A13: Publications
Enhancer evolution and the origins of morphological novelty
Mark Rebeiz, Miltos Tsiantis, Science Direct Volume 45, August 2017, Pages 115–123, 2017 May 18, https://doi.org/10.1016/j.gde.2017.04.006.
A central goal of evolutionary biology is to understand the genetic origin of morphological novelties—i.e. anatomical structures unique to a taxonomic group. Elaboration of morphology during development depends on networks of regulatory genes that activate patterned gene expression through transcriptional enhancer regions. We summarize recent case studies and genome-wide investigations that have uncovered diverse mechanisms though which new enhancers arise. We also discuss how these enhancer-originating mechanisms have clarified the history of genetic networks underlying diversification of genital structures in flies, limbs and neural crest in chordates, and plant leaves. These studies have identified enhancers that were pivotal for morphological divergence and highlighted how novel genetic networks shaping form emerged from pre-existing ones.
Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity
Vuolo F., Mentink R.A., Hajheidari M., Bailey C.D., Filatov D.A., Tsiantis M., 25. Oct. 2016, Genes Dev. 30:2370-2375 doi: 10.1101/gad.290684.116
Here we investigate mechanisms underlying the diversification of biological forms using crucifer leaf shape as an example. We show that evolution of an enhancer element in the homeobox gene REDUCED COMPLEXITY (RCO) altered leaf shape by changing gene expression from the distal leaf blade to its base. A single amino acid substitution evolved together with this regulatory change, which reduced RCO protein stability, preventing pleiotropic effects caused by its altered gene expression. We detected hallmarks of positive selection in these evolved regulatory and coding sequence variants and showed that modulating RCO activity can improve plant physiological performance. Therefore, interplay between enhancer and coding sequence evolution created a potentially adaptive path for morphological evolution.
Interspecies Gene Transfer as a Method for Understanding the Genetic Basis for Evolutionary Change: Progress, Pitfalls, and Prospects
Nikolov LA, Tsiantis M.
Front Plant Sci. 2015 Dec 22;6:1135. doi: 10.3389/fpls.2015.01135. eCollection 2015
The recent revolution in high throughput sequencing and associated applications provides excellent opportunities to catalog variation in DNA sequences and gene expression between species. However, understanding the astonishing diversity of the Tree of Life requires understanding the phenotypic consequences of such variation and identification of those rare genetic changes that are causal to diversity. One way to study the genetic basis for trait diversity is to apply a transgenic approach and introduce genes of interest from a donor into a recipient species. Such interspecies gene transfer (IGT) is based on the premise that if a gene is causal to the morphological divergence of the two species, the transfer will endow the recipient with properties of the donor. Extensions of this approach further allow identifying novel loci for the diversification of form and investigating cis- and trans-contributions to morphological evolution. Here we review recent examples from both plant and animal systems that have employed IGT to provide insight into the genetic basis of evolutionary change. We outline the practice of IGT, its methodological strengths and weaknesses, and consider guidelines for its application, emphasizing the importance of phylogenetic distance, character polarity, and life history. We also discuss future perspectives for exploiting IGT in the context of expanding genomic resources in emerging experimental systems and advances in genome editing.
Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta
Rast-Somssich MI, Broholm S, Jenkins H, Canales C, Vlad D, Kwantes M, Bilsborough G, Dello Ioio R, Ewing RM, Laufs P, Huijser P, Ohno C, Heisler MG, Hay A, Tsiantis M.
Genes Dev. 2015 Nov 15;29(22):2391-404. doi: 10.1101/gad.269050.115. Erratum in: Genes Dev. 2016 Jan 1;30(1):132
Two interrelated problems in biology are understanding the regulatory logic and predictability of morphological evolution. Here, we studied these problems by comparing Arabidopsis thaliana, which has simple leaves, and its relative, Cardamine hirsuta, which has dissected leaves comprising leaflets. By transferring genes between the two species, we provide evidence for an inverse relationship between the pleiotropy of SHOOTMERISTEMLESS (STM) and BREVIPEDICELLUS (BP) homeobox genes and their ability to modify leaf form. We further show that cis-regulatory divergence of BP results in two alternative configurations of the genetic networks controlling leaf development. In C. hirsuta, ChBP is repressed by the microRNA164A (MIR164A)/ChCUP-SHAPED COTYLEDON (ChCUC) module and ChASYMMETRIC LEAVES1 (ChAS1), thus creating cross-talk between MIR164A/CUC and AS1 that does not occur in A. thaliana. These different genetic architectures lead to divergent interactions of network components and growth regulation in each species. We suggest that certain regulatory genes with low pleiotropy are predisposed to readily integrate into or disengage from conserved genetic networks influencing organ geometry, thus rapidly altering their properties and contributing to morphological divergence.
From limbs to leaves: common themes in evolutionary diversification of organ form
Remco A. Mentink and Miltos Tsiantis, Front Genet. 2015; 6: 284
An open problem in biology is to derive general principles that capture how morphogenesis evolved to generate diverse forms in different organisms. Here we discuss recent work investigating the morphogenetic basis for digit loss in vertebrate limbs and variation in form of marginal outgrowths of angiosperm (flowering plant) leaves. Two pathways underlie digit loss in vertebrate limbs. First, alterations to digit patterning arise through modification of expression of the Patched 1 receptor, which senses the Sonic Hedgehog morphogen and limits its mobility in the limb bud. Second, evolutionary changes to the degree of programmed cell death between digits influence their development after their initiation. Similarly, evolutionary modification of leaf margin outgrowths occurs via two broad pathways. First, species-specific transcription factor expression modulates outgrowth patterning dependent on regulated transport of the hormone auxin. Second, species-specific expression of the newly discovered REDUCED COMPLEXITY homeodomain transcription factor influences growth between individual outgrowths after their initiation. These findings demonstrate that in both plants and animals tinkering with either patterning or post-patterning processes can cause morphological change. They also highlight the considerable flexibility of morphological evolution and indicate that it may be possible to derive broad principles that capture how morphogenesis evolved across complex eukaryotes.
Keywords: evolution and development, leaflet formation, digit formation, patterning versus post-patterning, morphological diversity
Leaf Shape Evolution Through Duplication, Regulatory Diversification, and Loss of a Homeobox Gene
Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, Galinha C, Gan X, Hajheidari M, Hay A, Smith RS, Huijser P, Bailey CD, Tsiantis M, Science Vol. 343 no. 6172 pp. 780-783 (2014)
In this work, we investigate morphological differences between Arabidopsis thaliana, which has simple leaves, and its relative Cardamine hirsuta, which has dissected leaves comprising distinct leaflets. With the use of genetics, interspecific gene transfers, and time-lapse imaging, we show that leaflet development requires the REDUCED COMPLEXITY (RCO) homeodomain protein. RCO functions specifically in leaves, where it sculpts developing leaflets by repressing growth at their flanks. RCO evolved in the Brassicaceae family through gene duplication and was lost in A. thaliana, contributing to leaf simplification in this species. Species-specific RCO action with respect to its paralog results from its distinct gene expression pattern in the leaf base. Thus, regulatory evolution coupled with gene duplication and loss generated leaf shape diversity by modifying local growth patterns during organogenesis.
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