Coordinated rates of evolution between interacting plastid and nuclear genes in geraniaceae

Plant Cell

Volumn 27, Issue 3, 2015, Pages 563-573

  Zhang, Jin ^a   Ruhlman, Tracey A ^a   Sabir, Jamal ^b   Blazier, J Chris ^a   Jansen, Robert K ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

GERANIACEAE; GERANIALES;

AMINO ACID SUBSTITUTION; ARABIDOPSIS; CELL NUCLEUS; GENETICS; GERANIACEAE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PLANT GENE; PLASTID; SPECIES DIFFERENCE;

AMINO ACID SUBSTITUTION; ARABIDOPSIS; CELL NUCLEUS; EVOLUTION, MOLECULAR; GENES, PLANT; GERANIACEAE; MOLECULAR SEQUENCE DATA; PLASTIDS; SPECIES SPECIFICITY;

EID: 84927714385     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.134353     Document Type: Article

References (65)

1. Agrafioti, I., Swire, J., Abbott, J., Huntley, D., Butcher, S., and Stumpf, M.P.H. (2005). Comparative analysis of the Saccharomyces cerevisiae and Caenorhabditis elegans protein interaction networks. BMC Evol. Biol. 5: 23.
2. Barreto, F.S., and Burton, R.S. (2013). Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Mol. Biol. Evol. 30: 310-314.
3. Campo, D.S., Dimitrova, Z., Mitchell, R.J., Lara, J., and Khudyakov, Y. (2008). Coordinated evolution of the hepatitis C virus. Proc. Natl. Acad. Sci. USA 105: 9685-9690.
4. Chen, Y., and Dokholyan, N.V. (2006). The coordinated evolution of yeast proteins is constrained by functional modularity. Trends Genet. 22: 416-419.
5. Chris Blazier, J., Guisinger, M.M., and Jansen, R.K. (2011). Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Mol. Biol. 76: 263-272.
6. Chumley, T.W., Palmer, J.D., Mower, J.P., Fourcade, H.M., Calie, P.J., Boore, J.L., and Jansen, R.K. (2006). The complete chloroplast genome sequence of Pelargonium x hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol. Biol. Evol. 23: 2175-2190.
7. Clark, N.L., Alani, E., and Aquadro, C.F. (2012). Evolutionary rate covariation reveals shared functionality and coexpression of genes. Genome Res. 22: 714-720.
8. Clark, N.L., and Aquadro, C.F. (2010). A novel method to detect proteins evolving at correlated rates: identifying new functional relationships between coevolving proteins. Mol. Biol. Evol. 27: 1152-1161.
9. Davis, J.C., and Petrov, D.A. (2004). Preferential duplication of conserved proteins in eukaryotic genomes. PLoS Biol. 2: E55.
10. de Juan, D., Pazos, F., and Valencia, A. (2013). Emerging methods in protein co-evolution. Nat. Rev. Genet. 14: 249-261.
11. Drouin, G., Daoud, H., and Xia, J. (2008). Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol. Phylogenet. Evol. 49: 827-831.
12. Duarte, J.M., Wall, P.K., Edger, P.P., Landherr, L.L., Ma, H., Pires, J.C., Leebens-Mack, J., and dePamphilis, C.W. (2010). Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol. Biol. 10: 61.
13. Durand, D., Halldórsson, B.V., and Vernot, B. (2006). A hybrid micromacroevolutionary approach to gene tree reconstruction. J. Comput. Biol. 13: 320-335.
14. Dutheil, J., and Galtier, N. (2007). Detecting groups of coevolving positions in a molecule: a clustering approach. BMC Evol. Biol. 7: 242.
15. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797.
16. Endo, T., Shikanai, T., Takabayashi, A., Asada, K., and Sato, F. (1999). The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett. 457: 5-8.
17. Fares, M.A., and Wolfe, K.H. (2003). Positive selection and subfunctionalization of duplicated CCT chaperonin subunits. Mol. Biol. Evol. 20: 1588-1597.
18. Favory, J.-J., Kobayshi, M., Tanaka, K., Peltier, G., Kreis, M., Valay, J.-G., and Lerbs-Mache, S. (2005). Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res. 33: 5991-5999.
19. Fraser, H.B., Hirsh, A.E., Wall, D.P., and Eisen, M.B. (2004). Coevolution of gene expression among interacting proteins. Proc. Natl. Acad. Sci. USA 101: 9033-9038.
20. Göbel, U., Sander, C., Schneider, R., and Valencia, A. (1994). Correlated mutations and residue contacts in proteins. Proteins 18: 309-317.
21. Greiner, S., Rauwolf, U., Meurer, J., and Herrmann, R.G. (2011). The role of plastids in plant speciation. Mol. Ecol. 20: 671-691.
22. Greiner, S., Wang, X., Herrmann, R.G., Rauwolf, U., Mayer, K., Haberer, G., and Meurer, J. (2008). The complete nucleotide sequences of the 5 genetically distinct plastid genomes of Oenothera, subsection Oenothera: II. A microevolutionary view using bioinformatics and formal genetic data. Mol. Biol. Evol. 25: 2019-2030.
23. Guisinger, M.M., Kuehl, J.V., Boore, J.L., and Jansen, R.K. (2008). Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc. Natl. Acad. Sci. USA 105: 18424-18429.
24. Hu, J., and Yan, C. (2009). A tool for calculating binding-site residues on proteins from PDB structures. BMC Struct. Biol. 9: 52.
25. Katoh, K., and Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772-780.
26. Lamesch, P., et al. (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40: D1202-D1210.
27. Larkin, M.A., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
28. Lerbs-Mache, S. (2011). Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription? Plant Mol. Biol. 76: 235-249.
29. Li, L., Huang, Y., Xia, X., and Sun, Z. (2006). Preferential duplication in the sparse part of yeast protein interaction network. Mol. Biol. Evol. 23: 2467-2473.
30. Lobo, F.P., Mota, B.E.F., Pena, S.D.J., Azevedo, V., Macedo, A.M., Tauch, A., Machado, C.R., and Franco, G.R. (2009). Virus-host coevolution: common patterns of nucleotide motif usage in Flaviviridae and their hosts. PLoS ONE 4: e6282.
31. Lovell, S.C., and Robertson, D.L. (2010). An integrated view of molecular coevolution in protein-protein interactions. Mol. Biol. Evol. 27: 2567-2575.
32. Marchler-Bauer, A., et al. (2013). CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 41: D348-D352.
33. Mintseris, J., and Weng, Z. (2005). Structure, function, and evolution of transient and obligate protein-protein interactions. Proc. Natl. Acad. Sci. USA 102: 10930-10935.
34. Neher, E. (1994). How frequent are correlated changes in families of protein sequences? Proc. Natl. Acad. Sci. USA 91: 98-102.
35. Osada, N., and Akashi, H. (2012). Mitochondrial-nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome C oxidase complex. Mol. Biol. Evol. 29: 337-346.
36. Pazos, F., Helmer-Citterich, M., Ausiello, G., and Valencia, A. (1997). Correlated mutations contain information about proteinprotein interaction. J. Mol. Biol. 271: 511-523.
37. Pazos, F., Ranea, J.A.G., Juan, D., and Sternberg, M.J.E. (2005). Assessing protein co-evolution in the context of the tree of life assists in the prediction of the interactome. J. Mol. Biol. 352: 1002-1015.
38. Pazos, F., and Valencia, A. (2008). Protein co-evolution, co-adaptation and interactions. EMBO J. 27: 2648-2655.
39. Pazos, F., and Valencia, A. (2001). Similarity of phylogenetic trees as indicator of protein-protein interaction. Protein Eng. 14: 609-614.
40. Pond, S.L.K., Frost, S.D.W., and Muse, S.V. (2005). HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
41. Rao, V.S., Srinivas, K., Sujini, G.N., and Kumar, G.N.S. (2014). Protein-protein interaction detection: methods and analysis. Int. J. Proteomics 2014: 147-648.
42. Ruckle, M.E., DeMarco, S.M., and Larkin, R.M. (2007). Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19: 3944-3960.
43. Sato, T., Yamanishi, Y., Kanehisa, M., and Toh, H. (2005). The inference of protein-protein interactions by co-evolutionary analysis is improved by excluding the information about the phylogenetic relationships. Bioinformatics 21: 3482-3489.
44. Schmitz-Linneweber, C., Kushnir, S., Babiychuk, E., Poltnigg, P., Herrmann, R.G., and Maier, R.M. (2005). Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase a-subunit mRNA. Plant Cell 17: 1815-1828.
45. Shiina, T., Tsunoyama, Y., Nakahira, Y., and Khan, M.S. (2005). Plastid RNA polymerases, promoters, and transcription regulators in higher plants. Int. Rev. Cytol. 244: 1-68.
46. Sloan, D.B., Triant, D.A., Wu, M., and Taylor, D.R. (2014). Cytonuclear interactions and relaxed selection accelerate sequence evolution in organelle ribosomes. Mol. Biol. Evol. 31: 673-682.
47. Smith, L. (1915). Variegation in Pelargonium. Proc. R. Hortic. Soc. 41: 36.
48. Sobolev, V., Eyal, E., Gerzon, S., Potapov, V., Babor, M., Prilusky, J., and Edelman, M. (2005). SPACE: a suite of tools for protein structure prediction and analysis based on complementarity and environment. Nucleic Acids Res. 33: W39-W43.
49. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
50. Subramanian, S., and Kumar, S. (2004). Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168: 373-381.
51. Tan, S., and Troxler, R.F. (1999). Characterization of two chloroplast RNA polymerase sigma factors from Zea mays: photoregulation and differential expression. Proc. Natl. Acad. Sci. USA 96: 5316-5321.
52. Taylor, W.R., and Hatrick, K. (1994). Compensating changes in protein multiple sequence alignments. Protein Eng. 7: 341-348.
53. Touloumenidou, T., Bakker, F.T., and Albers, F. (2007). The phylogeny of Monsonia L. (Geraniaceae). Plant Syst. Evol. 264: 1-14.
54. Weihe, A., Apitz, J., Pohlheim, F., Salinas-Hartwig, A., and Börner, T. (2009). Biparental inheritance of plastidial and mitochondrial DNA and hybrid variegation in Pelargonium. Mol. Genet. Genomics 282: 587-593.
55. Weng, M.-L., Blazier, J.C., Govindu, M., and Jansen, R.K. (2014). Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Mol. Biol. Evol. 31: 645-659.
56. Weng, M.-L., Ruhlman, T.A., Gibby, M., and Jansen, R.K. (2012). Phylogeny, rate variation, and genome size evolution of Pelargonium (Geraniaceae). Mol. Phylogenet. Evol. 64: 654-670.
57. Widler-Kiefer, H., and Yeo, P.F. (1987). Fertility relationships of Geranium (Geraniaceae): sect. Ruberta, Anemonifolia, Lucida and Unguiculata. Plant Syst. Evol. 155: 283-306.
58. Willett, C.S., and Burton, R.S. (2004). Evolution of interacting proteins in the mitochondrial electron transport system in a marine copepod. Mol. Biol. Evol. 21: 443-453.
59. Wolfe, K.H., Li, W.H., and Sharp, P.M. (1987). Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84: 9054-9058.
60. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586-1591.
61. Yao, J.-L., and Cohen, D. (2000). Multiple gene control of plastomegenome incompatibility and plastid DNA inheritance in interspecific hybrids of Zantedeschia. Theor. Appl. Genet. 101: 400-406.
62. Yeang, C.-H., and Haussler, D. (2007). Detecting coevolution in and among protein domains. PLOS Comput. Biol. 3: e211.
63. Yu, S.-N., and Horn, W.H. (1988). Additional chromosome numbers in Pelargonium (Geraniaceae). Plant Syst. Evol. 159: 165-171.
64. Zhang, F., and Broughton, R.E. (2013). Mitochondrial-nuclear interactions: compensatory evolution or variable functional constraint among vertebrate oxidative phosphorylation genes? Genome Biol. Evol. 5: 1781-1791.
65. Zhang, J., Ruhlman, T.A., Mower, J.P., and Jansen, R.K. (2013). Comparative analyses of two Geraniaceae transcriptomes using next-generation sequencing. BMC Plant Biol. 13: 228.