This site needs JavaScript to work properly. Please enable it to take advantage of the complete set of features!
Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

NIH NLM Logo
Log in
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2015 Feb 10:15:16.
doi: 10.1186/s12862-015-0286-4.

Extensive horizontal gene transfer, duplication, and loss of chlorophyll synthesis genes in the algae

Affiliations

Extensive horizontal gene transfer, duplication, and loss of chlorophyll synthesis genes in the algae

Heather M Hunsperger et al. BMC Evol Biol. .

Abstract

Background: Two non-homologous, isofunctional enzymes catalyze the penultimate step of chlorophyll a synthesis in oxygenic photosynthetic organisms such as cyanobacteria, eukaryotic algae and land plants: the light-independent (LIPOR) and light-dependent (POR) protochlorophyllide oxidoreductases. Whereas the distribution of these enzymes in cyanobacteria and land plants is well understood, the presence, loss, duplication, and replacement of these genes have not been surveyed in the polyphyletic and remarkably diverse eukaryotic algal lineages.

Results: A phylogenetic reconstruction of the history of the POR enzyme (encoded by the por gene in nuclei) in eukaryotic algae reveals replacement and supplementation of ancestral por genes in several taxa with horizontally transferred por genes from other eukaryotic algae. For example, stramenopiles and haptophytes share por gene duplicates of prasinophytic origin, although their plastid ancestry predicts a rhodophytic por signal. Phylogenetically, stramenopile pors appear ancestral to those found in haptophytes, suggesting transfer from stramenopiles to haptophytes by either horizontal or endosymbiotic gene transfer. In dinoflagellates whose plastids have been replaced by those of a haptophyte or diatom, the ancestral por genes seem to have been lost whereas those of the new symbiotic partner are present. Furthermore, many chlorarachniophytes and peridinin-containing dinoflagellates possess por gene duplicates. In contrast to the retention, gain, and frequent duplication of algal por genes, the LIPOR gene complement (chloroplast-encoded chlL, chlN, and chlB genes) is often absent. LIPOR genes have been lost from haptophytes and potentially from the euglenid and chlorarachniophyte lineages. Within the chlorophytes, rhodophytes, cryptophytes, heterokonts, and chromerids, some taxa possess both POR and LIPOR genes while others lack LIPOR. The gradual process of LIPOR gene loss is evidenced in taxa possessing pseudogenes or partial LIPOR gene compliments. No horizontal transfer of LIPOR genes was detected.

Conclusions: We document a pattern of por gene acquisition and expansion as well as loss of LIPOR genes from many algal taxa, paralleling the presence of multiple por genes and lack of LIPOR genes in the angiosperms. These studies present an opportunity to compare the regulation and function of por gene families that have been acquired and expanded in patterns unique to each of various algal taxa.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Comparison of the POR and LIPOR enzymes. The second to last step of chlorophyll synthesis can be catalyzed by either a light-dependent (POR) or light-independent (LIPOR) protochlorophyllide oxidoreductase (figure after [2,3]).
Figure 2
Figure 2
Sequence logos of cyanobacterial PORs and diatom POR1 and POR2 proteins. Alignment of sequence logos of cyanobacterial POR proteins with diatom POR1 and POR2 proteins. Amino acid position indicated at the right of each line, corresponding to cyanobacterium Synechocystis elongatus and diatom Phaeodactylum tricornutum. Boxes indicate characteristic motifs, with diagnostic amino acids marked with asterisks: (a) Rossman fold essential to NADPH binding; (b) Y, K residues essential to enzyme-cofactor-substrate coordination and proton donation; (c) cysteine essential to catalysis. Amino acids are colored according to their chemical properties: green are polar (GSTYC); purple are neutral (QN), blue are positively charged (KRH); red are negatively charged (DE); and black are hydrophobic (AVLIPWFM).
Figure 3
Figure 3
Por gene tree: rhodophytic identity of cryptophyte and some stramenopile por s; duplication of dinoflagellate and chlorarachniophyte por s. (A) Outline of the full por gene tree inferred from the 274 amino acid conserved core of 275 POR proteins from cyanobacteria, eukaryotic algae and land plants, representing 162 taxa. Branches are colored according to algal lineage (see legend). The corresponding, detailed phylogeny is split between Figures 3B and 4. Scale bar indicates 0.3 amino acid substitutions per site. (B) Basal portion of por gene tree. Branches are colored according to algal lineage (see legend), with symbols indicating origin of endosymbiont in dinoflagellate taxa whose ancestral plastids have been replaced. Bayesian and maximum-likelihood analyses recovered nearly identical trees. Posterior probabilities are shown above branches and bootstrap support is shown below branches. All dashed branches have less than 0.95 posterior probability. Scale bar indicates 0.3 amino acid substitutions per site. Gene duplication (GD) and horizontal gene transfer (HGT) events are indicated with arrows.
Figure 4
Figure 4
Por gene tree: duplication of xenologous stramenopile/haptophyte por genes. Bottom half of the por gene tree outlined in Figure 3A. Branches colored by lineage, with symbols indicating origin of endosymbiont in dinoflagellate taxa whose ancestral plastid has been replaced (see legend). Posterior probabilities are shown above branches and bootstrap support are shown below branches. All dashed branches have less than 0.95 posterior probability. Scale bar indicates 0.3 amino acid substitutions per site. Arrows indicate the inferred horizontal gene transfer (HGT) of a por gene from prasinophytes to the stramenopiles, and the subsequent gene duplication (GD3) to create por1 and por2.

References

    1. Willows RD. Chlorophyll synthesis. In: Wise RR, Hoober JK, editors. The structure and function of plastids. Dordrecht: Springer; 2006. pp. 295–313.
    1. Armstrong G. Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms. J Photochem Photobiol B Biol. 1998;43:87–100.
    1. Suzuki J, Bauer C. A prokaryotic origin for light-dependent chlorophyll biosynthesis of plants. Proc Natl Acad Sci U S A. 1995;92:3749–53. - PMC - PubMed
    1. Fujita Y, Bauer CE. The light-dependent protochlorophyllide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening in the dark. In: Kadish K, Smith K, Guilard R, editors. The porphyrin handbook. vol. 13. San Diego: Elsevier Science; 2003. pp. 109–56.
    1. Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H, et al. X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature. 2010;465:110–4. - PubMed

Publication types

Substances

LinkOut - more resources

Full text links
BioMed Central full text link BioMed Central Free PMC article
Cite

AltStyle によって変換されたページ (->オリジナル) /