spines in wild lettuce.
These findings provide new insights into the development of spines and facilitate the exploitation of wild genetic resources in future lettuce breeding programs.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>38584520</pmid><doi>10.1111/nph.19738</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-5620-6823</orcidid><orcidid>https://orcid.org/0000-0003-4870-0578</orcidid><orcidid>https://orcid.org/0000-0002-1690-8510</orcidid></addata></record> |
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subjects | alleles CACTA transposon Cultivars Domestication exons Genetic resources Genetics Homeobox Lactuca sativa Lactuca serriola lettuce loci loss-of-function mutation Plant breeding Spine transcription factors Transposons Vegetables WS1 |
title | A WOX homolog disrupted by a transposon led to the loss of spines and contributed to the domestication of lettuce |
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