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Trichomes control flower bud shape by linking together young petals

Abstract

Trichomes are widespread in plants and develop from surface cells on different tissues1. They have many forms and functions, from defensive spines to physical barriers that trap layers of air to insulate against desiccation, but there is growing evidence that trichomes can also have developmental roles in regulating flower structure2,3. We report here that the trichomes on petals of cotton, Gossypium hirsutum L., are essential for correct flower bud shape through a mechanical entanglement of the trichomes on adjacent petals that anchor the edges to counter the opposing force generated by asymmetric expansion of overlapping petals. Silencing a master regulator of petal trichomes, GhMYB-MIXTA-Like10 (GhMYBML10), by RNA interference (RNAi) suppressed petal trichome growth and resulted in flower buds forming into abnormal corkscrew shapes that exposed developing anthers and stigmas to desiccation damage. Artificially gluing petal edges together could partially restore correct bud shape and fertility. Such petal ‘Velcro’ is present in other Malvaceae and perhaps more broadly in other plant families, although it is not ubiquitous. This mechanism for physical association between separate organs to regulate flower shape and function is different from the usual organ shape control4 exerted through cell-to-cell communication and differential cell expansion within floral tissues5,6.

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Figure 1: Cotton petal trichomes are regulated by GhMYBML10.
Figure 2: Trichome-less GhMYBML10 RNAi flower buds have an abnormal shape.
Figure 3: Trichomes physically link petals together.
Figure 4: Trichome entanglement mechanically resists petal separation.

References

  1. 1

    Evert, R. F. in Esau's plant Anatomy 3rd edn, 211–254 (Wiley, 2006).

    Book  Google Scholar 

  2. 2

    Glover, B. J., Bunnewell, S. & Martin, C. Convergent evolution within the genus Solanum: the specialised anther cone develops through alternative pathways. Gene 331, 1–7 (2004).

    CAS  Article  Google Scholar 

  3. 3

    El Ottra, J. H. L., Pirani, J. R. & Endress, P. K. Fusion within and between whorls of floral organs in Galipeinae (Rutaceae): structural features and evolutionary implications. Ann. Bot. 111, 821–837 (2013).

    Article  Google Scholar 

  4. 4

    Johnson, K. & Lenhard, M. Genetic control of plant organ growth. New Phytol. 191, 319–333 (2011).

    Article  Google Scholar 

  5. 5

    Mirabet, V., Das, P., Boudaoud, A. & Hamant, O. The role of mechanical forces in plant morphogenesis. Ann. Rev. Plant Biol. 62, 365–385 (2011).

    CAS  Article  Google Scholar 

  6. 6

    Sampathkumar, A., Yan, A., Krupinski, P. & Meyerowitz, E. M. Physical forces regulate plant development and morphogenesis. Curr. Biol. 24, R475–R483 (2014).

    CAS  Article  Google Scholar 

  7. 7

    Stracke, R., Werber, M. & Weisshaar, B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447–456 (2001).

    CAS  Article  Google Scholar 

  8. 8

    Serna, L. & Martin, C. Trichomes: different regulatory networks lead to convergent structures. Trends Plant Sci. 11, 274–280 (2006).

    CAS  Article  Google Scholar 

  9. 9

    Ramsay, N. A. & Glover, B. J. MYB–bHLH–WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci. 10, 63–70 (2005).

    CAS  Article  Google Scholar 

  10. 10

    Noda, K., Glover, B. J., Linstead, P. & Martin, C. Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369, 661–664 (1994).

    CAS  Article  Google Scholar 

  11. 11

    Martin, C. et al. The mechanics of cell fate determination in petals. Phil. Trans. R. Soc. Lon. B Biol. Sci. 357, 809–813 (2002).

    CAS  Article  Google Scholar 

  12. 12

    Machado, A., Wu, Y., Yang, Y., Llewellyn, D. J. & Dennis, E. S. The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J. 59, 52–62 (2009).

    CAS  Article  Google Scholar 

  13. 13

    Walford, S. A., Wu, Y., Llewellyn, D. J. & Dennis, E. S. GhMYB25-like: a key factor in early cotton fibre development. Plant J. 65, 785–797 (2011).

    CAS  Article  Google Scholar 

  14. 14

    Paterson, A. H. et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492, 423–427 (2012).

    CAS  Article  Google Scholar 

  15. 15

    Bedon, F., Ziolkowski, L., Walford, S. A., Dennis, E. S. & Llewellyn, D. J. Members of the MYBMIXTA-like transcription factors may orchestrate the initiation of fibre development in cotton seeds. Front. Plant Sci. 5, 179 (2014).

    Article  Google Scholar 

  16. 16

    Endress, P. K. Symmetry in flowers: diversity and evolution. Int. J. Plant Sci. 160, S3–S23 (1999).

    CAS  Article  Google Scholar 

  17. 17

    Kohel, R. J. Genetic analysis of the open bud mutant in cotton. J. Hered. 64, 237–238 (1973).

    Article  Google Scholar 

  18. 18

    Qian, N., Zhang, X.-W., Guo, W.-Z. & Zhang, T.-Z. Fine mapping of open-bud duplicate genes in homoelogous chromosomes of tetraploid cotton. Euphytica 165, 325–331 (2009).

    Article  Google Scholar 

  19. 19

    Oshima, Y. et al. MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25, 1609–1624 (2013).

    CAS  Article  Google Scholar 

  20. 20

    Walford, S. A., Wu, Y., Llewellyn, D. J. & Dennis, E. S. Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. Plant J. 71, 464–478 (2012).

    CAS  PubMed  Google Scholar 

  21. 21

    Rao, S. S. R. Structure and distribution of plant trichomes in relation to taxonomy: Hibiscus L. Feddes Repertorium 102, 335–344 (1991).

    Google Scholar 

  22. 22

    Carvalho-SobrinhoI, J. G., Assis Ribeiro dos Santos, F. & Queiroz, L. P. Morphology of trichomes in petals of Pseudobombax Dugand (Malvaceae, Bombacoideae) species and its taxonomic significance. Acta Bot. Bras. 23, 929–934 (2009).

    Article  Google Scholar 

  23. 23

    Adedeji, O., Ajuwon, O. Y. & Babawale, O. O. Foliar epidermal studies, organographic distribution and taxonomic importance of trichomes in the family Solanaceae. Int. J. Bot. 3, 276–282 (2007).

    Article  Google Scholar 

  24. 24

    Weberling, F. Morphology of Flowers and Inflorescences 13–16 (Cambridge Univ. Press, 1992).

    Google Scholar 

  25. 25

    Douglas, A. W. The developmental basis of morphological diversification and synorganization in flowers of the Conospermeae (Stirlingia and Conosperminae: Proteaceae). Int. J. Plant Sci. 158, S13–S48 (1997).

    Article  Google Scholar 

  26. 26

    Zhang, T. et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fibre improvement. Nature Biotech. 33, 531–537 (2015).

    CAS  Article  Google Scholar 

  27. 27

    Helliwell, C. A., Wesley, S. V., Wielopolska, A. J. & Waterhouse, P. M. High-throughput vectors for efficient gene silencing in plants. Funct. Plant Biol. 29, 1217–1225 (2002).

    CAS  Article  Google Scholar 

  28. 28

    Talbot, M. & White, R. Methanol fixation of plant tissue for scanning electron microscopy improves preservation of tissue morphology and dimensions. Plant Meth. 9, 36 (2013).

    Article  Google Scholar 

  29. 29

    MacMillan, C. P., Mansfield, S. D., Stachurski, Z. H., Evans, R. & Southerton, S. G. Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J. 62, 689–703 (2010).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank E. Johnston, H. Martin and J. Radik for technical assistance, Z. Stachurski (Australian National University) for assistance with biomechanical testing and M. Talbot for assistance with SEM. The authors acknowledge the Black Mountain Bioimaging Centre for instrumentation, training and technical support. This work was supported by funding from the Monsanto Company and Cotton Breeding Australia (a joint venture between CSIRO and Cotton Seed Distributors).

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D.L. and E.S.D. conceived the project. D.L. and S.-A.W. provided materials. J.T. performed the experiments. All authors analysed data and wrote and approved the manuscript.

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Correspondence to Danny Llewellyn.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figs 1-10. (PDF 3232 kb)

Supplementary Video 1

Real-time imaging of the tension meter testing of the forces required to separate adjoined petals. (MP4 1895 kb)

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Tan, J., Walford, SA., Dennis, E. et al. Trichomes control flower bud shape by linking together young petals. Nature Plants 2, 16093 (2016). https://doi.org/10.1038/nplants.2016.93

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