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Reconstructing Trait Evolution in Plant Evo–Devo Studies

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Reconstructing Trait Evolution in Plant Evo–Devo Studies Current Biology Magazine Essay Marchantia is genetically tractable [10]. The diversifi cation of model species Reconstructing trait evolution in plant offers unprecedented opportunities to explore fundamental biological evo–devo studies processes. Furthermore, comparative studies with other plant clades have Pierre-Marc Delaux1,*, Alexander J. Hetherington2, Yoan Coudert3, the potential to unravel evolutionary Charles Delwiche4, Christophe Dunand1, Sven Gould5, Paul Kenrick6, events that shaped the diversity of Fay-Wei Li7,8, Hervé Philippe9,10, Stefan A. Rensing11,12,13, Mélanie Rich1, extant plant species. The access to Christine Strullu-Derrien6,14, and Jan de Vries15,16,17 many plant genomes, transcriptomes and new model species therefore Our planet is teeming with an astounding diversity of plants. In a mere single makes it an exciting time for studying group of closely related species, tremendous diversity can be observed in their plant evolution. However, as the form and function — the colour of petals in fl owering plants, the shape of the number of model species expands fronds in ferns, and the branching pattern of the gametophyte in mosses. Diversity and diversifi es, it is important to pay can also be found in subtler traits, such as the resistance to pathogens or the close attention to the method used ability to recruit symbiotic microbes from the environment. Plant traits can also to draw evolutionary comparisons be highly conserved — at the cellular and metabolic levels, entire biosynthetic between species. This becomes pathways are present in all plant groups, and morphological characteristics particularly important when drawing such as vascular tissues have been conserved for hundreds of millions of years. conclusions with the benchmark of The research community that seeks to understand these traits — both the Arabidopsis, when the species last diverse and the conserved — by taking an evolutionary point-of-view on plant shared a common ancestor with this biology is growing. Here, we summarize a subset of the different aspects of Brassicaceae hundreds of millions of plant evolutionary biology, provide a guide for structuring comparative biology years ago. approaches and discuss the pitfalls that (plant) researchers should avoid when The aim of this article is to provide a embarking on such studies. guide for structuring the rationale that is used when employing comparative biology approaches. We start fi rst by Plants are extremely diverse, whether biology is growing. There are a number highlighting the importance of drawing this be in the range of petal colours of reasons for this. Foremost is the conclusions based on precisely in angiosperms [1], the shape of the availability of whole plant genomes and reconstructed species phylogenies, fronds in ferns [2], the branching transcriptomes covering the breadth of and go on to outline a 5-step guide pattern of the gametophyte in mosses the plant phylogeny. This goes hand- for structuring evolutionary studies, [3] or their interactions with microbes in-hand with the development of model illustrated with examples from the and the environment. To understand systems beyond the fl owering plant literature. this diversity, it is essential to explore Arabidopsis thaliana (L.) Heynh. Such the genetic framework underlying any prospering models include a huge Species phylogenies and tree of these traits in light of evolution. diversity of angiosperm species, from thinking Researchers studying the evolution trees (such as Populus trichocarpa), Evolutionary relationships between of traits aim at determining “which to a range of species to study fl ower organisms are best expressed genes and what kinds of changes development (e.g., Antirrhinum majus through phylogenetic trees. The use in their sequences are responsible and Aquilegia caerulea), together with of DNA sequences to reconstruct for the evolution of [morphological] enormous progress with gymnosperms, phylogenies, particularly multi-loci diversity” [4]. This way of approaching including the fi rst genome assemblies phylogenomics, has improved the diversity was initiated by developmental and studies of gene expression and resolution of the plant tree of life biologists, leading to the emergence conservation. Major advances have (Figure 1). It is now widely accepted of evolutionary developmental biology also been made with lycophytes or that the closest extant relatives of land (evo–devo) that was later expanded monilophytes, such as the model fern plants are the streptophyte algae in to all aspects of plant biology, such Ceratopteris richardii, and fi nally the the Zygnematophyceae class [11–13]. as the interactions between plants development of liverwort, moss as well Within the land plants, the relationship and microbes [5,6] (evo–MPMI, for as algal model systems. among the major lineages is relatively evolutionary molecular plant–microbe The liverwort Marchantia polymorpha well supported (Figure 1). Living land interactions) or the study of cellular is being established as a major model plants constitute two main groups, biology [7] (evo–cell biology). The in plant science, mainly because it vascular and non-vascular plants. terms are different, but these fi elds of has a short life cycle and a relatively Vascular plants (tracheophytes) form research rely on the same comparative small genome with fewer paralogs a monophyletic group, encompassing approaches to characterise trait (see Glossary box) than most other the lycophytes, ferns and seed plants. evolution — they, hence, face similar land plant species [8]. Similar to the Uncertainty still remains regarding the challenges. model moss Physcomitrella patens — branching order of the non-vascular The research community taking an which has been extensively used plants, the bryophytes (hornworts, evolutionary point-of-view on plant throughout the last two decades [9] — liverworts and mosses), with three main R1110 Current Biology 29, R1105–R1121, November 4, 2019 © 2019 Elsevier Ltd. Current Biology Magazine A Angiosperms DEMosses Gymnosperms Vascular Gymnosperms Liverworts Angiosperms plants Ferns Hornworts Ferns or Lycophytes Angiosperms Lycophytes Tracheophytes Mosses Gymnosperms Hornworts Non-vascular Liverworts Ferns Liverworts plants or Hornworts Lycophytes Mosses Bryophytes Zygnematophyceae Rotate Zygnematophyceae Rotate Zygnematophyceae Coleochaetophyceae Coleochaetophyceae Coleochaetophyceae Streptophyte Charophyceae Charophyceae Charophyceae algae Klebsormidiophyceae Klebsormidiophyceae Klebsormidiophyceae or Chlorokybophyceae Chlorokybophyceae Chlorokybophyceae Charophytes Mesostigmatophyceae Mesostigmatophyceae Mesostigmatophyceae Chlorophytes Chlorophytes Chlorophytes B F Klebsormidiophyceae Angiosperms algae es yte yt ph Gymnosperms h pto op re t St ep Ferns tr Charophyceae S Coleochaetophyceae Lycophytes Hornworts Mosses Zygnematophyceae Chlorokybophyceae Liverworts Mesostigmatophyceae Zygnematophyceae Coleochaetophyceae Charophyceae Chlorophytes Klebsormidiophyceae Land plants Chlorokybophyceae Mesostigmatophyceae G Streptophyte algae Chlorophytes Chlorophytes Land plants C H Angiosperms Lycophytes Gymnosperms es Br yt yo Ferns h ph op y e te h s Lycophytes c F ra erns T Mosses osses Liverworts Gymnos M s Hornworts pe rms erwort Zygnematophyceae Liv Coleochaetophyceae Charophyceae Klebsormidiophyceae Angiosperms Hornworts Chlorokybophyceae Mesostigmatophyceae I Tracheophytes Bryophytes Chlorophytes Current Biology Figure 1. Navigating the plant phylogeny — one tree, different views. (A–C) The dendrograms depict the three most highly supported branching orders for algal and land plant groups forming the green lineage (after Puttick et al. [12]). (A) Bryophyte monophyletic; (B) Mosses and liverworts monophyletic, hornworts sister to tracheophytes; (C) Mosses and liverworts monophyletic with hornworts sister to all land plants. (D,E) Alternative views of (A) showing that nodes can be rotated in a tree without changing the topology or relationships between sister groups. (F) Alternative view of cladograms (A–C) depicting the paraphyly of streptophyte algae, the position of the Zygnematophyceae as sister lineage to land plants, and the position of the chlorophyte sister lineage to the strepto- phytes. (G) Condensed view of (H). (H) Cladogram depicting the relationships between the major groups of land plants as in (A,D,E). (I) Condensed view of (H) highlighting bryophyte and tracheophyte monophyly. Current Biology 29, R1105–R1121, November 4, 2019 R1111 Current Biology Magazine hypotheses equally well supported A guideline for plant evolutionary the origin of the fl ower, a synapomorphy (Figure 1A–C) [11,12,14]. biology studies of angiosperms (the ingroup), one One requirement for the study of can choose to compare with the evolution is the ability to navigate Step 1: Inferring trait evolution gymnosperms (the outgroup) that lack phylogenies. Rooted phylogenetic trees Any study on the evolution of form fl owers. By mapping a character of contain deep and shallow branches. and function (traits) should start by interest onto a species tree of both the In addition, for practical reasons trees precisely defi ning the trait of interest. in- and outgroup, it is possible to defi ne often include more species that are Given that the same term can be used the evolution of a trait based on extant closely related to the focal organisms — by different authors or by different fi elds species. which is referred to as selective, to mean different things, it is essential A trait
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