Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population

Abstract Background Lettuce is a globally important leafy vegetable that exhibits diverse horticultural types and strong population structure, which complicates genetic analyses. To address this challenge, we develop the first multi-parent, advanced generation inter-cross (MAGIC) population for lett...

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Main Authors: Hongyun Chen, Jiongjiong Chen, Ruifang Zhai, Dean Lavelle, Yue Jia, Qiwei Tang, Ting Zhu, Menglu Wang, Zedong Geng, Jianzhong Zhu, Hui Feng, Junru An, Jiansheng Liu, Weibo Li, Shenzhao Deng, Wandi Wang, Weiyi Zhang, Xiaoyan Zhang, Guangbao Luo, Xin Wang, Sunil Kumar Sahu, Huan Liu, Richard Michelmore, Wanneng Yang, Tong Wei, Hanhui Kuang
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Genome Biology
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Online Access:https://doi.org/10.1186/s13059-025-03541-6
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author Hongyun Chen
Jiongjiong Chen
Ruifang Zhai
Dean Lavelle
Yue Jia
Qiwei Tang
Ting Zhu
Menglu Wang
Zedong Geng
Jianzhong Zhu
Hui Feng
Junru An
Jiansheng Liu
Weibo Li
Shenzhao Deng
Wandi Wang
Weiyi Zhang
Xiaoyan Zhang
Guangbao Luo
Xin Wang
Sunil Kumar Sahu
Huan Liu
Richard Michelmore
Wanneng Yang
Tong Wei
Hanhui Kuang
author_facet Hongyun Chen
Jiongjiong Chen
Ruifang Zhai
Dean Lavelle
Yue Jia
Qiwei Tang
Ting Zhu
Menglu Wang
Zedong Geng
Jianzhong Zhu
Hui Feng
Junru An
Jiansheng Liu
Weibo Li
Shenzhao Deng
Wandi Wang
Weiyi Zhang
Xiaoyan Zhang
Guangbao Luo
Xin Wang
Sunil Kumar Sahu
Huan Liu
Richard Michelmore
Wanneng Yang
Tong Wei
Hanhui Kuang
author_sort Hongyun Chen
collection DOAJ
description Abstract Background Lettuce is a globally important leafy vegetable that exhibits diverse horticultural types and strong population structure, which complicates genetic analyses. To address this challenge, we develop the first multi-parent, advanced generation inter-cross (MAGIC) population for lettuce using 16 diverse founder lines. Results Whole-genome sequencing of the 16 founder lines and 381 inbred progeny reveal minimal population structure, enabling informative genome-wide association studies (GWAS). GWAS of the lettuce MAGIC population identifies numerous loci associated with key agricultural traits, including 51 for flowering time, 11 for leaf color, and 5 for leaf shape. Notably, loss-of-function mutations in the LsphyB and LsphyC genes, encoding phytochromes B and C, dramatically delay flowering in lettuce, which is in striking contrast to many other plant species. This unexpected finding highlights the unique genetic architecture controlling flowering time in lettuce. The wild-type LsTCP4 gene plays critical roles in leaf flatness and its expression level is negatively correlated with leaf curvature. Additionally, a novel zinc finger protein (ZFP) gene is required for the development of lobed leaves; a point mutation leads to its loss of function and consequently converted lobed leaves to non-lobed leaves, as exhibited by most lettuce cultivars. Conclusions The MAGIC population’s lack of structure and high mapping resolution enables the efficient dissection of complex traits. The identified loci and candidate genes provide significant genetic resources for improving agronomic performance and leaf quality in lettuce.
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spelling doaj-art-9dc36b22a34b43a3847a4d58a9459a242025-08-20T03:41:49ZengBMCGenome Biology1474-760X2025-03-0126112210.1186/s13059-025-03541-6Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC populationHongyun Chen0Jiongjiong Chen1Ruifang Zhai2Dean Lavelle3Yue Jia4Qiwei Tang5Ting Zhu6Menglu Wang7Zedong Geng8Jianzhong Zhu9Hui Feng10Junru An11Jiansheng Liu12Weibo Li13Shenzhao Deng14Wandi Wang15Weiyi Zhang16Xiaoyan Zhang17Guangbao Luo18Xin Wang19Sunil Kumar Sahu20Huan Liu21Richard Michelmore22Wanneng Yang23Tong Wei24Hanhui Kuang25National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityCollege of Informatics, Huazhong Agricultural UniversityGenome Center and Department of Plant Sciences, University of CaliforniaNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityCollege of Informatics, Huazhong Agricultural UniversityCollege of Informatics, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityBGI ResearchBGI ResearchNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityBGI ResearchState Key Laboratory of Genome and Multi-Omics Technologies, BGI ResearchGenome Center and Department of Plant Sciences, University of CaliforniaNational Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityBGI ResearchNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops; Hubei Hongshan Laboratory, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityAbstract Background Lettuce is a globally important leafy vegetable that exhibits diverse horticultural types and strong population structure, which complicates genetic analyses. To address this challenge, we develop the first multi-parent, advanced generation inter-cross (MAGIC) population for lettuce using 16 diverse founder lines. Results Whole-genome sequencing of the 16 founder lines and 381 inbred progeny reveal minimal population structure, enabling informative genome-wide association studies (GWAS). GWAS of the lettuce MAGIC population identifies numerous loci associated with key agricultural traits, including 51 for flowering time, 11 for leaf color, and 5 for leaf shape. Notably, loss-of-function mutations in the LsphyB and LsphyC genes, encoding phytochromes B and C, dramatically delay flowering in lettuce, which is in striking contrast to many other plant species. This unexpected finding highlights the unique genetic architecture controlling flowering time in lettuce. The wild-type LsTCP4 gene plays critical roles in leaf flatness and its expression level is negatively correlated with leaf curvature. Additionally, a novel zinc finger protein (ZFP) gene is required for the development of lobed leaves; a point mutation leads to its loss of function and consequently converted lobed leaves to non-lobed leaves, as exhibited by most lettuce cultivars. Conclusions The MAGIC population’s lack of structure and high mapping resolution enables the efficient dissection of complex traits. The identified loci and candidate genes provide significant genetic resources for improving agronomic performance and leaf quality in lettuce.https://doi.org/10.1186/s13059-025-03541-6LettuceGWASPhyBPhyCFlowering timeLobed leaves
spellingShingle Hongyun Chen
Jiongjiong Chen
Ruifang Zhai
Dean Lavelle
Yue Jia
Qiwei Tang
Ting Zhu
Menglu Wang
Zedong Geng
Jianzhong Zhu
Hui Feng
Junru An
Jiansheng Liu
Weibo Li
Shenzhao Deng
Wandi Wang
Weiyi Zhang
Xiaoyan Zhang
Guangbao Luo
Xin Wang
Sunil Kumar Sahu
Huan Liu
Richard Michelmore
Wanneng Yang
Tong Wei
Hanhui Kuang
Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population
Genome Biology
Lettuce
GWAS
PhyB
PhyC
Flowering time
Lobed leaves
title Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population
title_full Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population
title_fullStr Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population
title_full_unstemmed Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population
title_short Dissecting the genetic architecture of key agronomic traits in lettuce using a MAGIC population
title_sort dissecting the genetic architecture of key agronomic traits in lettuce using a magic population
topic Lettuce
GWAS
PhyB
PhyC
Flowering time
Lobed leaves
url https://doi.org/10.1186/s13059-025-03541-6
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