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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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Structure-based sequence alignment of the crystallized spinach CAB (code 1RWT) with proteins belonging to the LI818 clade. The secondary structure of the spinach CAB is shown above the alignment. Conserved amino acids highlighted by a red background are identical and those in red letters are similar. Alpha helices are represented as helices, and β-turns are marked with TT. Blue triangles indicate the conserved residues involved in the binding of chlorophyll a molecules. The green star shows the conserved glutamate in LI818-like proteins, predicted to preclude the binding of Chlb 607 observed in the spinach CAB. The colored frames indicate the three subgroups of helix α2 within the LI818 subfamilies.
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Figure 3: Structure-based sequence alignment of the crystallized spinach CAB (code 1RWT) with proteins belonging to the LI818 clade. The secondary structure of the spinach CAB is shown above the alignment. Conserved amino acids highlighted by a red background are identical and those in red letters are similar. Alpha helices are represented as helices, and β-turns are marked with TT. Blue triangles indicate the conserved residues involved in the binding of chlorophyll a molecules. The green star shows the conserved glutamate in LI818-like proteins, predicted to preclude the binding of Chlb 607 observed in the spinach CAB. The colored frames indicate the three subgroups of helix α2 within the LI818 subfamilies.

Mentions: The α-helices α1, α3 and α4 and most of the β-turns are well conserved for these proteins (Figure 2), which was confirmed by the multiple sequence alignment of the LI818-like proteins (Figure 3). In these regions, LI818-like proteins feature key residues strictly conserved with the spinach CAB: Asp47 (Asp28, Esi_02 numbering), Glu65 (Glu48), His68 (His51), Glu180 (Glu158), Arg185 (Arg163) and Gln197 (Gln175). The lysine 179 is also well conserved or replaced by polar glutamine. Almost all of these residues are involved in direct binding of chlorophyll a molecules (Chla 602, 603, 610, 612, and 613). The arginine 185 stabilizes Glu65 through an ionic interaction, which coordinates the magnesium ion of Chla 602 [42].


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)

Structure-based sequence alignment of the crystallized spinach CAB (code 1RWT) with proteins belonging to the LI818 clade. The secondary structure of the spinach CAB is shown above the alignment. Conserved amino acids highlighted by a red background are identical and those in red letters are similar. Alpha helices are represented as helices, and β-turns are marked with TT. Blue triangles indicate the conserved residues involved in the binding of chlorophyll a molecules. The green star shows the conserved glutamate in LI818-like proteins, predicted to preclude the binding of Chlb 607 observed in the spinach CAB. The colored frames indicate the three subgroups of helix α2 within the LI818 subfamilies.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Structure-based sequence alignment of the crystallized spinach CAB (code 1RWT) with proteins belonging to the LI818 clade. The secondary structure of the spinach CAB is shown above the alignment. Conserved amino acids highlighted by a red background are identical and those in red letters are similar. Alpha helices are represented as helices, and β-turns are marked with TT. Blue triangles indicate the conserved residues involved in the binding of chlorophyll a molecules. The green star shows the conserved glutamate in LI818-like proteins, predicted to preclude the binding of Chlb 607 observed in the spinach CAB. The colored frames indicate the three subgroups of helix α2 within the LI818 subfamilies.
Mentions: The α-helices α1, α3 and α4 and most of the β-turns are well conserved for these proteins (Figure 2), which was confirmed by the multiple sequence alignment of the LI818-like proteins (Figure 3). In these regions, LI818-like proteins feature key residues strictly conserved with the spinach CAB: Asp47 (Asp28, Esi_02 numbering), Glu65 (Glu48), His68 (His51), Glu180 (Glu158), Arg185 (Arg163) and Gln197 (Gln175). The lysine 179 is also well conserved or replaced by polar glutamine. Almost all of these residues are involved in direct binding of chlorophyll a molecules (Chla 602, 603, 610, 612, and 613). The arginine 185 stabilizes Glu65 through an ionic interaction, which coordinates the magnesium ion of Chla 602 [42].

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