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Phylogeny of C4-photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplication for most C4-related genes.

Chi S, Wu S, Yu J, Wang X, Tang X, Liu T - PLoS ONE (2014)

Bottom Line: Almost all of C4-related genes were annotated in extensive algal lineages with proteobacterial or archaeal origins, except for phosphoenolpyruvate carboxykinase (PCK) and aspartate aminotransferase (AST) with both cyanobacterial and archaeal/proteobacterial origin.Most C4 cycle-related genes endured duplication and gave rise to functional differentiation and adaptation in different algal lineages.C4-related genes of NAD-ME (NAD-malic enzyme) and PCK subtypes exist in most algae and may be primitive ones, while NADP-ME (NADP-malic enzyme) subtype genes might evolve from NAD-ME subtype by gene duplication in chlorophytes and tracheophytes.

View Article: PubMed Central - PubMed

Affiliation: Ocean University of China, Qingdao, Shandong Province, People's Republic of China.

ABSTRACT
Both Calvin-Benson-Bassham (C3) and Hatch-Slack (C4) cycles are most important autotrophic CO2 fixation pathways on today's Earth. C3 cycle is believed to be originated from cyanobacterial endosymbiosis. However, studies on evolution of different biochemical variants of C4 photosynthesis are limited to tracheophytes and origins of C4-cycle genes are not clear till now. Our comprehensive analyses on bioinformatics and phylogenetics of novel transcriptomic sequencing data of 21 rhodophytes and 19 Phaeophyceae marine species and public genomic data of more algae, tracheophytes, cyanobacteria, proteobacteria and archaea revealed the origin and evolution of C4 cycle-related genes. Almost all of C4-related genes were annotated in extensive algal lineages with proteobacterial or archaeal origins, except for phosphoenolpyruvate carboxykinase (PCK) and aspartate aminotransferase (AST) with both cyanobacterial and archaeal/proteobacterial origin. Notably, cyanobacteria may not possess complete C4 pathway because of the flawed annotation of pyruvate orthophosphate dikinase (PPDK) genes in public data. Most C4 cycle-related genes endured duplication and gave rise to functional differentiation and adaptation in different algal lineages. C4-related genes of NAD-ME (NAD-malic enzyme) and PCK subtypes exist in most algae and may be primitive ones, while NADP-ME (NADP-malic enzyme) subtype genes might evolve from NAD-ME subtype by gene duplication in chlorophytes and tracheophytes.

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Bayesian phylogenetic trees of MDH (A) and ME (B) enzymes with bootstrap values (when >50%) indicated at the nodes.The plastic type MDHs are in dark gray boxes, and mitochondrial types in light gray boxes. Eukaryotic MEs cluster in two clades, one clade in dark gray boxes consists of both plastic and mitochondrial type, the other one only contains mitochondrial type. ChlP, chlorophytes and plants. Gla, glaucophytes. Rho, rhodophytes. Och, ochrophytes. Cry, cryptophytes. Tri, trichomonad. Amo, amoeba. Cil, ciliates.
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pone-0110154-g003: Bayesian phylogenetic trees of MDH (A) and ME (B) enzymes with bootstrap values (when >50%) indicated at the nodes.The plastic type MDHs are in dark gray boxes, and mitochondrial types in light gray boxes. Eukaryotic MEs cluster in two clades, one clade in dark gray boxes consists of both plastic and mitochondrial type, the other one only contains mitochondrial type. ChlP, chlorophytes and plants. Gla, glaucophytes. Rho, rhodophytes. Och, ochrophytes. Cry, cryptophytes. Tri, trichomonad. Amo, amoeba. Cil, ciliates.

Mentions: In addition of diverse algal species and tracheophytes, wealth of candidate C4 gene sequences (Table S2) were also detected among archaea, proteobacteria and cyanobacteria. Therefore, we built phylogenetic trees that display relationships of full amino acid sequences of C4 related genes from archaea, proteobacteria, cyanobacteria, tracheophytes, and algae based on Bayesian method (only representative candidates are included to save space). The results show that the eukaryotic C4 enzymes have an archaeal/proteobacterial core (Fig. 2, 3, and 4). The phylogenetic trees of PEPC (phosphoenolpyruvate carboxylase), PPDK (pyruvate, orthophosphate dikinase), ALT (alanine transaminase), MDH (malate dehydrogenase), ME (malic enzyme), and PK (pyruvate kinase) (see Figs. 2, 3, and 4) support their non-cyanobacterial origin in primary endosymbiotic algae. However, almost all eukaryotic PCKs have a cyanobacterial origin through endosymbiosis gene transfer (EGT). Some genes of ochrophytes and cryptophytes potentially have a red algal origin (e.g., ME) as expected under the secondary endosymbiosis hypothesis, and others have archaeal/proteobacterial origins inherited from their endosymbiosis host genomes or acquired from non-cyanobacterial archaea or proteobacteria via horizontal gene transfer (HGT) (e.g., PEPC).


Phylogeny of C4-photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplication for most C4-related genes.

Chi S, Wu S, Yu J, Wang X, Tang X, Liu T - PLoS ONE (2014)

Bayesian phylogenetic trees of MDH (A) and ME (B) enzymes with bootstrap values (when >50%) indicated at the nodes.The plastic type MDHs are in dark gray boxes, and mitochondrial types in light gray boxes. Eukaryotic MEs cluster in two clades, one clade in dark gray boxes consists of both plastic and mitochondrial type, the other one only contains mitochondrial type. ChlP, chlorophytes and plants. Gla, glaucophytes. Rho, rhodophytes. Och, ochrophytes. Cry, cryptophytes. Tri, trichomonad. Amo, amoeba. Cil, ciliates.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4196954&req=5

pone-0110154-g003: Bayesian phylogenetic trees of MDH (A) and ME (B) enzymes with bootstrap values (when >50%) indicated at the nodes.The plastic type MDHs are in dark gray boxes, and mitochondrial types in light gray boxes. Eukaryotic MEs cluster in two clades, one clade in dark gray boxes consists of both plastic and mitochondrial type, the other one only contains mitochondrial type. ChlP, chlorophytes and plants. Gla, glaucophytes. Rho, rhodophytes. Och, ochrophytes. Cry, cryptophytes. Tri, trichomonad. Amo, amoeba. Cil, ciliates.
Mentions: In addition of diverse algal species and tracheophytes, wealth of candidate C4 gene sequences (Table S2) were also detected among archaea, proteobacteria and cyanobacteria. Therefore, we built phylogenetic trees that display relationships of full amino acid sequences of C4 related genes from archaea, proteobacteria, cyanobacteria, tracheophytes, and algae based on Bayesian method (only representative candidates are included to save space). The results show that the eukaryotic C4 enzymes have an archaeal/proteobacterial core (Fig. 2, 3, and 4). The phylogenetic trees of PEPC (phosphoenolpyruvate carboxylase), PPDK (pyruvate, orthophosphate dikinase), ALT (alanine transaminase), MDH (malate dehydrogenase), ME (malic enzyme), and PK (pyruvate kinase) (see Figs. 2, 3, and 4) support their non-cyanobacterial origin in primary endosymbiotic algae. However, almost all eukaryotic PCKs have a cyanobacterial origin through endosymbiosis gene transfer (EGT). Some genes of ochrophytes and cryptophytes potentially have a red algal origin (e.g., ME) as expected under the secondary endosymbiosis hypothesis, and others have archaeal/proteobacterial origins inherited from their endosymbiosis host genomes or acquired from non-cyanobacterial archaea or proteobacteria via horizontal gene transfer (HGT) (e.g., PEPC).

Bottom Line: Almost all of C4-related genes were annotated in extensive algal lineages with proteobacterial or archaeal origins, except for phosphoenolpyruvate carboxykinase (PCK) and aspartate aminotransferase (AST) with both cyanobacterial and archaeal/proteobacterial origin.Most C4 cycle-related genes endured duplication and gave rise to functional differentiation and adaptation in different algal lineages.C4-related genes of NAD-ME (NAD-malic enzyme) and PCK subtypes exist in most algae and may be primitive ones, while NADP-ME (NADP-malic enzyme) subtype genes might evolve from NAD-ME subtype by gene duplication in chlorophytes and tracheophytes.

View Article: PubMed Central - PubMed

Affiliation: Ocean University of China, Qingdao, Shandong Province, People's Republic of China.

ABSTRACT
Both Calvin-Benson-Bassham (C3) and Hatch-Slack (C4) cycles are most important autotrophic CO2 fixation pathways on today's Earth. C3 cycle is believed to be originated from cyanobacterial endosymbiosis. However, studies on evolution of different biochemical variants of C4 photosynthesis are limited to tracheophytes and origins of C4-cycle genes are not clear till now. Our comprehensive analyses on bioinformatics and phylogenetics of novel transcriptomic sequencing data of 21 rhodophytes and 19 Phaeophyceae marine species and public genomic data of more algae, tracheophytes, cyanobacteria, proteobacteria and archaea revealed the origin and evolution of C4 cycle-related genes. Almost all of C4-related genes were annotated in extensive algal lineages with proteobacterial or archaeal origins, except for phosphoenolpyruvate carboxykinase (PCK) and aspartate aminotransferase (AST) with both cyanobacterial and archaeal/proteobacterial origin. Notably, cyanobacteria may not possess complete C4 pathway because of the flawed annotation of pyruvate orthophosphate dikinase (PPDK) genes in public data. Most C4 cycle-related genes endured duplication and gave rise to functional differentiation and adaptation in different algal lineages. C4-related genes of NAD-ME (NAD-malic enzyme) and PCK subtypes exist in most algae and may be primitive ones, while NADP-ME (NADP-malic enzyme) subtype genes might evolve from NAD-ME subtype by gene duplication in chlorophytes and tracheophytes.

Show MeSH