Structural diversity of signal recognition particle RNAs in plastids

Abstract

One of the pathways for protein targeting to the plasma membrane in bacteria utilizes the co-translationally acting signal recognition particle (SRP), a universally conserved ribonucleoprotein complex consisting of a 54 kDa protein and a functional RNA. An interesting exception is the higher plant chloroplast SRP, which lacks the otherwise essential RNA component. Furthermore, green plant chloroplasts have an additional post-translational SRP-dependent transport system in which the chloroplast-specific cpSRP43 protein binds to imported substrate proteins and to the conserved 54 kDa SRP subunit (cpSRP54). While homologs to the bacterial SRP protein and RNA component previously have been identified in genome sequences of red algae and diatoms, a recent study investigated the evolution of the green plant SRP system.1 Analysis of hundreds of plastid and nuclear genomes showed a surprising pattern of multiple losses of the plastid SRP RNA during evolution and a widespread presence in all non-spermatophyte plants and green algae. Contrary to expectations, all green organisms that have an identified cpSRP RNA also contain a cpSRP43. Notably, the structure of the plastid SRP RNAs is much more diverse than that of bacterial SRP RNAs. The apical GNRA tetraloop is only conserved in organisms of the red lineage and basal organisms of the green lineage, whereas further chloroplast SRP RNAs are characterized by atypical, mostly enlarged apical loops.

The Chloroplast SRP Systems of Chaetosphaeridium globosum and Physcomitrella patens as Intermediates in the Evolution of SRP-Dependent Protein Transport in Higher Plants

“…In this study we show low affinity binding of cpSRP54 to cpSRP43 and to the cpSRP RNA in Chaetosphaeridium globosum and Physcomitrella patens . These findings together with the observation of conserved cpSRP54- and cpSRP43-binding motifs within charophytes and the widespread occurrence of cpSRP RNAs with atypical apical loops in charophytes and bryophytes ([9, 15, 17] and this work) indicate that the formation of the heterodimeric cpSRP complex has developed within the charophytes and that the cpSRP systems of charophytes and bryophytes represent evolutionary intermediates in the evolution of the high affinity posttranslational cpSRP complex, and the complete loss of the SRP RNA component. However, it remains unclear which role the cpSRP RNA in charophytes and bryophytes might play, and how higher plants compensate for the loss of the cpSRP RNA in cotranslational protein transport.…”

“…However, the structure of the chloroplast SRP RNAs is much more diverse than that of bacterial SRP RNAs. The moss Physcomitrella patens , for example, contains a cpSRP RNA with an elongated apical loop instead of the classical tetraloop, which is typically present in bacterial SRP RNAs [9, 17] (Fig 1B). Interestingly, a recent study demonstrated that the cpSRP system in chlorophytes (e.g., Chlamydomonas reinhardtii ) differs from that of land plants in that cpSRP43 is not complexed to cpSRP54 ([15], Fig 1A).…”

Co-Translational Protein Folding and Sorting in Chloroplasts

“…An additional challenge is the integration of chloroplast-encoded proteins together with subunit proteins that are of cytosolic origin and post-translationally imported across the chloroplast envelope, reviewed in [25,[93][94][95][96]. Chloroplasts possess a homologue of SRP54, called cpSRP54 but the RNA which is usually associated with the SRP machinery is absent in higher plants (Table 1) [97][98][99][100]. Another surprising feature is the additional, and plastid specific, protein cpSRP43, which associates with cpSRP54 during the post-translational integration of nuclear-encoded light-harvesting chlorophyll a/b binding proteins (LHCPs) into the thylakoid membranes in higher plants [101,102].…”

Co-evolution of Two GTPases Enables Efficient Protein Targeting in an RNA-less Chloroplast Signal Recognition Particle Pathway

“…Phylogenetic Analysis of Interaction Motifs in the cpSRP Pathway-To better understand how this new set of interactions evolved in the cpSRP pathway, we performed a phylogenetic analysis. Previously, Schunemann and co-workers (20,21) carried out a thorough analysis that identified SRP RNA genes and predicted their secondary structure across all lineages of photosynthetic organisms, ranging from red and blue algae to land green plants. This analysis showed that the SRP RNA exists in some branches of blue and red algae and is lost during the evolution to higher green plants.…”

“…Both pathways retain homologues of the SRP and SR GTPases (termed cpSRP54 and cpFtsY, respectively) (17)(18)(19). Surprisingly, the otherwise universally conserved SRP RNA is lost in cpSRP during the evolution of green plants from cyanobacteria (20,21).…”