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Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat

Abstract

The domestication of cereal crops such as wheat, maize, rice and barley has included the modification of inflorescence architecture to improve grain yield and ease harvesting1. Yield increases have often been achieved through modifying the number and arrangement of spikelets, which are specialized reproductive branches that form part of the inflorescence. Multiple genes that control spikelet development have been identified in maize, rice and barley25. However, little is known about the genetic underpinnings of this process in wheat. Here, we describe a modified spikelet arrangement in wheat, termed paired spikelets. Combining comprehensive QTL and mutant analyses, we show that Photoperiod-1 (Ppd-1), a pseudo-response regulator gene that controls photoperiod-dependent floral induction, has a major inhibitory effect on paired spikelet formation by regulating the expression of FLOWERING LOCUS T (FT)6,7. These findings show that modulated expression of the two important flowering genes, Ppd-1 and FT, can be used to form a wheat inflorescence with a more elaborate arrangement and increased number of grain producing spikelets.

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Figure 1: Characterization of paired spikelets.
Figure 2: Genome-wide plot displaying the 104 QTL (coloured dots/triangles) that contribute to paired spikelet development using the four-way MAGIC population across five independent experiments (five different colours).
Figure 3: The effect of allelic variation for Ppd-1 and photoperiod on inflorescence architecture.
Figure 4: Identification and phenotyping of Ppd-D1a mutants.
Figure 5: Deletion of FT-B1 promotes paired spikelet development.

References

  1. Doebley, J., Gaut, B. S. & Smith, B. D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).

    CAS  Article  Google Scholar 

  2. Vollbrecht, E., Springer, P. S., Goh, L., Buckler, E. S. IV & Martienssen, R. Architecture of floral branch systems in maize and related grasses. Nature 436, 1119–1126 (2005).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  5. 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. Nature Genet. 43, 169–172 (2011).

    CAS  Article  Google Scholar 

  6. Turner, A., Beales, J., Faure, S., Dunford, R. P. & Laurie, D. A. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031–1034 (2005).

    CAS  Article  Google Scholar 

  7. Beales, J., Turner, A., Griffiths, S., Snape, J. W. & Laurie, D. A. A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor. Appl. Genet. 115, 721–733 (2007).

    CAS  Article  Google Scholar 

  8. Sharman, B. C. Branched heads in wheat and wheat hybrids. Nature 153, 497–498 (1944).

    Article  Google Scholar 

  9. Sharman, B. C. Interpretation of the morphology of various naturally occurring abnormalities of the inflorescence of wheat (Triticum). Can. J. Bot. 45, 2073–2080 (1967).

    Article  Google Scholar 

  10. Dobrovolskaya, O. et al. FRIZZY PANICLE drives supernumerary spikelets in bread wheat (T. aestivum L.). Plant Physiol. http://dx.doi.org/10.1104/pp.114.250043 (2014).

  11. Yen, C. & Yang, J. L. The essential nature of organs in Gramineae, multiple secondary axes theory: A new concept. J. Sichuan Agric. Univ. 10, 544–565 (1992).

    Google Scholar 

  12. Koric, S . Branching genes in Triticum aestivum. Proc. Int. Wheat Genet. Symp. 4th, Colorado, Missouri, 283–288 (1973).

    Google Scholar 

  13. Pennell, A. L. & Halloran, G. M. Inheritance of supernumerary spikelets in wheat. Euphytica 32, 767–776 (1983).

    Article  Google Scholar 

  14. Eagles, H. A., Cane, K. & Vallance, N. The flow of alleles of important photoperiod and vernalisation genes through Australian wheat. Crop Pasture Sci. 60, 646 (2009).

    CAS  Article  Google Scholar 

  15. Huang, B. E. et al. A multiparent advanced generation inter-cross population for genetic analysis in wheat. Plant Biotech. J. 10, 826–839 (2012).

    CAS  Article  Google Scholar 

  16. Wingen, L. U. et al. Molecular genetic basis of pod corn (Tunicate maize). Proc. Natl Acad. Sci. USA 109, 7115–7120 (2012).

  17. Verbyla, A. P., Cullis, B. R. & Thompson, R. The analysis of QTL by simultaneous use of the full linkage map. Theor. Appl. Genet. 116, 95–111 (2007).

    Article  Google Scholar 

  18. Pastina, M. M. et al. A mixed model QTL analysis for sugarcane multiple-harvest-location trial data. Theor. Appl. Genet. 124, 835–849 (2011).

    Article  Google Scholar 

  19. Verbyla, A. P., Taylor, J. D. & Verbyla, K. L. RWGAIM: an efficient high-dimensional random whole genome average (QTL) interval mapping approach. Genet. Res. 94, 291–306 (2013).

    Article  Google Scholar 

  20. Nakamichi, N., Kita, M., Ito, S., Yamashino, T. & Mizuno, T. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 46, 686–698 (2005).

    CAS  Article  Google Scholar 

  21. Li, C., Distelfeld, A., Comis, A. & Dubcovsky, J. Wheat flowering repressor VRN2 and promoter CO2 compete for interactions with NUCLEAR FACTOR-Y complexes. Plant J. 67, 763–773 (2011).

    CAS  Article  Google Scholar 

  22. Díaz, A., Zikhali, M., Turner, A. S., Isaac, P. & Laurie, D. A. Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS ONE 7, e33234 (2012).

    Article  Google Scholar 

  23. Shaw, L. M., Turner, A. S. & Laurie, D. A. The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J. 71, 71–84 (2012).

    CAS  Article  Google Scholar 

  24. Shaw, L. M., Turner, A. S., Herry, L., Griffiths, S. & Laurie, D. A. Mutant alleles of Photoperiod-1 in wheat (Triticum aestivum L.) that confer a late flowering phenotype in long days. PLoS ONE 8, e79459 (2013).

    Article  Google Scholar 

  25. Yan, L. et al. Positional cloning of the wheat vernalization gene VRN1. Proc. Natl Acad. Sci. USA 100, 6263–6268 (2003).

    CAS  Article  Google Scholar 

  26. Zhao, T. et al. Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.). Mol. Genet. Genomics 276, 334–350 (2006).

    CAS  Article  Google Scholar 

  27. Kobayashi, K. et al. Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24, 1848–1859 (2012).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  29. Endo-Higashi, N. & Izawa, T. Flowering time genes Heading Date 1 and Early Heading Date 1 together control panicle development in rice. Plant Cell Physiol. 52, 1083–1094 (2011).

    CAS  Article  Google Scholar 

  30. Forster, B. P. et al. The barley phytomer. Ann. Bot. 100, 725–733 (2007).

    Article  Google Scholar 

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Acknowledgements

We thank Bjorg Sherman for technical assistance with plant husbandry, Mark Talbot for expert assistance with scanning electron microscopy and Carl Davies for photography. We thank Lindsay Shaw and Megan Hemming for helpful discussions. A CSIRO O.C.E. Postdoctoral Fellowship funded S.A.B.

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S.A.B., C.C., K.R., J.G., E.J.F., B.T. and S.M.S. performed experiments and collected phenotypic information. C.C. and B.R.C. designed the MAGIC experiments, performed QTL and statistical analysis. S.A.B., E.J.F., B.T. and S.M.S. contributed new materials. All authors contributed to the preparation of the manuscript.

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Correspondence to Steve M. Swain.

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The authors declare no competing financial interests.

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Boden, S., Cavanagh, C., Cullis, B. et al. Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nature Plants 1, 14016 (2015). https://doi.org/10.1038/nplants.2014.16

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  • DOI: https://doi.org/10.1038/nplants.2014.16

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