Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily

Abstract

BackgroundThe extended light-harvesting complex (LHC) protein superfamily is a centerpiece of eukaryotic photosynthesis, comprising the LHC family and several families involved in photoprotection, like the LHC-like and the photosystem II subunit S (PSBS). The evolution of this complex superfamily has long remained elusive, partially due to previously missing families.ResultsIn this study we present a meticulous search for LHC-like sequences in public genome and expressed sequence tag databases covering twelve representative photosynthetic eukaryotes from the three primary lineages of plants (Plantae): glaucophytes, red algae and green plants (Viridiplantae). By introducing a coherent classification of the different protein families based on both, hidden Markov model analyses and structural predictions, numerous new LHC-like sequences were identified and several new families were described, including the red lineage chlorophyll a/b-binding-like protein (RedCAP) family from red algae and diatoms. The test of alternative topologies of sequences of the highly conserved chlorophyll-binding core structure of LHC and PSBS proteins significantly supports the independent origins of LHC and PSBS families via two unrelated internal gene duplication events. This result was confirmed by the application of cluster likelihood mapping.ConclusionsThe independent evolution of LHC and PSBS families is supported by strong phylogenetic evidence. In addition, a possible origin of LHC and PSBS families from different homologous members of the stress-enhanced protein subfamily, a diverse and anciently paralogous group of two-helix proteins, seems likely. The new hypothesis for the evolution of the extended LHC protein superfamily proposed here is in agreement with the character evolution analysis that incorporates the distribution of families and subfamilies across taxonomic lineages. Intriguingly, stress-enhanced proteins, which are universally found in the genomes of green plants, red algae, glaucophytes and in diatoms with complex plastids, could represent an important and previously missing link in the evolution of the extended LHC protein superfamily.

Small One-Helix Proteins Are Essential for Photosynthesis in Arabidopsis

“…Within each branch, the topology roughly follows the species tree of Viridiplantae (Rodríguez-Ezpeleta et al, 2005) with a separate branch of OHP2 sequences in organisms of the red algae lineage. In the red lineage, no nuclear-encoded OHP1 was identified, but they contain a putatively ancestral plastid-encoded High Light Induced Protein (HLIP) that is not present in the green lineage (Engelken et al, 2010). Among higher plants, OHP1 sequences and likewise OHP2 sequences are highly conserved and typically have more than 75% identical amino acids in the analyzed region within the monocot and dicot clades, whereas OHP1 sequences share only 10–20% identical amino acids with OHP2 (Supplemental Figure 1).…”

Molecular and Photosynthetic Responses to Prolonged Darkness and Subsequent Acclimation to Re-Illumination in the Diatom Phaeodactylum tricornutum

“…A deviant P. tricornutum LHC protein called LHC17531 is found as part of an outgroup in the cladogram. In addition to the LHC proteins, P. tricornutum also express a member of the extended LHC superfamily named LHL1 that has recently been classified as a red lineage chlorophyll a/b -binding (CAB)-like protein (RedCAP) [35]. The LHL1 protein sequence was not included in the phylogenetic analyses of the LHC proteins due to low sequence similarities outside of the two chlorophyll-binding motifs [36].…”

“…In contrast to other LHC-like proteins (e.g. early light-induced proteins (ELIPs), stress-enhanced proteins (SEPs), one helix proteins (OHPs)) that are generally associated with stress conditions [35], [51]–[53], the gene encoding the P. tricornutum LHL1 protein show no signs of being stress-induced when exposed to sudden changes in light conditions. The transcriptional response of the LHL1 gene is similar to the response of the LHCF and LHCR-1 genes both in the present experiment and in our previous HL experiment (LHL1 data not included in [28]).…”

Hyperdiversity of Genes Encoding Integral Light-Harvesting Proteins in the Dinoflagellate Symbiodinium sp

“…It is proposed that the gene for the four membrane-spanning helices arose from gene duplication of membrane-spanning helices I and III with helix IV subsequently undergoing degeneration [15]. The conservation of helices I and III in a diverse range of organisms, including Symbiodinium , supports this hypothesis and that helices I and III and the associated Chl-binding residues represent the core of the light-harvesting complex [5], although alternative evolutionary scenarios have been suggested [4].…”