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

Autores
DeTar, Rachael A.; Chustecki, Joanna M.; Martinez Hottovy, Ana; Ceriotti, Luis Federico; Broz, Amanda K.; Lou, Xiaorui; Sánchez Puerta, María Virginia; Elowsky, Christian; Christensen, Alan C.; Sloan, Daniel B.
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: DeTar, Rachael A.. State University of Colorado - Fort Collins; Estados Unidos
Fil: Chustecki, Joanna M.. University of Nebraska; Estados Unidos
Fil: Martinez Hottovy, Ana. State University of Colorado - Fort Collins; Estados Unidos
Fil: Ceriotti, Luis Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Biología Agrícola de Mendoza. Universidad Nacional de Cuyo. Facultad de Ciencias Agrarias. Instituto de Biología Agrícola de Mendoza; Argentina
Fil: Broz, Amanda K.. State University of Colorado - Fort Collins; Estados Unidos
Fil: Lou, Xiaorui. State University of Colorado - Fort Collins; Estados Unidos
Fil: Sánchez Puerta, María Virginia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Biología Agrícola de Mendoza. Universidad Nacional de Cuyo. Facultad de Ciencias Agrarias. Instituto de Biología Agrícola de Mendoza; Argentina
Fil: Elowsky, Christian. Universidad de Nebraska - Lincoln; Estados Unidos
Fil: Christensen, Alan C.. Universidad de Nebraska - Lincoln; Estados Unidos
Fil: Sloan, Daniel B.. State University of Colorado - Fort Collins; Estados Unidos
Materia
ORGANELLE GENE EXPRESSION
AMINOACYL-TRNA SYNTHETASA
TRNA
PHOTOSYNTHESIS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/266468
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/266468
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organellesDeTar, Rachael A.Chustecki, Joanna M.Martinez Hottovy, AnaCeriotti, Luis FedericoBroz, Amanda K.Lou, XiaoruiSánchez Puerta, María VirginiaElowsky, ChristianChristensen, Alan C.Sloan, Daniel B.ORGANELLE GENE EXPRESSIONAMINOACYL-TRNA SYNTHETASATRNAPHOTOSYNTHESIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Eukaryotic 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.Fil: DeTar, Rachael A.. State University of Colorado - Fort Collins; Estados UnidosFil: Chustecki, Joanna M.. University of Nebraska; Estados UnidosFil: Martinez Hottovy, Ana. State University of Colorado - Fort Collins; Estados UnidosFil: Ceriotti, Luis Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Biología Agrícola de Mendoza. Universidad Nacional de Cuyo. Facultad de Ciencias Agrarias. Instituto de Biología Agrícola de Mendoza; ArgentinaFil: Broz, Amanda K.. State University of Colorado - Fort Collins; Estados UnidosFil: Lou, Xiaorui. State University of Colorado - Fort Collins; Estados UnidosFil: Sánchez Puerta, María Virginia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Biología Agrícola de Mendoza. Universidad Nacional de Cuyo. Facultad de Ciencias Agrarias. Instituto de Biología Agrícola de Mendoza; ArgentinaFil: Elowsky, Christian. Universidad de Nebraska - Lincoln; Estados UnidosFil: Christensen, Alan C.. Universidad de Nebraska - Lincoln; Estados UnidosFil: Sloan, Daniel B.. State University of Colorado - Fort Collins; Estados UnidosNational Academy of Sciences2024-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/266468DeTar, Rachael A.; Chustecki, Joanna M.; Martinez Hottovy, Ana; Ceriotti, Luis Federico; Broz, Amanda K.; et al.; Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles; National Academy of Sciences; Proceedings of the National Academy of Sciences of the United States of America; 121; 52; 12-2024; 1-120027-84241091-6490CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/doi/10.1073/pnas.2421485121info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.2421485121info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:00:29Zoai:ri.conicet.gov.ar:11336/266468instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:00:29.772CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
title Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
spellingShingle Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
DeTar, Rachael A.
ORGANELLE GENE EXPRESSION
AMINOACYL-TRNA SYNTHETASA
TRNA
PHOTOSYNTHESIS
title_short Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
title_full Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
title_fullStr Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
title_full_unstemmed Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
title_sort Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles
dc.creator.none.fl_str_mv DeTar, Rachael A.
Chustecki, Joanna M.
Martinez Hottovy, Ana
Ceriotti, Luis Federico
Broz, Amanda K.
Lou, Xiaorui
Sánchez Puerta, María Virginia
Elowsky, Christian
Christensen, Alan C.
Sloan, Daniel B.
author DeTar, Rachael A.
author_facet DeTar, Rachael A.
Chustecki, Joanna M.
Martinez Hottovy, Ana
Ceriotti, Luis Federico
Broz, Amanda K.
Lou, Xiaorui
Sánchez Puerta, María Virginia
Elowsky, Christian
Christensen, Alan C.
Sloan, Daniel B.
author_role author
author2 Chustecki, Joanna M.
Martinez Hottovy, Ana
Ceriotti, Luis Federico
Broz, Amanda K.
Lou, Xiaorui
Sánchez Puerta, María Virginia
Elowsky, Christian
Christensen, Alan C.
Sloan, Daniel B.
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ORGANELLE GENE EXPRESSION
AMINOACYL-TRNA SYNTHETASA
TRNA
PHOTOSYNTHESIS
topic ORGANELLE GENE EXPRESSION
AMINOACYL-TRNA SYNTHETASA
TRNA
PHOTOSYNTHESIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: DeTar, Rachael A.. State University of Colorado - Fort Collins; Estados Unidos
Fil: Chustecki, Joanna M.. University of Nebraska; Estados Unidos
Fil: Martinez Hottovy, Ana. State University of Colorado - Fort Collins; Estados Unidos
Fil: Ceriotti, Luis Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Biología Agrícola de Mendoza. Universidad Nacional de Cuyo. Facultad de Ciencias Agrarias. Instituto de Biología Agrícola de Mendoza; Argentina
Fil: Broz, Amanda K.. State University of Colorado - Fort Collins; Estados Unidos
Fil: Lou, Xiaorui. State University of Colorado - Fort Collins; Estados Unidos
Fil: Sánchez Puerta, María Virginia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Biología Agrícola de Mendoza. Universidad Nacional de Cuyo. Facultad de Ciencias Agrarias. Instituto de Biología Agrícola de Mendoza; Argentina
Fil: Elowsky, Christian. Universidad de Nebraska - Lincoln; Estados Unidos
Fil: Christensen, Alan C.. Universidad de Nebraska - Lincoln; Estados Unidos
Fil: Sloan, Daniel B.. State University of Colorado - Fort Collins; Estados Unidos
description 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.
publishDate 2024
dc.date.none.fl_str_mv 2024-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/266468
DeTar, Rachael A.; Chustecki, Joanna M.; Martinez Hottovy, Ana; Ceriotti, Luis Federico; Broz, Amanda K.; et al.; Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles; National Academy of Sciences; Proceedings of the National Academy of Sciences of the United States of America; 121; 52; 12-2024; 1-12
0027-8424
1091-6490
CONICET Digital
CONICET
url http://hdl.handle.net/11336/266468
identifier_str_mv DeTar, Rachael A.; Chustecki, Joanna M.; Martinez Hottovy, Ana; Ceriotti, Luis Federico; Broz, Amanda K.; et al.; Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles; National Academy of Sciences; Proceedings of the National Academy of Sciences of the United States of America; 121; 52; 12-2024; 1-12
0027-8424
1091-6490
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/doi/10.1073/pnas.2421485121
info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.2421485121
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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