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The Diverse Morphogenetic Patterns in Spirotrichs and Philasterids

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The Diverse Morphogenetic Patterns in Spirotrichs and Philasterids Available online at www.sciencedirect.com ScienceDirect European Journal of Protistology 61 (2017) 439–452 REVIEW The diverse morphogenetic patterns in spirotrichs and philasterids: Researches based on five-year-projects supported by IRCN-BC and NSFC a,b,1 a,c,1 a,1 a,d,1 e,∗ Xumiao Chen , Xiaoteng Lu , Xiaotian Luo , Jiamei Jiang , Chen Shao , f g a,h Khaled A.S. Al-Rasheid , Alan Warren , Weibo Song a Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China b Department of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China c University of Innstruck, Research Institute for Limnology, Mondseestrasse 9, 5310 Mondsee, Austria d College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai 201306, China e The Key Laboratory of Biomedical Information Engineering, Ministry of Education, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, China f Zoology Department, King Saud University, Riyadh 11451, Saudi Arabia g Department of Life Sciences, Natural History Museum, London SW7 5BD, UK h The Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China Available online 17 May 2017 Abstract In the five years 2012–2016, the ciliate research group at Ocean University of China and their collaborators have performed several investigations on the morphogenesis of ciliated protists during binary division. Multiple samples were collected from 17 cities and cortical development studied in 42 species belonging to 32 genera and 13 families (Amphisiellidae, Euploti- dae, Kahliellidae, Oxytrichidae, Philasteridae, Pseudokeronopsidae, Pseudourostylidae, Schmidingerotrichidae, Spirofilidae, Strobilidiidae, Uroleptidae, Uronychiidae and Urostylidae). Among these, 12 genera were investigated morphogenetically for the first time, revealing some unusual pattern formations and allowing four new genera to be established: Heterokeronopsis, Apobakuella, Parabistichella and Apoholosticha. The objective of this review is to: 1) summarize the morphogenetic studies supported by the IRCN-BC and NSFC projects during these five years; 2) summarize the patterns of development and document deviations from normal morphogenetic events within a group; 3) discuss how studies on morphogenesis have helped to advance understanding in the three dimensions of biodiversity, i.e. taxonomy, genetics and function; and 4) suggest potential future directions for the morphogenetic study of ciliated protists. © 2017 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). Keywords: Ciliates; Cortical patterns; Diversity; Morphogenesis; Ontogenesis Abbreviations: FVC, frontoventral cirri; FVT-anlage, anlage for fronto- ventral transverse cirri (sing.); FVTA, anlagen for frontoventral transverse Introduction cirri (pl.); FVTC, frontoventral transverse cirri; UM-anlage, anlage for undu- lating membranes. ∗ Among the protists, ciliates have some of the most complex Corresponding author at: The Key Laboratory of Biomedical Information and highly differentiated surface organelles. They exhibit Engineering, Ministry of Education, School of Life Science and Technology, high species diversity with over 4000 free-living ciliates hav- Xi’an Jiaotong University, Xi’an 710049, China. E-mail address: [email protected] (C. Shao). ing been described. The majority of these, however, were 1 All authors contribute equally. described only from living or fixed cells without details of http://dx.doi.org/10.1016/j.ejop.2017.05.003 0932-4739/© 2017 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). 440 X. Chen et al. / European Journal of Protistology 61 (2017) 439–452 the infraciliature or silver-line system. With improvements in Family Amphisiellidae Jankowski, 1979 is characterized optical microscopy, the wider application of silver staining by the presence of the amphisiellid median cirral row derived and the development of molecular methods, guidelines for from the two or three rightmost anlagen (Berger 2008; Huang acceptable species descriptions have recently been revised et al. 2016; Li et al. 2007). In the work performed by our (Warren et al. 2017). While not a requirement for inclusion group, four species of the genus Amphisiella, i.e. A. candida, in species descriptions, it was recommended that ontogenesis A. milnei, A. pulchra, and A. sinica were described in terms (i.e. cell division including stomatogenesis, morphogene- of their living features, infraciliature and morphogenetic pro- sis, and the regeneration of parental structures) should be cesses. The main morphogenetic features can be summarized included when it provides taxonomically relevant features, as follows: (1) in the proter, the parental adoral zone of mem- e.g. the position of the oral primordium in oligotrichid ciliates branelles is completely retained; and (2) the FVTC originate (Agatha 2004). from six cirral anlagen (Chen et al. 2013c; Li et al. 2016; Ontogenetic information has long provided a basis for Fig. 1A, B). inferring phylogenetic relationships among ciliates (Foissner In the family Kahliellidae Tuffrau, 1979, morphogene- 1996). Morphogenesis, which concerns the pattern of forma- sis in Perisincirra paucicirrata, Deviata parabacilliformis, tion of cortical structures during binary division, is of interest D. brasiliensis and D. rositae was described. The main for researchers engaged in cell differentiation, systematics characteristic features are: (1) the parental adoral zone of and evolution because these disciplines play an important role membranelles is retained unchanged by the proter; and (2) the both in deducing phylogenetic relationships and in outlining FVC originate from four cirral anlagen in Perisincirra pauci- or separating closely related taxa. In addition, the patterning cirrata and six cirral anlagen in Deviata parabacilliformis (Li of cortical structure development during the division process, et al. 2013, 2014; Luo et al. 2016; Fig. 1D–F). Berger (2011) such as the origin of the oral primordium and of various cirri, speculated that Perisincirra may have three FVTA and could indicate essential mechanisms of gene expression and cell not determine whether the inner right row is a marginal row differentiation (Kumar et al. 2014; Pan et al. 2011; Hu and or a frontoventral row (Berger 2011). Li et al. (2013) showed 2 Song 2000; Song et al. 2011). that P. paucicirrata has four frontoventral anlagen, and that In the five years from 2012 to 2016, the International the inner right row is a marginal row. Research Coordination Network for Biodiversity of Ciliates The family Schmidingerotrichidae Foissner, 2012 is proba- (IRCN-BC) and the Natural Science Foundation of China bly related to the family Cladotrichidae Small and Lynn, 1985 (NSFC) supported projects to study the formation of corti- (Foissner 2012). The ontogeny of Paracladotricha salina, cal patterns during the morphogenetic process in 42 ciliate isolated from hypersaline waters, was described. The main species. The three main aims of these studies were: 1) to features of the morphogenetic process are as follows: (1) the investigate morphogenetic patterns during cell division, par- parental adoral zone is inherited unchanged by the proter; (2) ticularly in unknown and poorly-known species; 2) to outline the FVC form independently in the proter and opisthe; and the modes of morphogenesis of new taxa and to compare the (3) no paroral, dorsal ciliature, and buccal, transverse and diversity of their pattern formation; and 3) to re-evaluate, caudal cirri formed during binary fission (Shao et al. 2014b; using morphological and molecular biological methods in Fig. 1H). Shao et al. (2014b) assigned Paracladotricha to the combination with ontogenetic data, the systematic position previously monotypic family Schmidingerotrichidae because of groups whose phylogenetic relationships are unclear. both Schmidingerothrix and Paracladotricha lack a paroral In the data given below, ‘our group’ designates all and a buccal cirrus, have three-rowed adoral membranelles, researchers led by W. Song and his collaborators. The term a very strongly reduced dorsal infraciliature, and are only ‘research projects’ refers to those supported by the IRCN-BC known from highly saline habitats (Shao et al. 2017). and NSFC. In the family Spirofilidae von Gelei, 1929, the ontoge- netic processes of three species have been described, namely Strongylidium orientale, Hypotrichidium paraconicum and Morphogenesis in stichotrichids Pseudouroleptus caudatus caudatus (Chen et al. 2013a,b, 2015a). The main features of the morphogenetic process in In the subclass Stichotrichida Faure-Fremiet, 1961, eight Strongylidium orientale are as follows: (1) the posterior part new species/subspecies representing four families and eight of the parental adoral zone of membranelles is renewed by genera were established during the course of these research dedifferentiation; (2) the left and right ventral cirral rows projects (Chen et al. 2013a,b,c, 2015a; Fan et al. 2014a; Li originate intrakinetally and the final left ventral cirral row et al. 2013, 2014, 2016; Shao et al. 2014b). is composed of an anterior portion formed by anteriorly migrating cirri of FVTA VI, a middle portion formed by
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