Physical mechanism for petal elongation in a flower

Flowers open. Flowers are beautiful. These seem to be so natural and obvious – but how can they develop so attractive morphology? We found an active mechanism to reduce the organ friction for proper flower morphogenesis.

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Flowers have evolved to attract pollinators. By opening flowers where petals/corolla expand widely, plants let pollinators to find them easily. Proper flowering requires the proper morphogenesis of petals, however, given that it is achieved in a restricted narrow space in closed floral buds, the mechanism of petal morphogenesis has been mysterious for me.

I have been working on petal/corolla development since I was a master’s student. My major research topic was a petal defective mutant of Arabidopsis thaliana. My former adviser gave me two excellent mutants - one was named ‘rabbit ears (rbe)’, where petals were lacking or deformed. For the other, I named it as ‘folded petals (fop)’ because the petals were folded when flowers open (I know that my naming-sense is not wonderful). I found that RBE was involved in petal primordia development, namely, at very early stage of flower development (Takeda et al., 2004), whereas FOP was required for later phase of petal morphogenesis.

He also showed me the folded-corolla mutant (cup flower) in the morning glory. The folded petals/corolla in different type of plants – choripetalous ones (those with separated petals; Arabidopsis thaliana) and sympetalous ones (those with fused petals; morning glory)! These mutants impressed me a lot, leading me to think that ‘There must be a hidden interesting mechanism there’.

Folded petals/corolla mutants in Arabidopsis and morning glory.

After finished my PhD and post-doc life, I started the FOLED PETALS project again. There were three fop mutants in Arabidopsis thaliana, and I found that FOP1 and FOP2 encoded wax synthase and ABC transporter, respectively, suggesting that wax synthesis and transport in petal epidermis were required for petal elongation in Arabidopsis thaliana (Takeda et al., 2013, 2014). But I could not fully understand the mechanism for corolla folding in the cup flower mutants in the morning glory.

There were several breakthroughs for the study of morning glory. The first one was provided by an undergraduate student in my laboratory – he found the defects of glandular secretory trichomes (GSTs) on corolla and sepals in the cup flower mutants. This was one of the highlights of this work.

The second breakthrough was the encounter with excellent collaborators: a physicist to do mathematical modelling, a technical specialist to do micro CT imaging, and informatician to do transcriptome analysis. The physicist established the physical model for corolla elongation with or without friction, elegantly showing the mechanical buckling (corolla folding) induced by growth and organ-organ friction. This physical mechanism resembles a simple experiment with an elastic sheet: it buckled when force is applied from both sides.  

Thanks to lab students and collaborators, we could finally reveal the physical regulation of petal/corolla elongation in the narrow space in the floral buds. In the morning glory flowers, secretion from GSTs on peripheral organs act as a lubricant, enabling corolla to elongate straight. In Arabidopsis thaliana that lacks the GSTs on floral organs, wax synthase and transport on petal epidermis play a role in smooth elongation of petals.

 

The main points of this work are:

 (1) Using the floral mutants of the Japanese morning glory described more than 200 years ago, we clarified the mechanical regulation of floral organ development within the narrow space in the floral bud.

 (2) The active reduction of physical friction between floral organs are conserved both in choripetalous plants (those with separated petals) and in sympetalous plants (those with fused petals).

 (3) Microstructure on floral organs, GSTs, are required for macroscopic flower morphology. This is the first report showing that the GSTs have an essential role in floral organ development, in addition to well-known functions in biotic- and abiotic-stress responses.

I have been focusing on cellular and genetic mechanism in flower development – and now, I realize the importance of the mechanical aspects for plant organ morphogenesis. We are now working on identification of the causal genes of corolla folding (we suppose that it is involved in GSTs development), and on production of horticultural plants with novel morphology by modifying the surface structure of flowers. I hope our work gives an impact to people who love flowers.

Based on the paper: Reduction in organ-organ friction is critical for corolla elongation in morning glory. Ayaka Shimoki, Satoru Tsugawa, Keiichiro Ohashi, Masahito Toda, Akiteru Maeno, Tomoaki Sakamoto, Seisuke Kimura, Takashi Nobusawa, Mika Nagao, Eiji Nitasaka, Taku Demura, Kiyotaka Okada, Seiji Takeda. Communications Biology 4, 285 (2021). https://doi.org/10.1038/s42003-021-01814-x

References

Seiji Takeda, Noritaka Matsumoto, and Kiyotaka Okada. RABBIT EARS, encoding a SUPERMAN-like zinc finger protein, regulates petal development in Arabidopsis thaliana. Development 131, 425-43 (2004). PubMed

Seiji Takeda, Akira Iwasaki, Noritaka Matsumoto, Tomohiro Uemura, Kiyoshi Tatematsu and Kiyotaka Okada. Physical interaction of floral organs controls petal morphogenesis in Arabidopsis thaliana. Plant Physiology 161, 1242-1250 (2013). 

Seiji Takeda, Akira Iwasaki, Kiyoshi Tatematsu, and Kiyotaka Okada. The half-size ABC transporter FOLDED PETALS 2/ABCG13 is involved in petal elongation through narrow spaces in Arabidopsis thaliana floral buds. Plants 3, 348-358 (2014). 

Seiji Takeda

Associate Professor, Kyoto Prefectural University