Xiaojian Fang, Hangqin Liu, Jiacheng Liu, Yang Song, Min Xu, Xing Jian, Li Dong, Qianwen Zhang, Le Xu, Guorui Fan, Zhaoying Wang, Yiwen You, Tianyu Feng, Wenyu Li, Yuling Li, Rentao Song, Zhongwei Lin
{"title":"Genome assembly and population genomic analysis reveal the genetic basis of popcorn evolution","authors":"Xiaojian Fang, Hangqin Liu, Jiacheng Liu, Yang Song, Min Xu, Xing Jian, Li Dong, Qianwen Zhang, Le Xu, Guorui Fan, Zhaoying Wang, Yiwen You, Tianyu Feng, Wenyu Li, Yuling Li, Rentao Song, Zhongwei Lin","doi":"10.1111/pbi.70125","DOIUrl":null,"url":null,"abstract":"SummaryPopcorn, one of the world's most popular snack foods, represents the most ancient type of maize domesticated by humans. However, the genetic basis underlying popcorn evolution and kernel‐popping traits remains largely unknown. In this study, we assembled a high‐quality genome sequence of the popcorn landrace <jats:italic>Strawberry Popcorn</jats:italic> (SP) and conducted extensive population genomic analyses. The SP genome spans 2.3 Gb and harbours a large inversion on chromosome 8, along with millions of genetic variants that enable the discovery of beneficial alleles. Translocations and substantial duplications of the <jats:italic>Ga1</jats:italic> gene occurred in the locus associated with unilateral cross‐incompatibility on chromosome 4. Tandemly duplicated <jats:italic>Ga1</jats:italic> genes underwent pseudogenisation and truncation with complete loss of gene function. The <jats:italic>P1</jats:italic> gene experienced gene expansion and regulatory modifications, leading to downregulation of transcription and subsequent loss of pericarp colour during maize domestication and improvement. Population genomic analysis further identified a subset of 12 marker genes from over 2494 genes under human selection, which were reshaped to enhance kernel‐popping traits during domestication. These marker genes include <jats:italic>Pl1</jats:italic> and <jats:italic>Dek1</jats:italic> for pericarp and aleurone layer thickness; <jats:italic>THP9</jats:italic>, <jats:italic>Sh2</jats:italic>, <jats:italic>SUS1</jats:italic>, <jats:italic>Smk10</jats:italic>, <jats:italic>KW1</jats:italic>, <jats:italic>O7</jats:italic>, and <jats:italic>NKD1</jats:italic> for protein and starch biosynthesis; and <jats:italic>VP5</jats:italic>, <jats:italic>CCD7</jats:italic>, and <jats:italic>Crti3</jats:italic> for carotene biosynthesis, which all influence endosperm vitreousness, a key factor determining kernel hardness for popping. Among these genes, <jats:italic>KW1</jats:italic> and <jats:italic>O7</jats:italic> stand out as pivotal genes with a significant impact on kernel‐popping performance. These results provide a wealth of gene targets to greatly accelerate the molecular breeding of improved popcorn varieties.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"46 1","pages":""},"PeriodicalIF":10.1000,"publicationDate":"2025-05-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Biotechnology Journal","FirstCategoryId":"5","ListUrlMain":"https://doi.org/10.1111/pbi.70125","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}
引用次数: 0
Abstract
SummaryPopcorn, one of the world's most popular snack foods, represents the most ancient type of maize domesticated by humans. However, the genetic basis underlying popcorn evolution and kernel‐popping traits remains largely unknown. In this study, we assembled a high‐quality genome sequence of the popcorn landrace Strawberry Popcorn (SP) and conducted extensive population genomic analyses. The SP genome spans 2.3 Gb and harbours a large inversion on chromosome 8, along with millions of genetic variants that enable the discovery of beneficial alleles. Translocations and substantial duplications of the Ga1 gene occurred in the locus associated with unilateral cross‐incompatibility on chromosome 4. Tandemly duplicated Ga1 genes underwent pseudogenisation and truncation with complete loss of gene function. The P1 gene experienced gene expansion and regulatory modifications, leading to downregulation of transcription and subsequent loss of pericarp colour during maize domestication and improvement. Population genomic analysis further identified a subset of 12 marker genes from over 2494 genes under human selection, which were reshaped to enhance kernel‐popping traits during domestication. These marker genes include Pl1 and Dek1 for pericarp and aleurone layer thickness; THP9, Sh2, SUS1, Smk10, KW1, O7, and NKD1 for protein and starch biosynthesis; and VP5, CCD7, and Crti3 for carotene biosynthesis, which all influence endosperm vitreousness, a key factor determining kernel hardness for popping. Among these genes, KW1 and O7 stand out as pivotal genes with a significant impact on kernel‐popping performance. These results provide a wealth of gene targets to greatly accelerate the molecular breeding of improved popcorn varieties.
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.