Jianbing Hu, Chenchen Liu, Zezhen Du, Furong Guo, Dan Song, Nan Wang, Zhuangmin Wei, Jingdong Jiang, Zonghong Cao, Chunmei Shi, Siqi Zhang, Chenqiao Zhu, Peng Chen, Robert M. Larkin, Zongcheng Lin, Qiang Xu, Junli Ye, Xiuxin Deng, Maurice Bosch, Vernonica E. Franklin-Tong, Lijun Chai
{"title":"转座因子导致柑橘丧失自交不亲和性。","authors":"Jianbing Hu, Chenchen Liu, Zezhen Du, Furong Guo, Dan Song, Nan Wang, Zhuangmin Wei, Jingdong Jiang, Zonghong Cao, Chunmei Shi, Siqi Zhang, Chenqiao Zhu, Peng Chen, Robert M. Larkin, Zongcheng Lin, Qiang Xu, Junli Ye, Xiuxin Deng, Maurice Bosch, Vernonica E. Franklin-Tong, Lijun Chai","doi":"10.1111/pbi.14250","DOIUrl":null,"url":null,"abstract":"<p>Self-incompatibility (SI) is a widespread prezygotic mechanism for flowering plants to avoid inbreeding depression and promote genetic diversity. Citrus has an <i>S</i>-RNase-based SI system, which was frequently lost during evolution. We previously identified a single nucleotide mutation in <i>S</i><sub><i>m</i></sub><i>-RNase,</i> which is responsible for the loss of SI in mandarin and its hybrids. However, little is known about other mechanisms responsible for conversion of SI to self-compatibility (SC) and we identify a completely different mechanism widely utilized by citrus. Here, we found a 786-bp miniature inverted-repeat transposable element (MITE) insertion in the promoter region of the <i>FhiS</i><sub><i>2</i></sub><i>-RNase</i> in <i>Fortunella hindsii</i> Swingle (a model plant for citrus gene function), which does not contain the <i>S</i><sub><i>m</i></sub><i>-RNase</i> allele but are still SC. We demonstrate that this MITE plays a pivotal role in the loss of SI in citrus, providing evidence that this MITE insertion prevents expression of the <i>S-RNase</i>; moreover, transgenic experiments show that deletion of this 786-bp MITE insertion recovers the expression of <i>FhiS</i><sub><i>2</i></sub><i>-RNase</i> and restores SI. This study identifies the first evidence for a role for MITEs at the <i>S</i>-locus affecting the SI phenotype. A family-wide survey of the <i>S</i>-locus revealed that MITE insertions occur frequently adjacent to <i>S-RNase</i> alleles in different citrus genera, but only certain MITEs appear to be responsible for the loss of SI. Our study provides evidence that insertion of MITEs into a promoter region can alter a breeding strategy and suggests that this phenomenon may be broadly responsible for SC in species with the <i>S</i>-RNase system.</p>","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":null,"pages":null},"PeriodicalIF":10.1000,"publicationDate":"2023-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/pbi.14250","citationCount":"0","resultStr":"{\"title\":\"Transposable elements cause the loss of self-incompatibility in citrus\",\"authors\":\"Jianbing Hu, Chenchen Liu, Zezhen Du, Furong Guo, Dan Song, Nan Wang, Zhuangmin Wei, Jingdong Jiang, Zonghong Cao, Chunmei Shi, Siqi Zhang, Chenqiao Zhu, Peng Chen, Robert M. Larkin, Zongcheng Lin, Qiang Xu, Junli Ye, Xiuxin Deng, Maurice Bosch, Vernonica E. Franklin-Tong, Lijun Chai\",\"doi\":\"10.1111/pbi.14250\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Self-incompatibility (SI) is a widespread prezygotic mechanism for flowering plants to avoid inbreeding depression and promote genetic diversity. Citrus has an <i>S</i>-RNase-based SI system, which was frequently lost during evolution. We previously identified a single nucleotide mutation in <i>S</i><sub><i>m</i></sub><i>-RNase,</i> which is responsible for the loss of SI in mandarin and its hybrids. However, little is known about other mechanisms responsible for conversion of SI to self-compatibility (SC) and we identify a completely different mechanism widely utilized by citrus. Here, we found a 786-bp miniature inverted-repeat transposable element (MITE) insertion in the promoter region of the <i>FhiS</i><sub><i>2</i></sub><i>-RNase</i> in <i>Fortunella hindsii</i> Swingle (a model plant for citrus gene function), which does not contain the <i>S</i><sub><i>m</i></sub><i>-RNase</i> allele but are still SC. We demonstrate that this MITE plays a pivotal role in the loss of SI in citrus, providing evidence that this MITE insertion prevents expression of the <i>S-RNase</i>; moreover, transgenic experiments show that deletion of this 786-bp MITE insertion recovers the expression of <i>FhiS</i><sub><i>2</i></sub><i>-RNase</i> and restores SI. This study identifies the first evidence for a role for MITEs at the <i>S</i>-locus affecting the SI phenotype. A family-wide survey of the <i>S</i>-locus revealed that MITE insertions occur frequently adjacent to <i>S-RNase</i> alleles in different citrus genera, but only certain MITEs appear to be responsible for the loss of SI. Our study provides evidence that insertion of MITEs into a promoter region can alter a breeding strategy and suggests that this phenomenon may be broadly responsible for SC in species with the <i>S</i>-RNase system.</p>\",\"PeriodicalId\":221,\"journal\":{\"name\":\"Plant Biotechnology Journal\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":10.1000,\"publicationDate\":\"2023-12-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://onlinelibrary.wiley.com/doi/epdf/10.1111/pbi.14250\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Plant Biotechnology Journal\",\"FirstCategoryId\":\"5\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1111/pbi.14250\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOTECHNOLOGY & APPLIED MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Biotechnology Journal","FirstCategoryId":"5","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/pbi.14250","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
Transposable elements cause the loss of self-incompatibility in citrus
Self-incompatibility (SI) is a widespread prezygotic mechanism for flowering plants to avoid inbreeding depression and promote genetic diversity. Citrus has an S-RNase-based SI system, which was frequently lost during evolution. We previously identified a single nucleotide mutation in Sm-RNase, which is responsible for the loss of SI in mandarin and its hybrids. However, little is known about other mechanisms responsible for conversion of SI to self-compatibility (SC) and we identify a completely different mechanism widely utilized by citrus. Here, we found a 786-bp miniature inverted-repeat transposable element (MITE) insertion in the promoter region of the FhiS2-RNase in Fortunella hindsii Swingle (a model plant for citrus gene function), which does not contain the Sm-RNase allele but are still SC. We demonstrate that this MITE plays a pivotal role in the loss of SI in citrus, providing evidence that this MITE insertion prevents expression of the S-RNase; moreover, transgenic experiments show that deletion of this 786-bp MITE insertion recovers the expression of FhiS2-RNase and restores SI. This study identifies the first evidence for a role for MITEs at the S-locus affecting the SI phenotype. A family-wide survey of the S-locus revealed that MITE insertions occur frequently adjacent to S-RNase alleles in different citrus genera, but only certain MITEs appear to be responsible for the loss of SI. Our study provides evidence that insertion of MITEs into a promoter region can alter a breeding strategy and suggests that this phenomenon may be broadly responsible for SC in species with the S-RNase system.
期刊介绍:
Plant Biotechnology Journal aspires to publish original research and insightful reviews of high impact, authored by prominent researchers in applied plant science. The journal places a special emphasis on molecular plant sciences and their practical applications through plant biotechnology. Our goal is to establish a platform for showcasing significant advances in the field, encompassing curiosity-driven studies with potential applications, strategic research in plant biotechnology, scientific analysis of crucial issues for the beneficial utilization of plant sciences, and assessments of the performance of plant biotechnology products in practical applications.