Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10

Monika Murcha, C. Rudhe, D. Elhafez, K.L. Adams, D.O. Daley, James Whelan

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

The minimal requirements to support protein import into mitochondria were investigated in the context of the phenomenon of ongoing gene transfer from the mitochondrion to the nucleus in plants. Ribosomal protein 10 of the small subunit is encoded in the mitochondrion in soybean and many other angiosperms, whereas in several other species it is nuclear encoded and thus must be imported into the mitochondrial matrix to function. When encoded by the nuclear genome, it has adopted different strategies for mitochondrial targeting and import. In lettuce ( Lactuca sativa) and carrot ( Daucus carota), Rps10 independently gained different N-terminal extensions from other genes, following transfer to the nucleus. ( The designation of Rps10 follows the following convention. The gene is indicated in italics. If encoded in the mitochondrion, it is rps10; if encoded in the nucleus, it is Rps10.) Here, we show that the N-terminal extensions of Rps10 in lettuce and carrot are both essential for mitochondrial import. In maize (Zea mays), Rps10 has not acquired an extension upon transfer but can be readily imported into mitochondria. Deletion analysis located the mitochondrial targeting region to the first 20 amino acids. Using site directed mutagenesis, we changed residues in the first 20 amino acids of the mitochondrial encoded soybean ( Glycine max) rps10 to the corresponding amino acids in the nuclear encoded maize Rps10 until import was achieved. Changes were required that altered charge, hydrophobicity, predicted ability to form an amphiphatic alpha-helix, and generation of a binding motif for the outermitochondrial membrane receptor, translocase of the outer membrane 20. In addition to defining the changes required to achieve mitochondrial localization, the results demonstrate that even proteins that do not present barriers to import can require substantial changes to acquire a mitochondrial targeting signal.
Original languageEnglish
Pages (from-to)2134-2144
JournalPlant Physiology
Volume138
Issue number4
DOIs
Publication statusPublished - 2005

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ribosomal proteins
gene transfer
imports
Mitochondria
mitochondria
Lettuce
Daucus carota
Soybeans
Zea mays
Genes
Amino Acids
carrots
lettuce
amino acids
soybeans
Angiosperms
Membranes
corn
Ribosomal Proteins
site-directed mutagenesis

Cite this

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title = "Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10",
abstract = "The minimal requirements to support protein import into mitochondria were investigated in the context of the phenomenon of ongoing gene transfer from the mitochondrion to the nucleus in plants. Ribosomal protein 10 of the small subunit is encoded in the mitochondrion in soybean and many other angiosperms, whereas in several other species it is nuclear encoded and thus must be imported into the mitochondrial matrix to function. When encoded by the nuclear genome, it has adopted different strategies for mitochondrial targeting and import. In lettuce ( Lactuca sativa) and carrot ( Daucus carota), Rps10 independently gained different N-terminal extensions from other genes, following transfer to the nucleus. ( The designation of Rps10 follows the following convention. The gene is indicated in italics. If encoded in the mitochondrion, it is rps10; if encoded in the nucleus, it is Rps10.) Here, we show that the N-terminal extensions of Rps10 in lettuce and carrot are both essential for mitochondrial import. In maize (Zea mays), Rps10 has not acquired an extension upon transfer but can be readily imported into mitochondria. Deletion analysis located the mitochondrial targeting region to the first 20 amino acids. Using site directed mutagenesis, we changed residues in the first 20 amino acids of the mitochondrial encoded soybean ( Glycine max) rps10 to the corresponding amino acids in the nuclear encoded maize Rps10 until import was achieved. Changes were required that altered charge, hydrophobicity, predicted ability to form an amphiphatic alpha-helix, and generation of a binding motif for the outermitochondrial membrane receptor, translocase of the outer membrane 20. In addition to defining the changes required to achieve mitochondrial localization, the results demonstrate that even proteins that do not present barriers to import can require substantial changes to acquire a mitochondrial targeting signal.",
author = "Monika Murcha and C. Rudhe and D. Elhafez and K.L. Adams and D.O. Daley and James Whelan",
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Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10. / Murcha, Monika; Rudhe, C.; Elhafez, D.; Adams, K.L.; Daley, D.O.; Whelan, James.

In: Plant Physiology, Vol. 138, No. 4, 2005, p. 2134-2144.

Research output: Contribution to journalArticle

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T1 - Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10

AU - Murcha, Monika

AU - Rudhe, C.

AU - Elhafez, D.

AU - Adams, K.L.

AU - Daley, D.O.

AU - Whelan, James

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AB - The minimal requirements to support protein import into mitochondria were investigated in the context of the phenomenon of ongoing gene transfer from the mitochondrion to the nucleus in plants. Ribosomal protein 10 of the small subunit is encoded in the mitochondrion in soybean and many other angiosperms, whereas in several other species it is nuclear encoded and thus must be imported into the mitochondrial matrix to function. When encoded by the nuclear genome, it has adopted different strategies for mitochondrial targeting and import. In lettuce ( Lactuca sativa) and carrot ( Daucus carota), Rps10 independently gained different N-terminal extensions from other genes, following transfer to the nucleus. ( The designation of Rps10 follows the following convention. The gene is indicated in italics. If encoded in the mitochondrion, it is rps10; if encoded in the nucleus, it is Rps10.) Here, we show that the N-terminal extensions of Rps10 in lettuce and carrot are both essential for mitochondrial import. In maize (Zea mays), Rps10 has not acquired an extension upon transfer but can be readily imported into mitochondria. Deletion analysis located the mitochondrial targeting region to the first 20 amino acids. Using site directed mutagenesis, we changed residues in the first 20 amino acids of the mitochondrial encoded soybean ( Glycine max) rps10 to the corresponding amino acids in the nuclear encoded maize Rps10 until import was achieved. Changes were required that altered charge, hydrophobicity, predicted ability to form an amphiphatic alpha-helix, and generation of a binding motif for the outermitochondrial membrane receptor, translocase of the outer membrane 20. In addition to defining the changes required to achieve mitochondrial localization, the results demonstrate that even proteins that do not present barriers to import can require substantial changes to acquire a mitochondrial targeting signal.

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DO - 10.1104/pp.105.062745

M3 - Article

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EP - 2144

JO - Plant Physiology (Online)

JF - Plant Physiology (Online)

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