Abstract
Key message
A set of RIL population was used to detect QTL associated with the sizes of eight consecutive leaves, across different environments, and ten QTL clusters were identified as main QTLs.
Abstract
One of the important parameters of the maize leaf architecture that affects light penetration into the canopy, leaf size, has long attracted breeders’ attention for optimizing the plant type of maize and for maximizing the grain yield (GY). In this study, we used 253 RIL lines derived from a cross between B73 and SICAU1212 to investigate the leaf widths (LWs), leaf lengths (LLs), and leaf areas (LAs) of eight consecutive leaves of maize below the tassel and GY across different environments and to identify quantitative traits loci (QTLs) controlling the above-mentioned traits, using inclusive interval mapping for single-environment analysis plus a mixed-model-based composite interval mapping for joint analysis. A total of 171 and 159 putative QTLs were detected through these two mapping methods, respectively. Single-environment mapping revealed that 39 stable QTLs explained more than 10 % of the phenotypic variance, and 35 of the 39 QTLs were also detected by joint analysis. In addition, joint analysis showed that nine of the 159 QTLs exhibited significant QTL × environment interaction and 15 significant epistatic interactions were identified. Approximately 47.17 % of the QTLs for leaf architectural traits in joint analysis were concentrated in ten main chromosomal regions, namely, bins 1.07, 2.02, 3.06, 4.09, 5.01, 5.02, 5.03–5.04, 5.07, 6.07, and 8.05. This study should provide a basis for further fine-mapping of these main genetic regions and improvement of maize leaf architecture.
Similar content being viewed by others
Abbreviations
- LW(s):
-
Leaf width(s)
- LL(s):
-
Leaf length(s)
- LA(s):
-
Leaf area(s)
- GY:
-
Grain yield
- ICIM:
-
Inclusive composite interval mapping
- MAS:
-
Marker-assisted selection
- MCIM:
-
Mixed-model-based composite interval mapping
- QTL(s):
-
Quantitative trait loci
- Q × E:
-
QTL × Environment
References
Agrama HAS, Zakaria AG, Said FB, Tuinstra M (1999) Identification of quantitative trait loci for nitrogen use efficiency in maize. Mol Breed 5:187–195
Allard RW, Zhang Q, Maroof MA, Muona OM (1992) Evolution of multilocus genetic structure in an experimental barley population. Genetics 131:957–969
Austin DF, Lee M (1998) Detection of quantitative trait loci for grain yield and yield components in maize across generations in stress and nonstress environments. Crop Sci 38:1296–1308
Bauer P, Lubkowitz M, Tyers R, Nemoto K, Meeley RB, Goff SA, Freeling M (2004) Regulation and a conserved intron sequence of liguleless3/4 knox class-I homeobox genes in grasses. Planta 219:359–368
Byrne ME (2005) Networks in leaf development. Curr Opin Plant Biol 8:59–66
Cai H, Chu Q, Yuan L, Liu J, Chen X, Chen F, Mi G, Zhang F (2012) Identification of quantitative trait loci for leaf area and chlorophyll content in maize (Zea mays) under low nitrogen and low phosphorus supply. Mol Breed 30:251–266
Camacho RG, Garrido O, Lima MG (1995) Caracterización de nueve genotipos de maíz (Zea mays L.) en relación a área foliar y coeficiente de extinción de luz. Sci Agric 52:294–298
Carlborg Ö, Haley CS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5:618–625
Carraro N, Forestan C, Canova S, Traas J, Varotto S (2006) ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol 142:254–264
Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761
Choe E, Rocheford TR (2012) Genetic and QTL analysis of pericarp thickness and ear architecture traits of Korean waxy corn germplasm. Euphytica 183:243–260
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Cowling SA, Field CB (2003) Environmental control of leaf area production: implications for vegetation and land-surface modeling. Glob Biogeochem Cycles 17:1007
Darvasi A, Soller M (1997) A simple method to calculate resolving power and confidence interval of QTL map location. Behav Genet 27:125–132
Donald CM (1968) The breeding of crop ideotypes. Euphytica 17:385–403
Dwyer L, Stewart D (1986) Leaf area development in field-grown maize. Agron J 78:334–343
Eastin JA (1969) Leaf position and leaf function in corn. Carbon-14 1abeled photosynthate distribution in corn in relation to leaf position and leaf function. In: Proceedings of the 24th Annual Corn and Sorghum Research Conference (Washington, DC: American Seed Trade Association), pp 81–89
Evans MMS, Passas HJ, Poethig RS (1994) Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120:1971–1981
Facette MR, Shen Z, Björnsdóttir FR, Briggs SP, Smith LG (2013) Parallel proteomic and phosphoproteomic analyses of successive stages of maize leaf development. Plant Cell 25:2798–2812
Foerster JM, Beissinger T, de Leon N, Kaeppler S (2015) Large effect QTL explain natural phenotypic variation for the developmental timing of vegetative phase change in maize (Zea mays L.). Theor Appl Genet 128:529–538
Forestan C, Varotto S (2010) PIN1 auxin efflux carriers localization studies in Zea mays. Plant Signal Behav 5:436–439
Forestan C, Farinati S, Varotto S (2012) The maize PIN gene family of auxin transporters. Front Plant Sci 3:16
Fowler JE, Freeling M (1996) Genetic analysis of mutations that alter cell fates in maize leaves: dominant Liguleless mutations. Dev Genet 18:198–222
Freire AI, Dias KOG, Oliveira LBV, Nalin RS, Guedes FL, Souza JC (2015) Genetic control of the number of leaves above the ear in maize. Genet Mol Res 14:1318–1323
Guo S, Ku L, Qi J, Tian Z, Han T, Zhang L, Su H, Ren Z, Chen Y (2015) Genetic analysis and major quantitative trait locus mapping of leaf widths at different positions in multiple populations. PLoS One 10:e0119095
Hake S, Freeling M (1986) Analysis of genetic mosaics shows that the extra epidermal cell divisions in Knotted mutant maize plants are induced by adjacent mesophyll cells. Nature 320:621–623
Hallauer AR, Miranda J (1988) Quantitative genetics in maize breeding, 2nd edn. Iowa State University Press, Ames
Harper L, Freeling M (1996) Interactions of liguleless1 and liguleless2 function during ligule induction in maize. Genetics 144:1871–1882
Hartwig T, Chuck GS, Fujioka S, Klempien A, Weizbauer R, Potluri DPV, Choe S, Johal GS, Schulz B (2011) Brassinosteroid control of sex determination in maize. Proc Natl Acad Sci 108:19814–19819
Hosseini M, Houshmand S, Mohamadi S, Tarang A, Khodambashi M, Rahimsoroush H (2012) Detection of QTLs with main, epistatic and QTL × environment interaction effects for rice grain appearance quality traits using two populations of backcross inbred lines (BILs). Field Crop Res 135:97–106
Hou X, Liu Y, Xiao Q, Wei B, Zhang X, Gu Y, Wang Y, Chen J, Hu Y, Liu H, Zhang J, Huang Y (2015) Genetic analysis for canopy architecture in an F2: 3 population derived from two-type foundation parents across multi-environments. Euphytica 205:421–440
Hu H, Liu W, Fu Z, Homann L, Technow F, Wang H, Song C, Li S, Melchinger AE, Chen S (2013) QTL mapping of stalk bending strength in a recombinant inbred line maize population. Theor Appl Genet 126:2257–2266
Jankovsky JP, Nelson T (1998) midribless1 (mrl1) is required for the correct timing of vascular initiation and the coordination of subsequent developmental events in the maize leaf. Maize Genet Coop Newslett 72:67
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
Juarez MT, Twigg RW, Timmermans MCP (2004) Specification of adaxial cell fate during maize leaf development. Development 131:4533–4544
Jurišić-Knežev D, Čudejková M, Zalabák D, Hlobilová M, Rolčík J, Pěnčík A, Bergougnoux V, Fellner M (2012) Maize AUXIN-BINDING PROTEIN 1 and AUXIN-BINDING PROTEIN 4 impact on leaf growth, elongation, and seedling responsiveness to auxin and light. Botany 90:990–1006
Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S (1994) Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6:1877–1887
Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis. Crop Sci 25:192–194
Ku L, Zhao W, Zhang J, Wu L, Wang C, Wang P, Zhang W, Chen Y (2010) Quantitative trait loci mapping of leaf angle and leaf orientation value in maize (Zea mays L.). Theor Appl Genet 121:951–959
Ku L, Zhang J, Guo S, Liu H, Zhao R, Chen Y (2011) Integrated multiple population analysis of leaf architecture traits in maize (Zea mays L.). J Exp Bot 63:261–274
Ku L, Zhang J, Zhang JC, Guo S, Liu H, Zhao R, Yan Q, Chen Y (2012) Genetic dissection of leaf area by jointing two F2: 3 populations in maize (Zea mays L.). Plant Breed 131:591–599
Langdale J (2005) The then and now of maize leaf development. Maydica 50:459–467
Li Z, Pinson SRM, Park WD, Paterson AH, Stansel JW (1997) Epistasis for three grain yield components in rice (Oryza sativa L.). Genetics 145:453–465
Li Z, Luo L, Mei H, Wang D, Shu Q, Tabien R, Zhong D, Ying C, Stansel JW, Khush GS, Paterson AH (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics 158:1737–1753
Li H, Ribaut J-M, Li Z, Wang J (2008a) Inclusive composite interval mapping (ICIM) for digenic epistasis of quantitative traits in biparental populations. Theor Appl Genet 116:243–260
Li Y, Dong Y, Niu S, Cui D, Wang Y, Liu Y, Wei M, Li X (2008b) Identification of agronomically favorable quantitative trait loci alleles from a dent corn inbred Dan232 using advanced backcross QTL analysis and comparison with the F2: 3 population in popcorn. Mol Breed 21:1–14
Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067
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:e0121624
Lincoln SE, Daly MJ, Lander ES (1993) Constructing linkage maps with MAPMAKER/Exp version 3.0. A tutorial reference manual. 3rd edn. Whitehead Institute for Medical Research, Cambridge
Liu J, Chu Q, Cai H, Mi G, Chen F (2010) SSR linkage map construction and QTL mapping for leaf area in maize. Hereditas 32:625–631
Liu Y, Wang L, Sun C, Zhang Z, Zheng Y, Qiu F (2014) Genetic analysis and major QTL detection for maize kernel size and weight in multi-environments. Theor Appl Genet 127:1019–1037
Loomis RS, Williams WA (1969) Productivity and the morphology of crop stands: patterns with leaves. Am Soc Agron 3:27–47
Lu C, Shen L, Tan Z, Xu Y, He P, Chen Y, Zhu L (1997) Comparative mapping of QTLs for agronomic traits of rice across environments by using a doubled-haploid population. Theor Appl Genet 94:145–150
Malosetti M, Ribaut JM, Vargas M, Crossa J, Van Eeuwijk FA (2008) A multi-trait multi-environment QTL mixed model with an application to drought and nitrogen stress trials in maize (Zea mays L.). Euphytica 161:241–257
McCouch S, Cho Y, Yano M, Paul E, Blinstrub M, Morishima H, Kinoshita T (1997) Report on QTL nomenclature. Rice Genet Newlett 14:11–131
McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, Brown P, Browne C, Eller M, Guil K, Harjes C, Kroon D, Lepak N, Mitchell SE, Peterson B, Pressoir G, Romero S, Rosas MO, Salvo S, Yates H, Hanson M, Jones E, Smith S, Glaubitz JC, Goodman M, Ware D, Holland JB, Buckler ES (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740
Messmer R, Fracheboud Y, Bänziger M, Vargas M, Stamp P, Ribaut JM (2009) Drought stress and tropical maize: QTL-by-environment interactions and stability of QTLs across environments for yield components and secondary traits. Theor Appl Genet 119:913–930
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 Sci 42:1902–1909
Mock J, Pearce R (1975) An ideotype of maize. Euphytica 24:613–623
Moon J, Hake S (2011) How a leaf gets its shape. Curr Opin Plant Biol 14:24–30
Moreno MA, Harper LC, Krueger RW, Dellaporta SL, Freeling M (1997) liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev 11:616–628
Muehlbauer GJ, Fowler JE, Girard L, Tyers R, Harper L, Freeling M (1999) Ectopic expression of the maize homeobox gene liguleless3 alters cell fates in the leaf. Plant Physiol 119:651–662
Nardmann J, Ji J, Werr W, Scanlon MJ (2004) The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–2839
Nelson T, Dengler N (1997) Leaf vascular pattern formation. Plant Cell 9:1121–1135
Pelleschi S, Leonardi A, Rocher JP, Cornic G, de Vienne D, Thevenot C, Prioul JL (2006) Analysis of the relationships between growth, photosynthesis and carbohydrate metabolism using quantitative trait loci (QTLs) in young maize plants subjected to water deprivation. Mol Breed 17:21–39
Pérez-Pérez JM, Serrano-Cartagena J, Micol JL (2002) Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 162:893–915
Phillips PC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9:855–867
Rae AM, Street N, Robinson K, Harris N, Taylor G (2009) Five QTL hotspots for yield in short rotation coppice bioenergy poplar: the poplar biomass loci. BMC Plant Biol 9:1–13
Reif JC, Maurer HP, Korzun V, Ebmeyer E, Miedaner T, Würschum T (2011) Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat. Theor Appl Genet 123:283–292
Reynolds JO, Eisses JF, Sylvester AW (1998) Balancing division and expansion during maize leaf morphogenesis: analysis of the mutant, warty-1. Development 125:259–268
Robertson DS (1985) A possible technique for isolating genic DNA for quantitative traits in plants. J Theor Biol 117:1–10
Saghai-Maroof M, Soliman K, Jorgensen RA, Allard R (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci 81:8014–8018
Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, Tanaka H, Iwahori S, Matsuoka M (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516
Santos FR, Pena SD, Epplen JT (1993) Genetic and population study of a Y-linked tetranucleotide repeat DNA polymorphism with a simple non-isotopic technique. Hum Genet 90:655–656
Scanlon MJ, Schneeberger RG, Freeling M (1996) The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 122:1683–1691
Scanlon MJ, Chen KD, McKnight CC (2000) The narrow sheath duplicate genes: sectors of dual aneuploidy reveal ancestrally conserved gene functions during maize leaf development. Genetics 155:1379–1389
Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66:553–563
Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–795
Smith LG, Hake S, Sylvester AW (1996) The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122:481–489
Steinhoff J, Liu W, Maurer HP, Würschum T, Friedrich C, Longin H, Ranc N, Reif JC (2011) Multiple-line cross quantitative trait locus mapping in European elite maize. Crop Sci 51:2505–2516
Steinhoff J, Liu W, Reif JC, Della Porta G, Ranc N, Würschum T (2012) Detection of QTL for flowering time in multiple families of elite maize. Theor Appl Genet 125:1539–1551
Stewart DW, Costa C, Dwyer LM, Smith DL, Hamilton RI, Ma BL (2003) Canopy structure, light interception, and photosynthesis in maize. Agron J 95:1465–1474
Sylvester AW, Cande WZ, Freeling M (1990) Division and differentiation during normal and liguleless-1 maize leaf development. Development 110:985–1000
Sylvester AW, Parker-Clark V, Murray GA (2001) Leaf shape and anatomy as indicators of phase change in the grasses: comparison of maize, rice, and bluegrass. Am J Bot 88:2157–2167
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 43:159–162
Upadyayula N, Da Silva H, Bohn M, Rocheford T (2006) Genetic and QTL analysis of maize tassel and ear inflorescence architecture. Theor Appl Genet 112:592–606
Utz H (2001) PLABSTAT: a computer program for statistical analysis of plant breeding experiments. Institute for Plant Breeding Seed Science and Population Genetics. University of Hohenheim, Stuttgart
Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Walsh J, Waters CA, Freeling M (1998) The maize geneliguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade–sheath boundary. Genes Dev 12:208–218
Wang P, Zhou G, Cui K, Li Z, Yu S (2012) Clustered QTL for source leaf size and yield traits in rice (Oryza sativa L.). Mol Breed 29:99–113
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 58:318–321
Watson D (1956) Leaf growth in relation to crop yield. In: Milthorpe FL (ed) Growth of leaves. Butterworth, London, pp 178–191
Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210
Xiong L, Liu K, Dai X, Xu C, Zhang Q (1999) Identification of genetic factors controlling domestication-related traits of rice using an F2 population of a cross between Oryza sativa and O. rufipogon. Theor Appl Genet 98:243–251
Yan W (2001) GGEbiplot—a Windows application for graphical analysis of multienvironment trial data and other types of two-way data. Agron J 93:1111–1118
Yan J, Tang H, Huang Y, Zheng Y, Li J (2006) Quantitative trait loci mapping and epistatic analysis for grain yield and yield components using molecular markers with an elite maize hybrid. Euphytica 149:121–131
Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536
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:e1004573
Yang C, Liu J, Rong T (2015a) Detection of quantitative trait loci for ear row number in F2 populations of maize. Genet Mol Res 14:14229–14238
Yang C, Tang D, Zhang L, Liu J, Rong T (2015b) Identification of QTL for ear row number and two-ranked versus many-ranked ear in maize across four environments. Euphytica 206:33–47
Yang G, Dong Y, Li Y, Wang Q, Shi Q, Zhou Q (2015c) Integrative detection and verification of QTL for plant traits in two connected RIL populations of high-oil maize. Euphytica 206:203–223
Yin C, Li H, Li S, Xu L, Zhao Z, Wang J (2015) Genetic dissection on rice grain shape by the two-dimensional image analysis in one japonica × indica population consisting of recombinant inbred lines. Theor Appl Genet 128:1969–1986
Yu S, Li J, Xu C, Tan Y, Gao Y, Li X, Zhang Q, Maroof MAS (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci 94:9226–9231
Zhang B, Ye W, Ren D, Tian P, Peng Y, Gao Y, Ruan B, Wang L, Zhang G, Guo L, Qian Q, Gao Z (2015) Genetic analysis of flag leaf size and candidate genes determination of a major QTL for flag leaf width in rice. Rice 8:1–10
Zheng Z, Liu X (2013) QTL identification of ear leaf morphometric traits under different nitrogen regimes in maize. Genet Mol Res 12:4342–4351
Acknowledgments
We deeply appreciated the editor and the anonymous reviewer for helpful comments and suggestions on the manuscript. We are very grateful to Pro. Yuanqi Wu and Dr. Zhengqiao Liao for performing the PCA, Pro. Street N.R. for supplying the R package and Dr. Uma Gaur for editing the English. We also thank graduate students K. Hu, A.M. Jia, B. Wu, Q. Jiang, C. Hu and Dr. J.W. Li in the maize institute of Sichuan Agricultural University for helping to collect the phenotypic data. This work was supported by grants from the National Basic Research Program of China (the “973” project, 2014CB138203).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
The experiments comply with the current laws of the country in which they were performed.
Additional information
Communicated by A. Charcosset.
C. Yang and D. Tang contributed equally to this study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yang, C., Tang, D., Qu, J. et al. Genetic mapping of QTL for the sizes of eight consecutive leaves below the tassel in maize (Zea mays L.). Theor Appl Genet 129, 2191–2209 (2016). https://doi.org/10.1007/s00122-016-2767-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-016-2767-2