Multiple Losses and Transfers to the Nucleus of Two Mitochondrial Succinate Dehydrogenase Genes During Angiosperm Evolution

Corresponding author: Keith L. Adams, Department of Botany, Iowa State University, Ames, IA 50011., kadams{at}bio.indiana.edu (E-mail)

Communicating editor: K. J. NEWTON

Unlike in animals, the functional transfer of mitochondrial genes to the nucleus is an ongoing process in plants. All but one of the previously reported transfers in angiosperms involve ribosomal protein genes. Here we report frequent transfer of two respiratory genes, sdh3 and sdh4 (encoding subunits 3 and 4 of succinate dehydrogenase), and we also show that these genes are present and expressed in the mitochondria of diverse angiosperms. Southern hybridization surveys reveal that sdh3 and sdh4 have been lost from the mitochondrion about 40 and 19 times, respectively, among the 280 angiosperm genera examined. Transferred, functional copies of sdh3 and sdh4 were characterized from the nucleus in four and three angiosperm families, respectively. The mitochondrial targeting presequences of two sdh3 genes are derived from preexisting genes for anciently transferred mitochondrial proteins. On the basis of the unique presequences of the nuclear genes and the recent mitochondrial gene losses, we infer that each of the seven nuclear sdh3 and sdh4 genes was derived from a separate transfer to the nucleus. These results strengthen the hypothesis that angiosperms are experiencing a recent evolutionary surge of mitochondrial gene transfer to the nucleus and reveal that this surge includes certain respiratory genes in addition to ribosomal protein genes.

This article has been cited by other articles:

				M. Groth-Malonek, U. Wahrmund, M. Polsakiewicz, and V. Knoop Evolution of a Pseudogene: Exclusive Survival of a Functional Mitochondrial nad7 Gene Supports Haplomitrium as the Earliest Liverwort Lineage and Proposes a Secondary Loss of RNA Editing in Marchantiidae Mol. Biol. Evol., April 1, 2007; 24(4): 1068 - 1074. [Abstract] [Full Text] [PDF]

				D. G. Durnford and M. W. Gray Analysis of Euglena gracilis Plastid-Targeted Proteins Reveals Different Classes of Transit Sequences Eukaryot. Cell, December 1, 2006; 5(12): 2079 - 2091. [Abstract] [Full Text] [PDF]

				M. Ueda, M. Fujimoto, S.-i. Arimura, N. Tsutsumi, and K.-i. Kadowaki Evidence for Transit Peptide Acquisition through Duplication and Subsequent Frameshift Mutation of a Preexisting Protein Gene in Rice Mol. Biol. Evol., December 1, 2006; 23(12): 2405 - 2412. [Abstract] [Full Text] [PDF]

				C. Noutsos, E. Richly, and D. Leister Generation and evolutionary fate of insertions of organelle DNA in the nuclear genomes of flowering plants Genome Res., May 1, 2005; 15(5): 616 - 628. [Abstract] [Full Text] [PDF]

				A. Elorza, G. Leon, I. Gomez, A. Mouras, L. Holuigue, A. Araya, and X. Jordana Nuclear SDH2-1 and SDH2-2 Genes, Encoding the Iron-Sulfur Subunit of Mitochondrial Complex II in Arabidopsis, Have Distinct Cell-Specific Expression Patterns and Promoter Activities Plant Physiology, December 1, 2004; 136(4): 4072 - 4087. [Abstract] [Full Text] [PDF]

				S. W. Clifton, P. Minx, C. M.-R. Fauron, M. Gibson, J. O. Allen, H. Sun, M. Thompson, W. B. Barbazuk, S. Kanuganti, C. Tayloe, et al. Sequence and Comparative Analysis of the Maize NB Mitochondrial Genome Plant Physiology, November 1, 2004; 136(3): 3486 - 3503. [Abstract] [Full Text] [PDF]

				D. O. Daley, R. Clifton, and J. Whelan Intracellular gene transfer: Reduced hydrophobicity facilitates gene transfer for subunit 2 of cytochrome c oxidase PNAS, August 6, 2002; 99(16): 10510 - 10515. [Abstract] [Full Text] [PDF]

				K. L. Adams, Y.-L. Qiu, M. Stoutemyer, and J. D. Palmer Inaugural Article: Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution PNAS, July 23, 2002; 99(15): 9905 - 9912. [Abstract] [Full Text] [PDF]

				K. L. Adams, H. C. Ong, and J. D. Palmer Mitochondrial Gene Transfer in Pieces: Fission of the Ribosomal Protein Gene rpl2 and Partial or Complete Gene Transfer to the Nucleus Mol. Biol. Evol., December 1, 2001; 18(12): 2289 - 2297. [Abstract] [Full Text] [PDF]

				K. L. Adams, D. O. Daley, J. Whelan, and J. D. Palmer Genes for Two Mitochondrial Ribosomal Proteins in Flowering Plants Are Derived from Their Chloroplast or Cytosolic Counterparts PLANT CELL, April 1, 2002; 14(4): 931 - 943. [Abstract] [Full Text] [PDF]