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Volvox and Volvocine Green Algae James G Umen EvoDevo (2020) 11:13 https://doi.org/10.1186/s13227-020-00158-7 EvoDevo REVIEW Open Access Volvox and volvocine green algae James G. Umen* Abstract The transition of life from single cells to more complex multicellular forms has occurred at least two dozen times among eukaryotes and is one of the major evolutionary transitions, but the early steps that enabled multicellular life to evolve and thrive remain poorly understood. Volvocine green algae are a taxonomic group that is uniquely suited to investigating the step-wise acquisition of multicellular organization. The multicellular volvocine species Volvox car- teri exhibits many hallmarks of complex multicellularity including complete germ–soma division of labor, asymmetric cell divisions, coordinated tissue-level morphogenesis, and dimorphic sexes—none of which have obvious analogs in its closest unicellular relative, the model alga Chlamydomonas reinhardtii. Here, I summarize some of the key questions and areas of study that are being addressed with Volvox carteri and how increasing genomic information and meth- odologies for volvocine algae are opening up the entire group as an integrated experimental system for exploring the evolution of multicellularity and more. Keywords: Volvox carteri, Chlamydomonas reinhardtii, Multicellularity, Green algae, Morphogenesis, Comparative genomics Natural habitat and lifecycle several additional multicellular genera with diferent Volvox is a polyphyletic genus of multicellular freshwater sizes, cell numbers and degrees of developmental com- green algae (Chlorophyta) that belong to a larger taxo- plexity (e.g., Tetrabaena, Gonium, Astrephomene, Pan- nomic grouping within the Order Chlamydomonadales dorina, Yamagishiella, Eudorina, Pleodorina), and a known as volvocine algae [1]. Te species Volvox carteri close unicellular outgroup species, the model alga Chla- f. nagariensis (hereafter V. carteri or Volvox unless oth- mydomonas reinhardtii (Chlamydomonas) [2, 5] (Fig. 1). erwise specifed) is the best-studied species in the genus, Te divergence time between the common ancestor of and has become an established model for developmental C. reinhardtii and multicellular volvocine species is esti- and evolutionary biology [2]. Two other V. carteri forma mated at around 250 MY [6], though the fossil record that are available in culture collections, f. kawasakiensis for green algae is sparse and complicated by homoplasy and f. weismannia, are closely related but diferent spe- that makes defnitive taxonomic afliation and time cali- cies from V. carteri f. nagariensis. Volvocine genera are bration difcult [7]. No other group of extant organisms cosmopolitan and have been collected on all continents captures the crucial transition of eukaryotic life from uni- except Antarctica [3, 4]. Te habitats of V. carteri include cellular to multicellular as lucidly as the volvocine clade, small bodies of water (ponds, rice paddies) and larger and much of modern Volvox research is motivated by the lakes/reservoirs [3]. potential to reconstruct the early stages of this transition While on its own Volvox is a highly tractable model in unprecedented detail [1, 8]. organism, it has even greater utility when it is studied in Vegetative phase V. carteri are spheroids of sev- the context of the volvocine algal clade which includes eral hundred microns diameter which are organ- ized in a simple radially symmetric multicellular *Correspondence: [email protected] body plan with just two cell types: ~ 2000 small ster- Donald Danforth Plant Science Center, 975 N. Warson Rd, St. Louis, MO ile biflagellate somatic cells that are similar in size to 63132, USA a Chlamydomonas cell, and 12–16 large aflagellate © 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. Umen EvoDevo (2020) 11:13 Page 2 of 9 Genetic modulation Organismal polarity Full ECM of cell number Partial inversion inversion expansion Cell-cell basal body rotation attachments Incomplete cytokinesis Chlamydomonas Tetrabaena Gonium Pandorina Eudorina Pleodorina Volvox reinhardtii socialis pectorale morum elegans starrii carteri 75 MYA Asymmetric cell 100 MYA division 150 MYA Partial germ- Complete germ- 200 MYA soma division soma division of 225 MYA of labor labor 250 MYA developmental complexity Anisogamy Oogamy Bifurcated embryonic cell cycle Fig. 1 Volvox and volvocine algae. Simplifed cladogram of selected volvocine species from representative genera shown in cartoon form with successive cellular and developmental innovations indicated by bulleted descriptions above or below the node in which they arose. Volvocine algal cells are polarized with an apical pair of fagella just above the nucleus and a single large chloroplast located basally. Species with published sequenced genomes have names in tan boxes. Light grey shading depicts extra cellular matrix (ECM) that occupies increasing amounts of spheroid volume in successive genera. Estimated divergence times at each node are based on data in [6]. This fgure was adapted from [92] and reproduced here under Creative Commons Licence CC BY 4.0 reproductive cells called gonidia (Fig. 2a–e). The Lab culture and feld collection somatic cells are positioned around the exterior of Field samples of Volvox are routinely collected in one the spheroid and provide motility, while the gonidia of two diferent ways: Starr and colleagues described a are distributed in the posterior region just below the simple means of germinating zygospores from dried soil surface. All of the cells are embedded within a clear samples that are usually collected near bodies of water secreted glycoprotein-rich extracellular matrix (ECM) where Volvox has been observed [14]. Dried soil is advan- that occupies around 99% of the spheroid volume. tageous as it can be transported and stored easily, though Volvox and all volvocine species have a haplontic life successful germination is never guaranteed. Te alterna- cycle (Fig. 3) where vegetative (i.e., mitotic) haploid- tive is collection of live samples using a phytoplankton phase reproduction can be maintained indefinitely, sieve as demonstrated in this video from Dr. Hisayoshi and where sex is triggered by either nutrient or hor- Nozaki’s feld studies [15]. monal signals. Nitrogen deficiency is the cue for sexual A single male–female pair HK9 and HK10 (a.k.a. Adm differentiation in most volvocine genera, but in Volvox, and Eve) germinated from soil collected near Kobe, a species-specific glycoprotein hormone called sex Japan, are founders for standard strains still used by most inducer (SI) is the trigger for sex. SI production can be laboratories [3, 14]. Te HK9 male strain acquired a mor- induced by heat shock [9], and when vegetative gonidia phological mutation and was replaced with a normal are exposed to SI they undergo modified embryogen- male progeny (69-1b) derived from a cross with HK10 esis leading to development of sexually dimorphic [16]. Additional strains, including newer isolates [17, 18], males or females under the control of a haploid UV are available from several culture collections (see below). sex chromosome system [10–12]. Fertilization pro- For routine studies female strains (e.g., Eve) are preferred, duces diploid zygotes which mature into thick-walled as males can spontaneously undergo sexual diferentia- dormant zygospores. Zygospores are environmentally tion—an irreversible developmental transition for males resistant and can remain viable for years in a frozen or whose sperm and somatic cells cannot de-diferentiate desiccated state. Exposure of zygospores to light and [3]. Because sexual males produce additional SI, a single nutrients initiates germination and meiosis to produce spontaneous sexual male arising in a culture can sexu- recombinant haploid progeny that re-enter the vegeta- ally induce the entire population of males, leading to its tive life cycle [13]. Detailed descriptions of mating and extinction. Cultures are usually maintained in defned fertilization can be found elsewhere [3, 14]. liquid media such as Standard Volvox Medium (SVM) Umen EvoDevo (2020) 11:13 Page 3 of 9 Fig. 2 Volvox carteri. a–d Light micrographs of vegetative phase Volvox carteri (Volvox) showing a mature pre-cleavage stage adult with the anterior (A) and posterior (P) poles labeled (a); a mother spheroid with juveniles (b); an isolated gonidium (c); a somatic cell from a mature pre-cleavage adult spheroid (d). The orange/brown-colored eyespot on the somatic cell is visible near the periphery at around 1 o’clock, and
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