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Fottea 8(2): 87–104, 2008 87

Review

Phylogeny and classification of (): current state of affairs

Andrey A. Go n t c h a r o v

Institute of Biology and Soil Science, 690022, Vladivostok-22, Russia, e-mail: [email protected]

Abstract: Conjugates (Zygnematophyceae) represent the most -rich (ca. 4000 spp) algal lineage within the Streptophyta. Studies using various molecular markers have placed the class as one of the crown groups in Streptophyta and even suggested a close relationship between the zygnematophycean and land . Phenotypic diversity complicates systematics of the class and the relationships between its taxa remain poorly understood. Molecular phylogenetic analyses have established a number of clades in the class and revealed a disagreement between the traditional taxonomic structure of Zygnematophyceae and the pattern of phylogenetic relationships between the class members. In this paper, an overview of recent advances in our understanding of the phylogeny and classification of conjugating is presented, with emphasis on the major clades established in the class, the clades’ structure and polyphyly of some genera. We describe the areas of conflict and agreement between molecular phylogeny and traditional morphology-based and stress that phenotypic characters provide little evidence for inferring relationships between taxa even at low taxonomic levels.

Key words: conjugates, phylogenetic relationship, polyphyly, Streptophyta, Zygnematophyceae

Introduction Ultrastructural and molecular phylogenetic data suggested clear affinities of the conjugating green Green conjugating algae comprise coccoid, algae with a paraphyletic assemblage of algae filamentous and colonial forms that are distinct in previously known as the (sensu a unique type of sexual (conjugation, Ma t t o x & St e w a r t 1984) and the land first recognized by aV u c h e r 1803), the complete plants (Pi c k e t t -He a p s 1975, Ma t t o x & St e w a r t absence of reproductive stages, and 1984, recent reviews by Le w i s & McCo u r t , 2004, centriolar centrosomes through the life cycle. McCo u r t et al. 2004). In a cladistic framework The conjugates have fascinated professional and (Br e m e r 1985, Br e m e r et al. 1987, Ke n r i c k & amateur microscopists for over 200 years because Cr a n e 1997) the conjugating green algae lineage of their morphological diversity and complex is designated as the class Zygnematophyceae symmetry, which make them organisms within the division Streptophyta [Streptobionta of great natural beauty. This attraction resulted (Ke n r i c k & Cr a n e 1997)], which, together with the in the description of more than 4000 species , form the green plants [ that are classified in ca. 60 genera (Ho s h a w & or Chlorobionta (Ca v a l i e r -Sm i t h 1981, Ke n r i c k McCo u r t 1988, Ge r r a t h 1993, Appendix). It is & Cr a n e 1997)]. It appears that the name of the not really known whether this number reflects class, Zygnematophyceae Ro u n d (1971), is an natural diversity in the group or not because illegitimate substitute for the Conjugatophyceae other estimates range from 1500 to 12000 spp En g l e r (1892) because Conjugata () is (Cr a n w e l l et al. 1990, Ho s h a w et al. 1990). not a synonym for (see Si l v a 1980). Also, the class was described without a Latin diagnosis The distinctness of the conjugates and their and therefore it is not a validly described taxon. alliance with the green algae has never been in doubt (Br o o k 1981). However, the relationships Classification schemes of the Zygnematophyceae between the families, genera and species of the have generally been based on morphology, conjugates as well as the concepts in the emphasizing ultrastructure, cellular group have remained controversial and elusive. organization (unicells, filaments), and 88 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

structure (Mi x 1972, Pr e s c o t t et al. 1972, 1975, was obtained as early as in 1985 (Ho r i et al. 1985), Ho s h a w & McCo u r t 1988, Ge r r a t h 1993). phylogenetic relationships in the group are far Two orders based on cell wall ultrastructure from being well established. Here my attempt is to are recognized within the Zygnematophyceae, summarize recent studies that have addressed the namely, the and the evolution and taxonomy of the Zygnematophyceae (Mi x 1972, Rů ž i č k a 1977). The Zygnematales from a molecular phylogenetic perspective. This are characterized by smooth cell walls consisting paper briefly discusses the class closest relatives, of a single piece lacking pores and other or- the types of molecular data used to analyse namentations. Zygnematalean taxa forming relationships within the Zygnematophyceae, the filaments are distinguished as the family major clades established in the class and point from the unicellular algae out discordance between the class phylogeny and classified as the , formerly known taxonomy, arguing that considerable work remains as ‘‘saccoderm desmids’’ (Tr a n s e a u 1951, to be done before a convincing picture emerges. Pr e s c o t t 1972, Ge r r a t h 1993, Ka d l u b o w s k a 1984). The Desmidiales (‘‘placoderm desmids’’) Phylogylogenetic position within Streptophyta have cell walls consisting of two or more pieces Conjugating green algae have been always having ornamentations and pores (Mix 1972). considered as members of the green Based on cellular organization and cell wall lineage because of their pigments and starch as features the Desmidiales are subdivided into a reserve product (Br o o k 1981), althought in three or four families (Mi x 1972, Ko u w e t s & some classification schemes conjugates have been Co e s e l 1984, Br o o k 1981, Ge r r a t h 1993), regarded as a class distinct from the other green the Peniaceae, , , algae (Fo t t 1971, Ro u n d 1971, Bo l d & Wy n n e and . Genera and species of 1985). Even when classified within Chlorophyta, the Zygnematophyceae are based mostly on the conjugates have been seen as a group with rather differences in cell organization (filaments/ unclear relationships due to the uniqueness of their unicells), cell symmetry, size and shape, cell wall defining characters. Ultrastructural studies in the projections and ornamentations, and chloroplast conjugates revealed cytokinesis by a structure. In most taxa neither the stability of the allying them with the , Coleochaete, a few taxonomic characters nor their evolutionary status other algal taxa and embryophyte plants (Fo w k e (plesiomorphic or apomorphic) has been studied & Pi c k e t t -He a p s 1969a, b, Pi c k e t t -He a p s 1975, in any detail. Ma t t o x & St e w a r t 1984, Gr o l i g 1992). Further biochemical and molecular data has shown an Generally, evolution of morphological traits advanced position of the class Zygnematophyceae in the class is not well understood. There was among streptophyte algae but were not conclusive a number of hypotheses regarding origin and regarding its exact placement there because evolution of certain phenotypical character but their results were affected by insufficient taxon these were largely logical constructions that often sampling, weak resolving power of the markers contradicted each other in very basic assumptions. used or long-branch attraction artefact (Kr a n z Particularly this refers to the ancestral growth habit & Hu s s 1996, Bh a t t a c h a r y a & Me d l i n 1998, (filamentous or unicellular), chloroplast type and Ch a pm a n et al. 1998, Qi u & Pa l m e r 1999, degree of the cell radiation (We s t & We s t 1904, McCo u r t et al. 2000). We s t & Fr i t s c h 1927, Pr e s c o t t 1948, Te i l i n g 1950, 1952, Ra n d h a w a 1959, Ya m a g i s h i 1963, A phylogeny based on four genes from three Pr e s c o t t et al. 1977, Ho s h a w & McCo u r t 1988). genomes (the nuclear 18S rRNA, the chloroplast atpB and rbcL and the mitochondrial nad5) In the last two decades molecular phylogenetic suggested that the conjugates diverged after analyses have advanced our understanding of the , and Klebsormidium relationships between plants at different levels, but before Coleochaete and Chara. The latter was have challenged many long-standing hypotheses resolved as a sister to the land plants with high on plants evolution and significantly affected their support (Ka r o l et al. 2001, McCo u r t et al. 2004). systematics. The conjugates are not an exception Generally this sistership is in agreement with in this respect, however, apart from the fact that the hypotheses on evolution of morphological, the first zygnematophycean nucleotide sequence ultrastructural and biochemical characters that Fottea 8(2): 87–104, 2008 89 accompanied the emergence of streptophyte algae many other groups of organisms where introns from an aquatic habitat and the colonization of generally have patchy distribution (Du j o n 1989, the land (Gr a h a m 1993, 1996, Le w i s & McCo u r t Bh a t t a c h a r y a et al. 1996). Analyses of the intron 2004, McCo u r t et al. 2004, Fig. 1). However, the secondary structure and self-splicing capacity in following analyses of chloroplast small and large the class revealed that it has undergone significant subunit rRNA contended the sister relationship changes after the enter event dated ca. 350-400 between Charales and (Tu r m e l Mya (Bh a t t a c h a r y a et al. 1994, 1996, Be s e n d a h l et al. 2002). As a further development in this & Bh a t t a c h a r y a 1999). controversial issue, analysis of 76 cpDNA- encoded genes resolved the conjugates as sister to A growing amount of new SSU rDNA and land plants with high support. This novel sistership rbcL sequences soon revealed a limited power was further corroborated by the chloroplast gene of their individual use, particularly at the deep order, gene and intron content, and synapomorphic and shallow branches of the conjugates tree. It indels (insertions and deletions) in the coding would be logical to expect that a larger number regions (Tu r m e l et al. 2005, 2007, Ad a m et al. of characters (analyses of several genes) may 2007). Large data sets, comprehensive taxon improve phylogenetic accuracy and resolution sampling and sophisticated analyses provided (Hi l l i s 1996) and an advantage of the combined solid evidence for the advanced position of the analyses of SSU rDNA and rbcL was explored by Zygnematophyceae but it is still hardly explainable Go n t c h a r o v et al. (2004). Concatenation of these from the traditional point of view on the course genes generally increased phylogenetic resolution of evolution in the Streptophyta. Coleochaete and could overcome a problem of accelerated and Chara are more complex than the conjugates evolutionary rates in some taxa in the individual in thallus organization, patterns of , data sets. As a further development of the multi- and share with land plants many phenotypical gene approach, Ha l l et al. (2008) combined traits (McCo u r t et al. 2004). We can expect chloroplast rbcL, psaA and mitochondrial coxIII that the sistership between the embryophytes genes (ca. 4050 nt) to analyse phylogenetic and zygnematophycean algae will be challenged relationships in the conjugating green algae. Their with more genes and data sets but not necessarily data set produced a tree that confirmed the results this intriguing issue will not necessarily be fully of previous single- and two-gene studies. The resolved soon. support for many branches was not much higher than that obtained with SSU rDNA along or in Types of molecular data combination with rbcL (Go n t c h a r o v et al. 2003, The first insights into the conjugates phylogeny 2004). According to Ha l l and his co-authors rbcL were obtained with nuclear-encoded SSU rRNA and psaA genes are more informative markers and chloroplast protein-coding rbcL genes and compared to coxIII that has a limited resolving these markers remain to be the major source of power. information in the class (Bh a t t a c h a r y a et al. 1994, McCo u r t et al. 1995, 2000, Be s e n d a h l & These analyses were mostly focused on studying Bh a t t a c h a r y a 1999, Go n t c h a r o v et al. 2003, relationships between orders and families of the 2004, Go n t c h a r o v 2005). In early phylogenetic conjugates. Go n t c h a r o v & Me l k o n i a n (in press) analyses these molecular markers independently used the same markers to address the genus concept confirmed monophyly of the class and the order in the family Desmidiaceae. Their relatively large Desmidiales but also rejected monophyly of data set (SSU rDNA+1506 group I intron+rbcL, the order Zygnematales and its two families 3260 nt) and an extensive taxon sampling (97 Zygnemataceae and Mesotaeniaceae. It was sequences) recovered a number of novel strongly found that in all (see however Go n t c h a r o v supported clades that combined representatives et al. 2003, Go n t c h a r o v & Me l k o n i a n 2004) of several traditional desmid genera. Within zygnematophycean taxa nuclear SSU rDNA the family these markers also successfully contains 1506 group I intron and it was seen as complemented each other and provided high another evidence for monophyletic origin of support for most of the clades established. Still, the conjugates. Likely, the intron entered SSU the phylogenetic signal was limited at the deeper rDNA of the conjugates ancestor and was then branches of the tree leaving the relationships vertically inherited by its descendants unlike between the clades largely unresolved. To increase 90 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

resolution further, the slow-evolving chloroplast- it was proposed only recently (De n b o h et al. encoded LSU rRNA gene was added to the data 2003, Go n t c h a r o v & Me l k o n i a n 2005). In both set (5509 nt, 40 taxa). That resulted in increased studies, analyses of the secondary structure-based resolution at some branches but not yet fully alignments were very informative and resulted resolved phylogeny. Reduced taxon sampling in in the largely resolved trees. We anticipate that this analysis could be partly responsible for still ribosomal non-coding sequences will be more unsatisfactory result. broadly used in analyses aiming phylogenetic relationships at and below the genus level. At the species level, non-coding sequences from Chloroplast intergenic spacers are also widely nuclear ribosomal operon (1506 group I intron, used to analyse relationships in many groups of ITS1 and ITS2) were used to address relationships land plants and algae (Sh a w et al. 2005, 2007), but in the genera (De n b o h et al. 2003), their utility for the zygnematophycean phylogeny , its putative relative is yet to be tested. and (Go n t c h a r o v & Me l k o n i a n 2005). Despite warnings about potential flaws It is almost inevitable that the spectrum of of the internal transcribed spacers, which may molecular markers in analyses addressing the ultimately lead to incorrect phylogeny, these deeper branches of the Zygnematophyceae should markers continue to be the most popular non- be also extended. Putatively slow-evolving plastid region for species-level phylogenetic sequences of the large subunits of nuclear studies in plants (Fe l i n e r & Ro s s e l l o 2007). and chloroplast ribosomal operons are logical candidates for these studies. Concatenation of two The ribosomal ITS and introns are subjected to operons will produce an alignment of ca. 10000 nt, evolutionary constraints related to the maintenance however, it is an open question whether this fairly of specific secondary structures necessary for the large data set is enough to resolve phylogeny of correct processing of mature RNAs (Ce c h 1988, the Zygnematophyceae. The protein-coding genes La mb o w i t z & Be l f o r t 1993, Sa l d a n h a 1993, could be also useful in this respect and may add Ma i & Co l e m a n 1997, Co l e m a n et al. 1998). In the signal needed (Mo o n & Le e 2003, 2007, most cases this structure is relatively conserved Mo o n et al. 2005, Ha l l et al. 2008). and once it has been established, it can serve as a guidance to align divergent sequences (Co l e m a n Monophyly of the class 2003). Secondary structure of the 1506 group I Conjugating green algae were always considered intron in the Zygnematophyceae is well known as a natural group, only affiliation of the genus (Bh a t t a c h a r y a et al. 1994, 1996 ,Be s e n d a h l Entransia Hu g h e s to it was somewhat questionable & Bh a t t a c h a r y a 1999) but for ITS1 and ITS2 (Ka d l u b o w s k a 1984, McCo u r t et al. 2000). Not

Fig. 1. Summary of the phylogenetic relationships among the major lineages of streptohytes based on analyses of DNA sequence data. Dotted line indicates the possible placement of the Zygnematophyceae supported by 76 cpDNA-encoded genes phylogeny, chloroplast gene order, gene and intron content, and synapomorphic indels in the coding regions (Ad a m et al. 2007,Tu r m e l et al. 2007). Fottea 8(2): 87–104, 2008 91

surprisingly, the first assessment with the molecular 1966, Ha g a & Eh a r a 1977). It is likely that the tools confirmed the anticipated monophyly differences mentioned above reflect different of the class (Bh a t t a c h a r y a et al. 1994, 1996, fine machinery of the conjugation process in two Be s e n d a h l & Bh a t t a c h a r y a 1999, McCo u r t at lineages and may support deep genetic divergence al. 2000, Go n t c h a r o v et al. 2003). However, later between the Zygnematophyceae and . it was found that one genus of the conjugates, Virtually, nothing is known about cytokinesis Spirotaenia, may be only distantly related to the in Spirotaenia and very little about the cell wall rest of the class or even not monophyletic with ultrastructure in this genus and we can expect new it (Go n t c h a r o v & Me l k o n i a n 2004, Go n t c h a r o v distinctive features to be found. It is obvious that 2005). This hypothesis contended McCo u r t it deserves further attention. at al. (1995, 2000) a conclusion on the close relationships between Spirotaenia condensata and Zygnematophyceae classification and Spirogyra, expected because of their similar spiral phylogeny: the order Zygnematales (Ho s h a w & McCo u r t 1988, McCo u r t Earlier molecular phylogenetic analyses resolved et al. 1995). The data obtained by Go n t c h a r o v & the order Zygnematales as not a monophyletic Me l k o n i a n suggested that McCo u r t et al. (1995, taxon because the root of the Zygnematophyceae 2000) result was based on a mix up of the strains was placed within this order, and, thus, revealed it or DNA samples. as paraphyletic (McCo u r t et al. 2000, Go n t c h a r o v et al. 2003). Molecular data also rejected Analyses of SSU rDNA and rbcL sequences monophyly of two zygnematalean families, positioned three Spirotaenia species apart from Zygnemataceae and Mesotaeniaceae, intermixing the other members of the class Zygnematophyceae their representatives. It was found that and among streptophyte algae in a clade with the Roya have more affinity to the Desmidiales than genus Chlorokybus (Go n t c h a r o v & Me l k o n i a n to the rest of Zygnematales. Zygnematalean algae 2004, Fig. 2). The distant relationship between (both filamentous and unicellular) are still poorly Spirotaenia and the rest of the class attained high sampled and phylogenetic structure of this group support and was further substantiated by the lack is tentative. Many genera are not represented in of 1506 group I intron in SSU rDNA, typical of the culture collections and their affiliation remains the conjugates, in all studied Spirotaenia species. unknown. In analyses without Chlorokybus, Spirotaenia was placed as a sister to the Zygnematopyceae but Currently seven lineages were identified within without any support for their short common branch the traditional Zygnematales, namely Roya, (Go n t c h a r o v & Me l k o n i a n 2004). Thus, it is not Netrium digitus and allied species, Spirogyra, clear yet, whether Spirotaenia is the first branch the ‘‘crown Zygnematales’’ that includes most of the conjugates tree or an independent lineage members of the order (see below), and three within Streptophyta, or a sister to Chlorokybus. individual taxa, endlicherianum, Netrium interruptum, and N. oblongum SVCK by conjugation, 255 (Go n t c h a r o v et al. 2004, Ha l l et al. 2008). synapomorphic feature of the class, has been Of these, Roya and Netrium taxa showed more documented in four species of Spirotaenia, and close relationships to the Desmidiales rather two of them were analysed by Go n t c h a r o v than to the Zygnematales suggesting that the & Me l k o n i a n (2004). However, the process Desmidiales likely originated from a paraphyletic of conjugation is rather diverse among the stock of derived unicellular Zygnematales (i.e., Zygnematophyceae (Br o o k 1981), and Spirotaenia Roya and Netrium, Fig. 3). Based on their plastid differs from all the other conjugating green algae in morphology (axial laminate chloroplasts as in producing no conjugation tube or vesicle. Instead, many Desmidiales), the two genera have often in members of this genus paired cell gelatinize cell been considered as transitional forms between walls completely prior to gamete fusion (Bi e b e l saccoderm (Mesotaeniaceae) and placoderm 1975, Ho s h a w & Hi l t o n 1966). Another peculiar desmids (Desmidiales, We s t & We s t 1904, character of sexual reproduction in Spirotaenia Ya m a g i s h i 1963, Br o o k 1981) and the molecular is a production of two gametes per cell that fuse data support this view. However, it is not yet with the respective gametes of the opposite cell clear what structural character(s) separates these to yield a pair of (Ho s h a w & Hi l t o n genera from the other Zygnematales and whether 92 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

Fig. 2. Summary tree of the Zygnematophyceae based on DNA sequence comparisons (Go n t c h a r o v 2005, Go n t c h a r o v et al. 2004, Go n t c h a r o v & Me l k o n i a n 2004, Ha l l et al. 2008, McCo u r t et al. 2000). any morphological synapomorphies for Netrium, as the growth habit (unicellular or filamentous) Roya, and the Desmidiales exist. Paraphyly and chloroplast shape (ribbonlike, stellate and of relatively small genus Netrium (10 species; laminate) above the genus and in some cases Appendix) further complicated the picture. even above the species levels (see below) was greatly overestimated. Similarity in chloroplast Pattern of relationships revealed in the morphology between unicellular and filamentous Zygnematales strongly suggests that an taxa was seen as an indication of their possible importance of morphological characters such common ancestry (Pa l l a 1894, Ra n d h a w a 1959, Fottea 8(2): 87–104, 2008 93

Ya m a g i s h i 1963) and these hypotheses gained and Gonatozygaceae received support only from some support in early molecular phylogenetic chloroplast protein-coding genes and it could be analyses (McCo u r t et al. 1995, 2000). However, explained by any phenotypic traits (Go n t c h a r o v more comprehensive taxon sampling revealed et al. 2004). Roya shares the cell wall features with rampant distribution of the stellate and laminate other Zygnematales (Mi x 1972) and it is rather chloroplasts and unicellular/filamentous habit in unlikely that they are a result of the secondary the Zygnematales rejecting their monophyletic simplification in this genus or that of the cell origin here (Go n t c h a r o v et al. 2003, 2004). It wall ornamentation and segmentation arose in the should be noted that there were no detailed study Gonatozygaceae independently from the rest of on chloroplast morphology in the Zygnematales the Desmidiales (possible evolutionary scenarios and the whole class Zygnematophyceae and it well implied by this sistership). Thus, homoplasy of could be that chloroplasts attributed to the same molecular characters is a more parsimonious morphological type are in fact distinct in their fine explanation for the affiliation of Roya with the structure and organisation. Polyphyletic nature Desmidiales. of zygnematalean genera based on chloroplast morphology (e. g. , Mesotaenium, Molecular data confirmed monophyly of the desmid Netrium; see below) provides good evidence for families Gonatozygaceae and Closteriaceae but that. questioned concepts of the families Peniaceae and Desmidiaceae, forming a crown clade of the tree. Although the traditional order Zygnematales Gonatozygaceae was resolved as a basal branch in requires further phylogenetic studies before it the order clade but support for its early divergence could be reshaped taxonomically, we can make is not very strong (McCo u r t et al. 2000, De n b o h some conclusion on the composition and structure et al. 2001, Go n t c h a r o v et al. 2003, 2004, Ha l l et of its family Zygnemataceae. The type genus of al. 2008, Fig. 2). The branching pattern within the the family, Zygnema, was resolved as a member of Desmidiales generally corresponds the traditional the clade ‘‘crown Zygnematales’’ (Fig. 2) binding hypotheses of relationships between desmid the family name to this clade. It is likely that the families (Mix 1972) and reflects the increasing clade/family will accommodate all filamentous complexity of the cell wall ultrastructure from more zygnematalean genera except Spirogyra and most primitive cell wall and pores (cell wall consisting unicellular saccoderms except Roya, Netrium, of several segments separated by shallow and perhaps Mesotaenium endlicherianum and groove(s); simple pores perforating only the outer its possible relatives (McCo u r t et al. 2000, cell wall layer, Gonatozygaceae, Closteriaceae, Gontcharov et al. 2003, 2004, Ha l l et al. and Peniaceae) towards derived character state 2008). It is obvious that the diagnosis of the (constricted cells composed of two semicells with family Zygnemataceae should be emended to complex cell wall pores) in the Desmidiaceae. Also accommodate the unicellular forms but also to molecular data clearly showed that the features of discriminate the family members from the other the cell wall ultrastructure in the Gonatozygaceae, taxa having similar morphology but showing Closteriaceae, and Peniaceae have plesiomorphic little affinity to the Zygnemataceae. It is quite character state rather than synapomorphic (Fig. 4). unlikely that the known characters of the cell-wall Not surprisingly, phylogenetic analyses rejected ultrastructure and/or gross cell and chloroplast monophyly of the suborder Archidesmidiineae morphology may serve this purpose. based on these features (McCo u r t et al. 2000, Go n t c h a r o v et al. 2003, Ha l l et al. 2008). It was The order Desmidiales also found that the families Gonatozygaceae and In contrast to the Zygnematales, monophyly of Peniaceae, indistinct in their cell wall ultrastructure the order Desmidiales, defined by the complex characters and therefore merged into one family cell wall ultrastructure and pores, received strong (Ko u w e t s & Co e s e l 1984), are only distantly support in most phylogenetic analyses (De n b o h related. et al. 2001, Go n t c h a r o v et al. 2003, 2004). Affiliation of the mesotaeniacean genus Roya to Molecular data resolved as a paraphyletic the Desmidiales challenging the order concept genus and allied one of its lineages, composed has been hypothesised (McCo u r t et al. 2000, by small-celled species (e. g. P. cylindrus, Ha l l et al. 2008). However, the sisteship of Roya P. exiguum) with the family Desmidiaceae 94 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

(Go n t c h a r o v et al. 2004, see however Ha l l nature of the omniradiate cell morphology and the et al. 2008). Close relationships between some stellate chloroplasts occurring in many desmid Penium spp. and in other cases spp. species (see also below). having semicells typical of the Desmidiaceae but primitive pores and not shading primary cell wall Challenge for the genus concept (En g e l s & Lo r c h 1981) suggest that they may According to the traditional morphology-based also share character states of the cell wall features taxonomy, conjugating green algae are classified transitional between the two families (Table 1). into 55-60 genera (Appendix). Most of these Further studies, both molecular and ultrastructural, were described more than 100 years ago and their are necessary to resolve major lineages in the concepts have not change much since then. In Desmidiaceae/Peniaceae assemblage and define the Zygnematophyceae, generic diagnoses rely them taxonomically. To my mind, combination mostly on the characters of gross morphology of the cell wall ultrastructure character states in such as habit, cell and semicell shape, type of the Phymatodocis is distinct enough to recognise this cell wall ornamentation and chloroplast shape. genus as a subfamily within the Desmidiaceae or Only some zygnematacean genera were based even an independent family. However, there was on distinct features of the sexual reproduction no support in molecular phylogenies so far for the (Ka d l u b o w s k a 1984). separate position of Phymatodocis (Go n t c h a r o v et al. 2004, Ha l l et al. 2008). Moreover, the Most characters defining the genera have a most recent analyses revealed alliance of two wide variability range and/or occur in different more desmid taxa, cruciferum and combinations across the class therefore many Cosmarium depressum, with small-celled Penium zygnematophycean generic diagnoses are rather spp. (Go n t c h a r o v & Me l k o n i a n , in press, Fig. 5). indistinct and often overlap with each other. As a result, it is hardly possible to find any genus of the conjugates whose original concept has never Table 1. Character states of the cell wall ultrastructure been disputed. Several exceptionally species-rich features in the families Peniaceae, Desmidiaceae and the and morphologically diverse desmid genera such genus Phymatodocis. as Cosmarium, Staurastrum and some of their putative relatives, , Staurodesmus, Taxon/character Complex pores Semicells and Eustrum, are particularly problematic in Peniaceae - - this respect (Pa l a m a r -Mordvintseva 1976a, b, Phymatodocis - + Br o o k 1981, Pr e s c o t t et al. 1982, Cr o a s d a l e et Desmidiaceae + + al. 1994, Ge r r a t h 1993). There were numerous attempts to split them into smaller, more natural (morphologically uniform) taxa that, however, Sequencing of multiple strains of Actinotaenium also could not withstand the same criticism and cruciferum rejects strain/sequence confusion as were finally abandoned. a possible explanation for such an unexpected relationship that requires further attention. The first assessment of the generic concepts in The sister relationship between Desmidiaceae and the Zygnematophyceae with the molecular tools Peniaceae generally supports Te i l i n g ’s, (1950, confirmed that many genera of the conjugates are 1952) hypothesis on origin of the current diversity not monophyletic indeed and require a revision of morphologies in the Desmidiaceae from rather (Go n t c h a r o v et al. 2003, 2004, Mo o n & Le e simple omniradiate ancestor with the stellate 2003). It was also found that a small number of chloroplasts (Penium morphology). However, species and their relatively uniform appearance an emerging pattern of relationships within this is not a warranty for the genus monophyly crown assemblage suggests a more complex (e.g. , Desmidiaum, , evolutionary scenario in the Desmidiaceae than Netrium, Cylindrocystis, Mesotaenium). These it was expected. Already one of branches of the preliminary results were indicative but not yet desmidiacean clade, Phymatodocis nordstedtiana, conclusive because the analyses suffered from the is characterised by 4-radiate cells with furcoid limited taxon sampling, presence of long branches chloroplasts, derived features according to Te i l i n g and limited resolving power of the markers used. (1950, 1952). As a result, this disputes an inherited Studies, specifically addressing the generic concepts Fottea 8(2): 87–104, 2008 95

in Staurastrum, Staurodesmus (Go n t c h a r o v – its species were distributed between 10 generally & Me l k o n i a n 2005, Mo o n et al. 2005, Mo o n highly supported clades, of these 6 included also & Le e 2007), Cosmarium and Actinotaenium Staurodesmus, Eustrum, members (Go n t c h a r o v & Me l k o n i a n , in press), based on and some filamentous desmid genera (Go n t c h a r o v large data sets and many strains, fully confirmed & Me l k o n i a n , in press, Fig. 5). Polyphyly of polyphyletic nature of these traditional genera. Staurodesmus and Staurastrum seems to be less In most cases their representatives were found in conspicuous; Staurodesmus was split into tree several distantly related clades of the tree, often independent lineages (two of them included together with representatives of other genera. Cosmarium spp. as well), while most (20 of its 23 Cosmarium is particularly notorious in this respect species analysed) Staurastrum members formed

Fig. 3. Paraphyletic divergence of three Netrium branches and Roya at the base of the Desmidiales clade according to Go n t c h a r o v et al. (2004). Each Netrium lineage is distinct in the number of chloroplasts per cell (2, 1 and 4, respectively) and, consequently, the positions of the nucleus in the cell (black arrowheads) and/or nuclear behaviour during cytokinesis (Ja r m a n & Pi c k e t t -He a p s 1990, Pi c k e t t -He a p s 1975). White arrowhead indicates the large vacuole separating two chloroplasts that harbours the daughter nucleus soon after cytokinesis in N. interruptum.

Fig. 4. Taxonomic (a, Mi x 1972) and phylogenetic (b; summary based on DNA sequence data) structures of the order Desmidiales with the characters of the cell wall ultrastructure mapped. 96 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

Fig. 6. Major clades of Desmidiaceae established in the combined analyses of nuclear SSU rDNA, 1506 group I intron and rbcL sequences (97 taxa, 3260 nt, ML topology). The tree was rooted with two Penium spp. Cosmarium species are shaded with grey. Clade Cosmarium 2 includes C. undulatum, the type species of the genus (Si l v a 1952). Fottea 8(2): 87–104, 2008 97

Fig. 5. Representatives of distinct lineages found in the genera Mesotaenium and Cylindrocystis. Note diversity of chloroplast morphology in Mesotaenium species and their difference with chloroplasts in putatively related Mougeotia. 1 – Mesotaenium macrococcum (Kü t z .) Ro y et Bi s s e t M 2214; 2 – M. kramstai Le mm e r m . UTEX 1024; 3 – (?) M. endlicherianum Nä g . SAG 12.97; 4- M. cf. chlamydosporum De Ba r y M 2155; 5 – M. caldariorum (La g e r h .) Ha n s g . ACOI 127; 6 – Mougeotia sp.; 7 – Cylindrocystis cf. brebissonii De Ba r y M 2213; 8 - C. crassa De Ba r y M 2328; 9 – C. cushleckae Br o o k M 2158. 98 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

Fig. 7. Bootstrap consensus topology of the major clades of desmids (Desmidiaceae) established in NJ(ML) analyses of rbcL sequence data (127 strains, Go n t c h a r o v & Me l k o n i a n , in press) with mapped features of cell and chloroplast morphology traditionally used to define genera. The data matrix was drawn up from the strains used to infer phylogeny. Fottea 8(2): 87–104, 2008 99

a strongly supported generic clade (Go n t c h a r o v retained but it is very likely that their species & Me l k o n i a n 2005, see also Mo o n et al. 2005, number will be altered, mostly reduced. Mo o n & Le e 2007). A deep divergence between most of the clades accommodating Cosmarium A great obstacle to this scenario is a process of and Staurodesmus species leave little chance that taxonomic circumscription of the new genera. In they may eventually form the respective generic order to be validly described a taxon should be assemblages. provided with a diagnosis that states the characters distinguishing the taxon from other taxa (Art. 32, Artificial nature of many morphologically ICBN). In most plant groups, and conjugating heterogeneous and species rich desmid genera green algae are not exceptional in this respect, was evident for a long time and discussed in the these characters relate to the morphology, rarely literature (Pa l a m a r -Mordvintseva 1976a, b, to biological properties or fine structures of the Br o o k 1981, Pr e s c o t t et al. 1982, Cr o a s d a l e et al. organisms. However, in the Zygnematophyceae 1994, Ge r r a t h 1993, 2003). The generic concept the results of phylogenetic analyses strongly in the saccoderm desmids (Mesotaeniaceae) suggest the inadequacy of the morphological was much less debated, however, largely due to features traditionally used to distinguish genera. the fact that this group was very poorly studied. Mapping of semicell shape, degree of radiation, Not surprisingly, all three major mesotaeniacean cell-wall features (smooth vs. ornamented), and genera, Netrium, Cylindrocystic and Mesotaenium, chloroplast morphology on the phylogenetic were also resolved as polyphyletic, each split into tree showed that each of these morphological three or more lineages (Go n t c h a r o v et al. 2004). characters has a mosaic distribution in the tree and In case of Netrium, distant relationships between does not characterise a specific clade (Go n t c h a r o v its species could be explained by differences in & Me l k o n i a n , in press, Fig. 7). It is obvious that their morphological traits. Each lineage is distinct these characters evolved several times in the class in the number of chloroplasts per cell (1, 2, and 4, and do not reflect common origin of the species Fig. 3), differing positions of the nucleus in the cell, they occur in. and varying nuclear behaviour during cytokinesis (Ja r m a n & Pi c k e t t -He a p s 1990, Pi c k e t t -He a p s Morphological heterogeneity of most novel clades 1975). What features differentiate Cylindrocystic and lack of information on other phenotypical and Mesotaenium branches remains unknown features currently do not allow conclusions (Fig. 6). As it has been noted above, phylogenetic to be drawn on the synapomorphies that may structure of the order Zygnematales and its clades unite their members or, more importantly, remains tentative mostly due to the limited taxon that differentiate the clades (potential genera). sampling and requires further scrutiny. Only a Hopefully, the phylogenetic structuring of the when it will be firmly established comparative class Zygnematophyceae, yet preliminary, will analyses of phenotypic traits within and between stimulate comparative studies on the conjugates the clades could shed a light on this issue. morphology, biology and ultrastructure that will eventually discover characters suitable for Thus, molecular data suggest that the generic purposes of genera and higher taxa diagnosing. structure of the class Zygnematophyceae should be significantly altered towards recognition of the new monophyletic lineages, mostly in the Conclusion family Desmidiaceae and in saccoderm desmids (traditional Mesotaeniaceae), as genera. In some Our understanding of phylogenetic relationships cases existing genera should be abandoned because in the class Zygnematophyceae is still incomplete they do not represent independent lineages but after almost 20 years of studies with molecular are embedded into their “mother” genera (e.g. tools. Further investigations are still needed to is a member of clade, clarify monophyly of the class, structure of the order is a part of Spirogyra, Zygnematales, some families and most genera. is a part of Closterium (Go n t c h a r o v et al. 2004, Molecular data have highlighted the inadequacy of 2004, Ha l l et al. 2008, see however Dr u mm o n d morphological features such as habit, chloroplast et al. 2005). 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Appendix. Genera of the Zygnematophyceae, their type species and estimated number of species (combined with changes from Ge r r a t h 1993, Ho s h a w & McCo u r t 1988).

Genus Type species Species Family Zygnemataceae Debarya (Wi t t r .) Tr a n s e a u 1934 Debarya glyptosperma (De Ba r y ) Wi t t r . 10 Hallasia Ro s e n v . 1924 H. reticulata (Ha l l a s ) Ro s e n v . 1 Mougeotia Ag a r d h M. genuflexa (Di l l w y n ) Ag a r d h 140 Mougeotiopsis Pa l l a 1894 M. calospora Pa l l a 1 Pleurodiscus La g e r h . 1895 ?P. borinquinae Ti ff a n y 1 Temnogametum W. et G.S. We s t 1897 T. heterosporum W. et G.S. We s t 16 Sirocladium Ra n d h a w a 1941 S. kumaoense Ra n d h a w a 5 Spirogyra Li n k 1820 S. porticalis (O.F. Mü l l e r ) Cl e v e >400 Zygnema Ag a r d h 1817 Z. cruciatum (Va u c h e r ) Ag a r d h 139 Zygnemopsis (Sk u j a ) Tr a n s e a u 1934 Z. desmidoides (W. et G. S. We s t ) Tr a n s e a u 43 Zygogonium Kü t z . 1843 Z. ericetorum Kü t z . 29 Family Mesotaeniaceae Ancylonema Be r gg r e n 1871 A. nordenskioeldii Be r gg e r n 1 Cylindrocystis Me n e g h . ex De Ba r y 1858 C. brebissonii (Me n e g h . ex Ra l f s ) De Ba r y 12 Geniculus Pr e s c o t t 1967 G. gatunensis Pr e s c o t t 1 Mesotaenium Nä g e l i 1849 M. endlicherianum Nä g e l i 12 Netrium (Nä g e l i ) It z i g s . et Ro t h e in Ra b e n h . N. digitus (Nä g e l i ) It z i g s . et Ro t h e in Ra b e n h . 10 1856 Roya W. et G.S. We s t 1896 R. obtusa (Br é b .) W. et G. S. We s t 4 Spirotaenia Br é b . ex Ra l f s 1848 S. condensata Br é b . ex Ra l f s 23 Family Gonatozygaceae Gonatozygon De Ba r y 1856 G. monotaenium De Ba r y 11 Family Closteriaceae Closterium Ni t z s c h ex Ra l f s 1848 C. lunula Ni t z s c h ex Ra l f s 190 Spinoclosterium Be r n a r d 1909 S. curvatum Be r n a r d 2 Family Peniaceae Penium Br é b . ex Ra l f s 1848 P. margaritaceum Br é b . ex Ra l f s 16 Family Desmidiaceae Actinotaenium (Nä g e l i ) Te i l i n g 1954 A. curtum (Br é b . ex Ra l f s ) Te i l i n g ex Rů ž i č k a et Po u z a r 50 Allorgeia Ga u t h .-Li è v r e 1958 A. valiae Ga u t h .-Li è v r e 2 Amscottia Gr ö n b l a d 1954 A. mira (Gr ö n b l a d ) Gr ö n b l a d 2 Kü t z . ex Kü t z . 1849 B. borreri De l p o n t e 6 Bourrellyodesmus Co mp é r e 1976 B. heimii Co mp é r e 5 Brachytheca Go n t c h a r o v et Wa t a n a b e 1999 B. sulcata Go n t c h a r o v et Wa t a n a b e 2 Cosmarium Co r d a ex Ra l f s 1848 C. undulatum Co r d a ex Ra l f s >1100 Br é b . 1856 C. pulchellum Br é b . 6 Ag a r d h ex Ra l f s 1848 D. swartzii Ag a r d h ex Ra l f s 20 Br é b . ex Ra l f s 1848 D. baculum Br é b . ex Ra l f s 8 Eh r e n b . ex Ra l f s 1848 ? E. ansatum Eh r e n b . ex Ra l f s 265 Te i l i n g 1952 G. neglecta (Ra c i b .) Te i l i n g 5 Haplotaenium Ba n d o 1988 H. minutum (Ra l f s ) Ba n d o 3 Heimansia Co e s e l 1993 H. pusilla (L. Hi l s e ) Co e s e l 1 Hyalotheca Eh r e n b . ex Ra l f s 1848 H. mucosa (Me r t .) Eh r e n b . ex Ra l f s 6 Ichthyocercus W. et G. S. We s t 1897 I. anglensis W. et G. S. We s t 6 Ichthyodontium Sc o t t et Pr e s c o t t 1956 I. sachlanii Sc o t t et Pr e s c o t t 1 Micrasterias Ag a r d ex Ra l f s 1848 M. furcata Ag a r d ex Ra l f s 75 Oocardium Nä g e l i 1849 O. stratum Nä g e l i 1 Phymatodocis No r d s t . 1877 P. alternanans No r d s t . 3-4 Nä g e l i 1849 P. trabecula (Eh r e n b .) Nä g e l i 50 Prescotiella Bi c u d o 1976 P. sudanensis Bi c u d o 1 Co r d a ex Ra l f s 1848 S. vertebrtum Br é b . ex Ra l f s 13 Spinocosmarium Pr e s c o t t et Sc o t t 1942 S. quadridens (Wo o d ) Pr e s c o t t et Sc o t t 2 Spondylosium Br é b . ex Kü t z . 1849 S. depressum Br é b . ex Kü t z . 34 Staurastrum Me y e n ex Ra l f s 1848 ? S. gracile Ra l f s 800 Staurodesmus Te i l i n g 1948 S. triangularis Te i l i n g 100 104 Go n t c h a r o v : Phylogeny and classification of Zygnematophyceae

Appendix Cont. Streptonema Wa l l . 1860 S. trilobatum Wa l l . 2 Teilingia Bo u r r . 1954 T. (Ra l f s ) Bo u r r . 7 Ra l f s 1848 T. granulatus Br é b . ex Ra l f s 6 Triplastrum Iy e n g a r et Ra m a n a t h a n 1942 T. abbreviatum (W. B. Tu r n e r ) Iy e n g a r et Ra m a n a t h a n 3 (Ba i l e y ex Ra l f s ) Ba i l e y 1851 T. verticillatum (Ba i l e y ex Ra l f s ) Ba i l e y 3 Xanthidium Eh r e n b . ex Ra l f s 1848 X. aculeatum Eh r e n b . ex Ra l f s 115

© Czech Phycological Society Received May 15, 2008 Accepted July 25, 2008