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Chlorophyll-binding proteins revisited--a multigenic family of light-harvesting and stress proteins from a brown algal perspective.

Dittami SM, Michel G, Collén J, Boyen C, Tonon T - BMC Evol. Biol. (2010)

Bottom Line: Three-dimensional modeling of two LI818 proteins revealed features common to all LI818 proteins that are likely to interfere with their capacity to bind chlorophyll b and lutein, but may enable binding of chlorophyll c and fucoxanthin.In addition, statistical analyses of phylogenetic trees show an independent origin in different eukaryotic lineages or a green algal origin of LI818 proteins to be highly unlikely.Instead, our data favor an origin in an ancestral chlorophyll a/c-containing organism and a subsequent lateral transfer to some green algae, although an origin of LI818 proteins in a common ancestor of red and green algae cannot be ruled out.

View Article: PubMed Central - HTML - PubMed

Affiliation: UPMC Université Paris 06, UMR 7139 Marine Plants and Biomolecules, Station Biologique, Roscoff, France. simon.dittami@bio.uio.no

ABSTRACT

Background: Chlorophyll-binding proteins (CBPs) constitute a large family of proteins with diverse functions in both light-harvesting and photoprotection. The evolution of CBPs has been debated, especially with respect to the origin of the LI818 subfamily, members of which function in non-photochemical quenching and have been found in chlorophyll a/c-containing algae and several organisms of the green lineage, but not in red algae so far. The recent publication of the Ectocarpus siliculosus genome represents an opportunity to expand on previous work carried out on the origin and function of CBPs.

Results: The Ectocarpus genome codes for 53 CBPs falling into all major families except the exclusively green family of chlorophyll a/b binding proteins. Most stress-induced CBPs belong to the LI818 family. However, we highlight a few stress-induced CBPs from Phaeodactylum tricornutum and Chondrus crispus that belong to different sub-families and are promising targets for future functional studies. Three-dimensional modeling of two LI818 proteins revealed features common to all LI818 proteins that are likely to interfere with their capacity to bind chlorophyll b and lutein, but may enable binding of chlorophyll c and fucoxanthin. In the light of this finding, we examined the possibility that LI818 proteins may have originated in a chlorophyll c/fucoxanthin containing organism and compared this scenario to three alternatives: an independent evolution of LI818 proteins in different lineages, an ancient origin together with the first CBPs, before the separation of the red and the green lineage, or an origin in the green lineage and a transfer to an ancestor of haptophytes and heterokonts during a cryptic endosymbiosis event.

Conclusions: Our findings reinforce the idea that the LI818 family of CBPs has a role in stress response. In addition, statistical analyses of phylogenetic trees show an independent origin in different eukaryotic lineages or a green algal origin of LI818 proteins to be highly unlikely. Instead, our data favor an origin in an ancestral chlorophyll a/c-containing organism and a subsequent lateral transfer to some green algae, although an origin of LI818 proteins in a common ancestor of red and green algae cannot be ruled out.

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Schematic representation of the possible evolution of CBPs from Chl a/b-, Chl a-, and Chl a/c-containing organisms. A: Simplified representation of the nuclear phylogeny of photosynthetic organisms according to Sanchez-Puerta and Delwiche [70,71]. Hypotheses 1, 2, 3, and 4 as well as blue arrows indicate possible origins of LI818 proteins (see B and text). Orange arrows designate possible horizontal gene transfers according to hypotheses 3 and 4. Names marked with "*" indicate branches with known LI818 proteins. PE = primary endosymbiosis, SE = secondary endosymbiosis, TE = tertiary endosymbiosis. B: Different hypotheses regarding the position of LI818 proteins and associated p-values using the Approximately Unbiased test (AU) and the Weighted Shimodaira-Hasegawa test (WSH). "Lost in" indicates lineages in which, based on currently available sequence data, we would assume LI818 proteins to have been lost according to these hypotheses. Hypothesis 1 assumes that LI818 originated independently in green plants and chlorophyll a/c-containing organisms; Hypothesis 2 assumes that LI818 proteins evolved before the separation of the red- and green lineage; Hypothesis 3 assumes a transfer of genes from the green lineage to a common ancestor of heterokonts and haptophytes (Chl a/c) during the cryptic endosymbiosis event proposed by Moustafa et al. [28]; Hypothesis 4 assumes a horizontal gene transfer from an ancestral chlorophyll a/c-containing organism to an early member of the green lineage.
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Figure 5: Schematic representation of the possible evolution of CBPs from Chl a/b-, Chl a-, and Chl a/c-containing organisms. A: Simplified representation of the nuclear phylogeny of photosynthetic organisms according to Sanchez-Puerta and Delwiche [70,71]. Hypotheses 1, 2, 3, and 4 as well as blue arrows indicate possible origins of LI818 proteins (see B and text). Orange arrows designate possible horizontal gene transfers according to hypotheses 3 and 4. Names marked with "*" indicate branches with known LI818 proteins. PE = primary endosymbiosis, SE = secondary endosymbiosis, TE = tertiary endosymbiosis. B: Different hypotheses regarding the position of LI818 proteins and associated p-values using the Approximately Unbiased test (AU) and the Weighted Shimodaira-Hasegawa test (WSH). "Lost in" indicates lineages in which, based on currently available sequence data, we would assume LI818 proteins to have been lost according to these hypotheses. Hypothesis 1 assumes that LI818 originated independently in green plants and chlorophyll a/c-containing organisms; Hypothesis 2 assumes that LI818 proteins evolved before the separation of the red- and green lineage; Hypothesis 3 assumes a transfer of genes from the green lineage to a common ancestor of heterokonts and haptophytes (Chl a/c) during the cryptic endosymbiosis event proposed by Moustafa et al. [28]; Hypothesis 4 assumes a horizontal gene transfer from an ancestral chlorophyll a/c-containing organism to an early member of the green lineage.

Mentions: This latter observation prompted us to reexamine the origin of LI818 proteins in greater detail. The absence of CBP proteins in cyanobacteria and in an extensive EST library of the glaucophyte Cyanophora paradoxa [43] indicates that ancestral CBPs evolved after the separation of glaucophytes from red algae and green plants (Figure 5A). The presence of red-, haptophyte-, and heterokont CBPs within the same group is in agreement with the hypothesis that these proteins originate from a photosynthetic organism from the red lineage, and were transferred during secondary endosymbiosis. This event, however, cannot explain the presence of green LI818 proteins in a branch of the tree (Figure 1) otherwise comprising purely red- and chlorophyll a/c-containing algae. Interestingly, very similar observations were previously made for another group of proteins: Frommelt et al. [27] found that 5 of 16 protein sequences from heterokonts, haptophytes, and cryptophytes involved in carotenoid synthesis were closest to prasinophytes and not to red algal sequences. Although genes involved in carotenoid biosynthesis and chlorophyll-binding proteins are not related, they are both involved in photosynthesis. Notably, the enzymes violaxanthin de-epoxidase and zeaxanthin epoxidase, both of which were closest to the green linage in the study of Frommelt et al. [27], are part of the xanthophyll cycle, and thus an important actor in the regulation of NPQ, just as it has been suggested for LI818 proteins [18,23,25].


Chlorophyll-binding proteins revisited--a multigenic family of light-harvesting and stress proteins from a brown algal perspective.

Dittami SM, Michel G, Collén J, Boyen C, Tonon T - BMC Evol. Biol. (2010)

Schematic representation of the possible evolution of CBPs from Chl a/b-, Chl a-, and Chl a/c-containing organisms. A: Simplified representation of the nuclear phylogeny of photosynthetic organisms according to Sanchez-Puerta and Delwiche [70,71]. Hypotheses 1, 2, 3, and 4 as well as blue arrows indicate possible origins of LI818 proteins (see B and text). Orange arrows designate possible horizontal gene transfers according to hypotheses 3 and 4. Names marked with "*" indicate branches with known LI818 proteins. PE = primary endosymbiosis, SE = secondary endosymbiosis, TE = tertiary endosymbiosis. B: Different hypotheses regarding the position of LI818 proteins and associated p-values using the Approximately Unbiased test (AU) and the Weighted Shimodaira-Hasegawa test (WSH). "Lost in" indicates lineages in which, based on currently available sequence data, we would assume LI818 proteins to have been lost according to these hypotheses. Hypothesis 1 assumes that LI818 originated independently in green plants and chlorophyll a/c-containing organisms; Hypothesis 2 assumes that LI818 proteins evolved before the separation of the red- and green lineage; Hypothesis 3 assumes a transfer of genes from the green lineage to a common ancestor of heterokonts and haptophytes (Chl a/c) during the cryptic endosymbiosis event proposed by Moustafa et al. [28]; Hypothesis 4 assumes a horizontal gene transfer from an ancestral chlorophyll a/c-containing organism to an early member of the green lineage.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3008699&req=5

Figure 5: Schematic representation of the possible evolution of CBPs from Chl a/b-, Chl a-, and Chl a/c-containing organisms. A: Simplified representation of the nuclear phylogeny of photosynthetic organisms according to Sanchez-Puerta and Delwiche [70,71]. Hypotheses 1, 2, 3, and 4 as well as blue arrows indicate possible origins of LI818 proteins (see B and text). Orange arrows designate possible horizontal gene transfers according to hypotheses 3 and 4. Names marked with "*" indicate branches with known LI818 proteins. PE = primary endosymbiosis, SE = secondary endosymbiosis, TE = tertiary endosymbiosis. B: Different hypotheses regarding the position of LI818 proteins and associated p-values using the Approximately Unbiased test (AU) and the Weighted Shimodaira-Hasegawa test (WSH). "Lost in" indicates lineages in which, based on currently available sequence data, we would assume LI818 proteins to have been lost according to these hypotheses. Hypothesis 1 assumes that LI818 originated independently in green plants and chlorophyll a/c-containing organisms; Hypothesis 2 assumes that LI818 proteins evolved before the separation of the red- and green lineage; Hypothesis 3 assumes a transfer of genes from the green lineage to a common ancestor of heterokonts and haptophytes (Chl a/c) during the cryptic endosymbiosis event proposed by Moustafa et al. [28]; Hypothesis 4 assumes a horizontal gene transfer from an ancestral chlorophyll a/c-containing organism to an early member of the green lineage.
Mentions: This latter observation prompted us to reexamine the origin of LI818 proteins in greater detail. The absence of CBP proteins in cyanobacteria and in an extensive EST library of the glaucophyte Cyanophora paradoxa [43] indicates that ancestral CBPs evolved after the separation of glaucophytes from red algae and green plants (Figure 5A). The presence of red-, haptophyte-, and heterokont CBPs within the same group is in agreement with the hypothesis that these proteins originate from a photosynthetic organism from the red lineage, and were transferred during secondary endosymbiosis. This event, however, cannot explain the presence of green LI818 proteins in a branch of the tree (Figure 1) otherwise comprising purely red- and chlorophyll a/c-containing algae. Interestingly, very similar observations were previously made for another group of proteins: Frommelt et al. [27] found that 5 of 16 protein sequences from heterokonts, haptophytes, and cryptophytes involved in carotenoid synthesis were closest to prasinophytes and not to red algal sequences. Although genes involved in carotenoid biosynthesis and chlorophyll-binding proteins are not related, they are both involved in photosynthesis. Notably, the enzymes violaxanthin de-epoxidase and zeaxanthin epoxidase, both of which were closest to the green linage in the study of Frommelt et al. [27], are part of the xanthophyll cycle, and thus an important actor in the regulation of NPQ, just as it has been suggested for LI818 proteins [18,23,25].

Bottom Line: Three-dimensional modeling of two LI818 proteins revealed features common to all LI818 proteins that are likely to interfere with their capacity to bind chlorophyll b and lutein, but may enable binding of chlorophyll c and fucoxanthin.In addition, statistical analyses of phylogenetic trees show an independent origin in different eukaryotic lineages or a green algal origin of LI818 proteins to be highly unlikely.Instead, our data favor an origin in an ancestral chlorophyll a/c-containing organism and a subsequent lateral transfer to some green algae, although an origin of LI818 proteins in a common ancestor of red and green algae cannot be ruled out.

View Article: PubMed Central - HTML - PubMed

Affiliation: UPMC Université Paris 06, UMR 7139 Marine Plants and Biomolecules, Station Biologique, Roscoff, France. simon.dittami@bio.uio.no

ABSTRACT

Background: Chlorophyll-binding proteins (CBPs) constitute a large family of proteins with diverse functions in both light-harvesting and photoprotection. The evolution of CBPs has been debated, especially with respect to the origin of the LI818 subfamily, members of which function in non-photochemical quenching and have been found in chlorophyll a/c-containing algae and several organisms of the green lineage, but not in red algae so far. The recent publication of the Ectocarpus siliculosus genome represents an opportunity to expand on previous work carried out on the origin and function of CBPs.

Results: The Ectocarpus genome codes for 53 CBPs falling into all major families except the exclusively green family of chlorophyll a/b binding proteins. Most stress-induced CBPs belong to the LI818 family. However, we highlight a few stress-induced CBPs from Phaeodactylum tricornutum and Chondrus crispus that belong to different sub-families and are promising targets for future functional studies. Three-dimensional modeling of two LI818 proteins revealed features common to all LI818 proteins that are likely to interfere with their capacity to bind chlorophyll b and lutein, but may enable binding of chlorophyll c and fucoxanthin. In the light of this finding, we examined the possibility that LI818 proteins may have originated in a chlorophyll c/fucoxanthin containing organism and compared this scenario to three alternatives: an independent evolution of LI818 proteins in different lineages, an ancient origin together with the first CBPs, before the separation of the red and the green lineage, or an origin in the green lineage and a transfer to an ancestor of haptophytes and heterokonts during a cryptic endosymbiosis event.

Conclusions: Our findings reinforce the idea that the LI818 family of CBPs has a role in stress response. In addition, statistical analyses of phylogenetic trees show an independent origin in different eukaryotic lineages or a green algal origin of LI818 proteins to be highly unlikely. Instead, our data favor an origin in an ancestral chlorophyll a/c-containing organism and a subsequent lateral transfer to some green algae, although an origin of LI818 proteins in a common ancestor of red and green algae cannot be ruled out.

Show MeSH
Related in: MedlinePlus