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Characterization and fine mapping of qkrnw4, a major QTL controlling kernel row number in maize

Abstract

Key message

A major QTL controlling kernel row number, qkrnw4, was identified by combining linkage analysis and association mapping. Within qkrnw4, on the basis of its expression and bioinformatics analysis, Zm00001d052910 was supposed to be the candidate gene for kernel row number.

Abstract

Kernel row number (KRN) is an important yield-related trait that affects kernel number in maize. Understanding the genetic basis of KRN is important for increasing maize yields. In the present study, by the use of a near-isogenic line (NIL) that has a B73 background and that consistently displays a low KRN across environments, qkrnw4, a major quantitative trait locus (QTL) associated with KRN within a yield trait-related QTL hotspot in bin 4.08, was finely mapped to an ~ 33-kb interval. Regional association analysis of a nested association mapping population comprising 5000 recombinant inbred lines revealed Zm00001d052910, which encodes a protein with an unknown function, as the important candidate gene responsible for qkrnw4. Different expression levels of this candidate gene in immature ears were detected between the NIL and its recurrent parent. Moreover, the expression of several auxin-related genes was consistent with that of the candidate gene. Furthermore, the potential associations of this candidate gene with well-known inflorescence-related genes were discussed. The results of this study provide important information for the genetic elucidation of KRN variation in maize.

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References

  1. Austin DF, Lee M (1996) Comparative mapping in F2:3 and F6:7 generations of quantitative trait loci for grain yield and yield components in maize. Theor Appl Genet 92:817–826

  2. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265

  3. Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M, Jackson D, Hake S, Werr W (2005) thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132:1235–1245

  4. Bommert P, Je BI, Goldshmidt A, Jackson D (2013) The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 502:555–558

  5. Bortiri E, Chuck G, Vollbrecht E, Rocheford T, Martienssen R, Hake S (2006) ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18:574–585

  6. 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 23:2633–2635

  7. Brouwer DJ, St Clair DA (2004) Fine mapping of three quantitative trait loci for late blight resistance in tomato using near isogenic lines (NILs) and sub-NILs. Theor Appl Genet 108:628–638

  8. Brown PJ, Upadyayula N, Mahone GS, Tian F, Bradbury PJ, Myles S, Holland JB, Flint-Garcia S, McMullen MD, Buckler ES, Rocheford TR (2011) Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genet 7:e1002383

  9. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325:714–718

  10. Carraro N, ForestanC 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

  11. Chen L, An Y, Li Y, Li C, Shi Y, Song Y, Zhang D, Wang T, Li Y (2017) Candidate loci for yield-related traits in maize revealed by a combination of metaQTL analysis and regional association mapping. Front Plant Sci 8:2190

  12. Chuck GS, Brown PJ, Meeley R, Hake S (2014) Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proc Natl Acad Sci USA 111:18775–18780

  13. Ding X, Wu X, Chen L, Li C, Shi Y, Song Y, Zhang D, Wang T, Li Y, Liu Z, Li Y (2017) Both major and minor QTL associated with plant height can be identified using near-isogenic lines in maize. Euphytica 213:21

  14. Doebley J (2004) The genetics of maize evolution. Ann Rev Genet 38:37–59

  15. Du Y, Liu L, Li M, Fang S, Shen X, Chu J, Zhang Z (2017) UNBRANCHED3 regulates branching by modulating cytokinin biosynthesis and signaling in maize and rice. New Phytol 214:721–733

  16. Gallavotti A, Barazesh S, Malcomber S, Hall D, Jackson D, Schmidt RJ, McSteen P (2008) sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proc Natl Acad Sci USA 105:15196–15201

  17. Hung HY, Shannon LM, Tian F, Bradbury PJ, Chen C, Flint-Garcia SA, McMullen MD, Ware D, Buckler ES, Doebley JF, Holland JB (2012) ZmCCT and the genetic basis of day-length adaptation underlying the post domestication spread of maize. Proc Natl Acad Sci USA 109:1913–1921

  18. Je BI, Gruel J, Lee YK, Bommert P, Arevalo ED, Eveland AL, Wu Q, Goldshmidt A, Meeley R, Bartlett M, Komatsu M, Sakai H, Jönsson H, Jackson D (2016) Signaling from maize organ primordia via fasciated ear3 regulates stem cell proliferation and yield traits. Nat Genet 48:785–791

  19. Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D, Balint-Kurti PJ, Holland JB (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43:163–168

  20. Li Y, Ma X, Wang T, Li Y, Liu C, Liu Z, Sun B, Shi Y, Song Y, Carlone M, Bubeck D, Bhardwaj H, Whitaker D, Wilson W, Jones E, Wright K, Sun S, Niebur W, Smith S (2011) Increasing maize productivity in China by planting hybrids with germplasm that responds favorably to higher planting densities. Crop Sci 51:2391–2400

  21. Li C, Li Y, Sun B, Peng B, Liu C, Liu Z, Yang Z, Li Q, Tan W, Zhang Y, Wang D, Shi Y, Song Y, Wang T, Li Y (2013) Quantitative trait loci mapping for yield components and kernel-related traits in multiple connected RIL populations in maize. Euphytica 193:303–316

  22. Li F, Jia H, Liu L, Zhang C, Liu Z, Zhang Z (2014) Quantitative trait loci mapping for kernel row number using chromosome segment substitution lines in maize. Genet Mol Res 13:1707–1716

  23. Li Y, Li C, Bradbury PJ, Liu X, Lu F, Romay CM, Glaubitz JC, Wu X, Peng B, Shi Y, Song Y, Zhang D, Buckler ES, Zhang Z, Li Y, Wang T (2016) Identification of genetic variants associated with maize flowering time using an extremely large multi-genetic background population. Plant J 86:391–402

  24. Liu L, Du Y, Huo D, Wang M, Shen X, Yue B, Qiu F, Zheng Y, Yan J, Zhang Z (2015a) Genetic architecture of maize kernel row number and whole genome prediction. Theor Appl Genet 128:2243–2254

  25. Liu L, Du Y, Shen X, Li M, Sun W, Huang J, Liu Z, Tao Y, Zheng Y, Yan J, Zhang Z (2015b) KRN4 controls quantitative variation in maize kernel row number. PLoS Genet 11:e1005670

  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

  27. McSteen P, Hake S (2001) barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128:2881–2891

  28. McSteen P, Laudencia-Chingcuanco D, Colasanti J (2000) A floret by any other name: control of meristem identity in maize. Trends Plant Sci 5:61–66

  29. Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212

  30. Peter B, Namiko Satoh N, David J (2013) Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus. Nat Genet 45:334–337

  31. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P (2011) vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23:550–566

  32. Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15

  33. Qiao W, Qi L, Cheng Z, Su L, Li J, Sun Y, Ren J, Zheng X, Yang Q (2016) Development and characterization of chromosome segment substitution lines derived from Oryza rufipogon in the genetic background of O. sativa spp. indica cultivar 9311. BMC Genom 17:580

  34. Qiu S, Chen J, Lin S, Lin X (2012) A comparison of silver staining protocols for detecting DNA in polyester-backed polyacrylamide gel. Braz J Microbiol 43:649–652

  35. Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashey S, Bruggemann E, Li B, Hainey CF, Radovic S, Zaina G, Rafalski JA, Tingey SV, Miao GH, Phillips RL, Tuberosa R (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104:11376–11381

  36. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441:227–230

  37. Sharma VK, Carles C, Fletcher JC (2003) Maintenance of stem cell populations in plants. Proc Natl Acad Sci USA 100:11823–11829

  38. Shen X, Liu L, Zhang Z (2014) Inflorescence architecture-related genes and their regulatory networks in maize. Sci Sin (Vitae) 44:775–783 (in Chinese)

  39. Taguchi-Shiobara F, Yuan Z, Hake S, Jackson D (2001) The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev 15:2755–2766

  40. 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

  41. Veldboom L, Lee M (1994) Molecular-marker-facilitated studies of morphological traits in maize. II: determination of QTLs for grain yield and yield components. Theor Appl Genet 89:451

  42. Vollbrecht E, Schmidt RJ (2009) Development of the inflorescences. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp 13–40

  43. Vollbrecht E, Springer PS, Goh L, Buckler ES, Martienssen R (2005) Architecture of floral branch systems in maize and related grasses. Nature 436:1119–1126

  44. Wang J, Li H, Zhang L, Meng L (2016) Users’ manual of QTL IciMapping. The Quantitative Genetics Group, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100081, China, and Genetic Resources Program, International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600 Mexico, DF, Mexico

  45. Williams L, Fletcher JC (2005) Stem cell regulation in the Arabidopsis shoot apical meristem. Curr Opin Plant Biol 8:582–586

  46. Wu X, Mcsteen P (2007) The role of auxin transport during inflorescence development in maize (Zea mays, Poaceae). Am J Bot 94:1745–1755

  47. Xie X, Song M, Jin F, Ahn SN, Suh JP, Hwang HG, Mc Couch SR (2006) Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon. Theor Appl Genet 113:885–894

  48. 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

  49. 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 38:203–208

  50. Yu J, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178:539–551

  51. Zhou Q, Wang P, Cheng B, Zhu S, Xie C (2014) Meta-analysis of QTL for ear row number in maize. J Maize Sci 22:35–40 (in Chinese)

  52. Zhu J (1995) Analysis of conditional genetic effects and variance components in developmental genetic. Genetics 141:1633–1639

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Acknowledgements

This work was partially supported by grants provided by the National Natural Science Foundation of China (31401395, 91735306), the Programs of MST of China (2016YFD0100303), and the CAAS (Innovation Program). We are grateful to CIMMYT for providing seeds of the NIL used in the study.

Author information

NN and XD conducted field and genetic experiment, analyzed the data, and drafted the manuscript; LC, XW, YA and CL phenotyped kernel traits and analyzed the data. YS and DZ conducted field trials. TW, YL and ZL supervised the experiment and edited the manuscript. YL and YS designed the experiment, analyzed the data and drafted the manuscript.

Correspondence to Yong-xiang Li or Yunsu Shi.

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Nie, N., Ding, X., Chen, L. et al. Characterization and fine mapping of qkrnw4, a major QTL controlling kernel row number in maize. Theor Appl Genet 132, 3321–3331 (2019). https://doi.org/10.1007/s00122-019-03427-9

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