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Journal of Integrative Agriculture
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High-resolution mapping through whole-genome resequencing identifies two novel QTLs controlling oil content in peanut

Nian Liu, Huaiyong Luo, Li Huang, Xiaojing Zhou, Weigang Chen, Bei Wu, Jianbin Guo, Dongxin Huai, Yuning Chen, Yong Lei, Boshou Liao, Huifang Jiang#

Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of Chinese Academy of Agricultural Sciences, Wuhan 430062, China
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摘要  

提高含油量是花生育种的重要目标。精准鉴定含油量相关位点及其连锁标记能够有助于在高油育种中开展分子标记辅助选择。通过对包含295个家系的重组自交系(ZH16×J11)开展全基因组重测序,构建了一张高密度的遗传连锁图谱。该图谱的遗传长度为1162.3cM,包含了4212位点。在该图谱的6个连锁群上共发现了10个含油量的遗传位点(QTLs)。其中两个QTLsqOCB03.1  qOCB06.1)能够在至少三个环境下被重复检测到,其遗传解释率可达13.62%。这两个QTL尚未在之前的研究中被报道,推测可能是两个新的位点。在该重组自交系群体中,聚合了这两个优异等位位点的家系的含油量,比没有聚合的家系在四个环境下高出1.50%2.46%。针对这两个新位点开发的紧密连锁的分子标记在其它群体中(ZH10×ICG12625)也被证实跟含油量性状密切相关。这个两个位点分别被定位到B03染色体的1.77MbB06染色体的1.51Mb物理区间内。进一步通过目标位点基因组序列变异分析,转录组测序分析以及对目标变异位点的表型效应分析,在qOCB03.1  qOCB06.1定位区间内各发现了两个候选基因与含油量相关。该候选基因的挖掘可以为下一步的图位克隆含油量关键基因提供参考。本文发现的新的稳定QTL及其连锁分子标记对于指导分子标记辅助选择育种提高花生含油量具有重要价值。



Abstract  

Increasing oil content is a key objective in peanut breeding programs.  Accurate identification of quantitative trait loci (QTLs) with linked markers for oil content can greatly aid in marker-assisted selection for high-oil breeding.  In this study, a high-density bin map was constructed by resequencing a recombinant inbred line (RIL) population (ZH16×J11) consisting of 295 lines.  The bin map contained 4,212 loci and had a total length of 1,162.3 cM.  Ten QTLs for oil content were identified in six linkage groups.  Notably, two of these QTLs, qOCB03.1 and qOCB06.1, were consistently detected in a minimum of three environments and explained up to 13.62% of phenotypic variation.  They have not been reported in previous studies and thus are novel QTLs.  The combination of favorable alleles from the qOCB03.1 and qOCB06 in the RIL population could increase oil content across multiple environments from 1.50 to 2.46%.  Two InDel markers linked to qOCB03.1 and qOCB06.1 were developed and validated to be associated with oil content in another RIL population (ZH10×ICG12625) with diverse phenotypes.  Additionally, the high-resolution map allowed for the precise positioning of qOCB03.1 and qOCB06.1 within a 1.77 Mb-interval on chromosome B03 and a 1.51 Mb- interval on chromosome B06, respectively.  Annotation of genomic variants, analysis of transcriptome sequencing, and evaluation of the allelic effects in 292 peanut varieties revealed two candidate genes associated with oil content for each of the two QTLs.  The identification of candidate genes in this study can enable the map-based cloning of key genes controlling oil content in peanut.  Furthermore, these novel and stable QTLs and their tightly linked markers are valuable for marker-assisted breeding for increased oil content in peanut.

Keywords:  peanut       oil content        QTL mapping        whole genome resequencing  
Online: 30 August 2024  
Fund: 

This work was supported by the National Key Research and Development Program of China (2022YFD1200400), the National Natural Science Foundation of China (32161143006 and 31971903), the National Peanut Industry Technology System Construction, China (CARS13), the National Crop Germplasm Resources Center, China (NCGRC-2022-036), the National Program for Crop Germplasm Protection of China (19210163), the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2021-OCRI), and the Guangdong Provincial Key Research and Development Program-Modern Seed Industry, China (2022B0202060004).

About author:  Nian Liu, E-mail: lnian0531@163.com; #Correspondence Huifang Jiang, Tel: +86-28-87283955, E-mail: peanutlab@oilcrops.cn

Cite this article: 

Nian Liu, Huaiyong Luo, Li Huang, Xiaojing Zhou, Weigang Chen, Bei Wu, Jianbin Guo, Dongxin Huai, Yuning Chen, Yong Lei, Boshou Liao, Huifang Jiang. 2024. High-resolution mapping through whole-genome resequencing identifies two novel QTLs controlling oil content in peanut. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.08.028

Baring M R, Wilson J N, Burow M D, Simpson C E, Ayers J L, Cason J M. 2013. Variability of total oil content in peanut across the state of texas. Journal of Crop Improvement, 27, 125–136.

Beisson F, Koo A J K, Ruuska S, Schwender J, Pollard M, Thelen J J, Paddock T, Salas J J, Savage L, Milcamps A, Mhaske V B, Cho Y, Ohlrogge J B. 2003. Arabidopsis genes involved in acyl lipid metabolism. A 2003 Census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiology, 132, 681–697.

Bertioli D J, Cannon S B, Froenicke L, Huang G, Farmer A D, Cannon E K S, Liu X, Gao D, Clevenger J, Dash S, Ren L, Moretzsohn M C, Shirasawa K, Huang W, Vidigal B, Abernathy B, Chu Y, Niederhuth C E, Umale P, Araújo A C G, et al. 2016. The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nature Genetics, 48, 438–446.

Bertioli D J, Jenkins J, Clevenger J, Dudchenko O, Gao D, Seijo G, Leal-Bertioli S C M, Ren L, Farmer A D, Pandey M K, Samoluk S S, Abernathy B, Agarwal G, Ballén-Taborda C, Cameron C, Campbell J, Chavarro C, Chitikineni A, Chu Y, Dash S, et al. 2019. The genome sequence of segmental allotetraploid peanut Arachis hypogaea. Nature Genetics, 51, 877–884.

Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.

Chen X, Lu Q, Liu H, Zhang J, Hong Y, Lan H, Li H, Wang J, Liu H, Li S, Pandey M K, Zhang Z, Zhou G, Yu J, Zhang G, Yuan J, Li X, Wen S, Meng F, Yu S, et al. 2019. Sequencing of cultivated peanut, Arachis hypogaea, yields insights into genome evolution and oil improvement. Molecular Plant, 12, 920–934.

Dong Z, Alam M K, Xie M, Yang L, Liu J, Helal M M U, Huang J, Cheng X, Liu Y, Tong C, Zhao C, Liu S. 2021. Mapping of a major QTL controlling plant height using a high-density genetic map and QTL-seq methods based on whole-genome resequencing in Brassica napus. G3-Genes Genomes Genetics, 11, jkab118.

FAOSTAT (2021) Statistical database FAOSTAT. http://faostat3.fao. org

Gangurde S S, Wang H, Yaduru S, Pandey M K, Fountain J C, Chu Y, Isleib T, Holbrook C C, Xavier A, Culbreath A K, Ozias-Akins P, Varshney R K, Guo B. 2020. Nested-association mapping (NAM)-based genetic dissection uncovers candidate genes for seed and pod weights in peanut (Arachis hypogaea). Plant Biotechnology Journal, 18, 1457–1471.

Gu Q, Ke H, Liu Z, Lv X, Sun Z, Zhang M, Chen L, Yang J, Zhang Y, Wu L, Li Z, Wu J, Wang G, Meng C, Zhang G, Wang X, Ma Z. 2020. A high-density genetic map and multiple environmental tests reveal novel quantitative trait loci and candidate genes for fibre quality and yield in cotton. Theoretical and Applied Genetics, 133, 3395–3408.

Guo J, Liu N, Li W, Wu B, Chen H, Huang L, Chen W, Luo H, Zhou X, Jiang H. 2021. Identification of two major loci and linked marker for oil content in peanut (Arachis hypogaea L.). Euphytica, 217, 29.

Huang B, Liu H, Fang Y, Miao L, Qin L, Sun Z, Qi F, Chen L, Zhang F, Li S, Zeng Q, Shi L, Wu J, Dong W, Zhang X. 2023. Identification of oil content QTL on Arahy12 and Arahy16 and development of KASP markers in cultivated peanut (Arachis hypogaea L.). Journal of Integrative Agriculture, 10.1016/j.jia.2023.11.010

Huang L, He H, Chen W, Ren X, Chen Y, Zhou X, Xia Y, Wang X, Jiang X, Liao B. 2015. Quantitative trait locus analysis of agronomic and quality-related traits in cultivated peanut (Arachis hypogaea L.). Theoretical and Applied Genetics, 128, 1103–1115.

Jadhav M P, Gangurde S S, Hake A A, Yadawad A, Mahadevaiah S S, Pattanashetti S K, Gowda M V C, Shirasawa K, Varshney R K, Pandey M K, Bhat R S. 2021. Genotyping-by-sequencing based genetic mapping identified major and consistent genomic regions for productivity and quality traits in peanut. Frontiers in Plant Science, 12, 668020.

Janila P, Variath M T, Pandey M K, Desmae H, Motagi B N, Okori P, Manohar S S, Rathnakumar A L, Radhakrishnan T, Liao B, Varshney R K. 2016. Genomic tools in groundnut breeding program: Status and Perspectives. Frontiers in Plant Science, 7, 289.

Jiang Y, Luo H, Yu B, Ding Y, Kang Y, Huang L, Zhou X, Liu N, Chen W, Guo J, Huai D, Lei Y, Jiang H, Yan L, Liao B. 2021. High-density genetic linkage map construction using whole-genome resequencing for mapping QTLs of resistance to Aspergillus flavus infection in peanut. Frontiers in Plant Science, 12, 745408.

Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357–360.

Li B, Dewey C N. 2011. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 323.

Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754–1760.

Li Q T, Lu X, Song Q X, Chen H W, Wei W, Tao J J, Bian X H, Shen M, Ma B, Zhang W K, Bi Y D, Li W, Lai Y C, Lam S M, Shui G H, Chen S Y, Zhang J S. 2017. Selection for a Zinc-Finger protein contributes to seed oil increase during soybean domestication. Plant Physiology, 173, 2208–2224.

Liu H, Sun Z, Zhang X, Qin L, Qi F, Wang Z, Du P, Xu J, Zhang Z, Han S, Li S, Gao M, Zhang L, Cheng Y, Zheng Z, Huang B, Dong W. 2020. QTL mapping of web blotch resistance in peanut by high-throughput genome-wide sequencing. BMC Plant Biology, 20, 249.

Liu N, Guo J, Zhou X, Wu B, Huang L, Luo H, Chen Y, Chen W, Lei Y, Huang Y, Liao B, Jiang H. 2020a. High-resolution mapping of a major and consensus quantitative trait locus for oil content to a ~ 0.8-Mb region on chromosome A08 in peanut (Arachis hypogaea L.). Theoretical and Applied Genetics, 133, 37–49.

Liu N, Huang L, Chen W, Wu B, Pandey M K, Luo H, Zhou X, Guo J, Chen H, Huai D, Chen Y, Lei Y, Liao B, Ren X, Varshney R K, Jiang H. 2020b. Dissection of the genetic basis of oil content in Chinese peanut cultivars through association mapping. BMC Genetics, 21, 60.

Liu Y F, Li Q T, Lu X, Song Q X, Lam S M, Zhang W K, Ma B, Lin Q, Man W Q, Du W G, Shui G H, Chen S Y, Zhang J S. 2014. Soybean GmMYB73 promotes lipid accumulation in transgenic plants. BMC Plant Biology, 14, 73.

Lu L, Wei W, Li Q, Bian X, Lu X, Hu Y, Cheng T, Wang Z, Jin M, Tao J, Yin C, He S, Man W, Li W, Lai Y, Zhang W, Chen S, Zhang J. 2021. A transcriptional regulatory module controls lipid accumulation in soybean. New Phytologist, 231, 661–678.

Manan S, Chen B, She G, Wan X, Zhao J. 2017. Transport and transcriptional regulation of oil production in plants. Critical Reviews in Biotechnology, 37, 641–655.

Pandey M K, Pandey A K, Kumar R, Bhat R S, Liao B. 2020. Translational genomics for achieving higher genetic gains in groundnut. Theoretical and Applied Genetics, 133, 1679-1702

Pandey M K, Roorkiwal M, Singh V K, Ramalingam A, Kudapa H, Thudi M, Chitikineni A, Rathore A, Varshney R K. 2016. Emerging genomic tools for legume breeding: Current status and future prospects. Frontiers in Plant Science, 7, 455.

Pandey M K, Wang M L, Qiao L, Feng S, Khera P, Wang H, Tonnis B, Barkley N A, Wang J, Holbrook C C, Culbreath A K, Varshney R K, Guo B. 2014. Identification of QTLs associated with oil content and mapping FAD2 genes and their relative contribution to oil quality in peanut (Arachis hypogaeaL.). BMC Genetics, 15, 133.

Sarvamangala C, Gowda M V C, Varshney R K. 2011. Identification of quantitative trait loci for protein content, oil content and oil quality for groundnut (Arachis hypogaea L.). Field Crops Research, 122, 49–59.

Shasidhar Y, Vishwakarma M K, Pandey M K, Janila P, Variath M T, Manohar S S, Nigam S N, Guo B, Varshney R K. 2017. Molecular mapping of oil content and fatty acids using dense genetic maps in groundnut (Arachis hypogaea L.). Frontiers in Plant Science, 8, 794.

Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology, 4, 447–456.

Sun Z, Qi F, Liu H, Qin L, Xu J, Shi L, Zhang Z, Miao L, Huang B, Dong W, Wang X, Tian M, Feng J, Zhao R, Zheng Z, Zhang X. 2022. QTL mapping of quality traits in peanut using whole-genome resequencing. The Crop Journal, 10, 177–184.

Tian Y, Yang L, Lu H F, Zhang B, Li Y F, Liu C, Ge T L, Liu Y L, Han J N, Li Y H, Qiu L J. 2022. QTL analysis for plant height and fine mapping of two environmentally stable QTLs with major effects in. Journal of Integrative Agriculture, 21, 933-946.

Tsay Y F, Chiu C C, Tsai C B, Ho C H, Hsu P K. 2007. Nitrate transporters and peptide transporters. FEBS Letters, 581, 2290–2300.

Varshney R K. 2016. Exciting journey of 10 years from genomes to fields and markets: Some success stories of genomics-assisted breeding in chickpea, pigeonpea and groundnut. Plant Science, 242, 98–107.

Wang K, Li M, Hakonarson H. 2010. ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Research, 38, e164.

Wang L, Feng Z, Wang X, Wang X, Zhang X. 2010. DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 26, 136–138.

Wilson J, Baring M, Burow M, Rooney W, Simpson C. 2013. Generation means analysis of oil concentration in peanut. Journal of Crop Improvement, 27, 85–95.

Wilson J N, Chopra R, Baring M R, Selvaraj M G, Simpson C E, Chagoya J, Burow M D. 2017. Advanced backcross quantitative trait loci (QTL) analysis of oil concentration and oil quality traits in peanut (Arachis hypogaea L.). Tropical Plant Biology, 10, 1–17.

Wu Y, Bhat P R, Close T J, Lonardi S. 2008. Efficient and accurate construction of genetic linkage maps from the minimum spanning tree of a graph. Plos Genetics, 4, e1000212.

Xie W, Feng Q, Yu H, Huang X, Zhao Q, Xing Y, Yu S, Han B, Zhang Q. 2010. Parent-independent genotyping for constructing an ultrahigh-density linkage map based on population sequencing. Proceedings of the National Academy of Sciences of the United States of America, 107, 10578–10583.

Yang B, Wang J, Yu M, Zhang M, Zhong Y, Wang T, Liu P, Song W, Zhao H, Fastner A, Suter M, Rentsch D, Ludewig U, Jin W, Geiger D, Hedrich R, Braun D M, Koch K E, McCarty D R, Wu W, et al. 2022. The sugar transporter ZmSUGCAR1 of the nitrate transporter 1/peptide transporter family is critical for maize grain filling. The Plant Cell, 34, 4232–4254.

Yang Y, Li Y, Cheng Z, Su Q, Jin X, Song Y, Wang J. 2023. Genetic analysis and exploration of major effect QTLs underlying oil content in peanut. Theoretical and Applied Genetics, 136, 97.

Yol E, Ustun R, Golukcu M, Uzun B. 2017. Oil content, oil yield and fatty acid profile of groundnut germplasm in mediterranean climates. Journal of the American Oil Chemists Society, 94, 1–18.

Zhou H, Duan H, Liu Y, Sun X, Zhao J, Lin H. 2019. Patellin protein family functions in plant development and stress response. Journal of Plant Physiology, 234–235, 94–97.

Zhuang W, Chen H, Yang M, Wang J, Pandey M K, Zhang C, Chang W C, Zhang L, Zhang X, Tang R, Garg V, Wang X, Tang H, Chow C N, Wang J, Deng Y, Wang D, Khan A W, Yang Q, Cai T, et al. 2019. The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication. Nature Genetics, 51, 865–876.

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