Abstract
Starch is a major component of cereals, comprising over 70% of dry weight. It serves as a primary carbon source for humans and animals. In addition, starch is an indispensable industrial raw material. While maize (Zea mays) is a key crop and the primary source of starch, the genetic basis for starch content in maize kernels remains poorly understood. In this study, using an enlarged panel, we conducted a genome-wide association study (GWAS) based on best linear unbiased prediction (BLUP) value for starch content of 261 inbred lines across three environments. Compared with previous study, we identified 14 additional significant quantitative trait loci (QTL), encompassed a total of 42 genes, and indicated that increased marker density contributes to improved statistical power. By integrating gene expression profiling, Gene Ontology (GO) enrichment and haplotype analysis, several potential target genes that may play a role in regulating starch content in maize kernels have been identified. Notably, we found that ZmAPC4, associated with the significant SNP chr4.S_175584318, which encodes a WD40 repeat-like superfamily protein and is highly expressed in maize endosperm, might be a crucial regulator of maize kernel starch synthesis. Out of the 261 inbred lines analyzed, they were categorized into four haplotypes. Remarkably, it was observed that the inbred lines harboring hap4 demonstrated the highest starch content compared to the other haplotypes. Additionally, as a significant achievement, we have developed molecular markers that effectively differentiate maize inbred lines based on their starch content. Overall, our study provides valuable insights into the genetic basis of starch content and the molecular markers can be useful in breeding programs aimed at developing maize varieties with high starch content, thereby improving breeding efficiency.
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Data availability
The genotype dataset included in this study is available in an online repository http://www.maizego.org/Resources.html.
References
Abu-Zaitoon YM, Bennett K, Normanly J, Nonhebel HM (2012) A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain-specific YUCCA. Physiol Plant 146(4):487–499. https://doi.org/10.1111/j.1399-3054.2012.01649
Basunia MA, Nonhebel HM (2019) Hormonal regulation of cereal endosperm development with a focus on rice (Oryza sativa). Funct Plant Biol 46(6):493–506. https://doi.org/10.1071/FP18323
Bello BK, Hou Y, Zhao J, Jiao G, Wu Y, Li Z, Wang Y, Tong X, Wang W, Yuan W, Wei X, Zhang J (2019) NF-YB1-YC12-bHLH144 complex directly activates Wx to regulate grain quality in rice (Oryza sativa L.). Plant Biotechnol J 17(7):1222–1235. https://doi.org/10.1111/pbi.13048
Best NB, Addo-Quaye C, Kim BS, Weil CF, Schulz B, Johal G, Dilkes BP (2021) Mutation of the nuclear pore complex component, aladin1, disrupts asymmetric cell division in Zea mays (maize). G3 (Bethesda) 11(7):jkab106. https://doi.org/10.1093/g3journal/jkab106
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Chang H, Hoshina N, Zhang C, Ma Y, Cao H, Wang Y, Wu DD, Bergen SE, Landén M, Hultman CM, Preisig M, Kutalik Z, Castelao E, Grigoroiu-Serbanescu M, Forstner AJ, Strohmaier J, Hecker J, Schulze TG, Müller-Myhsok B et al (2018) The protocadherin 17 gene affects cognition, personality, amygdala structure and function, synapse development and risk of major mood disorders. Mol Psychiatry 23(2):400–412. https://doi.org/10.1038/mp.2016.231
Chen E, Yu H, He J, Peng D, Zhu P, Pan S, Wu X, Wang J, Ji C, Chao Z, Xu Z, Wu Y, Chao D, Wu Y, Zhang Z (2023) The transcription factors ZmNAC128 and ZmNAC130 coordinate with Opaque2 to promote endosperm filling in maize. Plant Cell:koad215. https://doi.org/10.1093/plcell/koad215
Chen J, Wang Y, Wang F, Yang J, Gao M, Li C, Liu Y, Liu Y, Yamaji N, Ma JF, Paz-Ares J, Nussaume L, Zhang S, Yi K, Wu Z, Wu P (2015b) The rice CK2 kinase regulates trafficking of phosphate transporters in response to phosphate levels. Plant Cell 27(3):711–723. https://doi.org/10.1105/tpc.114.135335
Chen M, Zhang B, Li C, Kulaveerasingam H, Chew FT, Yu H (2015a) TRANSPARENT TESTA GLABRA1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiol 169(1):391–402. https://doi.org/10.1104/pp.15.00943
Chen W, Chen L, Zhang X, Yang N, Guo J, Wang M, Ji S, Zhao X, Yin P, Cai L, Xu J, Zhang L, Han Y, Xiao Y, Xu G, Wang Y, Wang S, Wu S, Yang F et al (2022) Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science 375(6587):eabg7985. https://doi.org/10.1126/science.abg7985
Cross FR, Umen JG (2015) The Chlamydomonas cell cycle. Plant J 82(3):370–392. https://doi.org/10.1111/tpj.12795
Dante RA, Larkins BA, Sabelli PA (2014) Cell cycle control and seed development. Front Plant Sci 23(5):493. https://doi.org/10.3389/fpls.2014.00493
Ding L, Zhao K, Zhang X, Song A, Su J, Hu Y, Zhao W, Jiang J, Chen F (2019) Comprehensive characterization of a floral mutant reveals the mechanism of hooked petal morphogenesis in Chrysanthemum morifolium. Plant Biotechnol J 17(12):2325–2340. https://doi.org/10.1111/pbi.13143
Dong Q, Xu Q, Kong J, Peng X, Zhou W, Chen L, Wu J, Xiang Y, Jiang H, Cheng B. (2019) Overexpression of ZmbZIP22 gene alters endosperm starch content and composition in maize and rice. 283:407-415. https://doi.org/10.1016/j.plantsci.2019.03.001.
Dossa K, Zhou R, Li D, Liu A, Qin L, Mmadi MA, Su R, Zhang Y, Wang J, Gao Y, Zhang X, You J (2021) A novel motif in the 5’-UTR of an orphan gene ‘Big Root Biomass’ modulates root biomass in sesame. Plant Biotechnol J 19(5):1065–1079. https://doi.org/10.1111/pbi.13531
Everett LJ, Huang W, Zhou S, Carbone MA, Lyman RF, Arya GH, Geisz MS, Ma J, Morgante F, St Armour G, Turlapati L, Anholt RRH, Mackay TFC (2020) Gene expression networks in the Drosophila Genetic Reference Panel. Genome Res 30(3):485–496. https://doi.org/10.1101/gr.257592.119
Finegan C, Boehlein SK, Leach KA, Madrid G, Hannah LC, Koch KE, Tracy WF, Resende MFR Jr (2022) Genetic perturbation of the starch biosynthesis in maize endosperm reveals sugar-responsive gene networks. Front Plant Sci 12:800326. https://doi.org/10.3389/fpls.2021.800326
Fu FF, Xue HW (2010) Co-expression analysis identifies Rice Starch Regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154(2):927–938. https://doi.org/10.1104/pp.110.159517
Gong J, Schumacher F, Lim U, Hindorff LA, Haessler J, Buyske S, Carlson CS, Rosse S, Bůžková P, Fornage M, Gross M, Pankratz N, Pankow JS, Schreiner PJ, Cooper R, Ehret G, Gu CC, Houston D, Irvin MR et al (2013) Fine mapping and identification of BMI loci in African Americans. Am J Hum Genet 93(4):661–671. https://doi.org/10.1016/j.ajhg.2013.08.012
Guo L, Jiang L, Lu XL, Liu CM (2018) ANAPHASE PROMOTIN COMPLEX/CYCLOSOME-mediated cyclin B1 degradation is critical for cell cycle synchronization in syncytial endosperms. J Integr Plant Biol 60(6):448–454. https://doi.org/10.1111/jipb.12641
Guo Z, Yang Q, Huang F, Zheng H, Sang Z, Xu Y, Zhang C, Wu K, Tao J, Prasanna BM, Olsen MS, Wang Y, Zhang J, Xu Y (2021) Development of high-resolution multiple-SNP arrays for genetic analyses and molecular breeding through genotyping by target sequencing and liquid chip. Plant Commun 2(6):100230. https://doi.org/10.1016/j.xplc.2021.100230
Han X, Zhang D, Hao H, Luo Y, Zhu Z, Kuai B (2023) Transcriptomic analysis of three differentially senescing maize (Zea mays L.) inbred lines upon heat stress. Int J Mol Sci 24(12):9782. https://doi.org/10.3390/ijms24129782
Hoopes GM, Hamilton JP, Wood JC, Esteban E, Pasha A, Vaillancourt B, Provart NJ, Buell CR (2019) An updated gene atlas for maize reveals organ-specific and stress-induced genes. Plant J 97(6):1154–1167. https://doi.org/10.1111/tpj.14184
Hu S, Wang M, Zhang X, Chen W, Song X, Fu X, Fang H, Xu J, Xiao Y, Li Y, Bai G, Li J, Yang X (2021) Genetic basis of kernel starch content decoded in a maize multi-parent population. Plant Biotechnol J 19(11):2192–2205. https://doi.org/10.1111/pbi.13645
Jeon JS, Ryoo N, Hahn TR, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiol Biochem 48(6):383–392. https://doi.org/10.1016/j.plaphy.2010.03.006
Kaushik RP, Khush GS (1991) Genetic analysis of endosperm mutants in rice Oryza sativa L. Theor Appl Genet 83(2):146–152. https://doi.org/10.1007/BF00226243
Kumar S, Li G, Huang X, Ji Q, Zhou K, Hou H, Ke W, Yang J (2021) Phenotypic, nutritional, and antioxidant characterization of blanched Oenanthe javanica for preferable cultivar. Front Plant Sci 12:639639. https://doi.org/10.3389/fpls.2021.639639
Leiva-Neto JT, Grafi G, Sabelli PA, Dante RA, Woo YM, Maddock S, Gordon-Kamm WJ, Larkins BA (2004) A dominant negative mutant of cyclin-dependent kinase A reduces endoreduplication but not cell size or gene expression in maize endosperm. Plant Cell 16(7):1854–1869. https://doi.org/10.1105/tpc.022178
Li C, Huang Y, Huang R, Wu Y, Wang W (2018b) The genetic architecture of amylose biosynthesis in maize kernel. Plant Biotechnol J 16(2):688–695. https://doi.org/10.1111/pbi.12821
Li C, Yue Y, Chen H, Qi W, Song R (2018a) The ZmbZIP22 transcription factor regulates 27-kD γ-zein gene transcription during maize endosperm development. Plant Cell 30(10):2402–2424. https://doi.org/10.1105/tpc.18.00422
Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N, Liu J, Warburton ML, Cheng Y, Hao X, Zhang P, Zhao J, Liu Y, Wang G, Li J, Yan J (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45(1):43–50. https://doi.org/10.1038/ng.2484
Li M, Zhang YW, Xiang Y, Liu MH, Zhang YM (2022) IIIVmrMLM: the R and C++ tools associated with 3VmrMLM, a comprehensive GWAS method for dissecting quantitative traits. Mol Plant 15(8):1251–1253. https://doi.org/10.1016/j.molp.2022.06.002
Liu G, Wu Y, Xu M, Gao T, Wang P, Wang L, Guo T, Kang G (2016b) Virus-induced gene silencing identifies an important role of the TaRSR1 transcription factor in starch synthesis in bread wheat. Int J Mol Sci 17(10):1557. https://doi.org/10.3390/ijms17101557
Liu J, Wu MW, Liu CM (2022) Cereal endosperms: development and storage product accumulation. Annu Rev Plant Biol 73:255–291. https://doi.org/10.1146/annurev-arplant-070221-024405
Liu N, Xue Y, Guo Z, Li W, Tang J (2016a) Genome-wide association study identifies candidate genes for starch content regulation in maize kernels. Front Plant Sci 7:1046. https://doi.org/10.3389/fpls.2016.01046
McGeachie MJ, Wu AC, Tse SM, Clemmer GL, Sordillo J, Himes BE, Lasky-Su J, Chase RP, Martinez FD, Weeke P, Shaffer CM, Xu H, Denny JC, Roden DM, Panettieri RA Jr, Raby BA, Weiss ST, Tantisira KG (2015) CTNNA3 and SEMA3D: promising loci for asthma exacerbation identified through multiple genome-wide association studies. J Allergy Clin Immunol 136(6):1503–1510. https://doi.org/10.1016/j.jaci.2015.04.039
Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18(12):613–615. https://doi.org/10.1016/s0168-9525(02)02820-2
Pal S, Gupta R, Kim H, Wickramasinghe P, Baubet V, Showe LC, Dahmane N, Davuluri RV (2011) Alternative transcription exceeds alternative splicing in generating the transcriptome diversity of cerebellar development. Genome Res 21(8):1260–1272. https://doi.org/10.1101/gr.120535.111
Qin P, Zhang G, Hu B, Wu J, Chen W, Ren Z, Liu Y, Xie J, Yuan H, Tu B, Ma B, Wang Y, Ye L, Li L, Xiang C, Li S (2021) Leaf-derived ABA regulates rice seed development via a transporter-mediated and temperature-sensitive mechanism. Sci Adv 7(3):eabc8873. https://doi.org/10.1126/sciadv.abc8873
Sabelli PA, Liu Y, Dante RA, Lizarraga LE, Nguyen HN, Brown SW, Klingler JP, Yu J, LaBrant E, Layton TM, Feldman M, Larkins BA (2013) Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endosperm. Proc Natl Acad Sci USA 110(19):E1827–E1836. https://doi.org/10.1073/pnas.1304903110
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Setter TL, Yan J, Warburton M, Ribaut JM, Xu Y, Sawkins M, Buckler ES, Zhang Z, Gore MA (2011) Genetic association mapping identifies single nucleotide polymorphisms in genes that affect abscisic acid levels in maize floral tissues during drought. J Exp Bot 62(2):701–716. https://doi.org/10.1093/jxb/erq308
She KC, Kusano H, Koizumi K, Yamakawa H, Hakata M, Imamura T, Fukuda M, Naito N, Tsurumaki Y, Yaeshima M, Tsuge T, Matsumoto K, Kudoh M, Itoh E, Kikuchi S, Kishimoto N, Yazaki J, Ando T, Yano M et al (2010) A novel factor FLOURY ENDOSPERM2 is involved in regulation of rice grain size and starch quality. Plant Cell 22(10):3280–3294. https://doi.org/10.1105/tpc.109.070821
Song L, Yu D, Zheng H, Wu G, Sun Y, Li P, Wang J, Wang C, Lv B, Tang X (2021) Weighted gene co-expression network analysis unveils gene networks regulating folate biosynthesis in maize endosperm. 3 Biotech 11(10):441. https://doi.org/10.1007/s13205-021-02974-7
Song Y, Luo G, Shen L, Yu K, Yang W, Li X, Sun J, Zhan K, Cui D, Liu D, Zhang A (2020) TubZIP28, a novel bZIP family transcription factor from Triticum urartu, and TabZIP28, its homologue from Triticum aestivum, enhance starch synthesis in wheat. New Phytol 226(5):1384–1398. https://doi.org/10.1111/nph.16435
Sreenivasulu N, Radchuk V, Alawady A, Borisjuk L, Weier D, Staroske N, Fuchs J, Miersch O, Strickert M, Usadel B, Wobus U, Grimm B, Weber H, Weschke W (2010) De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8. Plant J 64(4):589–603. https://doi.org/10.1111/j.1365-313X.2010.04350.x
Sun G, Zhang X, Duan H, Gao J, Li N, Su P, Xie H, Li W, Fu Z, Huang Y, Tang J (2022) Dissection of the genetic architecture of peduncle vascular bundle-related traits in maize by a genome-wide association study. Plant Biotechnol J 20(6):1042–1053. https://doi.org/10.1111/pbi.13782
Tedja MS, Wojciechowski R, Hysi PG, Eriksson N, Furlotte NA, Verhoeven VJM, Iglesias AI, Meester-Smoor MA, Tompson SW, Fan Q, Khawaja AP, Cheng CY, Höhn R, Yamashiro K, Wenocur A, Grazal C, Haller T, Metspalu A, Wedenoja J et al (2018) Genome-wide association meta-analysis highlights light-induced signaling as a driver for refractive error. Nat Genet 50(6):834–848. https://doi.org/10.1038/s41588-018-0127-7
Tetlow IJ (2011) Starch biosynthesis in developing seeds. Seed Sci Res 21(1):5–32
Wang T, Wang M, Hu S, Xiao Y, Tong H, Pan Q, Xue J, Yan J, Li J, Yang X (2015) Genetic basis of maize kernel starch content revealed by high-density single nucleotide polymorphism markers in a recombinant inbred line population. BMC Plant Biol 15:288. https://doi.org/10.1186/s12870-015-0675-2
Wang Y, Liu W, Wang H, Du Q, Fu Z, Li WX, Tang J (2020) ZmEHD1 is required for kernel development and vegetative growth through regulating auxin homeostasis. Plant Physiol 182(3):1467–1480. https://doi.org/10.1104/pp.19.01336
Wu B, Chang H, Marini R, Chopra S, Reddivari L (2021) Characterization of maize near-isogenic lines with enhanced flavonoid expression to be used as tools in diet-health complexity. Front Plant Sci 11:619598. https://doi.org/10.3389/fpls.2020.619598
Wu J, Chen L, Chen M, Zhou W, Dong Q, Jiang H, Cheng B (2019) The DOF-domain transcription factor ZmDOF36 positively regulates starch synthesis in transgenic maize. Front Plant Sci 10:465. https://doi.org/10.3389/fpls.2019.00465
Wu MW, Zhao H, Zhang JD, Guo L, Liu CM (2020) RADICLELESS 1 (RL1)-mediated nad4 intron 1 splicing is crucial for embryo and endosperm development in rice (Oryza sativa L.). Biochem Biophys Res Commun 523(1):220–225. https://doi.org/10.1016/j.bbrc.2019.11.084
Wu X, Liu J, Li D, Liu CM (2016) Rice caryopsis development II: dynamic changes in the endosperm. J Integr Plant Biol 58(9):786–798. https://doi.org/10.1111/jipb.12488
Xiao Q, Wang Y, Du J, Li H, Wei B, Wang Y, Li Y, Yu G, Liu H, Zhang J, Liu Y, Hu Y, Huang Y (2017) ZmMYB14 is an important transcription factor involved in the regulation of the activity of the ZmBT1 promoter in starch biosynthesis in maize. FEBS J 284(18):3079–3099. https://doi.org/10.1111/febs.14179
Yamaguchi-Kabata Y, Nakazono K, Takahashi A, Saito S, Hosono N, Kubo M, Nakamura Y, Kamatani N (2008) Japanese population structure, based on SNP genotypes from 7003 individuals compared to other ethnic groups: effects on population-based association studies. Am J Hum Genet 83(4):445–456. https://doi.org/10.1016/j.ajhg.2008.08.019
Yang N, Lu Y, Yang X, Huang J, Zhou Y, Ali F, Wen W, Liu J, Li J, Yan J (2014) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLoS Genet 10(9):e1004573. https://doi.org/10.1371/journal.pgen.1004573
Yang Q, Li Z, Li W, Ku L, Wang C, Ye J, Li K, Yang N, Li Y, Zhong T, Li J, Chen Y, Yan J, Yang X, Xu M (2013) CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci USA 110(42):16969–16974. https://doi.org/10.1073/pnas.1310949110
Yang X, Gao S, Xu S et al (2011) Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breed 28(4):511–526
Yang X, Yan J, Shah T, Warburton ML, Li Q, Li L, Gao Y, Chai Y, Fu Z, Zhou Y, Xu S, Bai G, Meng Y, Zheng Y, Li J (2010) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121(3):417–431. https://doi.org/10.1007/s00122-010-1320-y
Yin W, Xiao Y, Niu M, Meng W, Li L, Zhang X, Liu D, Zhang G, Qian Y, Sun Z, Huang R, Wang S, Liu CM, Chu C, Tong H (2020) ARGONAUTE2 enhances grain length and salt tolerance by activating BIG GRAIN3 to modulate cytokinin distribution in rice. Plant Cell 32(7):2292–2306. https://doi.org/10.1105/tpc.19.00542
Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208. https://doi.org/10.1038/ng1702
Zhang C, Zhu J, Chen S, Fan X, Li Q, Lu Y, Wang M, Yu H, Yi C, Tang S, Gu M, Liu Q (2019b) Wxlv, the ancestral allele of rice waxy gene. Mol Plant 12(8):1157–1166. https://doi.org/10.1016/j.molp.2019.05.011
Zhang F, Wu J, Sade N, Wu S, Egbaria A, Fernie AR, Yan J, Qin F, Chen W, Brotman Y, Dai M (2021) Genomic basis underlying the metabolome-mediated drought adaptation of maize. Genome Biol 22(1):260. https://doi.org/10.1186/s13059-021-02481-1
Zhang H, Lang Z, Zhu JK (2018) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19(8):489–506. https://doi.org/10.1038/s41580-018-0016-z
Zhang X, Wang M, Zhang C, Dai C, Guan H, Zhang R (2022) Genetic dissection of QTLs for starch content in four maize DH populations. Front Plant Sci 13:950664. https://doi.org/10.3389/fpls.2022.950664
Zhang X, Warburton ML, Setter T, Liu H, Xue Y, Yang N, Yan J, Xiao Y (2016b) Genome-wide association studies of drought-related metabolic changes in maize using an enlarged SNP panel. Theor Appl Genet 129(8):1449–1463. https://doi.org/10.1007/s00122-016-2716-0
Zhang XF, Tong JH, Bai AN, Liu CM, Xiao LT, Xue HW (2020) Phytohormone dynamics in developing endosperm influence rice grain shape and quality. J Integr Plant Biol 62(10):1625–1637. https://doi.org/10.1111/jipb.12927
Zhang Z, Dong J, Ji C, Wu Y, Messing J (2019a) NAC-type transcription factors regulate accumulation of starch and protein in maize seeds. Proc Natl Acad Sci USA 116(23):11223–11228. https://doi.org/10.1073/pnas.1904995116
Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355–360. https://doi.org/10.1038/ng.546
Zhang Z, Zheng X, Yang J, Messing J, Wu Y (2016a) Maize endosperm-specific transcription factors O2 and PBF network the regulation of protein and starch synthesis. Proc Natl Acad Sci USA 113(39):10842–10847. https://doi.org/10.1073/pnas.1613721113
Zhao Y, Zhou DX (2012) Epigenomic modification and epigenetic regulation in rice. J Genet Genomics 39(7):307–315. https://doi.org/10.1016/j.jgg.2012.02.009
Zheng XM, Chen J, Pang HB, Liu S, Gao Q, Wang JR, Qiao WH, Wang H, Liu J, Olsen KM, Yang QW (2019) Genome-wide analyses reveal the role of noncoding variation in complex traits during rice domestication. Sci Adv 5(12):eaax3619. https://doi.org/10.1126/sciadv.aax3619
Zhou YH, Li G, Zhang YM (2022) A compressed variance component mixed model framework for detecting small and linked QTL-by-environment interactions. Brief Bioinform 23(2):bbab596. https://doi.org/10.1093/bib/bbab596
Zhu Y, Cai XL, Wang ZY, Hong MM (2003) An interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. J Biol Chem 278(48):47803–47811. https://doi.org/10.1074/jbc.M302806200
Acknowledgements
We thank Jianbing Yan’s group at Huazhong Agricultural University for providing maize materials and genotype data.
Funding
This research was supported by the National Natural Science Foundation of China (32171980), a project funded by the China Postdoctoral Science Foundation (2020M682295), the Henan Province Science and Technology Attack Project (232102110181), a first-class postdoctoral research grant in Henan Province (202001032), the Henan Provincial Higher Education Key Research Project (24B210003), and the Research Start-up Fund for Youth Talents of Henan Agricultural University (30500563).
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X. Z. designed the study. X. Z. and J. T. supervised the study. H. D., J. L., L. S., X. X., S. X., Y. S., X. J., Z. X., J. G., Y. W., H. X., and DD performed the experiment and analyzed the data. HD and XZ prepared the manuscript and all authors read and approved the manuscript.
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Highlights
1.By utilizing an enlarged SNP panel, we identified 14 novel loci associated with starch content, highlighting the importance of increased marker density in improving statistical power.
2.The candidate gene ZmAPC4 encodes a protein belonging to the WD40 repeat-like superfamily and exhibits high expression in maize endosperm, it plays a pivotal role as a regulator in the synthesis of starch in maize kernel.
3.As a notable achievement, we have successfully developed molecular markers that can effectively distinguish maize inbred lines based on their starch content.
4.Our findings provide a valuable reference for enhancing starch content to generate more bioenergy and have the potential to contribute to the advancement of more productive and sustainable agricultural practices.
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ESM 1
Figure S1 (a) QQ plots of Q, K and Q+K models and (b) Manhattan plot of Q model for starch content based on 0.05M SNPs. The red dashed line represents the significance threshold for 0.05M SNPs, i.e., P=1/En, En=48393 (En is the number of effective markers). Figure S2 Manhattan plot (a) and QQ plot (b) for starch content based on 0.05M SNPs. Red and Purple dots represent the Q model and the 6PCs+K model, respectively. (DOCX 475 kb)
ESM 2
Table S1 All genes information within significant QTL associated with starch content by using enlarged SNP panel for GWAS. Table S2 Top 30 of GO enrichment in Biological Process. Table S3 The information of primers and system of PCR and enzyme digestion. Table S4 The information of eight lines with higher starch content and eight lines with lower starch content. (XLSX 27 kb)
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Duan, H., Li, J., Sun, L. et al. Identification of novel loci associated with starch content in maize kernels by a genome-wide association study using an enlarged SNP panel. Mol Breeding 43, 91 (2023). https://doi.org/10.1007/s11032-023-01437-6
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DOI: https://doi.org/10.1007/s11032-023-01437-6