Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus

Abstract

Domestication of cereal crops, such as maize, wheat and rice, had a profound influence on agriculture and the establishment of human civilizations. One major improvement was an increase in seed number per inflorescence, which enhanced yield and simplified harvesting and storage1,2. The ancestor of maize, teosinte, makes 2 rows of kernels, and modern varieties make 8–20 rows3. Kernel rows are initiated by the inflorescence shoot meristem, and shoot meristem size is controlled by a feedback loop involving the CLAVATA signaling proteins and the WUSCHEL transcription factor4,5. We present a hypothesis that variation in inflorescence meristem size affects kernel row number (KRN), with the potential to increase yield. We also show that variation in the CLAVATA receptor–like protein FASCIATED EAR2 leads to increased inflorescence meristem size and KRN. These findings indicate that modulation of fundamental stem cell proliferation control pathways has the potential to enhance crop yields.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Variation in maize ear inflorescence meristem size and KRN.
Figure 2: Isolation of weak alleles of FEA2 by TILLING.
Figure 3: Quantitative variation in FEA2 leads to enhanced KRN.

Similar content being viewed by others

References

  1. Bommert, P., Satoh-Nagasawa, N., Jackson, D. & Hirano, H.Y. Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol. 46, 69–78 (2005).

    Article  CAS  Google Scholar 

  2. Evans, L.T. Crop Evolution, Adaptation and Yield (Cambridge University Press, Cambridge, 1993).

  3. Doebley, J. The genetics of maize evolution. Annu. Rev. Genet. 38, 37–59 (2004).

    Article  CAS  Google Scholar 

  4. Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M. & Simon, R. Dependence of stem cell fate in Arabidopsis an a feedback loop regulated by CLV3 activity. Science 289, 617–619 (2000).

    Article  CAS  Google Scholar 

  5. Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644 (2000).

    Article  CAS  Google Scholar 

  6. Gregory, P.J. & George, T.S. Feeding nine billion: the challenge to sustainable crop production. J. Exp. Bot. 62, 5233–5239 (2011).

    Article  CAS  Google Scholar 

  7. Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).

    Article  CAS  Google Scholar 

  8. Jiao, Y. et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541–544 (2010).

    Article  CAS  Google Scholar 

  9. Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545–549 (2010).

    Article  CAS  Google Scholar 

  10. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741–745 (2005).

    Article  CAS  Google Scholar 

  11. Huang, X. et al. Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41, 494–497 (2009).

    Article  CAS  Google Scholar 

  12. Li, Y. et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43, 1266–1269 (2011).

    Article  CAS  Google Scholar 

  13. Barton, M.K. Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev. Biol. 341, 95–113 (2010).

    Article  CAS  Google Scholar 

  14. Ha, C.M., Jun, J.H. & Fletcher, J.C. Shoot apical meristem form and function. Curr. Top. Dev. Biol. 91, 103–140 (2010).

    Article  CAS  Google Scholar 

  15. Komatsuda, T. et al. Six-rowed barley originated from a mutation in a homeodomain–leucine zipper I–class homeobox gene. Proc. Natl. Acad. Sci. USA 104, 1424–1429 (2007).

    Article  CAS  Google Scholar 

  16. Ramsay, L. et al. INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat. Genet. 43, 169–172 (2011).

    Article  CAS  Google Scholar 

  17. Lu, M. et al. Mapping of quantitative trait loci for kernel row number in maize across seven environments. Mol. Breed. 28, 143–152 (2011).

    Article  CAS  Google Scholar 

  18. Upadyayula, N., da Silva, H.S., Bohn, M.O. & Rocheford, T.R. Genetic and QTL analysis of maize tassel and ear inflorescence architecture. Theor. Appl. Genet. 112, 592–606 (2006).

    Article  CAS  Google Scholar 

  19. Veldboom, L.R., Lee, M. & Woodman, W.L. Molecular marker–facilitated studies in an elite maize population. 1. Linkage analysis and determination of QTL for morphological traits. Theor. Appl. Genet. 88, 7–16 (1994).

    Article  CAS  Google Scholar 

  20. Lee, M. et al. Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population. Plant Mol. Biol. 48, 453–461 (2002).

    Article  CAS  Google Scholar 

  21. Wang, S., Basten, C.J. & Zeng, Z.B. Windows QTL Cartographer 2.5 (Department of Statistics, North Carolina State University, Raleigh, North Carolina, 2011).

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

    Article  CAS  Google Scholar 

  23. Jeong, S., Trotochaud, A.E. & Clark, S.E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor–like kinase. Plant Cell 11, 1925–1934 (1999).

    Article  CAS  Google Scholar 

  24. Fiers, M. et al. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17, 2542–2553 (2005).

    Article  CAS  Google Scholar 

  25. Guo, Y., Han, L., Hymes, M., Denver, R. & Clark, S.E. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889–900 (2010).

    Article  CAS  Google Scholar 

  26. McMullen, M.D. et al. Genetic properties of the maize nested association mapping population. Science 325, 737–740 (2009).

    Article  CAS  Google Scholar 

  27. Till, B.J. et al. Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol. 4, 12 (2004).

    Article  Google Scholar 

  28. Weil, C.F. TILLING in grass species. Plant Physiol. 149, 158–164 (2009).

    Article  CAS  Google Scholar 

  29. Ng, P.C. & Henikoff, S. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res. 31, 3812–3814 (2003).

    Article  CAS  Google Scholar 

  30. DeYoung, B.J. et al. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase–like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1–16 (2006).

    Article  CAS  Google Scholar 

  31. Deyoung, B.J. & Clark, S.E. BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180, 895–904 (2008).

    Article  CAS  Google Scholar 

  32. Müller, R., Bleckmann, A. & Simon, R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell–limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934–946 (2008).

    Article  Google Scholar 

  33. Kinoshita, A. et al. RPK2 is an essential receptor–like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911–3920 (2010).

    Article  CAS  Google Scholar 

  34. Betsuyaku, S. et al. Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol. 52, 14–29 (2011).

    Article  CAS  Google Scholar 

  35. Bommert, P. et al. thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor–like kinase. Development 132, 1235–1245 (2005).

    Article  CAS  Google Scholar 

  36. Suzaki, T. et al. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131, 5649–5657 (2004).

    Article  CAS  Google Scholar 

  37. Kinoshita, T. et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167–171 (2005).

    Article  CAS  Google Scholar 

  38. Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294 (2008).

    Article  CAS  Google Scholar 

  39. She, J. et al. Structural insight into brassinosteroid perception by BRI1. Nature 474, 472–476 (2011).

    Article  CAS  Google Scholar 

  40. Jaillais, Y., Belkhadir, Y., Balsemão-Pires, E., Dangl, J.L. & Chory, J. Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation. Proc. Natl. Acad. Sci. USA 108, 8503–8507 (2011).

    Article  CAS  Google Scholar 

  41. Nimchuk, Z.L., Tarr, P.T. & Meyerowitz, E.M. An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell 23, 851–854 (2011).

    Article  CAS  Google Scholar 

  42. Müller, R., Borghi, L., Kwiatkowska, D., Laufs, P. & Simon, R. Dynamic and compensatory responses of Arabidopsis shoot and floral meristems to CLV3 signaling. Plant Cell 18, 1188–1198 (2006).

    Article  Google Scholar 

  43. Nimchuk, Z.L., Tarr, P.T., Ohno, C., Qu, X. & Meyerowitz, E.M. Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol. 21, 345–352 (2011).

    Article  CAS  Google Scholar 

  44. Brown, P.J. et al. Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genet. 7, e1002383 (2011).

    Article  CAS  Google Scholar 

  45. Shepard, K.A. & Purugganan, M.D. Molecular population genetics of the Arabidopsis CLAVATA2 region. The genomic scale of variation and selection in a selfing species. Genetics 163, 1083–1095 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Muños, S. et al. Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol. 156, 2244–2254 (2011).

    Article  Google Scholar 

  47. Bomblies, K. & Doebley, J.F. Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics 172, 519–531 (2006).

    Article  CAS  Google Scholar 

  48. Searle, S.R. Linear Models (John Wiley & Sons, New York, 1971).

  49. Hallauer, A. & Miranda, J. Quantitative Genetics in Maize Breeding (Iowa State University Press, Ames, Iowa, 1985).

  50. Knapp, S.J., Stroup, W.W. & Ross, W.M. Exact confidence intervals for heritability on a progeny mean basis. Crop Sci. 25, 192–194 (1985).

    Article  Google Scholar 

  51. Utz, H.F. PLABSTAT. Ein Computerprogramm zur Statistischen Analyse von Pflanzenzüchterischen Experimenten (Universität Hohenheim, Stuttgart, Germany, 1998).

  52. Doerge, R.W. & Churchill, G.A. Permutation tests for multiple loci affecting a quantitative character. Genetics 142, 285–294 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We wish to thank C. Weil and the Maize TILLING facility for the isolation of the fea2 TILLING alleles, F. Taguchi Shiobara for SEM images, U. Au, L.A. Haller and K. Lau for KRN counting, P. Yin and K. Chen for assistance with genotyping, M. Bohn and S. Goldshmidt for assistance with statistical analysis, members of the Jackson laboratory for comments on the manuscript, T. Rocheford for growing IBM recombinant inbred lines, M. Komatsu, L. Heetland, K. Simcox and H. Sakai (DuPont- Pioneer) for grow-outs of TILLING populations and yield trait measurements, P. Brown and E. Buckler for discussions and A. Eveland for informatics. Funding from the US Department of Agriculture (USDA; grant NRICGP 2003-35304-13277), the National Science Foundation (NSF) Plant Genome Program (grant DBI-0604923) and the German Science Society (DFG) for a postdoctoral fellowship (grant Bo 3012/1-1) to P.B. is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Contributions

P.B. performed all experiments, except where noted below, analyzed the data and helped with writing the manuscript. N.S.N. generated the data on the variation in maize inflorescence meristem size in different inbred lines. D.J. assisted with data analysis and wrote the manuscript.

Corresponding author

Correspondence to David Jackson.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Tables 1–3 and 5 (PDF 289 kb)

Supplementary Table 4

Genes and gene density in the FEA2 QTL interval. See separate file: FEA2_interval_gene annotations.xls (XLS 60 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bommert, P., Nagasawa, N. & Jackson, D. Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus. Nat Genet 45, 334–337 (2013). https://doi.org/10.1038/ng.2534

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.2534

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing