Evolutionary loss of light‐harvesting proteins Lhcb6 and Lhcb3 in major land plant groups – break‐up of current dogma

Abstract

SummaryPhotosynthesis in plants and algae relies on the coordinated function of photosystems (PS) I and II. Their efficiency is augmented by finely-tuned light-harvesting proteins (Lhcs) connected to them. The most recent Lhcs (in evolutionary terms), Lhcb6 and Lhcb3, evolved during the transition of plants from water to land and have so far been considered to be an essential characteristic of land plants.We used single particle electron microscopy and sequence analysis to study architecture and composition of PSII supercomplex from Norway spruce and related species.We have found that there are major land plant families that lack functional lhcb6 and lhcb3 genes, which notably changes the organization of PSII supercomplexes. The Lhcb6 and Lhcb3 proteins have been lost in the gymnosperm genera Picea and Pinus (family Pinaceae) and Gnetum (Gnetales). We also revealed that the absence of these proteins in Norway spruce modifies the PSII supercomplex in such a way that it resembles its counterpart in the alga Chlamydomonas reinhardtii, an evolutionarily older organism.Our results break a deep-rooted concept of Lhcb6 and Lhcb3 proteins being the essential characteristic of land plants, and beg the question of what the evolutionary benefit of their loss could be.

Diversity of winter photoinhibitory responses: a case study in co‐occurring lichens, mosses, herbs and woody plants from subalpine environments

“…In that sense, a recent study of the photosynthetic apparatus in conifers revealed that the Pinaceae and Gnetales families lack the Lhcb3 and Lhcb6 proteins, which play a role in NPQ. Until now, this had been considered to be an essential characteristic of land plants (Kouril et al ). It is known that some antenna proteins play an important role in NPQ, as they interact with PsbS, facilitating the NPQ process (Kovács et al ).…”

“…Nevertheless, antennae protein composition is of paramount importance in the response under stress. Very recently, Kouril et al () challenged a widely accepted concept. They discovered that some species from the Pinaceae family present lhcsr‐like transcripts.…”

“…They discovered that some species from the Pinaceae family present lhcsr‐like transcripts. This, together with the absence of Lhcb3 and Lhcb6, indicates that some woody species present a different strategy to cope with changing light or, at least, that their PsbS protein presents a different mode of action (Kouril et al ), in principle, more similar to Chlamydomonas reinhardtii than to Arabidopsis thaliana .…”

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].…”

“…reinhardtii does not, suggesting its acquisition during plant terrestrialization [6] (however, Lhcb3 appears to have been lost during the divergence of Pinaceae and Gnetales [21]). The orthologs of three minor LHCII proteins (Lhcb4, Lhcb5, and Lhcb6) in A. thaliana are also found in P. patens [6].…”