Ectocarpus: an Evo‑Devo Model for the Brown Algae Susana M
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Coelho et al. EvoDevo (2020) 11:19 https://doi.org/10.1186/s13227-020-00164-9 EvoDevo REVIEW Open Access Ectocarpus: an evo-devo model for the brown algae Susana M. Coelho1* , Akira F. Peters2, Dieter Müller3 and J. Mark Cock1 Abstract Ectocarpus is a genus of flamentous, marine brown algae. Brown algae belong to the stramenopiles, a large super- group of organisms that are only distantly related to animals, land plants and fungi. Brown algae are also one of only a small number of eukaryotic lineages that have evolved complex multicellularity. For many years, little information was available concerning the molecular mechanisms underlying multicellular development in the brown algae, but this situation has changed with the emergence of Ectocarpus as a model brown alga. Here we summarise some of the main questions that are being addressed and areas of study using Ectocarpus as a model organism and discuss how the genomic information, genetic tools and molecular approaches available for this organism are being employed to explore developmental questions in an evolutionary context. Keywords: Ectocarpus, Life-cycle, Sex determination, Gametophyte, Sporophyte, Brown algae, Marine, Complex multicellularity, Phaeoviruses Natural habitat and life cycle Ectocarpus is a cosmopolitan genus, occurring world- Ectocarpus is a genus of small, flamentous, multicellu- wide in temperate and subtropical regions, and has been lar, marine brown algae within the order Ectocarpales. collected on all continents except Antarctica [1]. It is pre- Brown algae belong to the stramenopiles (or Heter- sent mainly on rocky shores where it grows on abiotic okonta) (Fig. 1a), a large eukaryotic supergroup that (rocks, pebbles, dead shells) and biotic (other algae, sea- is only distantly related to animals, plants and fungi. grass) substrata (Fig. 1b), and as a fouling organism it also Te stramenopiles include the macroscopic multicellu- colonises artifcial substrata. It is found from the sublitto- lar brown algae but also microbial algae (e.g., diatoms), ral to high intertidal pools, but it does not tolerate desic- diverse free-living heterotrophic or mixotrophic protists cation [2]. Ectocarpus sp. from Peru and northern Chile and important pathogens of animals and plants (e.g., (SE Pacifc) is the best studied species in the genus, and Blastocystis or oomycetes). Brown algae or brown sea- has become an established model for developmental biol- weeds are unique among stramenopiles (or heterokonts) ogy and evolutionary questions (see below). While most in developing into multicellular forms with diferenti- species are exclusively marine, some species such as Ecto- ated tissues, but they reproduce by means of fagellated carpus subulatus may also occur in permanently brackish spores and gametes that closely resemble cells of other habitats such as the inner Baltic Sea and has even been heterokonts. encountered in mineral-rich freshwater [3]. Numerous taxa of Ectocarpus have been described since the creation of the genus [4]. However the taxon- omy is complicated on one hand by oversplitting based *Correspondence: [email protected] on unreliable characters and on the other hand by the 1 CNRS, Sorbonne Université, UPMC University Paris 06, Algal Genetics presence of cryptic species and hybrids. Sequence-based Group, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscof, CS 90074, 29688 Roscof, France phylogenies have helped to disentangle the genus (e.g. Full list of author information is available at the end of the article [2, 5–7]) and molecular-assisted identifcation using © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Coelho et al. EvoDevo (2020) 11:19 Page 2 of 9 a ARCHEAPLASTIDA Ancoracysta AMORPHEA ChloroplastidRhodophyta * * Picozoa * *Glaucophyta CRYPTISTA * Apusomonada Palpitomonas a Breviates Katablepharida Opisthokonta Amoebozoa CRuMs Cryptophyta Diphylleida Rigifilida HAPTISTA Centrohelida Mantamonas Haptophyta Discoba ‘EXCAVATES’ TSAR Telonemia Metamonada Rhizaria Malawimonadida SAR Alveolata Ancyromonadida *Stramenopila Hemimastigophora b Ectocarpus sp. * * 0.5 cm 2 cm 20 µm Fig. 1 a Schematic view of the Eukaryotic tree, redrawn from [73]. The coloured groupings correspond to the currently recognised ‘supergroups’. Unresolved branching orders among lineages are shown as multifurcations. Broken lines refect lesser uncertainties about the monophyly of certain groups. Asterisks represent lineages where complex multicellularity emerged. Ectocarpus is a brown alga, belonging to the Stramenopila (indicated with an arrowhead). b Ectocarpus sp. gametophyte (asterisk) in the feld growing on the brown alga Scytosiphon lomentaria (arrowhead) (https :// www.algae base.org/searc h/speci es/detai l/?tc accep t&speci es_id 76) = = nuclear (ITS) and cytoplasmic (COI, rbcLS spacer) bar- phylogenies. Use of a combination of nuclear and mito- code markers permit reliable identifcation. However, chondrial markers has revealed the presence of natural nomenclature is still incomplete because it is difcult to hybrids [7, 8]. Te existence of several species at difer- link described taxa to the lineages obtained in molecular ent genetic distances and exhibiting diferences in sexual Coelho et al. EvoDevo (2020) 11:19 Page 3 of 9 compatibility, and the possibility of laboratory crosses [9] diferences between the two generations [15, 16]. Game- represent interesting options for genetic research. tophyte germlings are made up of a rhizoid and an Te Ectocarpus life cycle was frst described in 1964 upright flament, the latter consisting of cylindrical and 1967 [10, 11] using strains of Ectocarpus siliculo- cells (Fig. 2). Te upright flament grows and profusely sus from Naples, and later confrmed for other species branches to produce the mature thallus, which carries (e.g. [12]). Te sexual life cycle consists of an alternation plurilocular gametangia, the reproductive structures in between haploid male and female gametophyte and dip- which gametes are produced. Te developmental pro- loid sporophyte generations (a haploid-diploid life cycle gramme of the sporophyte is slightly more complex in with dioicy, Fig. 2). More details of the life cycle are given that it produces a basal system consisting of round and below. elongated cells before producing the upright flaments of the apical system (Fig. 2). Te upright flaments of the Laboratory culture and feld collections sporophyte resemble those of the gametophyte but are Ectocarpus is easily isolated in the laboratory from veg- less branched, and the angle of branching (about 90°) is etative or fertile feld material. Being a common alga, it is larger than in gametophytes ([16]; Fig. 2b). Sporophyte also regularly encountered as ‘contamination’ in isolates upright flaments produce two types of reproductive of other macroalgae, and is present as microstages on structure, plurilocular sporangia containing mito-spores natural substratum, from which it may be isolated using (which germinate to produce clones of the parent sporo- the germling emergence technique. Tis technique con- phyte) and unilocular sporangia in which a single meiotic sists of collecting substrata, incubating them in the labo- division followed by several mitotic divisions produces ratory and obtaining the alga as germlings that develop in the meio-spores (the initial cells of the gametophyte gen- culture [5]. In the feld, the two generations may inhabit eration) (Fig. 2). diferent niches and are often present at diferent seasons Ectocarpus sporophytes can be derived from zygotes of the year. Diferent populations may employ sexual and (i.e. formed by the fusion of two gametes to produce a asexual reproduction to diferent degrees [13]. Culture diploid individual) or can develop parthenogenetically in Petri dishes or in large fasks (when a large amount of from a gamete that has failed to fnd a partner of the material is needed, e.g. for protein or nucleic acid extrac- opposite sex (in which case they are called partheno-spo- tions) using standard seawater medium complemented rophytes). Being derived from a single gamete, most par- with nutrients is straightforward [13]. Gametophytes and theno-sporophytes are haploid (Fig. 2, but see [17]). Note sporophytes are grown under similar culture conditions that there are no conspicuous morphological diferences and the full life cycle can be completed in the laboratory between a diploid (zygote-derived) sporophyte and a par- in about 2 months [13]. Standard growth conditions are theno-sporophyte.