A Fragment of Chloroplast DNA Was Transferred Horizontally, Probably from Non-eudicots, to Mitochondrial Genome of Phaseolus

Overview

Journal Plant Mol Biol

Date 2005 Apr 2

PMID 15803417

Citations 14

Authors

Magdalena Woloszynska

Tomasz Bocer

Pawel Mackiewicz

Hanna Janska

Affiliations

Soon will be listed here.

Abstract

The mitochondrial genomes of some Phaseolus species contain a fragment of chloroplast trnA gene intron, named pvs-trnA for its location within the Phaseolus vulgaris sterility sequence (pvs). The purpose of this study was to determine the type of transfer (intracellular or horizontal) that gave rise to pvs-trnA. Using a PCR approach we could not find the respective portion of the trnA gene as a part of pvs outside the Phaseolus genus. However, a BLAST search revealed longer fragments of trnA present in the mitochondrial genomes of some Citrus species, Helianthus annuus and Zea mays. Basing on the identity or near-identity between these mitochondrial sequences and their chloroplast counterparts we concluded that they had relocated from chloroplasts to mitochondria via recent, independent, intracellular DNA transfers. In contrast, pvs-trnA displayed a relatively higher sequence divergence when compared with its chloroplast counterpart from Phaseolus vulgaris. Alignment of pvs-trnA with corresponding trnA fragments from 35 plant species as well as phylogenetic analysis revealed that pvs-trnA grouped with non-eudicot sequences and was well separated from all Fabales sequences. In conclusion, we propose that pvs-trnA arose via horizontal transfer of a trnA intron fragment from chloroplast of a non-eudicot plant to Phaseolus mitochondria. This is the first example of horizontal transfer of a chloroplast sequence to the mitochondrial genome in higher plants.

Citing Articles

New Insights into the Diversity of Mitochondrial Plastid DNA.

Nhat Nam N, Thi N, Do H Genome Biol Evol. 2024; 16(9).

PMID: 39231033 PMC: 11373515. DOI: 10.1093/gbe/evae184.

Phylogenetic incongruence in an Asiatic species complex of the genus Caryodaphnopsis (Lauraceae).

Yang S, Huang J, Qu Y, Zhang D, Tan Y, Wen S BMC Plant Biol. 2024; 24(1):616.

PMID: 38937691 PMC: 11212351. DOI: 10.1186/s12870-024-05050-3.

Comparative analysis of chloroplast and mitochondrial genomes of sweet potato provides evidence of gene transfer.

Li G, Zhang H, Lin Z, Li H, Xu G, Xu Y Sci Rep. 2024; 14(1):4547.

PMID: 38402284 PMC: 10894244. DOI: 10.1038/s41598-024-55150-1.

Comparative Analysis of Mitochondrial DNA Revealed Two Distinct Genome Structures.

Li J, Cullis C Biology (Basel). 2023; 12(9).

PMID: 37759643 PMC: 10525999. DOI: 10.3390/biology12091244.

The mitochondrial genome sequence of Abies alba Mill. reveals a high structural and combinatorial variation.

Kersten B, Rellstab C, Schroeder H, Brodbeck S, Fladung M, Krutovsky K BMC Genomics. 2022; 23(1):776.

PMID: 36443651 PMC: 9703787. DOI: 10.1186/s12864-022-08993-9.

References

Bruno W, Socci N, Halpern A . Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol. 2000; 17(1):189-97. DOI: 10.1093/oxfordjournals.molbev.a026231. View

de la Cruz F, Davies J . Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol. 2000; 8(3):128-33. DOI: 10.1016/s0966-842x(00)01703-0. View

Cho Y, Qiu Y, Kuhlman P, Palmer J . Explosive invasion of plant mitochondria by a group I intron. Proc Natl Acad Sci U S A. 1998; 95(24):14244-9. PMC: 24358. DOI: 10.1073/pnas.95.24.14244. View

Small I, Suffolk R, Leaver C . Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell. 1989; 58(1):69-76. DOI: 10.1016/0092-8674(89)90403-0. View

Watanabe N, Nakazono M, Kanno A, Tsutsumi N, Hirai A . Evolutionary variations in DNA sequences transferred from chloroplast genomes to mitochondrial genomes in the Gramineae. Curr Genet. 1994; 26(5-6):512-8. DOI: 10.1007/BF00309942. View

Doolittle W . Phylogenetic classification and the universal tree. Science. 1999; 284(5423):2124-9. DOI: 10.1126/science.284.5423.2124. View

Strimmer K, Rambaut A . Inferring confidence sets of possibly misspecified gene trees. Proc Biol Sci. 2002; 269(1487):137-42. PMC: 1690879. DOI: 10.1098/rspb.2001.1862. View

Unseld M, Marienfeld J, Brandt P, Brennicke A . The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997; 15(1):57-61. DOI: 10.1038/ng0197-57. View

Schmit V, du Jardin P, Baudoin J, Debouck D . Use of chloroplast DNA polymorphisms for the phylogenetic study of seven Phaseolus taxa including P. vulgaris and P. coccineus. Theor Appl Genet. 2013; 87(4):506-16. DOI: 10.1007/BF00215097. View

10.

Johns C, Lu M, Lyznik A, Mackenzie S . A mitochondrial DNA sequence is associated with abnormal pollen development in cytoplasmic male sterile bean plants. Plant Cell. 1992; 4(4):435-49. PMC: 160143. DOI: 10.1105/tpc.4.4.435. View

11.

Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M . The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics. 2002; 268(4):434-45. DOI: 10.1007/s00438-002-0767-1. View

12.

Goldman N, Anderson J, Rodrigo A . Likelihood-based tests of topologies in phylogenetics. Syst Biol. 2002; 49(4):652-70. DOI: 10.1080/106351500750049752. View

13.

Lawrence J, Hendrickson H . Lateral gene transfer: when will adolescence end?. Mol Microbiol. 2003; 50(3):739-49. DOI: 10.1046/j.1365-2958.2003.03778.x. View

14.

Gray M . The endosymbiont hypothesis revisited. Int Rev Cytol. 1992; 141:233-357. DOI: 10.1016/s0074-7696(08)62068-9. View

15.

Martin W . Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci U S A. 2003; 100(15):8612-4. PMC: 166356. DOI: 10.1073/pnas.1633606100. View

16.

Hervieu F, Charbonnier L, Bannerot H, Pelletier G . The cytoplasmic male-sterility (CMS) determinant of common bean is widespread in Phaseolus coccineus L. and Phaseolus vulgaris L. Curr Genet. 1993; 24(1-2):149-55. DOI: 10.1007/BF00324679. View

17.

Bergthorsson U, Adams K, Thomason B, Palmer J . Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature. 2003; 424(6945):197-201. DOI: 10.1038/nature01743. View

18.

Lyznik A, Woloszynska M, Janska H, Tohme J, Mackenzie S . Tracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean. Genetics. 2001; 158(2):851-64. PMC: 1461663. DOI: 10.1093/genetics/158.2.851. View

19.

Cummings M, Nugent J, Olmstead R, Palmer J . Phylogenetic analysis reveals five independent transfers of the chloroplast gene rbcL to the mitochondrial genome in angiosperms. Curr Genet. 2003; 43(2):131-8. DOI: 10.1007/s00294-003-0378-3. View

20.

Chase C, Ortega V . Organization of ATPA coding and 3' flanking sequences associated with cytoplasmic male sterility in Phaseolus vulgaris L. Curr Genet. 1992; 22(2):147-53. DOI: 10.1007/BF00351475. View