Cytonuclear evolution in fully heterotrophic plants: lifestyles and gene function determine scenarios

Guo, Xuelian; Wang, Hanchen; Lin, Dongliang; Wang, Yajun; Jin, Xiaohua

doi:10.1186/s12870-024-05702-4

Cited by 2 publications

References 61 publications

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Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

DeTar,

Chustecki,

Martinez-Hottovy

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Eukaryotic nuclear genomes often encode distinct sets of translation machinery for function in the cytosol vs. organelles (mitochondria and plastids). This raises questions about why multiple translation systems are maintained even though they are capable of comparable functions and whether they evolve differently depending on the compartment where they operate. These questions are particularly interesting in plants because translation machinery, including aminoacyl-transfer RNA (tRNA) synthetases (aaRS), is often dual-targeted to the plastids and mitochondria. These organelles have different functions, with much higher rates of translation in plastids to supply the abundant, rapid-turnover proteins required for photosynthesis. Previous studies have indicated that plant organellar aaRS evolve more slowly compared to mitochondrial aaRS in eukaryotes that lack plastids. Thus, we investigated the evolution of nuclear-encoded organellar and cytosolic aaRS and tRNA maturation enzymes across a broad sampling of angiosperms, including nonphotosynthetic (heterotrophic) plant species with reduced plastid gene expression, to test the hypothesis that translational demands associated with photosynthesis constrain the evolution of enzymes involved in organellar tRNA metabolism. Remarkably, heterotrophic plants exhibited wholesale loss of many organelle-targeted aaRS and other enzymes, even though translation still occurs in their mitochondria and plastids. These losses were often accompanied by apparent retargeting of cytosolic enzymes and tRNAs to the organelles, sometimes preserving aaRS–tRNA charging relationships but other times creating surprising mismatches between cytosolic aaRS and mitochondrial tRNA substrates. Our findings indicate that the presence of a photosynthetic plastid drives the retention of specialized systems for organellar tRNA metabolism.

show abstract

Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

DeTar,

Chustecki,

Martinez-Hottovy

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

DeTar,

Chustecki,

Martinez-Hottovy

et al. 2023

Preprint

View full text Add to dashboard Cite

Eukaryotic nuclear genomes often encode distinct sets of protein translation machinery for function in the cytosol vs. organelles (mitochondria and plastids). This phenomenon raises questions about why multiple translation systems are maintained even though they are capable of comparable functions, and whether they evolve differently depending on the compartment where they operate. These questions are particularly interesting in land plants because translation machinery, including aminoacyl-tRNA synthetases (aaRS), is often dual-targeted to both the plastids and mitochondria. These two organelles have quite different metabolisms, with much higher rates of translation in plastids to supply the abundant, rapid-turnover proteins required for photosynthesis. Previous studies have indicated that plant organellar aaRS evolve more slowly compared to mitochondrial aaRS in other eukaryotes that lack plastids. Thus, we investigated the evolution of nuclear-encoded organellar and cytosolic translation machinery across a broad sampling of angiosperms, including non-photosynthetic (heterotrophic) plant species with reduced rates of plastid gene expression to test the hypothesis that translational demands associated with photosynthesis constrain the evolution of bacterial-like enzymes involved in organellar tRNA metabolism. Remarkably, heterotrophic plants exhibited wholesale loss of many organelle-targeted aaRS and other enzymes, even though translation still occurs in their mitochondria and plastids. These losses were often accompanied by apparent retargeting of cytosolic enzymes and tRNAs to the organelles, sometimes preserving aaRS-tRNA charging relationships but other times creating surprising mismatches between cytosolic aaRS and mitochondrial tRNA substrates. Our findings indicate that the presence of a photosynthetic plastid drives the retention of specialized systems for organellar tRNA metabolism.

show abstract

Cytonuclear evolution in fully heterotrophic plants: lifestyles and gene function determine scenarios

Cited by 2 publications

References 61 publications

Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

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