Evolution: Dynamics of De Novo Gene Emergence

View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology Vol 24 No 6 R238 thought that here the outer epidermal might ask the legitimate question 10. Savaldi-Goldstein, S., and Chory, J. (2008). Growth coordination and the shoot epidermis. layer of the root represents the whether physical forces can act as Curr. Opin. Plant Biol. 11, 42–48. major mechanical constraint to bona fide signals or whether patterning 11. Kierzkowski, D., Nakayama, N., organogenesis [10]. The outer wall of is mainly a matter of biochemical Routier-Kierzkowska, A.-L., Weber, A., Bayer, E., Schorderet, M., Reinhardt, D., the meristem is much thicker than the gradients — at the molecular level, Kuhlemeier, C., and Smith, R.S. (2012). Elastic inner walls, and the shoot apical physics and chemistry are intimately domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335, meristem is sometimes compared to linked. 1096–1099. a balloon, with relatively soft, elastic 12. Fleming, A.J., McQueen-Mason, S., Mandel, T., inner compartments that do not play an and Kuhlemeier, C. (1997). Induction of leaf References primordia by the cell wall protein expansin. important mechanical role [11].Itis 1. Vermeer, J.E.M., von Wangenheim, D., Science 276, 1415–1418. widely accepted that organ formation Barberon, M., Lee, Y., Stelzer, E.H.K., 13. Peaucelle, A., Louvet, R., Johansen, J.N., Maizel, A., and Geldner, N. (2014). A spatial Ho¨ fte, H., Laufs, P., Pelloux, J., and Mouille, G. at the shoot apex involves the accommodation by neighboring cells is (2008). Arabidopsis phyllotaxis is controlled by modification of the outer epidermal required for organ initiation in Arabidopsis. the methyl-esterification status of cell-wall wall, causing it to bulge out [12,13]. Science 343, 178–183. pectins. Curr. Biol. 18, 1943–1948. 2. De Smet, I. (2012). Lateral root initiation: one 14. Peaucelle, A., Braybrook, S.a., Le Guillou, L., Since the walls of the inner cells are step at a time. New Phytol. 6, 867–873. Bron, E., Kuhlemeier, C., and Ho¨ fte, H. (2011). supposed to be much weaker, the 3. Lucas, M., Kenobi, K., von Wangenheim, D., Pectin-induced changes in cell wall mechanics Vob, U., Swarup, K., De Smet, I., Van underlie organ initiation in Arabidopsis. Curr. epidermis would simply draw the inner Damme, D., Lawrence, T., Pe´ ret, B., Biol. 21, 1720–1726. tissues with it, causing the primordium Moscardi, E., et al. (2013). Lateral root 15. Hamant, O., Heisler, M.G., Jo¨ nsson, H., to bulge out. morphogenesis is dependent on the Krupinski, P., Uyttewaal, M., Bokov, P., mechanical properties of the overlaying Corson, F., Sahlin, P., Boudaoud, A., Recent findings, however, suggest tissues. Proc. Natl. Acad. Sci. USA 110, Meyerowitz, E.M., et al. (2008). Developmental a different picture. When atomic 5229–5234. patterning by mechanical signals in 4. Swarup, K., Benkova´ , E., Swarup, R., Arabidopsis. Science 322, 1650–1655. force microscopy was employed to Casimiro, I., Pe´ ret, B., Yang, Y., Parry, G., 16. Uyttewaal, M., Burian, A., Alim, K., Landrein, B., measure the changes in wall stiffness Nielsen, E., De Smet, I., Vanneste, S., et al. Borowska-Wykre˛ t, D., Dedieu, A., Peaucelle, A., during organ initiation at the shoot (2008). The auxin influx carrier LAX3 promotes Ludynia, M., Traas, J., Boudaoud, A., et al. lateral root emergence. Nat. Cell Biol. 10, (2012). Mechanical stress acts via katanin to meristem, little or no changes in the 946–954. amplify differences in growth rate between mechanical properties of the outer 5. Ditengou, F.A., Teale, W.D., Kochersperger, P., adjacent cells in Arabidopsis. Cell 149, Flittner, K.A., Kneuper, I., van der Graaff, E., 439–451. wall layer were found. By contrast, Nziengui, H., Pinosa, F., Li, X., Nitschke, R., 17. Heisler, M.G., Hamant, O., Krupinski, P., the walls of inner layers were found to et al. (2008). Mechanical induction of lateral Uyttewaal, M., Ohno, C., Jo¨ nsson, H., Traas, J., soften significantly [14]. If confirmed, root initiation in Arabidopsis thaliana. Proc. and Meyerowitz, E.M. (2010). Alignment Natl. Acad. Sci. USA 105, 18818–18823. between PIN1 polarity and microtubule this would suggest a scenario where, 6. Laskowski, M., Grieneisen, V.a., Hofhuis, H., orientation in the shoot apical meristem reveals like in the root, inner cells are first Ten Hove, C.a., Hogeweg, P., Mare´ e, A.F.M., a tight coupling between morphogenesis and and Scheres, B. (2008). Root system auxin transport. PLoS Biol. 8, e1000516. driving organogenesis. However, in architecture from coupling cell shape to auxin 18. Nakayama, N., Smith, R.S., Mandel, T., contrast to the root, no breakthrough of transport. PLoS Biol. 6, e307. Robinson, S., Kimura, S., Boudaoud, A., and the epidermis occurs at the shoot. 7. Richter, G.L., Monshausen, G.B., Krol, A., and Kuhlemeier, C. (2012). Mechanical regulation of Gilroy, S. (2009). Mechanical stimuli modulate auxin-mediated growth. Curr. Biol. 22, Therefore, other accommodation lateral root organogenesis. Plant Physiol. 151, 1468–1476. mechanisms might have evolved to 1855–1866. 8. Moreno-Risueno, M.a., Van Norman, J.M., make way for the expanding inner Moreno, A., Zhang, J., Ahnert, S.E., and Laboratory of Plant Reproduction and cells and causing the epidermis to Benfey, P.N. (2010). Oscillating gene Development, ENS-Lyon, INRA, UCBL, expression determines competence for participate actively in organ periodic Arabidopsis root branching. Science CNRS, Lyon, France. outgrowth. It is worth pointing out 329, 1306–1311. *E-mail: [email protected] that the epidermal layer is capable 9. Sassi, M., and Vernoux, T. (2013). Auxin and self-organization at the shoot apical meristem. of reacting to mechanical stress J. Exp. Bot. 64, 2579–2592. http://dx.doi.org/10.1016/j.cub.2014.01.064 by modifying its microtubule organization and cell polarity [15–18]. This has the potential to alter auxin distribution and eventually organogenesis [17], although De Novo no experimental proof of Evolution: Dynamics of Gene mechanically induced organ initiation at the shoot has been Emergence provided so far. In conclusion, recent work depicts Comparative genomics have brought much insight into the de novo emergence plant morphogenesis as the result of genes. Two new studies in Drosophila explore the dynamics of gene gain and of a constant interplay between loss at the population and species levels, extending our view on the life cycle of biochemical and mechanical genes. interactions between neighboring cells and tissues. It should be noted that the discussion about the relative Rafik Neme and Diethard Tautz* intergenic non-coding sequences importance of physical and seemed remote. However, there is now biochemical processes in plant The emergence of new genes has long rapidly increasing evidence that de development is somewhat artificial, been thought to be almost exclusively novo evolution of transcripts and genes linked to the scale at which we driven by duplication or recombination is not only a theoretical possibility, but consider the system. Indeed, whereas of existing gene fragments. The might even have been a rather active at the level of an organ or tissue, we possibility of de novo evolution from process throughout evolution [1]. Dispatch R239 The laboratories of David Begun and Gene Christian Schlo¨ tterer are now providing duplication two further cornerstones for our retrotransposition understanding of de novo evolution of fusion / rearrangement genes [2,3]. horizontal gene transfer Working with population samples of Drosophila melanogaster, Zhao et al. [2] show that many polymorphisms for emerging genes exist within those Adaptive Protogene Pseudogene populations, allowing the authors Stochastic to trace the earliest steps of the Gene birth Gene death Gene death emergence of such genes. Palmieri et al. [3] estimate rates for birth and death processes within several closely Non-genic related species of the Drosophila sequence obscura group and show that rates of Current Biology gene loss balance rates of gain, thus explaining why genomes do not fill up with de novo genes over time. Both Figure 1. The life cycle of genes. studies imply that raw material for Blue arrows represent transitions which lead, either partially or completely, to a new gene, and genes is continuously being generated, are therefore dubbed processes of gene birth. Red arrows represent the loss of features which result in the degradation of the genic potential of a sequence. Green arrows represent the pro- available for selection to act upon. This cesses which increase the gene repertoire from existing genes. Raw material for genes is sto- would explain why higher rates of gene chastically generated as protogenes [13], entities that have gene-like properties (i.e. stable gains can be observed in times of major expression or translation), but may still lack a proper function. Once a protogene is able to radiations [1]. Ecological diversification perform a function that has an adaptive advantage, it will become fixed in a population. can lead to an increase in the retention Gene loss through pseudogenization can lead to the death of a gene in a lineage, when the rates of de novo genes, as they would selective pressure upon it is released. This will also be the case for protogenes which have not fully developed into genes. have more opportunities to fill a functional niche. This is consistent with our current understanding of new related lineages to better understand transcripts also code for slightly longer genes and their contribution to de novo emergence processes. The open reading frames than would be lineage-specific adaptations generated studies by Zhao et al. [2] and Palmieri expected by chance alone, and for during radiations [4]. et al. [3] thus constitute major steps a subset, the population genetic data The mechanisms of the emergence forward in this quest.

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