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. Access through your institution Buy or subscribe This is a preview of

subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 12 digital issues and online access to articles $119.00 per

year only $9.92 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated

during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS REDUCTION IN

ORGAN–ORGAN FRICTION IS CRITICAL FOR COROLLA ELONGATION IN MORNING GLORY Article Open access 05 March 2021 SPATIOTEMPORAL FORMATION OF GLANDS IN PLANTS IS MODULATED BY MYB-LIKE TRANSCRIPTION

FACTORS Article Open access 15 March 2024 LEAFY IS A PIONEER TRANSCRIPTION FACTOR AND LICENSES CELL REPROGRAMMING TO FLORAL FATE Article Open access 27 January 2021 REFERENCES * Evert, R.

F. in _Esau's plant Anatomy_ 3rd edn, 211–254 (Wiley, 2006). Book  Google Scholar  * 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). Article  CAS  Google Scholar  * 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  * Johnson, K.

& Lenhard, M. Genetic control of plant organ growth. _New Phytol_. 191, 319–333 (2011). Article  Google Scholar  * Mirabet, V., Das, P., Boudaoud, A. & Hamant, O. The role of

mechanical forces in plant morphogenesis. _Ann. Rev. Plant Biol_. 62, 365–385 (2011). Article  CAS  Google Scholar  * Sampathkumar, A., Yan, A., Krupinski, P. & Meyerowitz, E. M.

Physical forces regulate plant development and morphogenesis. _Curr. Biol_. 24, R475–R483 (2014). Article  CAS  Google Scholar  * Stracke, R., Werber, M. & Weisshaar, B. The R2R3-MYB

gene family in _Arabidopsis thaliana_. _Curr. Opin. Plant Biol_. 4, 447–456 (2001). Article  CAS  Google Scholar  * Serna, L. & Martin, C. Trichomes: different regulatory networks lead

to convergent structures. _Trends Plant Sci_. 11, 274–280 (2006). Article  CAS  Google Scholar  * Ramsay, N. A. & Glover, B. J. MYB–bHLH–WD40 protein complex and the evolution of

cellular diversity. _Trends Plant Sci_. 10, 63–70 (2005). Article  CAS  Google Scholar  * 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). Article  CAS  Google Scholar  * Martin, C. _et al._ The mechanics of cell fate

determination in petals. _Phil. Trans. R. Soc. Lon. B Biol. Sci_. 357, 809–813 (2002). Article  CAS  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  CAS  Google Scholar  * Paterson, A. H. _et al._ Repeated

polyploidization of _Gossypium_ genomes and the evolution of spinnable cotton fibres. _Nature_ 492, 423–427 (2012). Article  CAS  Google Scholar  * 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  * Endress, P. K. Symmetry in flowers: diversity and evolution. _Int. J. Plant Sci_. 160, S3–S23 (1999). Article  CAS  Google Scholar  * Kohel, R. J. Genetic

analysis of the open bud mutant in cotton. _J. Hered_. 64, 237–238 (1973). Article  Google Scholar  * 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  * 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). Article  CAS  Google Scholar  * 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  * Rao, S. S. R. Structure and distribution of plant trichomes in relation to taxonomy: _Hibiscus_ L. _Feddes Repertorium_ 102, 335–344 (1991). Google Scholar  * 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  * 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  * Weberling, F. _Morphology of Flowers and Inflorescences_ 13–16 (Cambridge Univ. Press, 1992).

Google Scholar  * 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  * 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). Article  CAS  Google Scholar  * 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). Article  CAS  Google Scholar  * 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  * 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). Article  CAS  Google Scholar  Download references 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). AUTHOR INFORMATION

AUTHORS AND AFFILIATIONS * CSIRO Agriculture, GPO Box 1600, Canberra, Australian Capital Territory 2601, New South Wales, Australia Jiafu Tan, Sally-Anne Walford, Elizabeth S. Dennis & 

Danny Llewellyn Authors * Jiafu Tan View author publications You can also search for this author inPubMed Google Scholar * Sally-Anne Walford View author publications You can also search for

this author inPubMed Google Scholar * Elizabeth S. Dennis View author publications You can also search for this author inPubMed Google Scholar * Danny Llewellyn View author publications You

can also search for this author inPubMed Google Scholar CONTRIBUTIONS 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. CORRESPONDING AUTHOR Correspondence to Danny Llewellyn. ETHICS DECLARATIONS COMPETING INTERESTS 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) RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE 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 Download citation * Received: 23 December 2015 *

Accepted: 23 May 2016 * Published: 20 June 2016 * DOI: https://doi.org/10.1038/nplants.2016.93 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content:

Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative