Does mRNA targeting explain gene retention in chloroplasts?

• Published in: Trends in plant science 2024-10
• Main Authors: Hess, Wolfgang R., Wilde, Annegret, Mullineaux, Conrad W.
• Format: Article
• Language: English
• Subjects: chloroplast; cyanobacteria; endosymbiosis; evolution; photosynthesis; thylakoid membrane
• ISSN: 1360-1385; 1878-4372; 1878-4372
• DOI: 10.1016/j.tplants.2024.09.017

Why did chloroplasts retain some genes from their free-living ancestors rather than transferring all of them to the nucleus following endosymbiosis?Nearly all the genes conserved between the cyanobacterium Synechocystis and all photosynthetic plastid genomes encode proteins directly involved in either electron transport-related processes or gene expression.The mRNAs encoding photosynthetic core proteins interact with members of a family of RNA-binding proteins (RBPs) in both cyanobacteria and chloroplasts.In cyanobacteria, the mRNA–RBP interaction strongly influences the levels and locations of photosynthetic mRNAs.RBPs are likely critical for regulating photosynthetic protein translation in time and space. During their evolution from cyanobacteria, plastids have relinquished most of their genes to the host cell nucleus, but have retained a core set of genes that are transcribed and translated within the organelle. Previous explanations have included incompatible codon or base composition, problems importing certain proteins across the double membrane, or the need for tight regulation in concert with the redox status of the electron transport chain. In this opinion article we propose the ‘mRNA targeting hypothesis’. Studies in cyanobacteria suggest that mRNAs encoding core photosynthetic proteins have features that are crucial for membrane targeting and coordination of early steps in complex assembly. We propose that the requirement for intimate involvement of mRNA molecules at the thylakoid surface explains the retention of core photosynthetic genes in chloroplasts. During their evolution from cyanobacteria, plastids have relinquished most of their genes to the host cell nucleus, but have retained a core set of genes that are transcribed and translated within the organelle. Previous explanations have included incompatible codon or base composition, problems importing certain proteins across the double membrane, or the need for tight regulation in concert with the redox status of the electron transport chain. In this opinion article we propose the ‘mRNA targeting hypothesis’. Studies in cyanobacteria suggest that mRNAs encoding core photosynthetic proteins have features that are crucial for membrane targeting and coordination of early steps in complex assembly. We propose that the requirement for intimate involvement of mRNA molecules at the thylakoid surface explains the retention of core photosynthetic genes in chloroplasts.