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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 . 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 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 . 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]. Working with population samples of , Zhao et al. [2] show that many polymorphisms for emerging genes exist within those Adaptive Protogene 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. supported an association with recent of completely new genes have long Using RNA-seq data for testis from positive selection. been a mystery. [5] the sequenced Raleigh (RAL) reference This fast rate of gene emergence stated in a comment on the first yeast strains of D. melanogaster, Zhao et al. raises the question why the genomes genome sequencing data that the most [2] searched specifically for transcripts do not fill up with such genes over time. surprising aspect was the relatively coming from intergenic sequences In spite of huge variation in total large number of genes that had no that are not annotated in the reference genome size, genomes do not show a homologues in other species. He genome. By comparing with data proportionally large variation in terms introduced the term ‘orphans’ for such from outgroups ( of protein-coding repertoires. Hence, genes and there was much subsequent and Drosophila yakuba), they could the emergence rate of new genes discussion about their origin and infer that the transcripts had arisen must in some way be balanced with their possible role. First ideas that specifically in D. melanogaster.Of a corresponding loss rate. de novo evolution could have these transcripts, 142 were found to be Palmieri et al. [3] explored the contributed to their emergence came polymorphic between strains and question of orphan gene turnover from comparative analyses of were found only in males. Contrary among species of the D. obscura Drosophila genomes and were to previous assumptions, based group, spanning divergence times of confirmed in further systematic on smaller datasets, they showed up to 10–15 million years. Their focus comparative studies in Drosophila and no over-representation on the was on the conservation pattern of [6–8]. Several studies have by X-chromosome. But otherwise these open reading frames of transcripts that now also shown that de novo emerged transcripts followed the general trend occur only within the D. obscura group. transcripts and proteins can assume a for orphan genes [14] of being shorter Their analyses of rates of evolution function within the organism [9–12]. All and containing fewer than older among these genes confirm that at of this provided solid evidence that de genes. For approximately one-third of least a portion of them bear signatures novo gene birth was indeed possible. the genes expressed in more than two of selective constraint at the protein However, it was an insight coming from strains it was possible to identify a level, thus complementing the findings re-analyses of translated transcripts in derived SNP within 500 bp upstream of Zhao et al. [2]. To estimate loss rates, yeast that suggested that de novo gene that correlates with a difference in gene they looked both at deletions as well as evolution could even be more prevalent expression. This supports the notion at the acquisition of stop codons that than -divergence that single nucleotide changes can interrupt these reading frames and processes [13]. In fact, we still need initiate effective transcription within found that the latter are rather more comparative studies from closely an intergenic sequence. The prevalent. Interestingly, they find that Current Biology Vol 24 No 6 R240 the newest genes are more likely to be particular interest to study the proteins 7. Zhou, Q., Zhang, G.J., Zhang, Y., Xu, S.Y., Zhao, R.P., Zhan, Z.B., Li, X., Ding, Y., Yang, S.A., lost than older ones, consistent with that emerge out of these de novo and Wang, W. (2008). On the origin of new genes either stochastic or weak-selection processes, to bring new light into the in Drosophila. Gen. Res. 18, 1446–1455. processes. Interestingly, they also question of the origin of new protein 8. Toll-Riera, M., Bosch, N., Bellora, N., Castelo, R., Armengol, L., Estivill, X., and found a correlation between the age domains and folds. It has been Alba, M.M. (2009). Origin of orphan of a gene and its expression levels, suggested that the seemingly finite genes: a comparative genomics approach. Mol. Biol. Evol. 26, 603–612. indicating that genes that have started amount of stable protein folds 9. Cai, J., Zhao, R.P., Jiang, H.F., and Wang, W. to become functional may become observed across all domains of life is (2008). De novo origination of a new optimized at both the protein and indicative of an early origin of all folds protein-coding gene in . Genetics 179, 487–496. expression level. [16–18], possibly under different 10. Heinen, T., Staubach, F., Haming, D., and Palmieri et al. [3] also revisit the conditions and functions than the ones Tautz, D. (2009). Emergence of a new gene from an intergenic region. Curr. Biol. 19, 1527–1531. question of male-biased expression today [17]. However, entirely new folds 11. Chen, S.D., Zhang, Y.E., and Long, M.Y. (2010). of new genes. It had previously been have been shown to arise de novo in New genes in Drosophila quickly become suggested that many new genes would viruses [19] and new domains are essential. Science 330, 1682–1685. 12. Reinhardt, J.A., Wanjiru, B.M., Brant, A.T., initially be expressed in the testis, present in recently acquired regions of Saelao, P., Begun, D.J., and Jones, C.D. (2013). given a more relaxed transcriptional old genes, as well as in young genes De novo ORFs in Drosophila are important to organismal fitness and evolved rapidly from environment associated with testis [20]. Until now, de novo evolved genes previously non-coding sequences. PLoS Genet. expression [15]. Such genes could then are largely underrepresented in 9, e1003860. become male-biased. However, structural analyses, and it seems that 13. Carvunis, A.R., Rolland, T., Wapinski, I., Calderwood, M.A., Yildirim, M.A., Simonis, N., Palmieri et al. [3] find that the fraction of resolving their structure is a challenge Charloteaux, B., Hidalgo, C.A., Barbette, J., male-biased genes increases with their that will provide us precious Santhanam, B., et al. (2012). Proto-genes and de novo gene birth. 487, 370–374. age. This suggests that male-biased information about the origin of stable 14. Neme, R., and Tautz, D. (2013). Phylogenetic gene expression of orphan genes is not folds, molecular functions and the patterns of emergence of new genes support a the result of a preferential recruitment interaction between genome and model of frequent de novo evolution. BMC Genomics 14, 117. of male-biased genes, but due to a environment. 15. Kaessmann, H. (2010). Origins, evolution, and higher loss rate of genes with unbiased phenotypic impact of new genes. Gen. Res. 20, 1313–1326. expression. References 16. Orengo, C.A., and Thornton, J.M. (2005). Protein The X-chromosome in the D. obscura 1. Tautz, D., and Domazet-Loso, T. (2011). The families and their evolution - A structural group has a particularly interesting evolutionary origin of orphan genes. Nat. Rev. perspective. Annu. Rev. Biochem. 74, 867–900. Gen. 12, 692–702. 17. Alva, V., Remmert, M., Biegert, A., Lupas, A.N., history in representing a fusion 2. Zhao, L., Saelao, P., Jones, C.D., and and Soding, J. (2010). A galaxy of folds. Prot. between an old X-chromosome and a Begun, D.J. (2014). Origin and spread of Sci. 19, 124–130. de novo genes in Drosophila melanogaster 18. Bornberg-Bauer, E., and Alba, M.M. (2013). previous autosome (called neo-X). This populations. Science 343, 769–772. Dynamics and adaptive benefits of modular allowed Palmieri et al. [3] to revisit the 3. Palmieri, N., Kosiol, C., and Schlo¨ tterer, C. protein evolution. Curr. Opin. Struct. Biol. 23, question of a prevalence of new gene (2014). The life cycle of Drosophila orphan 459–466. genes. eLife 3, e01311. 19. Pavesi, A., Magiorkinis, G., and Karlin, D.G. evolution on the X-chromosome [6]. 4. Khalturin, K., Hemmrich, G., Fraune, S., (2013). Viral proteins originated De Novo by They show that there is indeed an Augustin, R., and Bosch, T.C.G. (2009). More overprinting can be identified by codon usage: than just orphans: are taxonomically-restricted application to the ‘‘gene nursery’’ of over-representation of orphans on the genes important in evolution? Trends Genet. deltaretroviruses. PLoS Comp. Biol. 9, X, but only on the older chromosome 25, 404–413. e1003162. arm, not on the neo-X. Even more 5. Dujon, B. (1996). The yeast genome project: 20. Toll-Riera, M., and Alba` , M.M. (2013). What did we learn? Trends Genet. 12, Emergence of novel domains in proteins. BMC intriguingly, the orphan gene loss is 263–270. Evol. Biol. 13, 47. elevated on the neo-X, indicating 6. Levine, M.T., Jones, C.D., Kern, A.D., that genes that had originally evolved Lindfors, H.A., and Begun, D.J. (2006). Novel Max-Planck Institute for Evolutionary genes derived from noncoding DNA in Biology, 24306 Plo¨ n, Germany. on an autosome come under different Drosophila melanogaster are frequently *E-mail: [email protected] constraints when they become X-linked and exhibit testis-biased expression. Proc. Nat. Acad. Sci. USA 103, sex-chromosome associated. They 9935–9939. http://dx.doi.org/10.1016/j.cub.2014.02.016 thus confirm a difference in the dynamics of gene evolution on autosomes versus X-chromosomes, an effect that did not show up in the population study of Zhao et al. [2]. Therefore, this remains an open Organelle Interactions: Melanosomes question for the future. The results from the two papers and Mitochondria Get Cozy nicely complement our rapidly broadening concept of gene evolution. Melanosomes make pigments and mitochondria make ATP. A recent study has We can now draw a general life cycle shown that these two organelles are connected by fibrillar bridges and that for genes that includes a stochastic their close physical contact may promote the biogenesis of the melanosome phase in which new genes can emerge by providing it with ATP. from non-genic sequences (Figure 1). Although this early phase can only be studied among relatively recently Xufeng Wu and John A. Hammer* which is essential for normal cell diverged species, it seems likely that physiology. More and more, however, it has been active throughout all Organelles are defined by their unique we are learning about specific physical evolutionary times [1]. It will now be of structure and function, maintenance of contacts between different organelles