Evolution from the Prokaryotic to the Higher Plant Chloroplast Signal Recognition Particle: The Signal Recognition Particle RNA Is Conserved in Plastids of a Wide Range of Photosynthetic Organisms

Abstract

The protein targeting signal recognition particle (SRP) pathway in chloroplasts of higher plants has undergone dramatic evolutionary changes. It disposed of its RNA, which is an essential SRP component in bacteria, and uses a unique chloroplastspecific protein cpSRP43. Nevertheless, homologs of the conserved SRP54 and the SRP receptor, FtsY, are present in higher plant chloroplasts. In this study, we analyzed the phylogenetic distribution of SRP components in photosynthetic organisms to elucidate the evolution of the SRP system. We identified conserved plastid SRP RNAs within all nonspermatophyte land plant lineages and in all chlorophyte branches. Furthermore, we show the simultaneous presence of cpSRP43 in these organisms. The function of this novel SRP system was biochemically and structurally characterized in the moss Physcomitrella patens. We show that P. patens chloroplast SRP (cpSRP) RNA binds cpSRP54 but has lost the ability to significantly stimulate the GTPase cycle of SRP54 and FtsY. Furthermore, the crystal structure at 1.8-Å resolution and the nucleotide specificity of P. patens cpFtsY was determined and compared with bacterial FtsY and higher plant chloroplast FtsY. Our data lead to the view that the P. patens cpSRP system occupies an intermediate position in the evolution from bacterial-type SRP to higher plant-type cpSRP system.

Chloroplast SRP54 Was Recruited for Posttranslational Protein Transport via Complex Formation with Chloroplast SRP43 during Land Plant Evolution

“…However, a recent study analyzing the phylogenetic distribution of SRP components in photosynthetic organisms identified conserved chloroplast SRP RNAs within a wide range of green algae and land plants, which evolved earlier than spermatophytes, showing the simultaneous presence of a cpSRP RNA and cpSRP43 in these organisms (25). These findings demonstrated that the evolution of cpSRP43 is not correlated with a loss of the SRP RNA.…”

“…These findings demonstrated that the evolution of cpSRP43 is not correlated with a loss of the SRP RNA. The moss Physcomitrella patens was studied as an example for this type of SRP system, and Physcomitrella cpSRP54 was shown to be able to form a stable complex with cpSRP43 and to bind the cpSRP RNA (25).…”

Mitochondrial genomes are retained by selective constraints on protein targeting

“…One of the latter is a cotranslational SRP system that inserts plastid-encoded membrane proteins with hydrophobic TMDs in the thylakoid membrane (51). The other SRP system acts posttranslationally (51). Thus, neither of the plastid SRP systems would be able to transport proteins with hydrophobic TMDs to the thylakoid membrane if the genes were located in the nuclear genomes.…”

“…One is the cytosolic SRP system for transport to the ER, whereas the other two SRP systems specifically mediate protein targeting to the thylakoids. One of the latter is a cotranslational SRP system that inserts plastid-encoded membrane proteins with hydrophobic TMDs in the thylakoid membrane (51). The other SRP system acts posttranslationally (51).…”

“…Like mitochondria, chloroplasts have a double-membrane envelope, but additionally chloroplasts contain internal membrane structures (thylakoids) where the two photosystems are embedded. To accommodate this extra layer of complexity, higher plants contain three different SRP targeting systems (51). One is the cytosolic SRP system for transport to the ER, whereas the other two SRP systems specifically mediate protein targeting to the thylakoids.…”