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:

Sparse panicle1 is required for inflorescence development in Setaria viridis and maize

Abstract

Setaria viridis is a rapid-life-cycle model panicoid grass. To identify genes that may contribute to inflorescence architecture and thus have the potential to influence grain yield in related crops such as maize, we conducted an N-nitroso-N-methylurea (NMU) mutagenesis of S. viridis and screened for visible inflorescence mutant phenotypes. Of the approximately 2,700 M2 families screened, we identified four recessive sparse panicle mutants (spp1–spp4) characterized by reduced and uneven branching of the inflorescence. To identify the gene underlying the sparse panicle1 (spp1) phenotype, we performed bulked segregant analysis and deep sequencing to fine map it to an approximately 1 Mb interval. Within this interval, we identified disruptive mutations in two genes. Complementation tests between spp1 and spp3 revealed they were allelic, and deep sequencing of spp3 identified an independent disruptive mutation in SvAUX1 (AUXIN1), one of the two genes in the 1 Mb interval and the only gene disruption shared between spp1 and spp3. SvAUX1 was found to affect both inflorescence development and root gravitropism in S. viridis. A search for orthologous mutant alleles in maize confirmed a very similar role of ZmAUX1 in maize, which highlights the utility of S. viridis in accelerating functional genomic studies in maize.

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: Characterization of spp1 and spp3 in S. viridis and Zmaux1-0 in maize.
Figure 2: BSA mapping and variation of SvAUX1 and ZmAUX1 alleles.

Similar content being viewed by others

References

  1. Emerson, R. A. The inheritance of certain ‘Abnormalities’ in maize. J. Hered. 8, 385–399 (1912).

    Google Scholar 

  2. Ray, D. K., Mueller, N. D., West, P. C. & Foley, J. A. Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8, e66428 (2013).

    Google Scholar 

  3. Schnable, J. C. & Freeling, M. Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize. PLoS ONE 6, e17855 (2011).

    Google Scholar 

  4. Koornneef, M. & van der Veen, J. H. Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh. Theor. Appl. Genet. 58, 257–263 (1980).

    Google Scholar 

  5. Redei, G. P. Arabidopsis as a genetic tool. Annu. Rev. Genet. 9, 111–127 (1975).

    Google Scholar 

  6. Gallavotti, A. et al. The role of barren stalk1 in the architecture of maize. Nature 432, 630–635 (2004).

    Google Scholar 

  7. McSteen, P. et al. Barren inflorescence2 encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiol. 144, 1000–1011 (2007).

    Google Scholar 

  8. Wolfe, K. H., Gouy, M., Yang, Y. W., Sharp, P. M. & Li, W. H. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl Acad. Sci. USA 86, 6201–6205 (1989).

    Google Scholar 

  9. Brutnell, T. P., Bennetzen, J. L. & Vogel, J. P. Brachypodium distachyon and Setaria viridis: model genetic systems for the grasses. Annu. Rev. Plant Biol. 66, 465–485 (2015).

    Google Scholar 

  10. Brutnell, T. P. Model grasses hold key to crop improvement. Nat. Plants 1, 15062 (2015).

  11. Schnable, J. C., Freeling, M. & Lyons, E. Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biol. Evol. 4, 265–277 (2012).

    Google Scholar 

  12. Kellogg, E. Floral displays: genetic control of grass inflorescences. Curr. Opin. Plant Biol. 10, 26–31 (2007).

    Google Scholar 

  13. Sreenivasulu, N. & Schnurbusch, T. A genetic playground for enhancing grain number in cereals. Trends Plant Sci. 17, 91–101 (2012).

    Google Scholar 

  14. Jiang, H., Huang, P. & Brutnell, T. P. in Genetics and Genomics of Setaria (eds Doust, A. & Diao, X. ) 303–322 (Springer, 2016).

    Google Scholar 

  15. Michelmore, R. W., Paran, I. & Kesseli, R. V. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl Acad. Sci. USA 88, 9828–9832 (1991).

    Google Scholar 

  16. Takagi, H. et al. Mutmap accelerates breeding of a salt-tolerant rice cultivar. Nat. Biotechnol. 33, 445–449 (2015).

    Google Scholar 

  17. Swarup, R. et al. Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16, 3069–3083 (2004).

    Google Scholar 

  18. Yang, Y., Hammes, U. Z., Taylor, C. G., Schachtman, D. P. & Nielsen, E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123–1127 (2006).

    Google Scholar 

  19. Bennett, M. J. et al. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–950 (1996).

    Google Scholar 

  20. Zhao, H. et al. OsAUX1 controls lateral root initiation in rice (Oryza sativa L.). Plant Cell Environ. 38, 2208–2222 (2015).

    Google Scholar 

  21. Yu, C. et al. The auxin transporter, OsAUX1, is involved in primary root and root hair elongation and in Cd stress responses in rice (Oryza sativa L.). Plant J. 83, 818–830 (2015).

    Google Scholar 

  22. Baker, K. E. & Parker, R. Nonsense-mediated mRNA decay: terminating erroneous gene expression. Curr. Opin. Cell Biol. 16, 293–299 (2004).

    Google Scholar 

  23. Phillips, K. A. et al. Vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23, 550–566 (2011).

    Google Scholar 

  24. Gallavotti, A. et al. 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 (2008).

    Google Scholar 

  25. Gallavotti, A., Yang, Y., Schmidt, R. J. & Jackson, D. The relationship between auxin transport and maize branching. Plant Physiol. 147, 1913–1923 (2008).

    Google Scholar 

  26. Skirpan, A., Andrea, S., Xianting, W. & Paula, M. Genetic and physical interaction suggest that BARREN STALK1 is a target of BARREN INFLORESCENCE2 in maize inflorescence development. Plant J. 55, 787–797 (2008).

    Google Scholar 

  27. Barazesh, S. & McSteen, P. Barren inflorescence1 functions in organogenesis during vegetative and inflorescence development in maize. Genetics 179, 389–401 (2008).

    Google Scholar 

  28. Skirpan, A. et al. BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant Cell Physiol. 50, 652–657 (2009).

    Google Scholar 

  29. Bainbridge, K. et al. Auxin influx carriers stabilize phyllotactic patterning. Genes Dev. 22, 810–823 (2008).

    Google Scholar 

  30. Settles, A. M. et al. Sequence-indexed mutations in maize using the UniformMu transposon-tagging population. BMC Genomics 8, 116 (2007).

    Google Scholar 

  31. Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).

  32. McKenna, A. et al. The genome analysis toolkit: a mapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Google Scholar 

  33. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).

    Google Scholar 

  34. Hodge, J. G. & Kellogg, E. A. Patterns of inflorescence development of three prairie grasses (Andropogoneae, Poaceae). Int. J. Plant Sci. 175, 963–974 (2014).

    Google Scholar 

  35. Omasits, U., Ahrens, C. H., Müller, S. & Wollscheid, B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30, 884–886 (2014).

    Google Scholar 

  36. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Google Scholar 

  37. Katoh, K., Misawa, K., Kuma, K.-I. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).

    Google Scholar 

  38. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Google Scholar 

  39. Stelpflug, S. C. et al. An expanded maize gene expression Atlas based on RNA sequencing and its use to explore root development. Plant Genome http://dx.doi.org/10.3835/plantgenome2015.04.0025 (2016).

  40. Lambret-Frotté, J. et al. Validating internal control genes for the accurate normalization of qPCR expression analysis of the novel model plant Setaria viridis. PLoS ONE 10, e0135006 (2015).

    Google Scholar 

  41. Dong, M. A., Farré, E. M. & Thomashow, M. F. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 7241–7246 (2011).

    Google Scholar 

  42. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. & Vandesompele, J. Qbase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19 (2007).

    Google Scholar 

Download references

Acknowledgements

The authors thank A. Bray for his help in maize root gravitropism assay, C. Shyu for her help in qRT–PCR, and the DDPSC greenhouse staff for plant care. The work conducted by the US Department of Energy Joint Genome Institute was supported by the Office of Science of the US Department of Energy under contract number DE-AC02-05CH11231. This work was also supported by a Department of Energy grant to T.B.P. (DE-SC0008769), and a National Science Foundation grant to E.A.K. (IOS-1413824).

Author information

Authors and Affiliations

Authors

Contributions

P.H., H.J. and T.P.B. conceived and designed the study. H.J. performed the screen, crosses and DNA extraction. P.H. and H.J. performed bulked segregant analysis. K.B., J.J., L.S. and J.S. performed library construction and sequencing. P.H. performed sequencing and other data analysis. P.H., H.J., C.Z. and M.S.B. performed phenotypic characterizations in S. viridis and maize. P.H., H.J., C.Z., E.A.K. and T.P.B. wrote the manuscript.

Corresponding author

Correspondence to Thomas P. Brutnell.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–5. (PDF 1644 kb)

Supplementary Table 1

Mutant families and BSA pools that have been sequenced. (XLSX 26 kb)

Supplementary Table 2

Annotations of homozygous disruptive mutations in NMU00629, spp1 (line number exceeds 51 because of multiple transcripts for some genes). (XLSX 14 kb)

Supplementary Table 3

Annotations of homozygous disruptive mutations in NMU00933, spp3 (line number exceeds 98 because of multiple transcripts for some genes). (XLSX 13 kb)

Supplementary Table 4

Primers used in this study. (XLSX 11 kb)

File S1

Error-prone SNP calls from NMU mutants. (TXT 9831 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, P., Jiang, H., Zhu, C. et al. Sparse panicle1 is required for inflorescence development in Setaria viridis and maize. Nature Plants 3, 17054 (2017). https://doi.org/10.1038/nplants.2017.54

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.54

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