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. 2020 Mar;168(3):630-647.
doi: 10.1111/ppl.13008. Epub 2019 Aug 8.

Evolution of P2A and P5A ATPases: Ancient Gene Duplications and the Red Algal Connection to Green Plants Revisited

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Free PMC article

Evolution of P2A and P5A ATPases: Ancient Gene Duplications and the Red Algal Connection to Green Plants Revisited

Michael Palmgren et al. Physiol Plant. .
Free PMC article

Abstract

In a search for slowly evolving nuclear genes that may cast light on the deep evolution of plants, we carried out phylogenetic analyses of two well-characterized subfamilies of P-type pumps (P2A and P5A ATPases) from representative branches of the eukaryotic tree of life. Both P-type ATPase genes were duplicated very early in eukaryotic evolution and before the divergence of the present eukaryotic supergroups. Synapomorphies identified in the sequences provide evidence that green plants and red algae are more distantly related than are green plants and eukaryotic supergroups in which secondary or tertiary plastids are common, such as several groups belonging to the clade that includes Stramenopiles, Alveolata, Rhizaria, Cryptophyta and Haptophyta (SAR). We propose that red algae branched off soon after the first photosynthesizing eukaryote had acquired a primary plastid, while in another lineage that led to SAR, the primary plastid was lost but, in some cases, regained as a secondary or tertiary plastid.

Figures

Figure 1
Figure 1
Phylogenetic analysis of P2A SERCA‐like proteins reveals a gene duplication event at the time of the last common eukaryotic ancestor. Two major branches are identified (P2A‐I and P2A‐II; marked by different color shading), each characterized by its own synapomorphy indicated below each branch: P2A‐I: A deletion of a single residue in the phosphorylation (P) domain; P2A‐II: A double pro motif in transmembrane segment 6 (TM6). The tree is the result of a maximum likelihood analysis using RAxML and involving 177 amino acid sequences from 118 species. The best tree (likelihood −99 967.250889) after 1000 bootstrap rounds is shown, as described in section Methods. There were a total of 673 positions in the final dataset. The tree was rooted with eubacterial sequences (from Firmicutes). Scale bar, 0.2 amino acid substitutions per site. Abbreviated sequence names are given in full in Table S1. Each sequence in the tree is marked with a dot colored according to the taxonomic supergroup to which it belongs. Color codes are given below the figure.
Figure 2
Figure 2
Evolutionary relationship between clades of P2A ATPases. A bootstrap consensus tree was generated from the tree shown in Fig. 1 in which branches corresponding to partitions reproduced in fewer than 50% of the 1000 bootstrap replicates were collapsed. A separate Bayesian inference analysis was carried out using the program MrBayes, which resulted in a tree similar to that shown in Fig. 1. Black dots at nodes in the RAxML consensus tree indicate maximum statistical support (P = 1) in the Bayesian inference analysis. The Bayesian interference analysis was run for 1 000 000 generations and the average standard deviation of split frequencies between the resulting trees was 0.005606. Identified synapomorphies are given at the base of major clades. Abbreviated sequence names are given in full in Table S1. Color codes are given in the legend to Fig. 1.
Figure 3
Figure 3
Synapomorphies in catalytic domains and transmembrane segments of P2A SERCA‐like ATPases define two groups of eukaryotic P2A ATPases. One group of sequences (P2A‐I) carries a single amino acid residue deletion in the P domain and another group (P2A‐II) a PP motif in TM6. Chloroplastida and Stramenopiles (here represented with sequences from non‐photosynthetic organisms) are represented in both groups. Some sequences in Alveolata that lack the deletion in the P domain also lack the PP motif. Residues that are conserved in all species and those that represent synapomorphies are colored. Sequences are from selected organisms (abbreviated names are in parentheses): Animals (red text), Homo sapiens (Homsa) and Trichoplax adhaerens (triad); fungi (blue text), Aspergillus niger (Aspni) and Rhizophagus irregularis (Rhiir); Chloroplastida (green text), Arabidopsis thaliana (Arath), Oryza sativa (Orysa), Physcomitrella patens (Phypa) and Coccomyxa subellipsoidea (Cocsu); Stramenopiles (brown text), Aureococcus anophagefferens (Auran), Aurantiochytrium limacinum (Aurli), Aplanochytrium kerguelense (Aplke), and Phytophthora parasitica (Phypar); Rhizaria (black text), Plasmodiophora brassicae (Plabr) and Bigelowiella natans (Bigna); Rhodophyceae (cyan text), Cyanidioschyzon merolae (Cyame); Porphyridium purpureum (Porpu); Galdieria sulphuraria (Galsu); Chondrus crispus (Chocr); Gracilariopsis chorda (Grach); Alveolata (turquoise text), Toxoplasma gondii (Toxgo), Oxytricha trifallax (Oxytr) and Tetrahymena thermophila (Tetth); Discobids (light gray text), Leishmania major (Leima); and eubacteria (yellow text), Desulfitobacterium hafniense (Desha). Asterisks indicate the position of synapomorphies. Blue asterisks indicate synapomorphies common for major clades. Red asterisks indicate synapomorphies common for sub‐clades discussed in the text.
Figure 4
Figure 4
Phylogenetic analysis of P5A‐like proteins reveals a gene duplication event before eukaryotes diversified into supergroups. Two major branches are identified (P5A‐I and P5A‐II; marked by different color shading), each of which is characterized by two synapomorphies indicated below each branch: P5A‐I: KR…KGAP indicates a Lys‐Arg (KR) motif and a Lys‐Gly‐Ala‐Pro (KGAP) motif in the N domain; P5A‐II: QR…KGSP indicates a Gln‐Arg (QR) motif and a Lys‐Gly‐Ser‐Pro (KGSR) motif in the N domain. Each sequence in the tree is marked with a dot colored according to which taxonomic supergroup it belongs to. Color codes are given in Fig. 1. The tree is the result of a maximum likelihood analysis using RAxML and involving 111 amino acid sequences from 97 species. Shown is the best tree (likelihood – 149 464.799485) after 1000 bootstrap rounds, as described in section Methods. There were a total of 1058 positions in the final dataset. Scale bar, 0.2 amino acid substitutions per site. Abbreviated sequence names are given in full in Table S2. Color codes are given in the legend to Fig. 1.
Figure 5
Figure 5
Evolutionary relationship between clades of P5A ATPases. A bootstrap consensus tree was generated in which branches corresponding to partitions reproduced in fewer than 50% of the 1000 bootstrap replicates were collapsed. A separate Bayesian inference analysis was carried out using the program MrBayes, which resulted in a tree similar to that shown in Fig. 3. Black dots at nodes in the RAxML consensus tree indicate maximum statistical support (P = 1) in the Bayesian inference analysis. The Bayesian interference analysis was run for 1 000 000 generations and the average standard deviation of split frequencies between the resulting trees was 0.003138. Defining synapomorphies are given at the base of major clades. Abbreviated sequence names are given in full in Table S2. Color codes are given in the legend to Fig. 1.
Figure 6
Figure 6
Synapomorphies in catalytic domains and transmembrane segments of P5A ATPase‐like proteins define two groups of eukaryotic pumps. One group of sequences (P5A‐I: ‘KR…KGAP’) has KR and KGAP motifs in the N domain, whereas another group (P5A‐II: ‘QR…KGSP’) has QR and KGSP motifs. Chloroplastida, Stramenopiles and Alveolata are represented in both groups. Residues that are conserved in all species and those that represent synapomorphies are colored. Sequences are from selected organisms (abbreviated names are in parentheses): animals (red text), Homo sapiens (Homsa) and Amphimedon queenslandica (Ampqu); fungi (blue text), Saccharomyces cerevisiae (Sacce) and Rhizophagus irregularis (Rhiir); Chloroplastida (green text), Arabidopsis thaliana (Arath), Physcomitrella patens (Phypa), Coccomyxa subellipsoidea (Cocsu), Chlorella variabilis (Chlva), Ostreococcus tauri (Ostta), Micromonas commoda (Micco) and Bathycoccus prasinos (Batpr); Cryptophyta (black text), Guillardia theta (Guith); Stramenopiles (brown text), Thalassiosira pseudonana (Thaps), Aplanochytrium kerguelense (Aplke) and Phytophthora sojae (Physo); Alveolata (turquoise text), Tetrahymena thermophila (Tetth), Perkinsus marinus (Perma) and Toxoplasma gondii (Toxgo); Rhodophyceae (cyan text), Cyanidioschyzon merolae (Cyame), Porphyra umbilicalis (Porum); Galdieria sulphuraria (Galsu); Chondrus crispus (Chocr); Gracilariopsis chorda (Grach); and Discobids (light gray text), Leishmania major (Leima) and Trypanosoma cruzi (Trycr). Asterisks indicate the position of synapomorphies. Blue asterisks show synapomorphies common for major clades. Red asterisks show synapomorphies common for sub‐clades discussed in the text.
Figure 7
Figure 7
Phylogenetic tree depicting the evolutionary history of elongation factor 2 (EF2). Each sequence in the tree is marked with a dot colored according to the taxonomic supergroup to which it belongs. A group of sequences in the eEF2 clade is marked in which sequences share a number of common synapomorphies (shown in Fig. 9; here abbreviated as F…SA). The tree is the result of a maximum likelihood analysis using RAxML and involves 202 amino acid sequences from 110 species. Shown is the best tree (likelihood −158 581.149729) after 1000 bootstrap rounds, as described in section Methods. There were a total of 801 positions in the final dataset. As EF2 is derived from Archaea (Atkinson 2015), the tree was rooted with archaeal sequences. Scale bar, 0.2 amino acid substitutions per site.
Figure 8
Figure 8
Evolutionary relationship between clades of EF2. A bootstrap consensus tree was generated by conducting a maximum likelihood analysis using RAxML and 1000 bootstrap rounds. Branches corresponding to partitions reproduced in fewer than 50% of the 1000 bootstrap replicates were collapsed. A separate Bayesian inference analysis was carried out using the program MrBayes, which resulted in a tree similar to that shown in Fig. 7. Black dots at nodes in the RAxML consensus tree indicate maximum statistical support (P = 1) in the Bayesian inference analysis. The Bayesian interference analysis was run for 5 000 000 generations and the average standard deviation of split frequencies between the resulting trees was 0.010103.
Figure 9
Figure 9
Sequence signatures in EF2 are shared not only between Chloroplastida and Rhodophyceae but also with Crytophyta and Rhizaria. Conserved residues in EF2 are marked by bold type. Asterisks mark synapomorphies identified by Stiller et al. (2001). Homo, Homo sapiens (Metazoa); Sacce, Saccharomyces cerevisiae (fungi); Arath, Arabidopsis thaliana (Streptophyta, Chloroplastida); Cocsu, Coccomyxa subellipsoidea C‐169 (Chlorophyta, Chloroplastida); Ostta, Ostreococcus taurus (Chlorophyta, Chloroplastida); Lotoc, Lotharella oceanica (Rhizaria); Amam, Amorphochlora amoebiformis (Rhizaria); Chrme, Chroomonas mesostigmatica CCMP1168 (Cryptophyta); Heman, Hemiselmis andersenii (Cryptophyta); Guith, Guillardia theta (Cryptophyta); Crypa, Cryptomonas paramecium (Cryptophyta); Cyapa, Cyanophora paradoxa (Glaucophyta); Aphas, Aphanomyces astaci (Oomycetes, Stramenopiles); Toxgo, Toxoplasma gondii (Apicomplexa, Alveolata); and Sulac, Sulfolobus acidocaldarius (Archaea).
Figure 10
Figure 10
Models for evolution of eukaryotic supergroups. (A and B) Models for evolution of photosynthetic eukaryotes. (A) Monophyletic versus (B) paraphyletic relationship of red algae (Rhodophyceae) and green plants (Chloroplastida). Green branches are lineages with photosynthesis. Blue branches are lineages without photosynthesis. Filled arrows indicate gain of photosynthesis following primary endosymbiosis with a cyanobacterium. Open arrows show gain (A) or regain (B) of photosynthesis following secondary endosymbiosis with red or green algae. The SAR megagroup comprises the Stramenopiles, Alveolata, Rhizaria, Cryptophyta and Haptophyta supergroups. Some lineages within these supergroups carry out photosynthesis, whereas others do not. Secondary transfer of red and green plastids into the SAR could have involved serial events of endosymbiosis (Stiller 2014). Euglenoids (not shown in the figure) also have secondary green plastids but are not part of the SAR complex (Ebenezer et al. 2019). (C and D) Models for the evolution of P2A (C) and P5A (D) ATPases. Phylogenetic analyses in combination with the identification of synapomorphies suggest that a gene duplication event occurred at the time of the last eukaryotic common ancestor (LECA). After duplication, pumps were lost in some lineages (marked by light gray text) and maintained in others (colored text). Dashed lines represent connections that did not receive significant statistical support in the phylogenetic analysis. The red dot indicates an early gene duplication event.

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