群体基因组分析揭示玉米胚性愈伤组织诱导能力的关键遗传变异与驱动力

doi:10.1016/j.jia.2023.06.032

摘要/Abstract

摘要：

玉米遗传转化高度依赖于幼胚诱导的胚性愈伤组织（embryonic callus, EC），而玉米胚性愈伤组织的诱导能力具有严重的基因型限制。本研究对具有不同胚性愈伤组织诱导能力的80份玉米自交系进行了基因组测序，利用新开发的流程工具（MQ2Gpipe）构建了该群体的高密度变异图谱。基于胚性愈伤组织诱导率（ratio of embryonic callus induction, REC）表型，将该群体划分成三个亚群。与高REC亚群相比，低REC亚群具有更丰富的遗传多样性。结合全基因组受选择区域分析与候选区段关联分析，本研究鉴定了与REC相关的95.23 Mb的遗传分化区域及43个关联REC的遗传变异。这些变异位点可以解释21.46%–49.46%的REC表型变异。在这些显著关联位点的连锁不平衡区域内共鉴定到103个与愈伤诱导能力相关的候选基因。这些基因主要参与了细胞周期调控、细胞分裂素调控等过程，其中MYB15和EMB2745基因位于前人报道的一个与愈伤组织诱导相关的主效QTL区间。本研究发现，多个具有正效应的穗上叶面积遗传位点与几个高REC 关联的位点紧密连锁，这意味着在现代玉米自交系的选育过程中，高REC自交系可能在育种家选择优良株叶型的同时受到了协同负向选择而被淘汰。

Abstract:

Genetic transformation has been an effective technology for improving the agronomic traits of maize. However, it is highly reliant on the use of embryonic callus (EC) and shows a serious genotype dependence. In this study, we performed genomic sequencing for 80 core maize germplasms and constructed a high-density genomic variation map using our newly developed pipeline (MQ2Gpipe). Based on the induction rate of EC (REC), these inbred lines were categorized into three subpopulations. The low-REC germplasms displayed more abundant genetic diversity than the high-REC germplasms. By integrating a genome-wide selective signature screen and region-based association analysis, we revealed 95.23 Mb of selective regions and 43 REC-associated variants. These variants had phenotypic variance explained values ranging between 21.46 and 49.46%. In total, 103 candidate genes were identified within the linkage disequilibrium regions of these REC-associated loci. These genes mainly participate in regulation of the cell cycle, regulation of cytokinesis, and other functions, among which MYB15 and EMB2745 were located within the previously reported QTL for EC induction. Numerous leaf area-associated variants with large effects were closely linked to several REC-related loci, implying a potential synergistic selection of REC and leaf size during modern maize breeding.

Key words: maize , genetic transformation , embryonic callus , selective signal , association analysis

Peng Liu, Langlang Ma, Siyi Jian, Yao He, Guangsheng Yuan, Fei Ge, Zhong Chen, Chaoying Zou, Guangtang Pan, Thomas Lübberstedt, Yaou Shen. 群体基因组分析揭示玉米胚性愈伤组织诱导能力的关键遗传变异与驱动力[J]. Journal of Integrative Agriculture, 2024, 23(7): 2178-2195.

Peng Liu, Langlang Ma, Siyi Jian, Yao He, Guangsheng Yuan, Fei Ge, Zhong Chen, Chaoying Zou, Guangtang Pan, Thomas Lübberstedt, Yaou Shen. Population genomic analysis reveals key genetic variations and the driving force for embryonic callus induction capability in maize[J]. Journal of Integrative Agriculture, 2024, 23(7): 2178-2195.

参考文献

Alexander D, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655–1664.

Armstrong C, Green C. 1985. Establishment and maintenance of friable, embryogenic maize callus and the involvement of L-proline. Planta, 164, 207–214.

Astutik M, Suhartanto B, Umami N, Suseno N, Haq M. 2022. Auxin and cytokinin effect on in vitro callus induction of maize (Zea mays L.) srikandi putih. Atlantis Press, France. pp. 1–5.

Van der Auwera G, Carneiro M, Hartl C, Poplin R, del Angel G, Levy-Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J, Banks E, Garimella K V, Altshuler D, Gabriel S, DePristo M. 2013. From FastQ data to high-confidence variant calls: The genome analysis toolkit best practices pipeline. Current Protocols in Bioinformatics, 43, 11.10.1–11.10.33.

Badu-Apraku B, Fakorede M. 2017. Morphology and physiology of maize. Advances in Genetic Enhancement of Early and Extra-Early Maize for Sub-Saharan Africa. Springer, Cham, Switzerland. pp. 33–53.

Bhat J A, Yu D, Bohra A, Ganie S A, Varshney R K. 2021. Features and applications of haplotypes in crop breeding. Communications Biology, 4, 1–12.

Bouchabké-Coussa O, Obellianne M, Linderme D, Montes E, Maia-Grondard A, Vilaine F, Pannetier C. 2013. Wuschel overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro. Plant Cell Reports, 32, 675–686.

Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.

Browning B L, Zhou Y, Browning S R. 2018. A one-penny imputed genome from next-generation reference panels. The American Journal of Human Genetics, 103, 338–348.

Chen B, Maas L, Figueiredo D, Zhong Y, Reis R, Li M, Horstman A, Riksen T, Weemen M, Liu H, Siemons C, Chen S, Angenent G C, Boutilier K. 2022. BABY BOOM regulates early embryo and endosperm development. Proceedings of the National Academy of Sciences of the United States of America, 119, e2201761119.

Chen M, Li X, Cai Y, Zhang Y, Gu J, Yang L. 2020. Identification and expression pattern analysis of YUCCA and ARF gene families during somatic embryogenesis of Lilium spp. Biologia Plantarum, 64, 385–394.

Chen S, Zhou Y, Chen Y, Gu J. 2018. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34, i884–i890.

Cheng Y, Liu H, Cao L, Wang S, Li Y, Zhang Y, Jiang W, Zhou Y, Wang H. 2015. Down-regulation of multiple CDK inhibitor ICK/KRP genes promotes cell proliferation, callus induction and plant regeneration in Arabidopsis. Frontiers in Plant Science, 6, 825.

Climenco O, Kravchenko A, Jacota A. 2010. Callus genesis, somatic embryogenesis and plant regeneration in F1 hybrids of maize. Maize Genetics Cooperation Newsletter. Columbia, Maize Genetics Executive Committee (MGEC). USA. p. 10.

Czech L, Exposito-Alonso M. 2022. Grenepipe: A flexible, scalable and reproducible pipeline to automate variant calling from sequence reads. Bioinformatics, 38, 4809–4811.

Dai L, Han S, Zhang Y, Hao D. 2022a. Genetic architecture of embryogenic callus induction in maize from the perspective of population genomics. Plant Cell, Tissue and Organ Culture (PCTOC), 150, 345–359.

Dai L, Zhang Y, Han S, Hao D. 2022b. QTL mapping of somatic regeneration-related traits in maize. Agriculture, 12, 393.

Dai W, Yu H, Liu K, Cheng X, Yan J, Zhang C, Xi N, Liu H, Xiang C, Zou C, Zhang M, Gao S, Pan G, Ma L, Shen Y. 2023. Combined linkage mapping and association analysis uncovers candidate genes for 25 leaf-related traits across three environments in maize. Theoretical and Applied Genetics, 136, 1–14.

Dai X, Liu N, Wang L, Li J, Zheng X, Xiang F, Liu Z. 2020. MYB94 and MYB96 additively inhibit callus formation via directly repressing LBD29 expression in Arabidopsis thaliana. Plant Science, 293, 110323.

Danecek P, Auton A, Abecasis G, Albers C, Banks E, DePristo M, Handsaker R, Lunter G, Marth G, Sherry S, McVean G, Durbin R. 2011. The variant call format and VCFtools. Bioinformatics, 27, 2156–2158.

Danecek P, Bonfield J, Liddle J, Marshall J, Ohan V, Pollard M, Whitwham A, Keane T, McCarthy S, Davies R, Li H. 2021. Twelve years of SAMtools and BCFtools. GigaScience, 10, giab008.

Datta A. 2013. Genetic engineering for improving quality and productivity of crops. Agriculture & Food Security, 2, 15.

Diao S, Luo Y, Ma Y, Deng X, He Y, Gao N, Zhang H, Li J, Chen Z, Zhang Z. 2018. Genome-wide detection of selective signatures in a Duroc pig population. Journal of Integrative Agriculture, 17, 2528–2535.

Du X, Fang T, Liu Y, Huang L, Zang M, Wang G, Liu Y, Fu J. 2019. Transcriptome profiling predicts new genes to promote maize callus formation and transformation. Frontiers in Plant Science, 10, 1633.

Fan M, Xu C, Xu K, Hu Y. 2012. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Research, 22, 1169–1180.

Fang L, Wang Q, Hu Y, Jia Y, Chen J, Liu B, Zhang Z, Guan X, Chen S, Zhou B, Mei G, Sun J, Pan Z, He S, Xiao S, Shi W, Gong W, Liu J, Ma J, Cai C, et al. 2017. Genomic analyses in cotton identify signatures of selection and loci associated with fiber quality and yield traits. Nature Genetics, 49, 1089–1098.

Fehér A. 2015. Somatic embryogenesis - Stress-induced remodeling of plant cell fate. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1849, 385–402.

Feng K, Hou X L, Xing G M, Liu J X, Duan A Q, Xu Z S, Li M Y, Zhuang J, Xiong A S. 2020. Advances in AP2/ERF super-family transcription factors in plant. Critical Reviews in Biotechnology, 40, 750–776.

Jiang F, Guo M, Yang F, Duncan K, Jackson D, Rafalski A, Wang S, Li B. 2012. Mutations in an AP2 transcription factor-like gene affect internode length and leaf shape in maize. PLoS ONE, 7, e37040.

Ge F, Luo X, Huang X, Zhang Y, He X, Liu M, Lin H, Peng H, Li L, Zhang Z, Pan G, Shen Y. 2016. Genome-wide analysis of transcription factors involved in maize embryonic callus formation. Physiologia Plantarum, 158, 452–462.

Guo M, Rupe M A, Dieter J A, Zou J, Spielbauer D, Duncan K E, Howard R J, Hou Z, Simmons C R. 2010. Cell number regulator1 affects plant and organ size in maize: Implications for crop yield enhancement and heterosis. The Plant Cell, 22, 1057–1073.

Hallauer A, Lamkey K, White P. 1997. Registration of five inbred lines of maize: B102, B103, B104, B105, and B106. Crop Science, 37, 1405–1406.

van Heerwaarden J, Hufford M B, Ross-Ibarra J. 2012. Historical genomics of North American maize. Proceedings of the National Academy of Sciences of the United States of America, 109, 12420–12425.

Hodges T, Kamo K, Imbrie C, Becwar M. 1986. Genotype specificity of somatic embryogenesis and regeneration in maize. Nature Biotechnology, 4, 219–223.

Huang S, Gao Y, Li Y, Xu L, Tao H, Wang P. 2017. Influence of plant architecture on maize physiology and yield in the Heilonggang River valley. The Crop Journal, 5, 52–62.

Ikeuchi M, Sugimoto K, Iwase A. 2013. Plant callus: Mechanisms of induction and repression. The Plant Cell, 25, 3159–3173.

Ishida Y, Hiei Y, Komari T. 2007. Agrobacterium-mediated transformation of maize. Nature Protocols, 2, 1614–1621.

Iwase A, Ohme-Takagi M, Sugimoto K. 2011. WIND1: A key molecular switch for plant cell dedifferentiation. Plant Signaling & Behavior, 6, 1943–1948.

Junker A, Mönke G, Rutten T, Keilwagen J, Seifert M, Thi T M N, Renou J P, Balzergue S, Viehöver P, Hähnel U, Ludwig-Müller J, Altschmied L, Conrad U, Weisshaar B, Bäumlein H. 2012. Elongation-related functions of LEAFY COTYLEDON1 during the development of Arabidopsis thaliana. The Plant Journal, 71, 427–442.

Köster J, Rahmann S. 2012. Snakemake - A scalable bioinformatics workflow engine. Bioinformatics, 28, 2520–2522.

Letunic I, Bork P. 2021. Interactive Tree of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49, W293–W296.

Li C, Guan H, Jing X, Li Y Y, Wang B, Li Y X, Liu X, Zhang D, Liu C, Xie X, Zhao H, Wang Y, Liu J, Zhang P, Hu G, Li G, Li S, Sun D, Wang X, Shi Y, et al. 2022. Genomic insights into historical improvement of heterotic groups during modern hybrid maize breeding. Nature Plants, 8, 750–763.

Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv Preprint, arXiv:1303.3997.

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078–2079.

Li Y, Wang T. 2010. Germplasm base of maize breeding in China and formation of foundation parents. Journal of Maize Sciences, 18, 1–8. (in Chinese)

Li Z, Liu X, Xu X, Liu J, Sang Z, Yu K, Yang Y, Dai W, Jin X, Xu Y. 2020. Favorable haplotypes and associated genes for flowering time and photoperiod sensitivity identified by comparative selective signature analysis and GWAS in temperate and tropical maize. The Crop Journal, 8, 227–242.

Liang T, Hu Y, Xi N, Zhang M, Zou C, Ge F, Yuan G, Gao S, Zhang S, Pan G, Ma L, Lübberstedt T, Shen Y. 2023. GWAS across multiple environments and WGCNA suggest the involvement of ZmARF23 in embryonic callus induction from immature maize embryos. Theoretical and Applied Genetics, 136, 93.

Ligges U, Maechler M. 2003. Scatterplot3d - An R Package for visualizing multivariate data. Journal of Statistical Software, 8, 1–20.

Liu J, Qu J, Yang C, Tang D, Li J, Lan H, Rong T. 2015. Development of genome-wide insertion and deletion markers for maize, based on next-generation sequencing data. BMC Genomics, 16, 601.

Long Y, Liang T, Ma L, Liu P, Yang Y, Zhang X, Zou C, Zhang M, Ge F, Yuan G, Lübberstedt T, Pan G, Shen Y. 2022. Combined QTL mapping across multiple environments and co-expression network analysis identified key genes for embryogenic callus induction from immature maize embryos. International Journal of Molecular Sciences, 23, 8786.

Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho M J, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, et al. 2016. Morphogenic regulators baby boom and wuschel improve monocot transformation. The Plant Cell, 28, 1998–2015.

Lu Y, Shah T, Hao Z, Taba S, Zhang S, Gao S, Liu J, Cao M, Wang J, Prakash A B, Rong T, Xu Y. 2011. Comparative SNP and haplotype analysis reveals a higher genetic diversity and rapider LD decay in tropical than temperate germplasm in maize. PLoS ONE, 6, e24861.

Lu Y, Yan J, Guimarães C, Taba S, Hao Z, Gao S, Chen S, Li J, Zhang S, Vivek B, Magorokosho C, Mugo S, Makumbi D, Parentoni S N, Shah T, Rong T, Crouch J H, Xu Y. 2009. Molecular characterization of global maize breeding germplasm based on genome-wide single nucleotide polymorphisms. Theoretical and Applied Genetics, 120, 93–115.

Lurin C, Andreés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette M L, Mireau H, Peeters N, Renou J P, Szurek B, Taconnat L, Small I. 2004. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. The Plant Cell, 16, 2089–2103.

Maldonado C, Mora F, Scapim C A, Coan M. 2019. Genome-wide haplotype-based association analysis of key traits of plant lodging and architecture of maize identifies major determinants for leaf angle: hapLA4. PLoS ONE, 14, e0212925.

Malumbres M. 2014. Cyclin-dependent kinases. Genome Biology, 15, 122.

McLaren W, Gil L, Hunt S E, Riat H S, Ritchie G R S, Thormann A, Flicek P, Cunningham F. 2016. The ensembl variant effect predictor. Genome Biology, 17, 122.

Montesinos J, Abuzeineh A, Kopf A, Juanes-Garcia A, Ötvös K, Petrášek J, Sixt M, Benková E. 2020. Phytohormone cytokinin guides microtubule dynamics during cell progression from proliferative to differentiated stage. The EMBO Journal, 39, e104238.

Nielsen R. 2005. Molecular signatures of natural selection. Annual Review of Genetics, 39, 197–218.

Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. The Plant Cell, 19, 118–130.

Pan G, Zhang Z, Wei X, Song Y, Zhao M J, Xia Y. 2006. QTL analysis of maize (Zea mays L.) embryo culturing capacity. Acta Agronomica Sinica, 32, 7–13. (in Chinese)

Porebski S, Bailey L, Baum B. 1997. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter, 15, 8–15.

Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira M A R, Bender D, Maller J, Sklar P, de Bakker P I W, Daly M J, Sham P C. 2007. PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 81, 559–575.

Raji J A, Frame B, Little D, Santoso T J, Wang K. 2018. Agrobacterium- and biolistic-mediated transformation of maize B104 inbred. In: Methods in Molecular Biology. Humana Press, New York, USA. pp. 15–40.

Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A. 2001. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science, 294, 1519–1521.

Salvo S, Cook J, Carlson A R, Hirsch C, Kaeppler S M, Kaeppler H. 2018. Genetic fine-mapping of a quantitative trait locus (QTL) associated with embryogenic tissue culture response and plant regeneration ability in maize (Zea mays L.). The Plant Genome, 11, 170111.

de Sena Brandine G, Smith A. 2021. Falco: High-speed FastQC emulation for quality control of sequencing data. F1000Research, 8, 1874.

Serrote C, Reiniger L, Silva K, dos Santos Rabaiolli S, Stefanel C. 2020. Determining the polymorphism information content of a molecular marker. Gene, 726, 144175.

Shim H, Chasman D I, Smith J D, Mora S, Ridker P M, Nickerson D A, Krauss R M, Stephens M. 2015. A multivariate genome-wide association analysis of 10 LDL subfractions, and their response to statin treatment, in 1868 caucasians. PLoS ONE, 10, e0120758.

Singer J, Ruscheweyh H J, Hofmann A L, Thurnherr T, Singer F, Toussaint N C, Ng C K Y, Piscuoglio S, Beisel C, Christofori G, Dummer R, Hall M, Krek W, Levesque M P, Manz M G, Moch H, Papassotiropoulos A, Stekhoven D J, Wild P, Wüst T, et al. 2018. NGS-pipe: A flexible, easily extendable and highly configurable framework for NGS analysis. Bioinformatics, 34, 107–108.

Skoog F, Miller C O. 1957. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symposia of the Society for Experimental Biology, 11, 118–130.

Stephan W. 2019. Selective sweeps. Genetics, 211, 5–13.

Tariq M, Ali G, Hadi F, Ahmad S, Ali N, Shah A. 2008. Callus induction and in vitro plant regeneration of rice (Oryza sativa L.) under various conditions. Pakistan Journal of Biological Sciences, 11, 255–259.

Unterseer S, Pophaly S D, Peis R, Westermeier P, Mayer M, Seidel M A, Haberer G, Mayer K F X, Ordas B, Pausch H, Tellier A, Bauer E, Schön C. 2016. A comprehensive study of the genomic differentiation between temperate Dent and Flint maize. Genome Biology, 17, 137.

Utsunomiya Y T, Milanesi M, Utsunomiya A T H, Ajmone-Marsan P, Garcia J F. 2016. GHap: An R package for genome-wide haplotyping. Bioinformatics, 32, 2861–2862.

Wang K, Wu P, Chen D, Zhou J, Yang X, Jiang A, Ma J, Tang Q, Xiao W, Jiang Y, Zhu L, Qiu X, Li M, Li X, Tang G. 2021. Genome-wide scan for selection signatures based on whole-genome re-sequencing in Landrace and Yorkshire pigs, Journal of Integrative Agriculture, 20, 1898–1906.

Wang Y, He S, Long Y, Zhang X, Zhang X, Hu H, Li Z, Hou F, Ge F, Gao S, et al. 2022. Genetic variations in ZmSAUR15 contribute to the formation of immature embryo-derived embryonic calluses in maize. The Plant Journal, 109, 980–991.

Wójcikowska B, Gaj M D. 2017. Expression profiling of AUXIN RESPONSE FACTOR genes during somatic embryogenesis induction in Arabidopsis. Plant Cell Reports, 36, 843–858.

Wu Z, Yang X, Zhao Y, Jia L. 2022. Identifying candidate genes involved in trichome formation on carrot stems by transcriptome profiling and resequencing. Journal of Integrative Agriculture, 21, 3589–3599.

Xie W, Ding C, Hu H, Dong G, Zhang G, Qian Q, Ren D. 2022. Molecular events of rice AP2/ERF transcription factors. International Journal of Molecular Sciences, 23, 12013.

Yamaguchi M, Kato H, Yoshida S, Yamamura S, Uchimiya H, Umeda M. 2003. Control of in vitro organogenesis by cyclin-dependent kinase activities in plants. Proceedings of the National Academy of Sciences of the United States of America, 100, 8019–8023.

Yang C, Tang D, Qu J, Zhang L, Zhang L, Chen Z, Liu J. 2016. Genetic mapping of QTL for the sizes of eight consecutive leaves below the tassel in maize (Zea mays L.). Theoretical and Applied Genetics, 129, 2191–2209.

Yang J, Lee S H, Goddard M E, Visscher P M. 2011. GCTA: A tool for genome-wide complex trait analysis. The American Journal of Human Genetics, 88, 76–82.

Yang L, Zhou H, Bo W, Li Y, Pan X. 2019. Identification of genes related with jujube fruit size based on selective sweep analysis. Journal of Beijing Forestry University, 41, 30–36. (in Chinese)

Yang Y, Wang N, Zhao S. 2020. Functional characterization of a WRKY family gene involved in somatic embryogenesis in Panax ginseng. Protoplasma, 257, 449–458.

Yuan G, He D, Shi J, Li Y, Yang Y, Du J, Zou C, Ma L, Gao S, Pan G, Shen Y. 2023. Genome-wide association study discovers novel germplasm resources and genetic loci with resistance to Gibberella ear rot caused by Fusarium graminearum. Phytopathology, 113, 1317–1324.

Zaid C, Siffat U K, Zhang X, Leng P, Zong N, Zhao J. 2023. Characterization of transgenic wheat lines expressing maize ABP7 involved in kernel development. Journal of Integrative Agriculture, 22, 389–399.

Zeng L, Tu X, Dai H, Han F M, Lu B, Wang M, Nanaei H, Tajabadipour A, Mansouri M, Li X, Ji L, Irwin D, Zhou H, Liu M, Zheng H K, Esmailizadeh A, Wu D D. 2019. Whole genomes and transcriptomes reveal adaptation and domestication of pistachio. Genome Biology, 20, 79.

Zhang C, Dong S, Xu J, He W, Yang T. 2019. PopLDdecay: A fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics, 35, 1786–1788.

Zhang H, Liu Y, Guo X, Zhang F, Li J, Tan Z, Chen G, Sun D. 2006. QTL mapping for callus induction and plant regeneration in maize immature embryo. Acta Agronomica Sinica, 32, 385–389. (in Chinese)

Zhang W, Xu W, Zhang H, Liu X, Cui X, Li S, Song L, Zhu Y, Chen X, Chen H. 2021. Comparative selective signature analysis and high-resolution GWAS reveal a new candidate gene controlling seed weight in soybean. Theoretical and Applied Genetics, 134, 1329–1341.

Zhang X, Guan Z, Li Z, Liu P, Ma L, Zhang Y C, Pan L, He S, Zhang Y L, Li P, Ge F, Zou C, He Y, Gao S, Pan G, Shen Y. 2020. A combination of linkage mapping and GWAS brings new elements on the genetic basis of yield-related traits in maize across multiple environments. Theoretical and Applied Genetics, 133, 2881–2895.

Zhang X, Zhang H, Li L, Lan H, Ren Z, Liu D, Wu L, Liu H, Jaqueth J, Li B, Pan G, Gao S. 2016. Characterizing the population structure and genetic diversity of maize breeding germplasm in Southwest China using genome-wide SNP markers. BMC Genomics, 17, 1–16.

Zhao H, Tian R, Xia H, Li C, Li G, Li A, Zhang X, Zhou X, Ma J, Huang H, Zhang K, Thudi M, Ma C, Wang X, Zhao C. 2022. High-density genetic variation map reveals key candidate loci and genes associated with important agronomic traits in peanut. Frontiers in Genetics, 13, 845602.

Zheng M, Konzak C. 1999. Effect of 2,4-dichlorophenoxyacetic acid on callus induction and plant regeneration in anther culture of wheat (Triticum aestivum L.). Plant Cell Reports, 19, 69–73.

Zheng Q, Zheng Y, Ji H, Burnie W, Perry S E. 2016. Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiology, 172, 2374–2387.

Zhou X, Stephens M. 2012. Genome-wide efficient mixed-model analysis for association studies. Nature Genetics, 44, 821–824.