Background and Aims

The charophyte green algae (CGA) are thought to be the closest living relatives to the land plants, and ancestral CGA were unique in giving rise to the land plant lineage. The cell wall has been suggested to be a defining structure that enabled the green algal ancestor to colonize land. These cell walls provide support and protection, are a source of signalling molecules, and provide developmental cues for cell differentiation and elongation. The cell wall of land plants is a highly complex fibre composite, characterized by cellulose cross-linked by non-cellulosic polysaccharides, such as xyloglucan, embedded in a matrix of pectic polysaccharides. How the land plant cell wall evolved is currently unknown: early-divergent chlorophyte and prasinophyte algae genomes contain a low number of glycosyl transferases (GTs), while land plants contain hundreds. The number of GTs in CGA is currently unknown, as no genomes are available, so this study sought to give insight into the evolution of the biosynthetic machinery of CGA through an analysis of available transcriptomes.

Methods

Available CGA transcriptomes were mined for cell wall biosynthesis GTs and compared with GTs characterized in land plants. In addition, gene cloning was employed in two cases to answer important evolutionary questions.

Key Results

Genetic evidence was obtained indicating that many of the most important core cell wall polysaccharides have their evolutionary origins in the CGA, including cellulose, mannan, xyloglucan, xylan and pectin, as well as arabino-galactan protein. Moreover, two putative cellulose synthase-like D family genes (CSLDs) from the CGA species Coleochaete orbicularis and a fragment of a putative CSLA/K-like sequence from a CGA Spirogyra species were cloned, providing the first evidence that all the cellulose synthase/-like genes present in early-divergent land plants were already present in CGA.

Conclusions

The results provide new insights into the evolution of cell walls and support the notion that the CGA were pre-adapted to life on land by virtue of the their cell wall biosynthetic capacity. These findings are highly significant for understanding plant cell wall evolution as they imply that some features of land plant cell walls evolved prior to the transition to land, rather than having evolved as a result of selection pressures inherent in this transition.

INTRODUCTION

The colonization of land by the ancestral green algae was one of the most important events in the history of life. This transition and the subsequent explosive radiation of land plants triggered the development of diverse ecosystems that support other life forms and led to significant changes in atmospheric conditions. Land colonization is thought to have occurred around 470 million years ago (Kenrick and Crane, 1997; Waters, 2003; Niklas and Kutschera, 2010) and is believed to have occurred only once, giving rise to a vast diversity of land plant species (Graham, 1993; Karol et al., 2001; Lewis and McCourt, 2004; McCourt et al., 2004; Becker and Marin, 2009).

The charophyte green algae (CGA) are considered the closest living relatives of the land plants. The CGA include six monophyletic classes: the Mesostigmatophyceae, Chlorokybophyceae, Klebsormidiaceae, Charophyceae, Coleochaetophyceae and Zygnematophyceae. Mesostigmatophyceae and Chlorokybophyceae are together thought to represent the early divergent Streptophyta (Lemieux et al., 2007; Rodriguez-Ezpeleta et al., 2007; Timme et al., 2012). The Mesostigmatophyceae is represented by a single scaly biflaggelate species, Mesostigma viride (Karol et al., 2001; Lemieux et al., 2007), while the Chlorokybophyceae is represented by a single sarcinoid (non-motile cells occurring in packages of four) species (Chlorokybus atmophyticus) (Lemieux et al., 2007; Rodriguez-Ezpeleta et al., 2007). The Klebsormidiaceae comprises three genera and approx. 45 species and is believed to be the earliest divergent class after the Mesostigmatophyceae and Chlorokybophyceae (Timme et al., 2012). While the earliest emerging branches of the CGA are considered phylogenetically well resolved, the closest living relative to the land plants, thought to be in either the Zygnematophyceae (∼6000 species in ∼50 genera), the Coleochaetophyceae (∼20 species in three genera) or the Charophyceae (∼81 species in six genera), has not yet been conclusively determined (Turmel et al., 2006, 2007; Becker and Marin, 2009; Wodniok et al., 2011; Timme et al., 2012; Turmel et al., 2013; Zhong et al., 2013). However, although no CGA genomes have been published to date, chloroplast genome analysis as well as recent evidence from phylogenetic analysis of transcriptomic data has suggested that the Zygnematophyceae is the closest living relative of land plants (Turmel et al., 2006, 2007; Wodniok et al., 2011; Timme et al., 2012; Zhong et al., 2013).

The morphology of the CGA varies from unicellular species to species with complex multicellular body plans as in the Charophyceae (Lewis and McCourt, 2004). Certain ancestral CGA are thought to have possessed particular properties that enabled only them to colonize land, although these characteristics are not necessarily in ‘plant-like’ body plans (Stebbins and Hill, 1980; Wodniok et al., 2011). Particular cell wall architectural designs are one feature of the ancestral CGA that are thought to have been important in conferring a pre-adaptation to life on land. Cell walls are crucial for protection against biotic and abiotic stress and play key roles in cell differentiation and in the ability for upright growth of many land plants (Carpita and Gibeaut, 1993; Graham et al., 2000; Cosgrove, 2005; Harris, 2005; Sørensen et al., 2010). Moreover, cell wall compositions are commonly used characters informing the phylogenetic classification of algae (Stebbins, 1992; Buckeridge et al., 1999; Graham and Wilcox, 1999; Xue and Fry, 2012).

As subtle modifications in the cell wall polymers can have profound effects on cell wall function (Niklas, 2004), the adaptations necessary for life on land probably required changes in the chemical composition and overall architectural arrangement of the cell walls (Tsekos 1999; Popper and Fry, 2003, 2004; Niklas, 2004; Carafa et al., 2005; Van Sandt et al., 2007; Fry et al., 2008a, b; Sørensen et al., 2008, 2010).

To better understand the complexities and diversity of green plant cell walls we must understand the origins of individual components, including the constituent polymers and the enzyme-encoding genes responsible for their synthesis. Considerable research has focused on the investigation of cell wall structure and composition of terrestrial plants, in particular flowering plants. These studies underpin our current understanding that cell walls are fibre composite materials based on a load-bearing network of cellulose microfibrils cross-linked by non-cellulosic polysaccharides, including xyloglucan, xylans, mixed linkage (1–3), (1,4)-β-d-glucans (Bacic et al., 1988; Fry, 2004; Scheller and Ulvskov, 2010), and probably also pectins (Zykwinska et al., 2007). The primary cell wall of most land plant species also contains pectins, a highly diverse group of polysaccharides (Ridley et al., 2001). In addition to the polysaccharides, the land plant cell wall also contains glycoproteins and in some cell types also the phenylpropanoid polymer lignin (Boerjan et al., 2003).

The cell walls of the earliest divergent land plants to the flowering plants all consist of similar groups of polysaccharides, although their fine structures have undergone extensive modifications (Peña et al., 2008; Popper and Tuohy, 2010; Sørensen et al., 2010; Popper et al., 2011). Recent work has shown that several of the extant CGA share many cell wall components with land plants (Popper and Fry, 2003; Domozych et al., 2007a; Eder et al., 2008; Popper, 2008; Eder and Lütz-Meindl, 2009; Sørensen et al., 2010, 2011).

The biosynthesis of highly complex cell wall polysaccharides and glycoproteins requires a wide array of glycosyltransferases (GTs). To some extent these have been characterized, although many catalytic activities and functions remain to be elucidated. Analysis of the available moss and lycopod genomes suggests that the families of GT-encoding genes in flowering plants are mostly represented, although the number of GTs is usually considerably smaller (Harholt et al., 2012). Consistent with this, the prasinophyte and chlorophyte algae, representing the earliest divergent green plants, contain a significantly lower number of GTs in their genomes than any land plants (Ulvskov et al., 2013).

Due to the lack of a sequenced CGA genome, only a few GTs in the CGA have been cloned or otherwise described. Here, we provide genetic evidence of the evolution of cell wall biosynthesis in the CGA through analysis of available CGA transcriptomic data and newly cloned sequences. We show that the CGA contain many GT sequences related to land plant genes known to be involved in the synthesis of the highly specialized land plant cell wall, including cellulose, mannans, xyloglucan, xylans, pectins, arabinonogalactan proteins (AGPs) and extensins. Furthermore, we present the full-length sequences of two cellulose synthase-like D (CSLD) proteins from Coleochaete orbicularis and a partial sequence of a CSLA/K-like sequence from Spirogyra sp., both presenting particularly important evolutionary steps in the cell wall biosynthesis machinery. Together, these data suggest that many GTs involved in the biosynthesis of cell wall polysaccharides and glycoproteins of the land plant cell wall evolved before terrestrialization of the extant algal ancestor.

MATERIAL AND METHODS

Proteomes and database creation

Translated expressed sequence tag (EST) sequences were screened for putative GT-encoding hits according to Ulvskov et al. (2013) but with some minor modifications to allow for quality control of relatively short ESTs. Most notably, the CCD (NCBI's conserved domain database), which is very useful for quality control of full-length sequence hits, is not guaranteed to work for short sequences. The revised procedure used was as follows. All sequences in the CAZy-database as of September 2013 were downloaded except those that were annotated in CAZy as fragments or partial sequences. Also eliminated were sequences regarded as outdated by NCBI. An NCBI blast+ database was prepared from the sequences, and used with blastx at an E-value cut-off of 10–10. Control for false positives was a three-step procedure. The same translated ESTs were blasted against an Arabidopsis thaliana protein blast database (TAIR10 from www.arabidopsis.org) from which all known GTs were subtracted. Translated ESTs giving better hits to the GT-depleted database were eliminated. Both the top hit and the second best hit were examined from the blast against CAZy. ‘Close in E-value’ is defined as less than 30 orders of magnitude difference for E-values better than 10–100, and less than 20, 10 and 5 orders of magnitude for E-values better than 10–50, 10–20 and 10–10, respectively. The third level of quality control is manual inspection of alignments of the translated EST, the bait that pulled out the hit and selected members of the particular clade in the CAZy-family in question. It must also be taken into consideration that some impurities from other organisms can give false positive results, although these were minimized in many cases by more thorough investigations.

Phylogenetic analysis

Phylogenetic analysis was performed via http://www.phylogeny.fr (Dereeper et al., 2008, 2010). The sequences were aligned using Muscle v. 3.7 with default settings. The positions with gaps were removed and the curated sequences were used for building maximum-likelihood phylogenetic trees using phyML with default settings, including the WAG substitution matrix. The phylogenetic trees were statistically supported by approximate likelihood-ratio tests using default settings and values between 0 and 1 were obtained, as with bootstrap values. Approximate likelihood-ratio-test (aLRT) values are included for described clades and when values are under 0·7 where CGA sequences are present. Additionally, aLRT values are also included in Figure 3 and Supplementary Data Fig. S3 for low supported clustering of chlorophyte sequences.

In two instances aLRT values are not included for a clade (Fig. 5, branch point before the E and F clade; Supplementary Data Fig. S7, branch point before the A clade), due to very short branches annotated with a 0·0 score that the algorithm inserts, as it can only make strictly bifurcating trees.

For clarification, cosmetic rearrangement of the trees was made using Adobe Illustrator. When constructing trees, CGA sequences were chosen that span the same part of the land plant sequences in the alignment and sequences long enough to not change the clade structure of the land plant sequences, while all CGA sequences are included and divided into GT families in Supplementary Data File S1. CGA sequences probably originating from the same gene were not excluded in our analysis, and hence one gene might be represented by more than one accession in the phylogenetic trees. Only CGA sequences long enough to not disturb the clustering of the land plant sequences were used to generate the trees, and alignments are included in Supplementary Data File S2.

Cloning of CSLD orthologues from C. orbicularis

The C. orbicularis culture was obtained from David S. Domozych, Skidmore College, and was grown for 10–14 d in 250-mL Falcon 353136 flasks with 0·2-μm vented plugs in a Sanyo Versatile Environment Test Chamber at 23 °C with 16 h illumination per day from Philips master TL-D 36W/840 lamps. The medium containing 80 % Bold Basal Medium (BBM) (Sigma, B5282, 500 mL), 5·88 mm NaNO3, 100 mL soil extract, 1 mL vitamin mix (Sigma G1019, 50 mL), pH 6·5–6·8, was sterilized by autoclaving. Soil extract was prepared from 200 mL unfertilized garden soil mixed with 700 mL deionized water. The mixture was heated to near boiling point and incubated at 90 °C in a waterbath for 2 h and left to cool overnight. The heat treatment was repeated and, after cooling overnight, the extract was left for 24 h to run through a filter paper.

Cells were harvested by centrifugation and resuspended in four volumes of BBM soil medium with 2 mg mL–1 Drisilase (Sigma D9515-G), 20 mm MES, pH5·5, 85 mg mL–1 mannitol and incubated for 30 min at room temperature. Cells were harvested by centrifugation at 4000 g for 5 min, homogenized in liquid nitrogen and RNA was extracted from approx. 100 mg protoplasts using the Spectrum Plant Total RNA Kit (Sigma-Aldrich, St Louis, MO, USA). cDNA was synthesized using the SuperScript Reverse Transcriptase kit and OligodT primers according to the manufacturer's protocol (Life Technologies, Carlsbad, CA, USA).

Based on an alignment of CSLD sequences from A. thaliana, Physcomitrella patens and Selaginella moellendorffii, the degenerate primers, forward: 5′-GGIWSICAYTGGCCIGGIACNTGG-3′ and reverse: 5′-GTSTTGTCYTCATACCAGCTGC-3′ were used to PCR-amplify a central 985-bp fragment of CoCSLD. Two sequences identified among the PCR products were named CoCSLD1 and CoCSLD2. The 5′ sequence of CoCSLD1 and CoCSLD2 were obtained by 5′-RACE (Clontech SMARTER RACE, Palo Alto, CA, USA) using GSP primers, forward: 5′-GAGGGAGACGGGTGTCGACATCCGTG-3′ and reverse 5′-GCGGCAATCGCGTGTCCACCTCACTC-3′, respectively. Among C. orbicularis ESTs, GW592522 (758 bp) and GW593916 (694 bp) were identified as CSLD-like. Amplification and sequencing of the predicted open reading frames showed that the 3′ sequence of CoCSLD1 and CoCSLD2 corresponded to GW593916 and GW592522, respectively. The sequence of 5′ untranslated regions and complete open reading frames were assigned GenBank accession numbers KF928161 and KF928162, respectively.

Cloning of Spirogyra sp. CSLA/K EST

The Spirogyra sp. culture was obtained from David S. Domozych, Skidmore College, and was grown for 10–14 d in Petri dishes in a Sanyo Versatile Environmental Test Chamber at 18 °C with 16 h illumination per day from Philips master TL-D 36W/840 lamps. The medium containing 800 mL BBM, 5·88 mm NaNO3 and 1 mL vitamin mix (Sigma G1019, 50 mL), pH 6·8–7·2, was sterilized by autoclaving.

Cells were harvested and washed over a 5-μm nylon mesh (Streno, Farum, Denmark) with sterile water and RNA extracted from approx. 100 mg material as described above. cDNA was also synthesized as previously described. Alignments of translated land plant CSLA sequences were used to design degenerate primers 5′-GTICARYTICCIATGTAYAAYGAR-3′ and 5′-AMNGCCATRTCCATRTCYTC-3′. A 573-bp fragment was amplified (KF928160) from Spirogyra sp. cDNA.

RESULTS AND DISCUSSION

To investigate the evolutionary origins of the land plant cell wall, available CGA transcriptomes were searched for genes related to land plant cell wall biosynthesis (GT) genes. The available CGA transcriptomes analysed are from different classes of CGA, covering species from the early divergent Mesostigmatophyceae (Mesostigma viride), Chlorokybophyceae (Chlorokybus atmophyticus) and Klebsormidiophyceae (Klebsormidium flaccidum and Klebsormidium subtile) to species of the later divergent Charaphyceae (Nitella mirabilis, Nitella hyalina and Chara vulgaris), Coleochaetophyceae (Chaetosphaeridium globosum, Coleochaete orbicularis and Coleochaete scutata) and Zygnematophyceae (Closterium peracerosum, Penium margaritaceum and Spirogyra pratensis) (Table 1). We recognize the limitations of these data: transcriptomes reflect the expression profiles of the different CGA in one or at best multiple but not all developmental stages when the RNA was extracted and is influenced by the quality of the extraction and subsequent sequencing. All these factors contribute to the total number of ESTs and also the number and type of GTs identified. Nevertheless, it was assumed that if land plant-type GT genes were present in the CGA genomes, there would be a reasonable chance that they would be represented in at least one of the sampled transcriptomes.

Table 1.

Number of GTs found in the analysed CGA transcriptomes

Class Order Family Species Reference No. of ESTs No. of GT hits* GTs/ESTs (%) 
Mesostigmatophyceae Mesostigmatales Mesostigmataceae Mesostigma viride **EC: Nedelcu et al. (2006); **DN: Simon et al. (2006) 15 972 19 0·12 
Chlorokybophyceae Chlorokybales Chlorokybaceae Chlorokybus atmophyticus Timme et al. (2012) 12 496 158 1·3 
Klebsomidiophyceae Klebsormidiales Klebsormidiaceae Klebsormidium flaccidum Timme et al. (2012) 24 913 282 1·1 
Klebsomidiophyceae Klebsormidiales Klebsormidiaceae Klebsormidium subtile Wodniok et al. (2011) 4827 0·19 
Charaphyceae Charales Characeae Nitella mirabilis J. H. Thierer et al. (unpublished) 83 522 419 0·5 
Charaphyceae Charales Characeae Nitella hyalina Timme et al. (2012) 40 615 176 0·4 
Charaphyceae Charales Characeae Chara vulgaris Wodniok et al. (2011) 13 615 17 0·12 
Coleochaetophyceae Chaetosphaeridiales Chaetosphaeridiaceae Chaetosphaeridium globosum Timme et al. (2012) 24 200 165 0·7 
Coleochaetophyceae Coleochaetales Colechaetaceae Coleochaete orbicularis Timme and Delwiche (2010) 18 386 188 
Coleochaetophyceae Coleochaetales Colechaetaceae Coleochaete scutata Wodniok et al. (2011) 5346 25 0·5 
Zygnematophyceae Desmidiales Closteriaceae Closterium peracerosum **AU: Sekimoto et al. (2003); **BW: Sekimoto et al. (2006) 3236 12 0·4 
Zygnematophyceae Desmidiales Peniaceae Penium margaritaceum Timme et al. (2012) 29 220 345 1·2 
Zygnematophyceae Zygnematales Zygnemataceae Spirogyra pratensis Timme and Delwiche (2010) 9587 168 1·8 
Class Order Family Species Reference No. of ESTs No. of GT hits* GTs/ESTs (%) 
Mesostigmatophyceae Mesostigmatales Mesostigmataceae Mesostigma viride **EC: Nedelcu et al. (2006); **DN: Simon et al. (2006) 15 972 19 0·12 
Chlorokybophyceae Chlorokybales Chlorokybaceae Chlorokybus atmophyticus Timme et al. (2012) 12 496 158 1·3 
Klebsomidiophyceae Klebsormidiales Klebsormidiaceae Klebsormidium flaccidum Timme et al. (2012) 24 913 282 1·1 
Klebsomidiophyceae Klebsormidiales Klebsormidiaceae Klebsormidium subtile Wodniok et al. (2011) 4827 0·19 
Charaphyceae Charales Characeae Nitella mirabilis J. H. Thierer et al. (unpublished) 83 522 419 0·5 
Charaphyceae Charales Characeae Nitella hyalina Timme et al. (2012) 40 615 176 0·4 
Charaphyceae Charales Characeae Chara vulgaris Wodniok et al. (2011) 13 615 17 0·12 
Coleochaetophyceae Chaetosphaeridiales Chaetosphaeridiaceae Chaetosphaeridium globosum Timme et al. (2012) 24 200 165 0·7 
Coleochaetophyceae Coleochaetales Colechaetaceae Coleochaete orbicularis Timme and Delwiche (2010) 18 386 188 
Coleochaetophyceae Coleochaetales Colechaetaceae Coleochaete scutata Wodniok et al. (2011) 5346 25 0·5 
Zygnematophyceae Desmidiales Closteriaceae Closterium peracerosum **AU: Sekimoto et al. (2003); **BW: Sekimoto et al. (2006) 3236 12 0·4 
Zygnematophyceae Desmidiales Peniaceae Penium margaritaceum Timme et al. (2012) 29 220 345 1·2 
Zygnematophyceae Zygnematales Zygnemataceae Spirogyra pratensis Timme and Delwiche (2010) 9587 168 1·8 

* The number of GTs determined in this study may include false positive sequences.

** Accession number prefix.

The translated CGA transcriptomes were blasted against an in-house database constructed from GTs extracted from the CAZy database (www.cazy.org; Lombard et al., 2013) to identify putative candidate GTs. False positive hits were minimized, but probably not completely eliminated, as some transcriptomic sequences were very short. The analysed transcriptomes are presented in Table 1, including the number of sequences and GT hits in each transcriptome, while strains and cell types are presented in Supplementary Data Table S1. Generally, a higher number of GT hits was found in the transcriptomes with a greater total number of ESTs. However, the percentage of GTs still varies considerably, from 0·12 to 1·3, i.e. over 10-fold difference, probably indicative of large differences in the data-sets, rather than true evolutionary differences (Table 1).

The presence of a sequence with significant similarity to a land plant GT in one or more CGA provides evidence that the evolution of the GT sequence, and hence the biosynthesis of the implicated cell wall polymer, is likely to have occurred prior to the transition to land. The present study focuses on CGA sequences orthologous to known land plant genes and genes identified in selected prasinophyte algae (Ostreococcus tauri, Ostreococcus lucimarinus and Micromonas sp. RCC299). The cell wall-related GT hits from CGA have been divided into families in Fig. 1, while other GT families are listed in Supplementary Data Table S2. Only the cell wall-related GT families are discussed in this paper and are presented in the section relevant to the polymer they may be involved in producing.

Fig. 1.

GT family members found in CGA transcriptomes, selected prasinophyte algae and sequenced land plants. The numbers depict how many sequences were found in the different species and are also illustrated by the intensity of the colours. Full gene sequences from sequenced genomes are shown in yellow–orange, while transcriptome partial sequences are shown in blue. (Only GTs discussed in the text are shown; the other GT families are shown in Supplementary Data Table S2.)

Fig. 1.

GT family members found in CGA transcriptomes, selected prasinophyte algae and sequenced land plants. The numbers depict how many sequences were found in the different species and are also illustrated by the intensity of the colours. Full gene sequences from sequenced genomes are shown in yellow–orange, while transcriptome partial sequences are shown in blue. (Only GTs discussed in the text are shown; the other GT families are shown in Supplementary Data Table S2.)

Cellulose and cellulose synthase-like Ds

Cellulose synthases

Cellulose is the most abundant polymer in nature and has been found not only in plants and algae but also in bacteria, cyanobacteria and tunicates (Hess et al., 1928; Naylor and Russell-Wells, 1934; Brown, 1985; Kimura and Itoh, 1995; Nobels et al., 2001; Roberts et al., 2002). While the chlorophyte algae synthesize cellulose in linear terminal complexes (TCs), land plants and also CGA primarily synthesize cellulose in rosette TCs, an ability probably derived from their CGA ancestor (Tsekos, 1999; Baldan et al., 2001; Roberts et al., 2002, Roberts and Roberts, 2007). Both K. flaccidum and C. atmophyticus have been shown to produce only small amounts of cellulose, suggesting that the later divergent CGA more closely resemble land plants with respect to usage of cellulose as a major polysaccharide in the cell wall (Sørensen et al., 2011).

In embryophytes, cellulose derived from rosettes is produced by cellulose synthases (CESAs), members of the GT2 family. Other distantly related GT2 CESA sequences are present in bacteria, cyanobacteria, ascomycetes, some red algae and early evolved land plants [these are often referred to as linear CESAs (Fangel et al., 2012; Ulvskov et al., 2013)]. In addition to various chlorophytes, several bacteria, stramenopiles, rhodophytes, glaucophytes, slime moulds, dinoflagellates and tunicates have been found to produce cellulose using linear TCs (Brown et al., 1976; Tsekos and Reiss, 1994; Kimura and Itoh, 1995; Tsekos, 1999; Blanton et al., 2000; Nobles et al., 2001; Sekida et al., 2004; Okuda and Sekida, 2007; Robert and Robert, 2009). The bacterial-type CESAs lack domains characteristic of the rosette-forming TC CESAs including a Zn-binding domain, a plant conserved region (P-CR) and a hypervariable region (HVR; Pear et al., 1996; Roberts et al., 2002; Gu and Somerville, 2010). Several lines of evidence have been provided to suggest that these domains may be involved in forming the rosette TC structure (Arioli et al., 1998; Delmer, 1999; Kurek et al., 2002).

While no bacterial-type CESAs has yet been found in the few available sequenced genomes of chlorophytes, P. patens and S. moellendorffii possess both bacterial- and rosette-type CESAs (Harholt et al., 2012; Ulvskov et al., 2013). Only rosette TCs have been found in P. patens, which are presumed to produce cellulose (Roberts et al., 2012). The bacterial-type CESAs in S. moellendorffii and P. patens may participate in cellulose synthesis but evidence for this remains lacking. The intermediate state of having both bacterial- and vascular plant-type CESAs is nonetheless very interesting and analysing the transcriptomes of the CGAs shows that this transition in CESA types may date further back in evolutionary history. The CGA transcriptomes also contain both types of CESAs (Fig. 2, Supplementary Data Fig. S1). This is in agreement with the previously cloned and predicted rosette TC-forming McCESA1 (AAM83096.1) from the later divergent CGA Mesotaenium caldariorum, showing 59 % identity to land plant CESAs (Roberts et al., 2002).

Fig. 2.

Phylogenetic tree of the GT2 rosette-forming CESAs and CSLDs. Full-length C. orbicularis CoCSLD1 (KF928161) and CoCSLD2 (KF928162) sequences cluster closely to the land plant CSLDs. The C. atmophyticus sequence lies ancestral to both the land plant clades CESA (green) and CSLD (brown, including AtCSLD5), while the later divergent C. orbicularis and S. pratensis, M. caldariorum and P. margaritaceum sequences are more closely related to the land plant sequences. CGA sequences are indicated by accession numbers following a two-letter code for the species: P. margaritaceum (Pm), S. pratensis (Sp), K. flaccidum (Kf), C. atmophyticus (Ca), N. mirabilis (Nm). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when under 0.7. The scale bar is an indicator of genetic distance based on branch length.

Fig. 2.

Phylogenetic tree of the GT2 rosette-forming CESAs and CSLDs. Full-length C. orbicularis CoCSLD1 (KF928161) and CoCSLD2 (KF928162) sequences cluster closely to the land plant CSLDs. The C. atmophyticus sequence lies ancestral to both the land plant clades CESA (green) and CSLD (brown, including AtCSLD5), while the later divergent C. orbicularis and S. pratensis, M. caldariorum and P. margaritaceum sequences are more closely related to the land plant sequences. CGA sequences are indicated by accession numbers following a two-letter code for the species: P. margaritaceum (Pm), S. pratensis (Sp), K. flaccidum (Kf), C. atmophyticus (Ca), N. mirabilis (Nm). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when under 0.7. The scale bar is an indicator of genetic distance based on branch length.

Several bacterial-type CESA sequences were found in the CGA transcriptomes of N. mirabilis and a low scoring sequence in N. hyalina (JO290135; Supplementary Data Table S1). The sequences found in N. mirabilis (JV751589, JV751588, JV741555, JV812725, JV746415, JV762468, JV762467, JV774960, JV774959) have low E-values (down to 6.00E-84 over a maximum of 606 amino acid residues) compared with S. moellendorffi and P. patens sequences, suggesting that the bacterial-type CESA is present in some if not all CGA.

The rosette-type CESA sequences found in the later divergent CGA (examples: JO182980, JO205702) share high identity with the land plant genes, as evidenced by the cloned CESA gene from M. caldariorum (Fig. 2, Supplementary Data Fig. S1). Interestingly, a 162 amino acid-long sequence was found in the earlier divergent CGA C. atmophyticus (JO201441) showing as much similarity to land plant CESAs as to the closely related clade of land plant CESA-like proteins, the CSLDs (Fig. 2, Supplementary Data Fig. S1). This might indicate that the protein is a very close relative of the ancestral CESA/CSLD protein before it evolved into the two separate CESA and CSLD proteins. The C. atmophyticus sequence is closely related to the CESA/CSLDs and does not resemble the bacterial-type CESAs, suggesting that the divergence from bacterial-type CESAs may have occurred before the divergence of the later CGA (Supplementary Data Fig. S1). Several similarly intermediate CESA/CSLD sequences were found in the CGA, perhaps reflecting the evolution of the CESA/CSLD clades. The C. atmophyticus sequence represents the earliest divergent CGA example, while a sequence from K. flaccidum (JO257201) clusters nearer the land plant CESAs, although more distantly than the later divergent P. margaritaceum and S. pratensis sequences (JO205702, JO182980), the latter closely related to the McCESA1.

CSLDs

Several land plant CSLDs have been investigated and they have been characterized as either β-1,4-glucan synthases (Manfield et al., 2004; Park et al., 2011) or β-1,4-mannan synthases (Yin et al., 2011). The CSLDs have been shown to be implicated in early cell differentiation and tip growth (Bernal et al., 2007; Yin et al., 2011) and they have been found in all land plants investigated dating back to the early divergent mosses and lycopods (Harholt et al., 2012). Evidence has recently been provided for the likely existence of a CSLD in CGA with three CSLD-type ESTs being identified from Coleochaete nitellarum (Sørensen et al., 2011).

The CGA transcriptomes were also found to contain a few sequences resembling land plant CSLDs (JO249957, JO249127, JG446158, JO276353, JO271158, JO253400) but could not be included in the tree due to their sequence location (Supplementary Data File S1). As the existence of CSLDs in CGA could prove an important evolutionary step in cell wall biosynthesis, we decided to clone the full-length gene from the CGA C. orbicularis using degenerate primers designed towards JO249957 and JO249127. To our surprise, C. orbicularis does not only contain one CSLD sequence, it contains at least two distinctly different genes. The encoding proteins were named CoCSLD1 and CoCSLD2 (GenBank accession numbers KF928161 and KF928162, respectively) and are 1310 and 1312 amino acids long with 51·6 and 50·8 % amino acid identity to AtCSLD5 (NP_171773.1), respectively. The CoCSLDs contain all the rosette TC CESA-specific domains, including the Zn-binding domain, P-CR, HVR, as well as the conserved sub-regions U1–4 containing the D-D-D-QXXRW motif (Supplementary Data Fig. S2). This finding further supports the observation by Roberts et al. (2002) that these regions are not embryophyte-specific but rather streptophyte-specific.

The CoCSLDs cluster together, somewhat separated from the land plant proteins, comparable to the distance the McCESA clusters from the land plant CESAs (Fig. 2). This means that not only did the CGAs have CESAs before land colonization, they also possessed CSLDs (Fig. 2). Together with the sequence found in C. atmophyticus, the evolution of the CESA/CSLD branch of the GT2 family seems to have been somewhat resolved, probably starting with one ancestral gene sharing resemblance to the C. atmophyticus sequence that evolved into two distinctly different protein clades, CESA and CSLD, present in the later divergent CGA and land plants.

Mannan and xyloglucan backbone

In higher plants, the backbone of mannans and xyloglucan (XyG) is synthesized by the CSLAs and CSLCs of the GT2 family, respectively (Dhugga et al., 2004; Liepman et al., 2005; Cocuron et al., 2007; Goubet et al., 2009). The mannan backbone consists of β-1,4-linked mannose that can be interspaced with β-1,4-linked glucose in glucomannan, while the backbone of XyG consists of β-1,4-linked glucose. Mannans have been found throughout Viridiplantae from prasinophyte algae to flowering plants, including CGA (Morrison et al., 1993; Pettolino et al., 2001; Dunn et al., 2007; Domozych et al., 2009b; Estevez et al., 2009; Ordaz-Ortiz et al., 2009; Sørensen et al., 2011).

While mannan is produced by CSLAs in terrestrial plants, in the prasinophyte and chlorophyte algae, only one ancestral CSLK gene has been identified, which has been suggested to encode a protein that produces mannan in these algae (Yin et al., 2009; Fangel et al., 2012; Ulvskov et al., 2013). The CSLKs cluster between the CSLAs and the CSLCs. The CSLKs seem to have evolved into CSLAs and CSLCs before the divergence of land plants from the chlorophyte algae, as P. patens and S. moellendorffii have both CSLA and CSLC but no CSLK-like proteins (Harholt et al., 2012). As the early divergent land plants contain CSLAs and CSLCs with high sequence identity to their counterparts in flowering plants, the split is likely to have occurred in the CGA.

In searches of the CGA transcriptomes, some CSLC-like sequences were identified including a sequence from S. pratensis (JO191557) that clusters with the land plant sequences and one full-length CSLC from Chara globularis is available online (AY995817, Fig. 3, Supplementary Data Fig. S3). This suggests strongly that although somewhat distantly related to the land plants, CSLC proteins seem to have been present in the later divergent CGA. This could imply that the split from CSLK to CSLC and CSLA families occurred in the ancestral CGA. No CSLA-like sequences were identified in the CGA transcriptomes, however, which counters this hypothesis.

Fig. 3.

Phylogenetic tree of the GT2 CSLA, CSLC and CSLK clades. The Spirogyra sp. CSLA/K-like sequence (KF928160) clusters distantly in the CSLK clade (brown) in an unresolved branch, while the C. globosum sequence (AAX98242) clusters ancestral to the land plant CSLC clade (orange). Land plant CSLAs are depicted in red. Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. Chlorophyte and prasinophyte sequences are VcCSLK: Volvox carteri XP_002945948.1, CrCSLK: Chlamydomonas reinhardtii XP_001696519.1, MpCSLK: Micromonas pusilla XP_003064171.1, MprCSLK: Micromonas sp. RCC299 XP_002508565.1, OtCSLK: O. tauri XP_003083844.1, OlCSLK: O. lucimarinus XP_001421850.1, CsCSLK: Coccomyxa subellipsoidea XP_005648248.1, CvCSLK: Chlorella variabilis XP_005844039.1. aLRT values are shown for major clades and for CGA containing branches when below 0·7. The scale bar is an indicator of genetic distance based on branch length.

Fig. 3.

Phylogenetic tree of the GT2 CSLA, CSLC and CSLK clades. The Spirogyra sp. CSLA/K-like sequence (KF928160) clusters distantly in the CSLK clade (brown) in an unresolved branch, while the C. globosum sequence (AAX98242) clusters ancestral to the land plant CSLC clade (orange). Land plant CSLAs are depicted in red. Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. Chlorophyte and prasinophyte sequences are VcCSLK: Volvox carteri XP_002945948.1, CrCSLK: Chlamydomonas reinhardtii XP_001696519.1, MpCSLK: Micromonas pusilla XP_003064171.1, MprCSLK: Micromonas sp. RCC299 XP_002508565.1, OtCSLK: O. tauri XP_003083844.1, OlCSLK: O. lucimarinus XP_001421850.1, CsCSLK: Coccomyxa subellipsoidea XP_005648248.1, CvCSLK: Chlorella variabilis XP_005844039.1. aLRT values are shown for major clades and for CGA containing branches when below 0·7. The scale bar is an indicator of genetic distance based on branch length.

To address the issue of whether CSLA-type sequences were either missing from the CGA transcriptomes or are truly absent from their genomes, we sought to clone a CSLA-like sequence from a CGA species. We cloned a sequence encoding a 191 amino acid-long polypeptide from Spirogyra sp. (KF928160), covering approximately one-third of the predicted full-length sequence of land plant CSLAs. The sequence was verified by comparisons to as yet unpublished CGA sequence contigs from the 1KP dataset (http://www.onekp.com/). Interestingly, the translated Spirogyra sp. sequence resembled CSLKs more than CSLAs in an unresolved branch with a low aLRT test value of only 0·16, and we therefore call it CSLA/K-like (Fig. 3). This low value is due to the sequence length and position of the CSLA/CSLK-like sequence compared with the land plant sequences and this also results in a low resolution of the CSLK clade. The CSLK clustering is better resolved in Supplementary Data Fig. S3, where the analysed CGA transcriptome sequence is around half of the land plant sequence length.

The S. pratensis transcriptome contains a sequence clustering into the land plant CSLCs, strongly suggesting that Spirogyra contains both a CSLC and a CSLA/K-like sequence (Supplementary Data Fig. S3). Spirogyra therefore can be considered to represent a snapshot of evolution in a transition stage of the CGA CSLA/K-like gene just before its evolution into a CSLA gene. CSLCs seem to have diverged from the CSLKs faster than the CSLAs, implying that there must have been a greater evolutionary pressure towards the development of the CSLCs compared with the CSLAs.

Together, these findings suggest that the CESA and CSL proteins present in the earlier divergent land plants P. patens and S. moellendorffii were already present in CGA, although the CGA CSLA/K-like protein is still not completely diverged towards the CSLAs. This could further imply that the cell wall polymers the land plant-encoding proteins produce, mannans and xyloglucan, might already have been produced to some extent by orthologous proteins in CGA before the transition to land.

Galactomannan

The mannan backbone in galactomannan can be substituted with galactose. A GalT from Trigonella foenum-graecum (CAB52246.1) found in the GT34B clade has been characterized as a galactomannan galactosyltransferase (Edwards et al., 1999) and orthologues of this protein seem to be present in all the terrestrial plants sequenced, although no orthologous sequences were found in the CGA transcriptomes (Fig. 4). While it cannot be ruled out that a gene will be revealed when a CGA genome is fully sequenced, the lack of an orthologous GalT sequence in the analysed CGA transcriptomes might suggest that CGA make mannan without galactose branching. In-depth analyses of CGA cell walls will be required to confirm this hypothesis.

Fig. 4.

Phylogenetic tree of the GT34 family. An S. pratensis sequence clusters together with land plant GT34A clade (blue), while most other CGA sequences included cluster ancestral to the GT34B clade (brown), which includes GalT from Trigonella foenum-graecum. No CGA sequences are found in the GT34C clade (green) or the GT34D clade (orange). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0·7. Accession numbers and a two-letter code are noted on each translated CGA EST: S. pratensis (Sp), C. globosum (Cg), N. mirabilis (Nm), N. hyalina (Nh). For layout purposes long branches are bent. The scale bar is an indicator of genetic distance based on branch length.

Fig. 4.

Phylogenetic tree of the GT34 family. An S. pratensis sequence clusters together with land plant GT34A clade (blue), while most other CGA sequences included cluster ancestral to the GT34B clade (brown), which includes GalT from Trigonella foenum-graecum. No CGA sequences are found in the GT34C clade (green) or the GT34D clade (orange). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0·7. Accession numbers and a two-letter code are noted on each translated CGA EST: S. pratensis (Sp), C. globosum (Cg), N. mirabilis (Nm), N. hyalina (Nh). For layout purposes long branches are bent. The scale bar is an indicator of genetic distance based on branch length.

Xyloglucan

XyG is a major hemicellulose in land plants and possesses a complex side-chain arrangement that differs between species and between tissues of the same species (Penã et al., 2008, 2012). It seems that XyG biosynthesis has undergone elaborate diversification after the transition to land, as evidenced by the wide variety of side-chains identified in numerous species (Hoffman et al., 2005; Penã et al., 2008; Hsieh and Harris, 2009; Hsieh et al., 2009).

XyG in CGA has not been detected using conventional biochemical methods using hydrolytic enzymes and it has therefore been suggested that XyG was an embryophyte invention (Popper and Fry, 2003). However, XyG has been detected in many CGA species including Netrium digitus, Chara corallina, C. nitellarum, Cosmarium turpini and Spirogyra sp. using XyG-specific monoclonal antibodies (Ikegaya et al., 2008; Domozych et al., 2009b; Sørensen et al., 2011). Characteristic glucan and xylosic linkages, 4,6-Glcp, 1,4-Glcp and terminal xylose have also been detected through methylation analysis in Spirogyra sp. (Sørensen et al., 2011). Further evidence for the presence of XyG in CGA has come from biochemical activity and sequence analysis of endotransglucosylases and endotransglucosylases/hydrolases, including an XTH EST from C. nitellarum (HO204633.1; Van Sandt et al., 2007; Fry et al., 2008a, b; Del Bem and Vincentz, 2010; Sørensen et al., 2011).

In addition to an ancestral CSLC in CGA, other proteins seem to be present that in land plants are involved in the biosynthesis of the XyG side-chains. GT family 34 contains land plant xylosyltransferases shown to add a side-chain xylose to the glucan backbone of XyG, all of which cluster in the GT34A clade (Cavalier et al., 2008). Oryza sativa and S. moellendorffii have one and two proteins in this clade, respectively, while P. patens has none (Harholt et al., 2012). P. patens proteins instead cluster in the GT34D clade, which have also been suggested to have XyG xylosyltransferase activity (Zabotina et al., 2008).

The S. pratensis transcriptome contains one sequence (JO183280) that covers 58 % of A. thaliana xyloglucan xylosyltransferase 5 with an E-value of 1E-148 (Supplementary Data File S1). This sequence is surprisingly not ancestral to the land plant clade, strongly suggesting that the XyG biosynthetic machinery is present in some if not all CGA (Fig. 4).

In most land plants, the XyG side-chain can be further galactosylated and three GT47 proteins have been proposed to be involved in this process in A. thaliana, including MUR3 and XLT2 (NP_179627.2, NP_201028.1; Madson et al., 2003; Li et al., 2004; Jensen et al., 2012). MUR3 and XLT2 are found in the A clade of GT47 along with P. patens, S. moellendorffii and O. sativa sequences (Harholt et al., 2012). XyG in A. thaliana roots can also be branched with galactoronic acid, an activity performed by XUT1, which also clusters into the A clade (NP_176534.2; Peña et al., 2012). Sequences ancestral to the land plant MUR3 clade were found in the CGA P. margaritaceum and K. flaccidum (Fig. 5), suggesting that the machinery for the next level of XyG side-chain biosynthesis, at least in a land plant polymer-directed sense, could be present in CGA.

Fig. 5.

Phylogenetic tree of the GT47 family. Translated CGA ESTs fall in all land plant clades in GT47, including GT47B (AtARAD1, blue), GT47A (AtMUR3, orange), GT47D (AtGUT1 and 2, brown), GT47C (AtXGD1, red), GT47E (purple), and GT47F (green). Accession numbers and a two-letter code are noted on each CGA sequence: P. margaritaceum (Pm), S. pratensis (Sp), K. flaccidum (Kf), C. atmophyticus (Ca), N. mirabilis (Nm), N. hyalina (Nh), C. orbicularis (Co). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0.7. The scale bar is an indicator of genetic distance based on branch length.

Fig. 5.

Phylogenetic tree of the GT47 family. Translated CGA ESTs fall in all land plant clades in GT47, including GT47B (AtARAD1, blue), GT47A (AtMUR3, orange), GT47D (AtGUT1 and 2, brown), GT47C (AtXGD1, red), GT47E (purple), and GT47F (green). Accession numbers and a two-letter code are noted on each CGA sequence: P. margaritaceum (Pm), S. pratensis (Sp), K. flaccidum (Kf), C. atmophyticus (Ca), N. mirabilis (Nm), N. hyalina (Nh), C. orbicularis (Co). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0.7. The scale bar is an indicator of genetic distance based on branch length.

Fucosylated XyG has been shown in several seed plants including A. thaliana as well as in the seedless vascular plant S. moellendorffii, while no fucosylated XyG has been found in P. patens, nor any CGA tested to date (Puhlmann et al., 1994; Moller et al., 2007; Sørensen et al., 2011; Harholt et al., 2012). Fucosylated XyG has therefore been suggested to have evolved after the divergence of mosses and hornworts (Peña et al., 2008; Sørensen et al., 2011).

AtFUT1 (Q9SWH5.2) from GT37 is involved in fucosylation of XyG in A. thaliana, while other fucosyltransferases from the GT37 clade are implicated in fucosylation of AGPs (Sarria et al., 2001; Wu et al., 2010a). Several GT37-type encoding sequences were found amongst the CGA ESTs [JO291477 (Nh), JO274235 (Kf), JO190875 (Sp), JO184025 (Sp), JO183715 (Sp), JV812705 (Nm)] and these cluster together with P. patens and S. moellendorffii sequences in another clade separate to the O. sativa and A. thaliana sequences (Fig. 6). This might indicate an alternative function of these divergent proteins. Such a suggestion has already been made by Harholt et al. (2012) who hypothesized them to be xylosyltransferases, although biochemical evidence is still lacking (Moller et al., 2007; Harholt et al., 2012).

Fig. 6.

Phylogenetic tree of the GT37 family. All translated CGA ESTs fall ancestral to the FUT clade (AtFUT1, grey) and cluster together with or ancestral to sequences from early divergent land plants (arch). Accession numbers and a two-letter codes are noted on each CGA sequence: S. pratensis (Sp), K. flaccidum (Kf), N. mirabilis (Nm), N. hyalina (Nh). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0·7. The scale bar is an indicator of genetic distance based on branch length.

Fig. 6.

Phylogenetic tree of the GT37 family. All translated CGA ESTs fall ancestral to the FUT clade (AtFUT1, grey) and cluster together with or ancestral to sequences from early divergent land plants (arch). Accession numbers and a two-letter codes are noted on each CGA sequence: S. pratensis (Sp), K. flaccidum (Kf), N. mirabilis (Nm), N. hyalina (Nh). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0·7. The scale bar is an indicator of genetic distance based on branch length.

Together, these data suggest that although XyG has not yet been detected in CGA by conventional biochemical procedures (Popper and Fry, 2003), the CGA are likely to at least have the genetic machinery for making xylosylated and perhaps even galactosylated XyG comparable to terrestrial plants.

Mixed-linkage (1,3–1,4)-β-d-glucan (MLG) has been found in grasses, the horsetail Equisetum arvense (Buckeridge et al., 2004; Fry et al., 2008b; Sørensen et al., 2008), the CGA Micrasterias denticulata (Eder et al., 2008) and several other CGA species (Eder et al., 2008; Sørensen et al., 2011). In grasses, MLG is synthesized by two clades of the GT2 family, the CSLFs and CSLHs (Burton et al., 2006, 2011; Doblin et al., 2009). None of these genes has been found in any of the other MLG-producing plants and it has therefore been postulated that other genes, evolved through convergent evolution, are responsible for producing MLG in these plants (Harholt et al., 2012). Consistent with this, CGA transcriptomes lack CSLF and CSLH sequences and like the earlier divergent land plants P. patens and S. moellendorffii, only contain members of the CESA, CSLD, CSLA and CSLC clades of GT2 (Harholt et al., 2012). It cannot, however, be ruled out that complete genome sequencing of a CGA might reveal one or more genes from other GT2 clades.

Xylan

Xylans are a major and diverse group of cell wall polysaccharides and xylan backbone biosynthesis has in several land plant species been shown to involve a complex, reducing end-oligosaccharide. This oligosaccharide might function as either a biosynthesis primer or a terminator (York and O'Neill, 2008).

Immuno-glycan microarray analysis has indicated the presence of 4-linked xylose in several CGA, including species in the Charophyceae, Coleochaetophyceae and Zygnematophyceae, which was verified by methylation analysis (Morrison et al., 1993; Domozych et al., 2009b; Sørensen et al., 2011).

Xylan biosynthesis requires many GTs, involving at least seven different GT activities and several GT families, including GT8, GT43 and GT47. In A. thaliana IRX8/GAUT12 (Q9FH36.1, GT8), PARVUS (Q9LN68.1; GATL clade of GT8) and IRX7/FRA8 (Q9ZUV3.1; GT47) have all been suggested to be involved in the synthesis of the complex reducing end of xylan (Brown et al., 2005, 2007; Lee et al., 2007; Peña et al., 2007; York and O'Neill, 2008; Cantarel et al., 2009). Orthologous genes have been found in the earlier divergent land plants P. patens and S. moellendorffii, suggesting that their origins might date back to before land colonization (Harholt et al., 2012). In the CGA transcriptomes, there are many sequences sharing similarities to all GAUT clades in GT8 (Fig. 7) including several sequences related to AtIRX8/AtGAUT12 (JO271878, JV740401, JV799913, JO283871). The latter suggests that synthesis of the complex reducing end of xylan might pre-date colonization of land. In addition, a couple of distantly related GATL-encoding ESTs (JO257712, JV745132) are also present in CGA (data not shown). The GATL sequences in CGA seem more distantly related to the flowering plant proteins; however, this is not surprising, as this is also the case for the GATL-related S. moellendorffii sequence (Harholt et al., 2012).

Fig. 7.

Phylogenetic tree of GAUT from the GT8 family. Translated CGA ESTs fall inside land plant GAUT-B (AtGAUT8, red) and GAUT-C (AtGAUT12, brown) clades, while other CGA sequences lie ancestral to the GAUT-A clade (AtGAUT1 and AtGAUT7, blue). Accession numbers and a two-letter code are noted on each CGA EST: S. pratensis (Sp), K. flaccidum (Kf), N. mirabilis (Nm), N. hyalina (Nh), C.orbicularis (Co), C. globosum. Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0·7. The scale bar is an indicator of genetic distance based on branch length.

Fig. 7.

Phylogenetic tree of GAUT from the GT8 family. Translated CGA ESTs fall inside land plant GAUT-B (AtGAUT8, red) and GAUT-C (AtGAUT12, brown) clades, while other CGA sequences lie ancestral to the GAUT-A clade (AtGAUT1 and AtGAUT7, blue). Accession numbers and a two-letter code are noted on each CGA EST: S. pratensis (Sp), K. flaccidum (Kf), N. mirabilis (Nm), N. hyalina (Nh), C.orbicularis (Co), C. globosum. Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are shown for major clades and for CGA containing branches when below 0·7. The scale bar is an indicator of genetic distance based on branch length.

Elongation of the xylan backbone has been suggested to be performed by the IRX9 (Q9ZQC6.1, GT43), IRX14 (Q8L707.1, GT43), GUT2/IRX10 (ABF58973.1, GT47) and GUT1/IRX10-like (Q940Q8.1, GT47) proteins in A. thaliana (Brown et al., 2005, 2007, 2009; Lee et al., 2007; Penã et al., 2007; York and O'Neill, 2008; Cantarel et al., 2009; Wu et al., 2009, 2010b). Orthologous genes are also present in P. patens and S. moellendorffii, except for IRX9, where S. moellendorffii only has an IRX9-like protein (Harholt et al., 2012).

A C. orbicularis sequence (JO238317) falls nicely into the GT43B clade with the land plant IRX14 and IRX14-like sequences (Supplementary Data Fig. S4). A sequence from S. pratensis (JO191580) clusters near the IRX9-like land plant sequences, although a longer sequence is necessary to make any conclusions (139 amino acids compared with 394 amino acids of IRX9H (Q9SXC4.2) from A. thaliana). In CGA, the GT47D clade, including the IRX7/FRA8 branch, the GUT1/IRX10-like and GUT2/IRX10 branch, is represented by long sequences with high identity to the land plant sequences (Fig. 5). In the GUT clade, as in some of the other phylogenetic trees, a branch point has a low aLRT value, indicating that the CGA sequences cluster ancestral to the land plant sequences but that the internal phylogeny between the CGA sequences cannot be fully resolved. Glucuronic and methyl-glucuronic acid are added to xylan by the GT8 GUX-type glucuronosyltransferases (Mortimer et al., 2010; Oikawa et al., 2010). Several sequences from CGA cluster at the base of the GUX clade, as in the P. patens and S. moellendorffii GUX-like proteins (Supplementary Data Fig. S5). As the GUX clade also contains starch initiation proteins (PGSIP6, which are not included in the tree; Lao et al., 2003; Chatterjee et al., 2005), the CGA-encoded proteins may together with the P. patens and S. moellendorffii proteins be involved in starch initiation and not xylan biosynthesis, although this needs further investigation.

In the GT61 family, the GT61C clade has been shown to be involved in side-chain addition to xylan (Anders et al., 2011; Chiniquy et al., 2012). While the earlier divergent land plants species under investigation in this study do not contain members of the GT61C clade, K. flaccidum contains a sequence (JO255459) that lies ancestral to both GT61A and GT61C, but it is not of sufficient length to determine the phylogenetic relationship between JO255459 and GT61A and GT61C (data not shown). Only full-length or near to full-length sequences will enable us to further analyse whether a true GT61C clade protein exists in CGA. In S. pratensis, JO186429 shows high sequence identity (4.00E-38 over 115 amino acids) to the land plant GT61A clade, although no function has yet been determined for members of this clade (Supplementary Data Files S1, S2). Furthermore, several of the CGA species analysed contain sequences similar to those in the GT61B clade that are involved in N-glycosylation in land plants (Strasser et al., 2000).

In summary, parts of or perhaps the whole xylan biosynthesis machinery was already present in CGA, suggesting that xylan biosynthesis in its complexity may also very well pre-date the transition to land.

Pectin

Pectins are matrix polysaccharides that play important roles such as controlling cell wall porosity and calcium complexations in land plant cell walls. Pectins consist of three domains, homogalacturonan (HG), rhamnogalacturonan I (RG-I) and rhamnogalacturonan II (RG-II). The biosynthesis of pectin is not well understood, with only four different types of verified GTs and one putative activity identified to date (Atmodjo et al., 2013). Complex formation and GTs with apparent lack of catalytic activity also complicate elucidation of pectin biosynthesis (Atmodjo et al., 2011; Harholt et al., 2012). Despite these difficulties, activities or putative activities have been found for all the major pectin components except the RG-I backbone.

In higher plants, the most abundant pectin polymer is HG. HG has been found in the later divergent CGA orders Charophyceae, Coleochaetophyceae and Zygnematophyceae (Domozych et al., 2009a; Sørensen et al., 2011) and is abundant in species such as P. margaritaceum and C. corallina (Proseus and Boyer, 2006; Domozych et al., 2007b; Sørensen et al., 2011), where it forms complexes with calcium, as in land plants (Sørensen et al., 2011). The degree of methyl esterification has been found to vary in P. margaritaceum and N. digitus (Popper and Fry, 2003; Domozych et al., 2007b; Eder and Lütz-Meindl, 2009; Sørensen et al., 2011).

The GAUT family members of GT8 have been shown to synthesize HG in land plants (Sterling et al., 2006). A. thaliana has 15 GAUT homologues with single mutants displaying varying phenotypes, but all are believed to be galacturonosyltransferases with the majority involved in HG biosynthesis (Atmodjo et al., 2013).

A total of 37 CGA sequences orthologous to GAUT were found, including 17 in the phylogenetic tree shown in Fig. 7, the earliest occurrence being observed in K. flaccidum (JO253621, JO254590, JO271878). Not all CGA sequences were of sufficient quality and length to be included in the phylogenetic tree but enough are present to obtain meaningful information.

The most thoroughly characterized GAUT activity is encoded by GAUT1 (Q9LE59.1; GAUT-A clade) from A. thaliana (Sterling et al., 2006), orthologues of which were identified from several CGA including C. orbicularis, C. globosum and K. flaccidum (JO248621, JO160886, JO253621); this is in agreement with an already released GAUT1 orthologous EST from C. nitellarum (Sørensen et al., 2011). GAUT1 functions in a complex with GAUT7 (Q9ZVI7.2, GAUT-A clade) in A. thaliana (Atmodjo et al., 2011). Only very ancestral GAUT7 orthologues were identified in CGA, supporting the suggestion by Harholt et al. (2012) that the anchoring function of GAUT7 is specific for later divergent land plants. No clear orthologues of GAUT2–GAUT7 (GAUT-A) were found in CGA, but some ancestral sequences cluster at the base of these sequences (JO191147, JV741764, JO292792). CGA sequences group in the remaining clades, including QUA1/GAUT8 (Q9LSG3.1, GAUT-B clade) and GAUT12 (GAUT-C) (Bouton et al., 2002; Orfila et al., 2004; Persson et al., 2007), consistent with previous findings of a GAUT8 EST in C. nitellarum (Sørensen et al., 2011).

HG can be xylosylated to produce xylogalacturonan. This xylosylation is catalysed by XGD1 (Q94AA9.2) in A. thaliana and which is found in a specific part of clade GT47C (Jensen et al., 2008). No clear orthologues of this specific part of GT47C were identified in the CGA transcriptomes (Fig. 5) and as neither S. moellendorffii nor P. patens has more than ancestral members of GT47C, xylosylation of HG, or at least the proliferation of members of GT47C, appears to be a late embryophyte invention (Harholt et al., 2012).

RG-I in terrestrial plants can have various side-chains, most notably arabinans and galactans. The existence of arabinans and galactans in earlier divergent taxa of the green plant lineage has not been thoroughly investigated. Short linear stretches of arabinosyl residues have, however, been shown to be present in C. corallina cells through immunolabelling with an arabinan-specific antibody (Domozych et al., 2009b). The protein synthesizing the RG-I backbone has not yet been identified, while ARAD1 (NP_850241.1) and GalS1 (AAP68307·1) from A. thaliana have been suggested to be arabinan and galactan side-chain synthases, respectively (Harholt et al., 2006; Liwanag et al., 2012). ARAD1 is found in clade GT47B and similar CGA sequences were found to be present in the analysed transcriptomes from K. flaccidum and N. mirabilis (JO262416, JV801369, respectively) (Fig. 5). ARAD1 is the only characterized GT47B member and some CGA sequences cluster in the other sub-clades of GT47B (Fig. 5). In addition, two CGA sequences from N. mirabilis lie ancestral to the GT47B clade (JV802040, JV802041).

The galactan synthase GalS1 is located in clade GT92/DUF23. We cannot find a clear distinction between GT92 and DUF23 and have therefore collapsed these two families into one. In this screen, we found CGA sequences that are ancestral to the higher plant GalS sequences, clustering close to one S. moellendorfii and two P. patens sequences (Supplementary Data Fig. S6).

The GT65 protein ECTOPICALLY PARTING CELLS 1 (EPC1; NP_191142.1) from A. thaliana has also been suggested to be involved in galactan synthesis because knock-out mutants show decreased galactan content (Singh et al., 2005; Bown et al., 2007). However, EPC1 orthologues have been found in Galdieria sulphuraria, a red alga that contains no galactan in its wall. It therefore seems unlikely that EPC1 is directly involved in galactan biosynthesis at least in red algae (Ulvskov et al., 2013). EPC1-like sequences are present in the analysed CGA transcriptomes (data not shown) but a function cannot be suggested for them as yet.

The distinct structure of RG-II shows a great degree of conservation between embryophyte species, despite the recent finding of minor differences in size and methylation patterning (Pabst et al., 2013). RG-II is believed to be a land plant feature, emerging at least partly in mosses and has not been detected in green algae (Domozych et al., 1980; Becker et al., 1994, 1998; Matsunaga et al., 2004; Sørensen et al., 2011). Moss RG-II has not been purified and structurally characterized, but some diagnostic sugars have been identified (Matsunagu et al., 2004). Some unusual sugars of RG-II are present in algae, including 2-keto-3-deoxyoctonate (KDO) (York et al., 1985) and 3-deoxy-2-heptulosaric acid (DHA) (Becker et al., 1994, 1998; Domozych et al., 1991, 1992), the former found in the scales or theca of prasinophyte species and the latter in the scales of M. viride (York et al., 1985; Becker et al., 1991; Domozych et al., 1991). Furthermore, low levels of 3,4-linked GalA, an RG-II-specific sugar linkage, has been found in C. nitellarum (Sørensen et al., 2011).

One RG-II biosynthetic activity has been identified in A. thaliana to date, the xylosylation reaction performed by RGXT from the GT77B clade (Egelund et al., 2006, 2008). While three or four RGXT homologues are found in A. thaliana, only a single RGXT orthologue is found in O. sativa, P. patens and S. moellendorffii (Egelund et al., 2006, 2008; Harholt et al., 2012). Surprisingly, we found 34 RGXT CGA sequences in total (at least 14 N. mirabilis sequences lie ancestral to GT77B), including two in the earlier divergent K. flaccidum (JO269496, JO255157; Fig. 8). This finding could point towards a gradual evolution of RG-II, starting in CGA and not in mosses as previously thought. The high number of CGA sequences found could, however, indicate that the RGXTs in CGA are not involved in RG-II synthesis, as only a quantitatively minute amount of RG-II is produced in mosses (Fry, 2011). We propose that RGXT was recruited from the CGA ancestor for making RG-II in embryophytes but whether its role in the CGA is making a polysaccharide unrelated to RG-II, or what might be termed an evolutionary precursor of RG-II, needs further investigation.

Fig. 8.

Phylogenetic tree of the GT77 family. Translated CGA ESTs fall inside the land plant GT77A (blue) and GT77D (green) clades, while other CGA sequences lie more ancestral to the GT77B (brown) and GT77C (AtXEG113, orange) clades and the uncharacterized last land plant clade. Accession numbers and a two-letter code are noted on each CGA sequence: P. margaritaceum (Pm), S. pratensis (Sp), K. flaccidum (Kf), C. atmophyticus (Ca), N. mirabilis (Nm), N. hyalina (Nh), C. orbicularis (Co). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are indicated for major clades and for branches with CGA sequences when below 0.7. The scale bar is an indicator of genetic distance based on branch length.

Fig. 8.

Phylogenetic tree of the GT77 family. Translated CGA ESTs fall inside the land plant GT77A (blue) and GT77D (green) clades, while other CGA sequences lie more ancestral to the GT77B (brown) and GT77C (AtXEG113, orange) clades and the uncharacterized last land plant clade. Accession numbers and a two-letter code are noted on each CGA sequence: P. margaritaceum (Pm), S. pratensis (Sp), K. flaccidum (Kf), C. atmophyticus (Ca), N. mirabilis (Nm), N. hyalina (Nh), C. orbicularis (Co). Land plant sequences are from A. thaliana, O. sativa, P. patens and S. moellendorffi. aLRT values are indicated for major clades and for branches with CGA sequences when below 0.7. The scale bar is an indicator of genetic distance based on branch length.

Extensins and AGPs

The family of hydroxyproline (Hyp)-rich glycoproteins comprises several sub-classes of structural and chimeric proteins (Showalter et al., 2010). The latter kind includes, for example, the plasma membrane-localized extensin-like receptor kinases that may be involved in cell wall signalling (Bai et al., 2012). These are not dealt with here; only the glycosylation enzymes of the two overlapping sub-classes, extensins and AGPs, were analysed. Both extensins and AGPs are non-enzymatic cell wall proteins with characteristic patterns of glycosylation. Extensins feature single Gal residues α-linked to Ser or Thr and short arabinan side-chains linked in the β-configuration to hydroxyproline (Kieliszewski et al., 2011). The glycans of AGPs are quite complex and no AGP-glycan structure has yet been fully elucidated. Two glycan models have been proposed, one quite compact and suggestive of a repeating building block (Tan et al., 2012) and one more extended model without repeating motifs (Tryfona et al., 2012). Both feature a β-1,3-galactan linked to Hyp, but the latter model provides evidence for extended β-1,6-linked side chains while the β-1,6-links are merely single residue kinks in the former. The galactans are decorated with rhamnose, arabinofuranose (Araf) and methyl-glucuronic acid residues.

Whether Hyps are glycosylated by AGP or extensin-like glycan structures is determined by the context in which the Hyp is situated in the amino acid sequence of the protein. Single Hyps carry AGP-type glycans and contiguous Hyps are preferentially arabinosylated (Tan et al., 2003). Extensins quite similar to vascular plant extensins, albeit with a somewhat richer set of glycan structures, are found as the major constituent of the cell wall of the chlorophyte alga Chlamydomonas reinhardtii (Bollig et al., 2007). This finding and the presence of orthologous extensin biosynthetic genes in the prasinophytes indicate that extensins are ancestral to Viridiplantae (Ulvskov et al., 2013). The biosynthesis of extensins is rather well understood in A. thaliana, where SGT1 encoded by At3g01720 galactosylates Ser or Thr residues (Saito et al., 2014). The GT that adds the innermost Ara is unknown, but the next β-1,2-linked Arafs are believed to be transferred by XEG113 (NP_850250.1) from the C clade of GT77 and the third Araf by the REDUCED RESIDUAL ARABINOSE proteins (RRAs) of GT77 clade A (Egelund et al., 2007; Gille et al., 2009; Velasquez et al., 2011; Fig. 8). The GT that adds the fourth Araf residue, which is linked in α-1,3 is presently unknown. CGA sequences similar to the three known GTs that glycosylate extensin were identified [JV747861 (Nm), JV77 4710 (Nm), JO197897 (Ca), JO210666 (Pm), JO158654 (Cg), JO192987 (Ca), JO255878 (Kf); Fig. 8]. This is in good agreement with the omnipresence of extensins throughout Viridiplantae.

Glycosylation that results in the arabinogalactan structures of AGPs is far from being elucidated. It is generally believed to involve GTs from families GT31, GT14 and GT14-like. The plant members of the GT14-like family were formerly known as DUF266 s and we find this discrimination useful for functional annotation and thus retain the term DUF266.

GT31 enzymes all appear to transfer hexosyl monosaccharides, but linkage and acceptor vary (Narimatsu, 2006; Strasser et al., 2007; Egelund et al., 2011; Basu et al., 2013; Geshi et al., 2013). At least two A. thaliana GT31 proteins are involved in AGP biosynthesis, namely GALT2 (NP_193838.2) and GALT31A (NP_174569.1), adding the first galactose residue to Hyp and extending the 1,6-galactose side-chains, respectively (Basu et al., 2013; Geshi et al., 2013). As GALT1 (Q8L7F9.1) is involved in N-glycosylation, it cannot be concluded that all Viridiplantae GT31 are involved in AGP biosynthesis and therefore only orthologues to the two known AGP activities are discussed.

GALT2 is found in GT31 clade B (Supplementary Data Fig. S7) and two short CGA sequences (JO246062, JO214276, 136 and 149 amino acids, respectively) with good sequence similarity to this cluster of higher plant sequences were identified, but which are too short to include in phylogenetic analyses. The second known activity, GALT31A, is located in GT31 clade A and two long CGA sequences cluster closely in the same clade (Fig. S7, JO249593, JO185579, 323 and 355 amino acids, respectively).

GT14 is involved in AGP biosynthesis via the glucuronosyltransferase activity of GlcAT14 (NP_198815.1, Knoch et al., 2013). No clear orthologues to GlcAT14 were found in the CGA transcriptomes, although some ancestral GT14 sequences were identified (Supplementary Data Fig. S8), suggesting that this family of proteins is present in CGA. Based on mutant studies in O. sativa, BC10 (ABN72585.1) was identified as a putative AGP biosynthetic GT (Zhou et al., 2009). BC10 features a DUF266 domain which is closely related to GT14 enzymes (Hansen et al., 2012). At least one sequence with good similarity (with 42 % identity and an E-value of 4e-78) to BC10 can be identified in C. globosum (JO162810; Supplementary Data Fig. S9), indicating that BC10, as opposed to GlcAT14, has an evolutionary origin in CGA or earlier.

CONCLUDING REMARKS

CGA occupy an especially significant position in the tree of life between basal green algae and terrestrial plants. Our transcriptomic analysis of cell wall biosynthetic genes traces evolution in three distinct ways: (1) genes encoding GTs involved in extensin biosynthesis form an unbroken sequence of homologous genes at the base of Viridiplantae and are also found in the most divergent chlorophyte algae; (2) bacterial-type CESA genes are probably inherited from prokaryotes, yet the evolutionary lineage seems broken as it is absent from sequenced prasinophytes, chlorophytes and glaucophytes but appears in N. mirabilis, a later divergent CGA, as well as in earlier divergent land plants; and finally (3) we observe an explosion of polysaccharide biosynthetic genes in the CGAs representing the genetic complement required to synthesize the major polysaccharide classes found in walls of vascular plants.

These findings are highly significant for understanding plant cell wall evolution as they imply that some features of land plant cell walls evolved prior to the transition to land, rather than having evolved as a result of selection pressures inherent in this transition. Indeed, it is possible that the ability to synthesize such walls was an aspect of the pre-adaptation that could explain in part why the ancestors of the CGA and not other algae gave rise to the land plant lineage.

SUPPLEMENTARY DATA

Supplementary data are available online at www.aob.oxfordjournals.org and consist of the following. Table S1: description of trancriptomes analysed, including strains and growth stages. Table S2: GT family members found in CGA transcriptomes, selected prasinophyte algae and sequenced land plants. Fig. S1: phylogenetic tree of GT2 rosette-forming CESA, CSLD and bacterial-type CESAs. Fig. S2: alignment of CoCSLDs, CESAs, CSLDs and bacterial-type CESAs. Fig. S3: phylogenetic tree of GT2 CSLA, CSLC and CSLK clades. Fig. S4: phylogenetic tree of GT43. Fig. S5: phylogenetic tree of the GUX clade of GT8. Fig. S6: phylogenetic tree of GT92/DUF23. Fig. S7: phylogenetic tree of GT31. Fig. S8: phylogenetic tree of GT14. Fig. S9: phylogenetic tree of DUF266. Data file S1: GTs found in the analysed CGA transcriptomes. Data file S2: sequence alignments from the presented phylogenetic trees.

ACKNOWLEDGEMENTS

Special thanks to Professor David S. Domozych for the algal starter cultures used for cloning the full-length Coleochaete orbicularis CoCSLD sequences and the Spirogyra sp. CSLA/K-like fragment. We thank Karin Olesen for expertise and technical assistance with growing the algal cultures. We also thank the 1KP initiative (http://www.onekp.com/) for allowing us to verify the cloned Spirogyra sp. CSLA/K-like sequence in their large transcriptomic data sets. M.S.D. and A.B wish to acknowledge the support of the Australian Research Council for funding to the ARC Centre of Excellence in Plant Cell Walls (CE11000010007). J.H. was supported by the Villum Foundation's Young Investigator Programme. M. D. M. was supported by The Danish Council for Strategic Research (101597).

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