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Plant Molecular Biology

, Volume 48, Issue 5–6, pp 805–820 | Cite as

Phylogenetic analysis of the acetyl-CoA carboxylase and 3-phosphoglycerate kinase loci in wheat and other grasses

  • Shaoxing Huang
  • Anchalee Sirikhachornkit
  • Justin D. Faris
  • Xiujuan Su
  • Bikram S. Gill
  • Robert Haselkorn
  • Piotr Gornicki
Article

Abstract

We have applied a two-gene system based on the sequences of nuclear genes encoding multi-domain plastid acetyl-CoA carboxylase (ACCase) and plastid 3-phosphoglycerate kinase (PGK) to study grass evolution. Our analysis revealed that these genes are single-copy in most of the grass species studied, allowing the establishment of orthologous relationships between them. These relationships are consistent with the known facts of their evolution: the eukaryotic origin of the plastid ACCase, created by duplication of a gene encoding the cytosolic multi-domain ACCase gene early in grass evolution, and the prokaryotic (endosymbiont) origin of the plastid PGK. The major phylogenetic relationships among grasses deduced from the nucleotide sequence comparisons of ACCase and PGK genes are consistent with each other and with the milestones of grass evolution revealed by other methods. Nucleotide substitution rates were calculated based on multiple pairwise sequence comparisons. On a relative basis, with the divergence of the Pooideae and Panicoideae subfamilies set at 60 million years ago (MYA), events leading to the Triticum/Aegilops complex occurred at the following intervals: divergence of Lolium (Lolium rigidum) at 35 MYA, divergence of Hordeum (Hordeum vulgare) at 11 MYA and divergence of Secale (Secale cereale) at 7 MYA. On the same scale, gene duplication leading to the multi-domain plastid ACCase in grasses occurred at 129 MYA, divergence of grass and dicot plastid PGK genes at 137 MYA, and divergence of grass and dicot cytosolic PGK genes at 155 MYA. The ACCase and PGK genes provide a well-understood two-locus system to study grass phylogeny, evolution and systematics.

evolution gene sequence grass plant Poaceae Pooideae Triticeae 

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References

  1. Barker, N.P. and Linder, H.P. 1995. Polyphyly of Arundinoideae (Poaceae): evidence from rbcL sequence data. Syst. Bot. 20: 423-435.Google Scholar
  2. Bennetzen, J.L. and Kellogg, E.A. 1997. Do plants have a one-way ticket to genomic obesity? Plant Cell 9: 1509-1514.Google Scholar
  3. Catalan, P., Kellogg, E.A. and Olmsted, R.G. 1997. Phylogeny of Poaceae subfamily Pooideae based on chloroplast ndhF gene sequence. Mol. Phylogenet. Evol. 8; 150-166.Google Scholar
  4. Chen, M., SanMiguel, P., DeOliveira, A.C., Woo, S.-S., Zhang, H., Wing, R.A. and Bennetzen, J.L. 1998. Microcolinearity in sh2-homologous regions of maize, rice and sorghum genomes. Proc. Natl. Acad. Sci. USA 95: 3431-3435.Google Scholar
  5. Christopher, J.T. and Holtum, J.A.M. 2000. Dicotyledons lacking the multisubunit form of the herbicide-target enzyme acetyl coenzyme A carboxylase may be restricted to the family Geraniaceae. Aust. J. Plant Physiol. 27: 845-850.Google Scholar
  6. Clark, L.G., Kobayashi, M., Mathews, S., Spangler, R.E. and Kellog, E.A. 2000. The Puelioideae, a new subfamily of Poaceae. Syst. Bot. 25: 181-187.Google Scholar
  7. Clark, L.G., Zhang, W. and Wendel, J.F. 1995. A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Syst. Bot. 20: 436-460.Google Scholar
  8. Clegg, M.T. 1997. Plant genetic diversity and the struggle to measure selection. J. Hered. 88: 1-7.Google Scholar
  9. Clegg, M.T., Cummings, M.P. and Durbin, M.L. 1997. The evolution of plant nuclear genes. Proc. Natl. Acad. Sci. USA 94: 7791-7798.Google Scholar
  10. Cox, T.S. 1998. Deepening the wheat gene pool. J. Crop Prod. 1: 1-25.Google Scholar
  11. Crepet, W.L. and Feldman, G.D. 1991. The earliest remains of grasses in the fossil record. Am. J. Bot. 78: 1010-1-14.Google Scholar
  12. Cummings, M.P. and Clegg, M.T. 1998. Nucleotide sequence diversity at the alcohol dehydrogenase 1 locus in wild barley (Hordeum vulgare ssp. spontaneum): an evaluation of the background selection hypothesis. Proc. Natl. Acad. Sci. USA 95: 5637-5642.Google Scholar
  13. Devos, K.M. and Gale, M.D. 1997. Comparative genetics in the grasses. Plant Mol. Biol. 35: 3-15.Google Scholar
  14. Doyle, J.J. and Gaut, B.S. 2000. Evolution of genes and taxa: a primer. Plant Mol. Biol. 42: 1-23.Google Scholar
  15. Dvorak, J. 1998. Genome analysis in the Triticum-Aegilops alliance. Cytogenet. Evol. 1: 8-11.Google Scholar
  16. Dvorak, J., DiTerlizzi, P., Zhang, H.-B. and Resta, P. 1993. The evolution of polyploid wheats: identification of the A genome donor species. Genome 36: 21-31.Google Scholar
  17. Dvorak, J., Luo, M.-C., Yang, Z.-L. and Zhang, H.-B. 1998. The structure of the Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor. Appl. Genet. 97: 657-670.Google Scholar
  18. Dvorak, J. and Zhang, H.B. 1990. Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes. Proc. Natl. Acad. Sci. USA 87: 9640-9644.Google Scholar
  19. Eyre-Walker, A., Gaut, R.L., Hilton, H., Feldman, D.L. and Gaut, B.S. 1998. Investigation of the bottleneck leading to the domestication of maize. Proc. Natl. Acad. Sci. USA 95: 4441-1116.Google Scholar
  20. Faris, J., Sirikhachornkit, A., Haselkorn, R., Gill, B. and Gornicki, P. 2001. Chromosome mapping and phylogenetic analysis of the cytosolic acetyl-CoA carboxylase loci in wheat. Mol. Biol. Evol. 18, 1720-1733.Google Scholar
  21. Faris, J.D., Haen, K.M. and Gill, B.S. 2000. Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics 154: 823-835.Google Scholar
  22. Gandolfo, M.A., Nixon, K.C., Crepet, W.L., Stevenson, D.W. and Friss, E.M. 1998. Oldest known fossils of monocotyledons. Nature 394: 532-533.Google Scholar
  23. Gaut, B.S. 1998. Molecular clocks and nucleotide substitution rates in higher plants. Evol. Biol. 30: 93-120.Google Scholar
  24. Gaut, B.S., Clark, L.G., Wendel, J.F. and Muse, S.V. 1997. Comprison of the molecular evolutionary process at rbcL and ndhF in the grass family (Poaceae). Mol. Biol. Evol. 14: 769-777.Google Scholar
  25. Gaut, B.S. and Doebley, J.F. 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. USA 94: 6809-6814.Google Scholar
  26. Gaut, B.S., Morton, B.R., McCaig, B.C. and Clegg, M.T. 1996. Substitution rate comparison between grasses and palms: synonymous rate difference at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl. Acad. Sci. USA 93: 10274-10278.Google Scholar
  27. Gaut, B.S., Tredway, L.P., Kubik, C., Gaut, R.L. and Meyer, W. 2000. Phylogenetic relationship and genetic diversity among members of the Festuca-Lolium complex (Poaceae) based on ITS sequence data. Plant Syst. Evol. 224: 33-53.Google Scholar
  28. Gimenez-Espinosa, R., Plaisance, K.L., Plank, D.W., Gronwald, J.W. and De Prado, R. 1999. Propaquizafop absorption, translocation, metabolism and effect on acetyl-CoA carboxylase isoforms in chickpea (Cicer arietinum L.). Pestic. Biochem. Physiol. 65: 140-150.Google Scholar
  29. Gornicki, P., Fans, J., King, I., Podkowinski, J., Gill, B. and Haselkorn, R. 1997. Plastid-localized acetyl-CoA carboxylase of bread wheat is encoded by a single gene on each of the three ancestral chromosome sets. Proc. Natl. Acad. Sci. USA 94: 1417-14185.Google Scholar
  30. Gornicki, P., Podkowinski, J., Scappino, L.A., DiMaio, J., Ward, E. and Haselkorn, R. 1994. Wheat acetyl-CoA carboxylase: cDNA and protein structure. Proc. Natl. Acad. Sci. USA 91: 6860-6864.Google Scholar
  31. Hilton, H. and Gaut, B.S. 1998. Speciation and domestication in maize and its wild relatives: evidence from the Globulin-1 gene. Genetics 150: 863-872.Google Scholar
  32. Hsiao, C., Chatterton, N.J., Asay, K.H. and Jensen, KB. 1994. Phylogenetic relationships of 10 grass species: an assesment of phylogenetic utility of the internal transcribed spacer region in nuclear ribosomal DNA in monocots. Genome 37: 112-120.Google Scholar
  33. Hsiao, C., Chatterton, N.J., Asay, K.H. and Jensen, K.B. 1995. Molecular phylogeny of the Pooideae (Poaceae) based on nuclear rDNA (ITS) sequences. Theor. Appl. Genet. 90: 389-398.Google Scholar
  34. Hsiao, C., Jacobs, S.W.L., Barker, N.P. and Chatterton, N.J. 1998. A molecular phylogeny of the subfamily Arundinoideae (Poaceae) based on sequences of rDNA. Aust. Syst. Bot. 11: 41-52.Google Scholar
  35. Incledon, B.J. and Hall, J.C. 1997. Acetyl-coenzyme A carboxylase: quaternary structure and inhibition by graminicidal herbicides. Pestic. Biochem. Physiol. 57: 255-271.Google Scholar
  36. Kellog, E.A., Appels, R. and Mason-Gamer, R.J. 1996. When genes tell different stories: the diploid genera of Triticeae (Gramineae). Syst. Bot. 21: 321-347.Google Scholar
  37. Kellogg, E.A. 1998. Relationships of cereal crops and other grasses. Proc. Natl. Acad. Sci. USA 95: 2005-2010.Google Scholar
  38. Li, P. and Bousquet, J. 1992. Relative-rate test for nucleotide substitutions between two lineages. Mol. Biol. Evol. 9: 1185-1189.Google Scholar
  39. Martin, W. and Schnarrenberger, C. 1997. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32: 1-18.Google Scholar
  40. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegava, M. and Kowallik, K.V. 1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162-165.Google Scholar
  41. Mason-Gamer, R.J., Weil, C.F. and Kellog, E.A. 1998. Granulebound starch synthase: structure, function and phylogenetic utility. Mol. Biol. Evol. 15: 1658-1673.Google Scholar
  42. Mathews, S., Tsai, R.C. and Kellog, E.A. 2000. Phylogenetic structure in the grass family (Poaceae): evidence from the nuclear gene phytochrome B. Am. J. Bot. 87: 96-107.Google Scholar
  43. McFadden, E.S. and Sears, E.R. 1946. The origin of Triticum speltoides and its free-threshing hexaploid relatives. J. Hered. 37: 81-89.Google Scholar
  44. Muse, S.V. 2000. Examining rates and patterns of nucleotide substitutions in plants. Plant Mol. Biol. 42: 25-43.Google Scholar
  45. Muse, S.V. and Gaut, B.S. 1997. Comparing patterns of nucleotide substitution rates among chloroplast loci using the relative ratio test. Genetics 146: 393-399.Google Scholar
  46. Petersen, G. and Seberg, 0. 1997. Phylogenetic analysis of the Triticeae (Poaceae) based on rpoA sequence data. Mol. Phylog. Evol. 7: 217-230.Google Scholar
  47. Podkowinski, J., Sroga, G.E., Haselkorn, R. and Gornicki, P. 1996. Structure of a gene encoding a cytosolic acetyl-CoA carboxylase of hexaploid wheat. Proc. Natl. Acad. Sci. USA 93: 1870-1874.Google Scholar
  48. Pryer, K.M., Schneider, H., Smith, A.R., Cranfill, R., Wolf, P.G., Hunt, J.S. and Sipes, S.D. 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409: 618-622.Google Scholar
  49. SanMiguel, P., Gaut, B.S., Tikhonov, A., Nakajima, Y. and Bennetzen, J.L. 1999. The paleontology of intergene retrotransposons of maize. Nature Genet 20: 43-45.Google Scholar
  50. Sasaki, Y., Konishi, T. and Nagano, Y. 1995. The compartmentation of acetyl-coenzyme a carboxylase in plants. Plant Physiol. 108: 445-449.Google Scholar
  51. Schulte, W., Topfer, R., Stracke, R., Schell, J. and Martini, N. 1997. Multi-functional acetyl-CoA carboxylase from Brassica napus is encoded by a multi-gene family: indication for plastidic localization of at least one isoform. Proc. Natl. Acad. Sci. USA 94: 3465-3470.Google Scholar
  52. Soltis, E.D. and Soltis, P.S. 2000. Contributions of plant molecular systematics to studies of molecular evolution. Plant Mol. Biol. 42: 45-75.Google Scholar
  53. Soreng, R.J. and Davis, J.I. 1998. Phylogenetics and character evolution in the grass family (Poaceae): simultaneous analysis of morphological and chloroplast DNA restriction site data sets. Bot. Rev. 64: 1-85.Google Scholar
  54. Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673-4680.Google Scholar
  55. Tsunewaki, K. 1991. A historical review of cytoplasmic studies in wheat. In: T. Sasakuma and T. Kinoshita (Eds) Nuclear and Organelle Genomes of Wheat Species, Kihara Memorial Foundation, Yokohama) pp. 16-28.Google Scholar
  56. Wang, G.-Z., Miyashita, N.T. and Tsunewaki, K. 1997. Plasmon analyses of Triticum (wheat) and Aegilops: PCR-single-strand conformational polymorphism (PCR-SSCP) analyses of organellar DNAs. Proc. Natl. Acad. Sci. USA 94: 14570-14577.Google Scholar
  57. Wolfe, K.H., Gouy, M.L., Yang, Y.W., Sharp, P.M. and Li, W.H. 1989. Date of the monocot dicot divergence estimated from chloroplast DNA-sequence. Proc. Natl. Acad. Sci USA 86; 6201-6205.Google Scholar
  58. 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.Google Scholar
  59. Zhang, W.P. 2000. Phylogeny of the grass family (Poaceae) from rp116 intron sequence data. Mol. Phylogenet. Evol. 15: 135-146.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Shaoxing Huang
    • 1
  • Anchalee Sirikhachornkit
    • 1
  • Justin D. Faris
    • 2
  • Xiujuan Su
    • 1
  • Bikram S. Gill
    • 2
  • Robert Haselkorn
    • 1
  • Piotr Gornicki
    • 1
  1. 1.Department of Molecular Genetics and Cell BiologyUniversity of ChicagoChicagoUSA
  2. 2.Department of Plant PathologyKansas State UniversityManhattanUSA

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