Evolution of Plant Body Plans

The conquest of land by plants over 450 million years ago was one of the most significant events in our planet's history, and was underpinned by a series of key innovations in plant architecture during evolution1.

Our group aims to identify the developmental and genetic basis of two such innovations- three dimensional shoot growth and branching- in a range of model systems representing different stages of plant evolution.

1. The molecular basis of three dimensional shoot growth.

The aquatic algal relatives of the land plants are constrained to string or mat-like forms with a planar (2D) growth habit, and capacity for 3D growth was gained as plants colonized land2. The earliest land plants resembled modern bryophytes in which the 3D growth phase is preceded by a 2D phase during the gametophyte stage of the life cycle2, 3. In mosses, the 2D to 3D transition is marked by cell swelling and a change of division plane in stem cells at the growing tips4, 5. The DEK1 calpain protease regulates stem cell division planes at a late stage of the transition to 3D growth6-8

We are using a reverse genetic approach to identify early-acting molecular determinants of the switch to 3D growth.

Figure 1: Mutants in which cell division planes (blue and yellow arrows) during the transition to 3D shoot growth are disrupted.

2. The evolution of branching mechanisms.

Diverse branching forms have arisen independently in both the gametophyte and sporophyte stages of plant life cycles during evolution. In Arabidopsis, the hormones auxin and cytokinin regulate branch initiation, and auxin, cytokinin and strigolactone regulate branch outgrowth. PIN auxin transporters generate a basipetal polar auxin transport stream in the main stem and co-ordinate the action of all three hormones9.

In mosses, sporophytes comprise a single stem, and gametophytes have lateral branching10. Bulk basipetal auxin transport has been detected in sporophytes, and we have found that mosses with defective auxin transport have branching sporophytes11, 12. These data suggest that the function of PIN proteins in polar auxin transport and branching is a homology of land plant sporophytes. However, bulk basipetal auxin transport is not detectable in the gametophyte generation11. Although we have found that auxin, cytokinin and strigolactone regulate gametophytic branching in a moss, our results suggest that the auxin transport required to generate branch patterning is non-polar and not mediated by PIN proteins. Instead, they suggest a callose based mechanism10

We are currently testing the above hypotheses by further functional work in a moss, and will build on this work by bringing other living and fossil plant groups into the lab.


Figure 2: Diverse branching forms in mosses reproduced from The Node: http://thenode.biologists.com/towards-a-mechanistic-understanding-of-branching-innovations-in-plant-evolution/research/.

 

References

1.Langdale, J.A., and Harrison, C.J. (2008) Developmental changes during the evolution of plant form. In Evolving Pathways: Key Themes in Evolutionary Developmental Biology (Fusco, A.M.a.G., ed), 299-315, Cambridge University Press, Cambridge.

2.Graham, L.E., et al. (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc. Natl. Acad. Sci. 97, 4535-4540.

3.Parihar, N.S. (1967) Bryophyta. Indian Universities Press.

4.Harrison, C.J., et al. (2009) Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Current Biology 19, 461-471.

5.Aoyama T, et al. (2012) AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139, 3120-3129.

6.Perroud, P.F., et al. (2014) Defective Kernel 1 (DEK1) is required for three-dimensional growth in Physcomitrella patens. New Phytologist 203, 794-804.

7.Demko, V., et al. (2014) Genetic analysis of DEK1 Loop function in three-dimensional body patterning in Physcomitrella patens. Plant Physiology 166, 903-919.

8.Olsen, O.A., et al. (2105) DEK1; missing piece in puzzle of plant development. Trends in Plant Science 20, 70-71.

9.Domagalska, M.A., and Leyser, O. (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12, 211-221.

10.Coudert, Y., et al. (2015) Three ancient hormonal cues co-ordinate shoot branching in a moss. eLIFE.

11.Fujita, T., et al. (2008) Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evolution and Development 10, 176-186.

12.Bennett, T.A., et al. (2014) Plasma membrane-targeted PIN proteins drive shoot development in a moss. Current Biology 24, 2776-2785.

 

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