Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (12): 3501-3513    DOI: 10.1016/j.jia.2022.08.090
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
QTL analysis of the developmental changes in cell wall components and forage digestibility in maize (Zea mays L.)
LI Kun1, 2*, YANG Xue1, 2*, LIU Xiao-gang1, 2, HU Xiao-jiao1, 2, WU Yu-jin1, 2, WANG Qi1, 2, MA Fei-qian1, 2, LI Shu-qiang1, WANG Hong-wu1, 2, LIU Zhi-fang1, 2, HUANG Chang-ling1, 2
1 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 The National Engineering Laboratory for Crop Molecular Breeding, Beijing 10081, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      


Abstract  Cell wall architecture plays a key role in stalk strength and forage digestibility.  Lignin, cellulose, and hemicellulose are the three main components of plant cell walls, and they can impact stalk quality by affecting the structure and strength of the cell wall.  To explore cell wall development during secondary cell wall lignification in maize stalks, conventional and conditional genetic mapping were used to identify the dynamic quantitative trait loci (QTLs) of the cell wall components and digestibility traits during five growth stages after silking.  Acid detergent lignin (ADL), cellulose (CEL), acid detergent fiber (ADF), neutral detergent fiber (NDF), and in vitro dry matter digestibility (IVDMD) were evaluated in a maize recombinant inbred line (RIL) population.  ADL, CEL, ADF, and NDF gradually increased from 10 to 40 days after silking (DAS), and then they decreased.  IVDMD initially decreased until 40 DAS, and then it increased slightly.  Seventy-two QTLs were identified for the five traits, and each accounted for 3.48–24.04% of the phenotypic variation.  Six QTL hotspots were found, and they were localized in the 1.08, 2.04, 2.07, 7.03, 8.05, and 9.03 bins of the maize genome.  Within the interval of the pleiotropic QTL identified in bin 1.08 of the maize genome, six genes associated with cell wall component biosynthesis were identified as potential candidate genes for stalk strength as well as cell wall-related traits.  In addition, 26 conditional QTLs were detected in the five stages for all of the investigated traits.  Twenty-two of the 26 conditional QTLs were found at 30 DAS conditioned using the values of 20 DAS, and at 50 DAS conditioned using the values of 40 DAS.  These results indicated that cell wall-related traits are regulated by many genes, which are specifically expressed at different stages after silking.  Simultaneous improvements in both forage digestibility and lodging resistance could be achieved by pyramiding multiple beneficial QTL alleles identified in this study.
Keywords:  quantitative trait locus        maize (Zea mays L.)        cell wall components        forage quality  
Received: 23 June 2021   Accepted: 08 September 2021
Fund: This research was supported by the National Natural Science Foundation of China (31801367), the National Key Research and Development Program of China (2016YFD0101200) and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences.

About author:  LI Kun, E-mail:; YANG Xue, E-mail:; Correspondence HUANG Chang-ling, Tel/Fax: +86-10-82108738, E-mail:; WANG Hong-wu, Tel: +86-10-82108582, E-mail:; LIU Zhi-fang, Tel: +86-10-82108629, E-mail: * These authors contributed equally to this study.

Cite this article: 

LI Kun, YANG Xue, LIU Xiao-gang, HU Xiao-jiao, WU Yu-jin, WANG Qi, MA Fei-qian, LI Shu-qiang, WANG Hong-wu, LIU Zhi-fang, HUANG Chang-ling. 2022. QTL analysis of the developmental changes in cell wall components and forage digestibility in maize (Zea mays L.). Journal of Integrative Agriculture, 21(12): 3501-3513.

Arends D, Prins P, Jansen R, Broman K. 2010. R/qtl: High-throughput multiple QTL mapping. Bioinformatics, 26, 2990–2992.
Argillier O, Barrière Y, Hébert Y. 1995. Genetic variation and selection criterion for digestibility traits of forage maize. Euphytica, 82, 175–184.
Barrière Y. 2017. Brown-midrib genes in maize and their efficiency in dairy cow feeding. Perspectives for breeding improved silage maize targeting gene modifications in the monolignol and p-hydroxycinnamate pathways. Maydica, 62, M21.
Barrière Y, Gibelin C, Argillier O, Méchin V. 2001. Genetic analysis in recombinant inbred lines of early dent forage maize. I: QTL mapping for yield, earliness, starch and crude protein contents from per se value and top cross experiments. Maydica, 46, 253–266.
Barrière Y, Guillet C, Goffner D, Pichon M. 2003. Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review. Animal Research, 52, 193–228.
Barrière Y, Méchin V, Denoue D, Bauland C, Laborde J. 2010. QTL for yield, earliness, and cell wall quality traits in topcross experiments of the F838×F286 early maize RIL progeny. Crop Science, 50, 1761–1772.
Barrière Y, Ralph J, Méchin V, Guillaumie S, Grabber J H, Argillier O, Chabbert B, Lapierre C. 2004. Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. Comptes Rendus Biologies, 327, 847–860.
Barrière Y, Riboulet C, Méchin V, Maltese S, Pichon M, Cardinal A, Lapierre C, Lubberstedt T, Martinant J P. 2007. Genetics and genomics of lignification in grass cell walls based on maize as model species. Genes Genomes Genomics, 1, 133–156.
Barrière Y, Thomas J, Denoue D. 2008. QTL mapping for lignin content, lignin monomeric composition, p-hydroxycinnamate content, and cell wall digestibility in the maize recombinant inbred line progeny F838×F286. Plant Science, 175, 585–595.
Bohn M, Schulz B, Kreps R, Klein D, Melchinger A E. 2000. QTL mapping for resistance against the European corn borer (Ostrinia nubilalis H.) in early maturing European dent germplasm. Theoretical and Applied Genetics, 101, 907–917.
Cardinal A J, Lee M, Moore K J. 2003. Genetic mapping and analysis of quantitative trait loci affecting fiber and lignin content in maize. Theoretical and Applied Genetics, 106, 866–874.
Chen W, VanOpdorp N, Fitzl D, Tewari J, Friedemann P, Greene T, Thompson S, Kumpatla S, Zheng P. 2012. Transposon insertion in a cinnamyl alcohol dehydrogenase gene is responsible for a brown midrib1 mutation in maize. Plant Molecular Biology, 80, 289–297.
Chen Y, Liu H, Ali F, Scott M P, Ji Q, Frei U K, Lübberstedt T. 2012. Genetic and physical fine mapping of the novel brown midrib gene bm6 in maize (Zea mays L.) to a 180 kb region on chromosome 2. Theoretical and Applied Genetics, 125, 1223–1235.
Churchill G A, Doerge R W. 1994. Empirical threshold values for quantitative trait mapping. Genetics, 138, 963–971.
Fontaine A, Briand M, Barrière Y. 2003. Genetic variation and QTL mapping of para-coumaric and ferulic acid. Maydica, 48, 75–84.
Halpin C, Holt K, Chojecki J, Oliver D, Chabbert B, Monties B, Edwards K, Barakate A, Foxon G A. 1998. Brown-midrib maize (bm1) - A mutation affecting the cinnamyl alcohol dehydrogenase gene. The Plant Journal, 14, 545–553.
Haney L J, Hake S, Scott M P. 2008. Allelism testing of maize coop stock center lines containing unknown brown midrib alleles. Maize Genetics Cooperative Newsletter, 82, 4–5. 
Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M. 2004. Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. The Plant Cell, 16, 1446–1465.
Knapp S J, Stroup W W, Ross W M. 1985. Exact confidence intervals for heritability on a progeny mean basis. Crop Science, 25, 192–194.
Krakowsky M D, Lee M, Beeghly H H, Coors J G. 2003. Characterization of quantitative trait loci affecting fiber and lignin in maize (Zea mays L.). Maydica, 48, 283–292.
Krakowsky M D, Lee M, Coors J G. 2005. Quantitative trait loci for cell-wall components in recombinant inbred lines of maize (Zea mays L.) I: Stalk tissue. Theoretical and Applied Genetics, 111, 337–346.
Krakowsky M D, Lee M, Coors J G. 2006. Quantitative trait loci for cell wall components in recombinant inbred lines of maize (Zea mays L.) II: Leaf sheath tissue. Theoretical and Applied Genetics, 112, 717–726.
Li B, Gao F, Ren B Z, Dong S T, Liu P, Zhao B, Zhang J W. 2021. Lignin metabolism regulates lodging resistance of maize hybrids under varying planting density. Journal of Integrative Agriculture, 20, 2077–2089.
Li K, Wang H, Hu X, Ma F, Wu Y, Wang Q, Liu Z, Huang C. 2017. Genetic and quantitative trait locus analysis of cell wall components and forage digestibility in the Zheng58×HD568 maize RIL population at anthesis stage. Frontiers in Plant Science, 8, 1472.
Li L, Hill-Skinner S, Liu S, Beuchle D, Tang H M, Yeh C T, Nettleton D, Schnable P S. 2015. The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase. The Plant Journal, 81, 493–504.
Liu X, Hu X, Li K, Liu Z, Wu Y, Wang H, Huang C. 2020. Genetic mapping and genomic selection for maize stalk strength. BMC Plant Biology, 20, 196.
Lübberstedt T, Melchinger A E, Fähr S, Klein D, Dally A, Westhoff P. 1998. QTL mapping in testcrosses of flint lines of maize: III. Comparison across populations for forage traits. Crop Science, 38, 1278–1289.
Lübberstedt T, Melchinger A E, Klein D, Degenhardt H, Paul C. 1997a. QTL mapping in testcrosses of European flint lines of maize: II. Comparison of different testers for forage quality traits. Crop Science, 37, 1913–1922.
Lübberstedt T, Melchinger A E, Schön C C, Utz H F, Klein D. 1997b. QTL mapping in testcrosses of European flint lines of maize: I. Comparison of different testers for forage yield traits. Crop Science, 37, 921–931.
Méchin V, Argillier O, Hébert Y, Guingo E, Moreau L, Charcosset A, Barrière Y. 2001. Genetic analysis and QTL mapping of cell wall digestibility and lignification in silage maize. Crop Science, 41, 690–697.
Méchin V, Argillier O, Menanteau V, Barrière Y, Mila I, Pollet B, Lapierre C. 2000. Relationship of cell wall composition to in vitro cell wall digestibility of maize inbred line stems. Journal of the Science of Food & Agriculture, 80, 574–580.
Murray M G, Thompson W F. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8, 4321–4325.
Papst C, Melchinger A E, Eder J, Schulz B, Klein D, Bohn M. 2001. QTL mapping for resistance to European corn borer (Ostrinia nubilalis HB.) in early maturing European dent maize (Zea mays L.) germplasm and comparison of genomic regions for resistance across two populations of F3 families. Maydica, 46, 195–205.
Purcell S, Neale B, Toddbrown K, Thomas L, Ferreira M A R, Bender D, Maller J, Sklar P, Bakker P I W D, Daly M J. 2007. PLINK: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559–575.
Riboulet C, Fabre F, Dénoue D, Martinant J P, Lefevre B, Barrière Y. 2008. QTL mapping and candidate gene research from lignin content and cell wall digestibility in a top-cross of a flint maize recombinant inbred line progeny harvested at silage stage. Maydica, 53, 1–9.
Roussel V, Gibelin C, Fontaine A S, Barrière Y. 2002. Genetic analysis in recombinant inbred lines of early dent forage maize. II. QTL mapping for cell wall constituents and cell wall digestibility from per se value and top cross experiments. Maydica, 47, 9–20.
Scholey D V, Burton E J, Williams P E V. 2016. The bio refinery; producing feed and fuel from grain. Food Chemistry, 197, 937–942.
Tang H M, Liu S, Hill-Skinner S, Wu W, Reed D, Yeh C T, Nettleton D, Schnable P S. 2014. The maize brown midrib2 (bm2) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation. The Plant Journal, 77, 380–392.
Taylor J, Butler D. 2017. R package ASMap: Efficient genetic linkage map construction and diagnosis. Journal of Statistical Software, 79, 1–28.
Truntzler M, Barrière Y, Sawkins M C, Lespinasse D, Betran J, Charcosset A, Moreau L. 2010. Meta-analysis of QTL involved in silage quality of maize and comparison with the position of candidate genes. Theoretical and Applied Genetics, 121, 1465–1482.
Vermerris W, Mcintyre L M. 2010. Time to flowering in brown midrib mutants of maize: An alternative approach to the analysis of developmental traits. Heredity, 83, 171–178.
Vignols F, Rigau J, Torres M A, Capellades M, Puigdomènech P. 1995. The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. The Plant Cell, 7, 407–416.
Wu Z, Wang N, Hisano H, Cao Y, Wu F, Liu W, Bao Y, Wang Z Y, Fu C. 2019. Simultaneous regulation of F5H in COMT-RNAi transgenic switchgrass alters effects of COMT suppression on syringyl lignin biosynthesis. Plant Biotechnology Journal, 17, 836–845.
Xiong W, Wu Z, Liu Y, Li Y, Su K, Bai Z, Guo S, Hu Z, Zhang Z, Bao Y, Sun J, Yang G, Fu C. 2019. Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants. Biotechnology for Biofuels, 12, 82–94.
Xu C, Ren Y, Jian Y, Guo Z, Zhang Y, Xie C, Fu J, Wang H, Wang G, Xu Y. 2017. Development of a maize 55 K SNP array with improved genome coverage for molecular breeding. Molecular Breeding, 37, 1–12.
Yan J, Yang X, Shah T, Sánchez-Villeda H, Li J, Warburton M, Yi Z, Crouch J H, Xu Y. 2010. High-throughput SNP genotyping with the GoldenGate assay in maize. Molecular Breeding, 25, 441–451.
Zhong R, Cui D, Ye Z H. 2018. Secondary cell wall biosynthesis. New Phytologist, 221, 1703–1723.
Zhu J. 1996. Analysis of conditional genetic effects and variance components in developmental genetics. Genetics, 141, 1633–1639.

[1] ZHANG Sheng-zhong, HU Xiao-hui, WANG Fei-fei, CHU Ye, YANG Wei-qiang, XU Sheng, WANG Song, WU Lan-rong, YU Hao-liang, MIAO Hua-rong, FU Chun, CHEN Jing. A stable and major QTL region on chromosome 2 conditions pod shape in cultivated peanut (Arachis hyopgaea L.)[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2323-2334.
[2] GAO Shang-qing, CHEN Guang-deng, HU De-yi, ZHANG Xi-zhou, LI Ting-xuan, LIU Shi-hang, LIU Chun-ji. A major quantitative trait locus controlling phosphorus utilization efficiency under different phytate-P conditions at vegetative stage in barley[J]. >Journal of Integrative Agriculture, 2018, 17(2): 285-295.
[3] CAI Wen-yang, TAN Lu-bin, LIU Feng-xia, SUN Chuan-qing. Identification of quantitative trait loci and candidate genes associated with ABA sensitivity in common wild rice (Oryza rufipogon Griff.)[J]. >Journal of Integrative Agriculture, 2017, 16(11): 2375-2385.
[4] DONG Xiao-yan, FAN Shu-xiu, LIU Jin, WANG Qi, LI Mei-rong, JIANG Xin, LIU Zhen-yu, YIN Ye-chao, WANG Jia-yu. Identification of QTLs for seed storability in rice under natural aging conditions using two RILs with the same parent Shennong 265[J]. >Journal of Integrative Agriculture, 2017, 16(05): 1084-1092.
[5] LI Chun-lian, LI Ting-ting, LIU Tian-xiang, SUN Zhong-pei, BAI Gui-hua, JIN Feng, WANG Yong, WANG Zhong-hua. Identification of a major QTL for flag leaf glaucousness using a high-density SNP marker genetic map in hexaploid wheat[J]. >Journal of Integrative Agriculture, 2017, 16(02): 445-453.
[6] WANG Zhen, CHEN Jun-yu, ZHU Yu-jun, FAN Ye-yang, ZHUANG Jie-yun. Validation of qGS10, a quantitative trait locus for grain size on the long arm of chromosome 10 in rice (Oryza sativa L.)[J]. >Journal of Integrative Agriculture, 2017, 16(01): 16-26.
[7] ZENG Yu-xiang, XIA Ling-zhi, WEN Zhi-hua, JI Zhi-juan, ZENG Da-li, QIAN Qian, YANG Chang-deng. Mapping resistant QTLs for rice sheath blight disease with a doubled haploid population[J]. >Journal of Integrative Agriculture, 2015, 14(5): 801-810.
[8] DONG Yong-bin, ZHANG Zhong-wei, SHI Qing-ling, WANG Qi-lei, ZHOU Qiang, DENG Fei, MA Zhi-yan, QIAO Da-he, LI Yu-ling. QTL consistency for agronomic traits across three generations and potential applications in popcorn[J]. >Journal of Integrative Agriculture, 2015, 14(12): 2547-2557.
[9] DONG Wei, CHENG Zhi-jun, XU Jian-long, ZHENG Tian-qing, WANG Xiao-le, ZHANG Hong-zheng, WANG Jie , WAN Jian-min. Identification of QTLs Underlying Folate Content in Milled Rice[J]. >Journal of Integrative Agriculture, 2014, 13(8): 1827-1834.
[10] ZHANG Hong-jun, WANG Hui, YE Guo-you, QIAN Yi-liang, SHI Ying-yao, XIA Jia-fa, LI Ze-fu, ZHU Ling-hua, GAO Yong-ming, LI Zhi-kang. Improvement of Yield and Its Related Traits for Backbone Hybrid Rice Parent Minghui 86 Using Advanced Backcross Breeding Strategies[J]. >Journal of Integrative Agriculture, 2013, 12(4): 561-570.
[11] MEI De-yong, ZHU Yu-jun, YU Yong-hong, FAN Ye-yang, HUANG De-run, ZHUANG Jie-yun. Quantitative Trait Loci for Grain Chalkiness and Endosperm Transparency Detected in Three Recombinant Inbred Line Populations of Indica Rice[J]. >Journal of Integrative Agriculture, 2013, 12(1): 1-11.
[12] LV Ai-zhi, ZHANG Hao, ZHANG Zu-xin, TAO Yong-sheng, YUE Bing , ZHENG Yong-lian. Conversion of the Statistical Combining Ability into a Genetic Concept[J]. >Journal of Integrative Agriculture, 2012, 12(1): 43-52.
No Suggested Reading articles found!