Abstract
Leaf angle (LA) and leaf orientation value (LOV) are two crucial traits constituting the plant architecture (PA) of maize. Screening of quantitative trait loci (QTLs) and candidate genes (CGs) related to leaf angle and leaf orientation value provides the molecular basis for the improvement of maize plant architecture. In this study, we utilized genotyping by sequencing (GBS) on 179 maize recombined inbred lines (RILs) obtained by crossing two inbred lines with significant variation in leaf angle and leaf orientation value. A total of 4235 markers were used for the construction of the genetic linkage map. The total length of the genetic map was 1514.57 cM with the average genetic distance between each marker of 0.36 cM. On association of this map with phenotypic data from four environments, nine QTLs associated with leaf angle and nine QTLs associated with leaf orientation value were identified, explaining 78.89% and 59.71% of the phenotypic variation of leaf angle and leaf orientation value, respectively. Two QTLs explained greater than 10% of the phenotypic variation and three QTLs controlling both leaf angle and leaf orientation value were screened. Three candidate genes were identified as the most possible genes associated with leaf angle and leaf orientation value by screening the annotations of genes underlying these crucial QTLs. These were Zm00001d019053 might be associated with leaf angle, Zm00001d028164 and Zm00001d025352 might be associated with leaf angle and leaf orientation value, respectively. Expression analysis of candidate genes from parents and subsets also confirmed the significant variation in expression. Differences in DNA of the inbred lines with different phenotype were identified based on analysis of allelic variations in the candidate genes. These results not only enrich QTLs and candidate genes associated with leaf angle and leaf orientation value of maize, but also provide references for the improvement of plant architecture and molecular marker-assisted breeding.
Similar content being viewed by others
References
Arihara J, Watanabe K, Iwata F (1980) Effects of upright leaves on corn grain yield with different weather conditions. Japanese J Crop Sci 49(1):20–25. https://doi.org/10.1626/jcs.49.20
Austin RB (1989) Genetic variation in photosynthesis. J Agric Sci 112(3):87–294. https://doi.org/10.1017/s0021859600085737
Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79(3):31–348. https://doi.org/10.1023/b:pres.0000017196.95499.11
Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). Adv Agronomy 86:83–145. https://doi.org/10.1016/S0065-2113(05)86002-X
Duvick DN, Cassman KG (1999) Post-green revolution trends in yield potential of temperate maize in the north-Central United States. Crop Sci 39(6):1622–1630. https://doi.org/10.2135/cropsci1999.3961622x
Friedrich JW, Schrader LE (1978) Sulfur deprivation and nitrogen metabolism in maize seedlings. Plant Physiol 61(6):900–903. https://doi.org/10.1104/pp.61.6.900
Guo Y, Shi G, Liu Z, Zhao Y, Yang X, Zhu J, Li K, Guo X (2015) Using specific length amplified fragment sequencing to construct the high-density genetic map for Vitis (Vitis vinifera L. × Vitis amurensis Rupr.). Front Plant Sci 6:393–393. https://doi.org/10.3389/fpls.2015.00393
Knaff DB (1996) Ferredoxin and Ferredoxin-dependent enzymes. In: Oxygenic Photosynthesis: The Light Reactions Kluwer Academic Publishers. https://doi.org/10.1007/0-306-48127-8_17
Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis 1. Crop Sci 25(1):192–194. https://doi.org/10.2135/cropsci1985.0011183x002500010046x
Ku LX, Zhao WM, Zhang J, Wu LC, Wang CL, Wang PA, Zhang WQ, Chen YH (2010) Quantitative trait loci mapping of leaf angle and leaf orientation value in maize (Zea mays L.). Theor Appl Genet 121(5):951–959. https://doi.org/10.1007/s00122-010-1364-z
Ku L, Wei X, Zhang S, Zhang J, Guo S, Chen Y (2011) Cloning and characterization of a putative TAC1 Ortholog associated with leaf angle in maize (Zea mays L.). PLoS One 6(6):e20621. https://doi.org/10.1371/journal.pone.0020621
Ku LX, Zhang J, Guo SL, Liu HY, Zhao RF, Chen YH (2012) Integrated multiple population analysis of leaf architecture traits in maize (Zea mays L.). J Exp Bot 63(1):261–274. https://doi.org/10.1093/jxb/err277
Kurisu G, Kusunoki M, Katoh E, Yamazaki T, Teshima K, Onda Y, Kimata-Ariga Y, Hase T (2001) Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductase. Nat Struct Biol 8(2):117–121
Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120(3):637–644. https://doi.org/10.1104/pp.120.3.637
Li H, Durbin R (2010) Fast and accurate long-read alignment with burrows-wheeler transform. Bioinformatics 26(5):589–595. https://doi.org/10.1093/bioinformatics/btp698
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 (SAM) format and SAMtools. Bioinformatics, 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li Y, Li P, Wang Y, Dong R, Yu H, Hou B (2014) Genome-wide identification and phylogenetic analysis of Family-1 UDP glycosyltransferases in maize (Zea mays). Planta 239(6):1265–1279. https://doi.org/10.1007/s00425-014-2050-1
Li C, Li Y, Shi Y, Song Y, Zhang D, Buckler ES, Zhang Z, Wang T, Li Y (2015) Genetic control of the leaf angle and leaf orientation value as revealed by ultra-high density maps in three connected maize populations. PLoS One 10(3):e0121624–e0121624. https://doi.org/10.1371/journal.pone.0121624
Lu S, Zhang M, Zhang Z, Wang Z, Wu N, Song Y, Wang P (2018) Screening and verification of genes associated with leaf angle and leaf orientation value in inbred maize lines. PLoS One 13(12):e0208386–e0208386. https://doi.org/10.1371/journal.pone.0208386
Ludwig-Müller J, Walz A, Slovin JP, Epstein E, Cohen JD, Dong W, Town CD (2005) Overexpression of maize IAGLU in Arabidopsis thaliana alters plant growth and sensitivity to IAA but not IBA and 2,4-D. J Plant Growth Regul 24(2):127–141. https://doi.org/10.1007/s00344-004-0006-6
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3(3):269–283. https://doi.org/10.1016/j.cj.2015.01.001
Merk HL, Foolad MR (2011) Parent-offspring correlation estimate of heritability for late blight resistance conferred by an accession of the tomato wild species Solanum pimpinellifolium. Plant Breed 131(1):203–210. https://doi.org/10.1111/j.1439-0523.2011.01898.x
Mickelson SM, Stuber CS, Senior L, Kaeppler SM (2002) Quantitative trait loci controlling leaf and tassel traits in a b73 × mo17 population of maize. Crop Ence 42(6):1902–1909. https://doi.org/10.2135/cropsci2002.1902
Mock JJ, Pearce RB (1975) An ideotype of maize. Euphytica 24(3):613–623. https://doi.org/10.1007/bf00132898
Moss DN, Musgrave RB (1971) Photosynthesis and Crop Production. In: Advances in Agronomy. Elsevier
Oputa CO (1972) Amide nitrogen and soluble sugar interrelationships in Zea mays L. as influenced by sulfur nutrition. PhD thesis. University of California, Davis
Pan QC, Xu YC, Li K et al (2017) The genetic basis of plant architecture in 10 maize recombinant inbred line populations. Plant Physiol 175(2):00709. https://doi.org/10.1104/pp.17.00709
Papendick RI, Sanchez PA, Triplett GB, Trenbath BR (1976) Plant Interactions in Mixed Crop Communities. In: Multiple Cropping. American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
Pepper GE, Pearce RB, Mock JJ (1977) Leaf orientation and yield of maize 1. Crop Sci 17(6):883–886. https://doi.org/10.2135/cropsci1977.0011183x001700060017x
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Saitoh T, Ikegami T, Nakayama M, Teshima K, Akutsu H, Hase T (2006) NMR study of the Electron transfer complex of plant Ferredoxin and sulfite Reductase. J Biol Chem 281(15):10482–10488. https://doi.org/10.1074/jbc.m510530200
Shinohara F, Kurisu G, Hanke G, Bowsher C, Hase T, Kimata-Ariga Y (2017) Structural basis for the isotype-specific interactions of ferredoxin and ferredoxin: NADP+ oxidoreductase: an evolutionary switch between photosynthetic and heterotrophic assimilation. Photosynth Res 134(3):281–289. https://doi.org/10.1007/s11120-016-0331-1
Szerszen J, Szczyglowski K, Bandurski R (1994) Iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid. Science 265(5179):1699–1701. https://doi.org/10.1126/science.8085154
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94(20):11102–11107. https://doi.org/10.1073/pnas.94.20.11102
Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43(2):159–162. https://doi.org/10.1038/ng.746
Wang B, Liu H, Liu Z, Dong X, Guo J, Li W, Chen J, Gao C, Zhu Y, Zheng X, Chen Z, Chen J, Song W, Hauck A, Lai J (2018) Identification of minor effect QTLs for plant architecture related traits using super high density genotyping and large recombinant inbred population in maize (Zea mays). BMC Plant Biol 18(1):17–17. https://doi.org/10.1186/s12870-018-1233-5
Wassom JJ (2013) Quantitative trait loci for leaf angle, leaf width, leaf length, and plant height in a maize (Zea mays L) B73× Mo17 population. Maydica 58(3–4):318–321
Wu Y, Bhat PR, Close TJ, Lonardi S (2008) Efficient and accurate construction of genetic linkage maps from the minimum spanning tree of a graph. PLoS Genet 4(10):e1000212–e1000212. https://doi.org/10.1371/journal.pgen.1000212
Xie C, Weng J, Liu W, Zou C, Hao Z, Li W, Li M, Guo X, Zhang G, Xu Y, Li X, Zhang S (2013) Zea mays (L.) P1 locus for cob glume color identified as a post-domestication selection target with an effect on temperate maize genomes. Crop J 1(1):15–24. https://doi.org/10.1016/j.cj.2013.07.002
Yue X, Zhao X, Fei Y, Zhang X (2012) Correlation of aquaporins and transmembrane solute transporters revealed by genome-wide analysis in developing maize leaf. Comparative Function Genom 2012:546930–546930. https://doi.org/10.1155/2012/546930
Zhang J, Zhang Q, Cheng T, Yang W, Pan H, Zhong J, Huang L, Liu E (2015) High-density genetic map construction and identification of a locus controlling weeping trait in an ornamental woody plant (Prunus mume Sieb. Et Zucc). DNA Res: Int J Rapid Publ Reports Genes Genomes 22(3):183–191. https://doi.org/10.1093/dnares/dsv003
Zhang D, Li H, Wang J, Zhang H, Hu Z, Chu S, Lv H, Yu D (2016a) High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Front Plant Sci 7:372–372. https://doi.org/10.3389/fpls.2016.00372
Zhang Z, Shang H, Shi Y, Huang L, Li J, Ge Q, Gong J, Liu A, Chen T, Wang D, Wang Y, Palanga KK, Muhammad J, Li W, Lu Q, Deng X, Tan Y, Song W, Cai J, Li P, Rashid H, Gong W, Yuan Y (2016b) Construction of a high-density genetic map by specific locus amplified fragment sequencing (SLAF-seq) and its application to quantitative trait loci (QTL) analysis for boll weight in upland cotton (Gossypium hirsutum.). BMC Plant Biol 16:79–79. https://doi.org/10.1186/s12870-016-0741-4
Zhao Z, Gu H, Sheng X, Yu H, Wang J, Huang L, Wang D (2016) Genome-wide single-nucleotide polymorphisms discovery and high-density genetic map construction in cauliflower using specific-locus amplified fragment sequencing. Front Plant Sci 7:334–334. https://doi.org/10.3389/fpls.2016.00334
Zhao P, Zhou HJ, Potter D, Hu YH, Feng XJ, Dang M, Feng L, Zulfiqar S, Liu WZ, Zhao GF, Woeste K (2018) Population genetics, phylogenomics and hybrid speciation of Juglans in China determined from whole chloroplast genomes, transcriptomes, and genotyping-by-sequencing (GBS). Mol Phylogenet Evol 126:250–265. https://doi.org/10.1016/j.ympev.2018.04.014
Zhou Z, Zhang C, Zhou Y, Hao Z, Wang Z, Zeng X, di H, Li M, Zhang D, Yong H, Zhang S, Weng J, Li X (2016) Genetic dissection of maize plant architecture with an ultra-high density bin map based on recombinant inbred lines. BMC Genomics 17:178–178. https://doi.org/10.1186/s12864-016-2555-z
Zhu Y, Yin Y, Yang K, Li J, Sang Y, Huang L, Fan S (2015) Construction of a high-density genetic map using specific length amplified fragment markers and identification of a quantitative trait locus for anthracnose resistance in walnut (Juglans regia L.). BMC Genomics 16(1):614–614. https://doi.org/10.1186/s12864-015-1822-8
Zhu WY, Huang L, Chen L, Yang JT, Wu JN, Qu ML, Yao DQ, Guo CL, Lian HL, He HL, Pan JS, Cai R (2016) A high-density genetic linkage map for cucumber (Cucumis sativus L.): based on specific length amplified fragment (SLAF) sequencing and QTL analysis of fruit traits in cucumber. Front Plant Sci 7:437–437. https://doi.org/10.3389/fpls.2016.00437
Acknowledgments
The authors thank the Breeding Biotech Company (Shanxi, China) for providing sequencing services.
Funding
This study was funded by the Modern Crop Seed Industry development of Jilin Province, China (Grand NO. jnz291205).
Author information
Authors and Affiliations
Contributions
PW and SG designed and led this study, MZ, JK, YM, QZ, QW, NJ and HZ performed field experiment. MZ, JK, HZ, and JQ analyzed data of experiment. MZ wrote the manuscript.
Corresponding authors
Additional information
Communicated by: Yann-Rong Lin
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhang, M., Jin, Y., Ma, Y. et al. Identification of QTLs and Candidate Genes Associated with Leaf Angle and Leaf Orientation Value in Maize (Zea mays L.) Based on GBS. Tropical Plant Biol. 14, 34–49 (2021). https://doi.org/10.1007/s12042-020-09270-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12042-020-09270-3