Tracing the Evolution of the Light-Harvesting Antennae in Chlorophyll a/b-Containing Organisms

Abstract

The light-harvesting complexes (LHCs) of land plants and green algae have essential roles in light capture and photoprotection. Though the functional diversity of the individual LHC proteins are well described in many land plants, the extent of this family in the majority of green algal groups is unknown. To examine the evolution of the chlorophyll a/b antennae system and to infer its ancestral state, we initiated several expressed sequence tag projects from a taxonomically broad range of chlorophyll a/b-containing protists. This included representatives from the Ulvophyceae (Acetabularia acetabulum), the Mesostigmatophyceae (Mesostigma viride), and the Prasinophyceae (Micromonas sp.), as well as one representative from each of the Euglenozoa (Euglena gracilis) and Chlorarachniophyta (Bigelowiella natans), whose plastids evolved secondarily from a green alga. It is clear that the core antenna system was well developed prior to green algal diversification and likely consisted of the CP29 (Lhcb4) and CP26 (Lhcb5) proteins associated with photosystem II plus a photosystem I antenna composed of proteins encoded by at least Lhca3 and two green algal-specific proteins encoded by the Lhca2 and 9 genes. In organisms containing secondary plastids, we found no evidence for orthologs to the plant/algal antennae with the exception of CP29. We also identified PsbS homologs in the Ulvophyceae and the Prasinophyceae, indicating that this distinctive protein appeared prior to green algal diversification. This analysis provides a snapshot of the antenna systems in diverse green algae, and allows us to infer the changing complexity of the antenna system during green algal evolution.

Zeaxanthin Binds to Light-Harvesting Complex Stress-Related Protein to Enhance Nonphotochemical Quenching in Physcomitrella patens

“…Consistent with this, NPQ in P. patens depends on both PSBS and LHCSR (Alboresi et al, 2010;Gerotto et al, 2011) and presents an active xanthophyll cycle (Alboresi et al, 2008). The analysis of the P. patens genome (Koziol et al, 2007;Alboresi et al, 2008Alboresi et al, , 2011Rensing et al, 2008) revealed that the composition of its antenna system is more similar to that of vascular plants than to unicellular green algae due to the presence of genes encoding LHCb3 and LHCb6, which are not found in Chlamydomonas reinhardtii (Elrad and Grossman, 2004). Both carotenoid accumulation and NPQ are enhanced by abiotic stress Azzabi et al, 2012).…”

Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants

“…It appears that none of the P. patens Lhcb4 (PpLhcb4; "Pp" for P. patens, hereafter) isoforms are related to AtLhcb4.3 [6], which is found only in dicots and is now classified as Lhcb8 due to its distinct function from AtLhcb4.1 and AtLhcb4.2 [22]. Further, as the ortholog of AtLhcb6 has not been found in green algae so far [11,12], the presence of an AtLhcb6 ortholog in P. patens suggests its uniqueness to land plants, although it is absent in Pinaceae and Gnetales, similar to the case of Lhcb3 [21]. In addition to major and minor LHCIIs, the ortholog of AtLhcb7, which is rarely expressed [22], is present in P. patens [6].…”

“…In A. thaliana, Lhcb1, Lhcb2, and Lhcb3 encode major LHCIIs, and Lhcb4, Lhcb5, and Lhcb6 encode minor LHCIIs [10]. In green algae, the genes encoding major LHCIIs are designated as Lhcbm ("m" for major) and have relatively low amino acid sequence similarity to A. thaliana Lhcb1 (AtLhcb1; "At" for A. thaliana, hereafter), AtLhcb2, and AtLhcb3 [11,12].…”

“…For example, the orthologs of AtLhca1 and AtLhca2 are encoded by 3 and 5 paralogous genes in P. patens, respectively ( Figure 1). The homologs of AtLhca3 seem to have arisen prior to the divergence of green algal lineages [12], and both C. reinhardtii and A. thaliana have one Lhca3 gene. However, the P. patens genome contains four paralogs for Lhca3.…”

Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model

“…The PsbS protein is critical for qE in vascular land plants [32] but its role in green algae is unclear [33] and diatoms apparently do not encode this protein [34]. Conversely, the qE mechanism of eukaryotic algae, for example, Chlamydomonas, relies heavily on the light-harvesting complex stress-related (LHCSR) proteins, which are absent in vascular land plants [34]. State transitions also differ substantially between land plants and algae.…”