Molecular evolution of the endosperm starch synthesis pathway genes in rice (Oryza sativa L.) and its wild ancestor, O. rufipogon L.

Molecular Biology and Evolution

Volumn 28, Issue 1, 2011, Pages 659-671

  Yu, Guoqin ^a,b   Olsen, Kenneth M ^a   Schaal, Barbara A ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

domestication; positive selection; rice; starch synthesis pathway

Indexed keywords

ADP GLUCOSE PYROPHOSPHORYLASE LARGE SUBUNIT 2; ADP GLUCOSE PYROPHOSPHORYLASE SMALL SUBUNIT 2B; GRANULE BOUND STARCH SYNTHASE 1; ISOAMYLASE; ISOAMYLASE 1; STARCH; STARCH BRANCHING ENZYME 2B; STARCH PHOSPHORYLASE; STARCH SYNTHASE; STARCH SYNTHASE 2A; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DEMOGRAPHY; DOMESTICATION; ENDOSPERM; GENE SEQUENCE; GENE SYNTHESIS; GENETIC SELECTION; GRAIN; LAST COMMON ANCESTOR; METABOLIC PARAMETERS; MOLECULAR EVOLUTION; NONHUMAN; ORYZA RUFIPOGON; PROTEIN PURIFICATION; RICE; SEQUENCE TAGGED SITE; SIGNAL TRANSDUCTION; SPECIES CULTIVATION; SPECIES DIVERSITY; WILD TYPE;

BASE SEQUENCE; CROPS, AGRICULTURAL; ENDOSPERM; EVOLUTION, MOLECULAR; GENES, PLANT; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; SELECTION, GENETIC; STARCH;

JAPONICA; ORYZA SATIVA;

EID: 78650464345     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq243     Document Type: Article

References (70)

1. Andolfatto P. 2008. Controlling type-I error of the McDonald-Kreitman test in genome wide scans for selection on noncoding DNA. Genetics 180:1767-1771.
2. Atkinson DE. 1977. Cellular energy metabolism and its regulation. New York: Academic Press.
3. Bhave MR, Lawrence S, Barton C, Hannah LC. 1990. Identification and molecular characterization of shrunken-2 cDNA clones of maize. Plant Cell. 2:581-588.
4. Briggs WH, Goldman IL. 2006. Genetic variation and selection response in model breeding populations of Brassica rapa following a diversity bottleneck. Genetics 172:457-465.
5. Buléon A, Colonna P, Planchot V, Ball S. 1998. Starch granules: structure and biosynthesis. Int J Biol Macromol. 23:85-112.
6. Bureau TE, Wessler SR. 1994. Stowaway: a new family of inverted repeat elements associated with the genes of both mono-cotyledonous and dicotyledonous plants. Plant Cell. 6:907-916.
7. Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL. 2002. The cost of inbreeding in Arabidopsis. Nature 416:531-534.
8. Caicedo A, Williamson S, Hernandez RD, et al. (12 co-authors). 2007. Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 3:e163.
9. Campbell SL, Khosravi-Far R, Rossman KL, Clark GJ, Der CJ. 1998. Increasing complexity of Ras signaling. Oncogene 17:1395-1413.
10. Clegg MT. 1997. Plant genetic diversity and the struggle to measure selection. J Hered. 88:1-7.
11. Collado-Vides J, Hofestadt R. 2002. Gene regulation and metabolism: post-genomic computational approaches. Cambridge: MIT Press.
12. Crabtree B, Newsholme EA. 1987. The deviation and interpretation of control coefficient. J Biochem. 247:113-120.
13. Doyle JJ, Doyle JL. 1990. Isolation of plant DNA from fresh tissue. Focus. 12:13-15.
14. Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online. 1:47-50.
15. Eyre-Walker A, Gaut RL, Hilton H, Feldman DL, Gaut BS. 1998. Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci USA. 95:4441-4446.
16. Fay JC, Wu CI. 2000. Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413.
17. Frances H, Bligh H, Larkin PD, Roach PS, Jones CA, Fu HY, Park WD. 1998. Use of alternate splice sites in granule-bound starch synthase mRNA from low-amylose rice varieties. Plant Mol.Biol. 38:407-415.
18. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW. 2002. Evolutionary rate in the protein interaction network. Science 296:750.
19. Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
20. Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S. 2005. Genetic structure and diversity in Oryza sativa L. Genetics 169:1631-1638.
21. Georgelis N, Braun EL, Hannah LC. 2008. Duplications and functional divergence of ADP-glucose pyrophosphorylase genes in plants. BMC Evol Biol. 8:232.
22. Giroux M, Smithwhite B, Gilmore V, Hannah LC, Preiss J. 1995. The large subunit of the embryo isoform of Adp glucose pyrophosphorylase from maize. Plant Physiol. 108:1333-1334.
23. Hahn MW, Kern AD. 2005. Comparative genomics of centrality and essentiality in three eukaryotic protein-interaction networks. Mol Biol Evol. 22:803-806.
24. Haudry A, Cenci A, Ravel C, et al. (11 co-authors). 2007. Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol. 24:1506-1517.
25. Hirano HY, Eiguchi M, Sano Y. 1998. A single base change altered the regulation of the waxy gene at the posttranscriptional level during the domestication of rice. Mol Biol Evol. 15:978-987.
26. Hudson RR. 2001. Two-locus sampling distributions and their application. Genetics 159:1805-1817.
27. Hudson RR, Kaplan NL. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA-sequences. Genetics 111:147-164.
28. Hudson RR, Kreitman M, Aguade M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
29. Hyten DL, Song QJ, Zhu YL, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB. 2006. Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA. 103:16666-16671.
30. James MG, Denyer K, Myers AM. 2003. Starch synthesis in the cereal endosperm. Curr Opin Plant Biol. 6:215-222.
31. Kavar T, Dovc P. 2008. Domestication of the horse: genetic relationships between domestic and wild horses. Livest Sci. 116:1-14.
32. Khush GS. 1997. Origin, dispersal, cultivation and variation of rice. Plant Mol Biol. 35:25-34.
33. Kim Y, Nielsen R. 2004. Linkage disequilibrium as a signature of selective sweeps. Genetics 167:1513-1524.
34. Koga A, Iida A, Hori H, Shimada A, Shima A. 2006. Vertebrate DNA transposon as a natural mutator: the medaka fish Tol2 element contributes to genetic variation without recognizable traces. Mol Biol Evol. 23:1414-1419.
35. Lee SK, Hwang SK, Han M, et al. (13 co-authors). 2007. Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol. 65:531-546.
36. Li HP, Stephan W. 2005. Maximum-likelihood methods for detecting recent positive selection and localizing the selected site in the genome. Genetics 171:377-384.
37. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
38. Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA. 2006. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci USA. 103:9578-9583.
39. Manicacci D, Falque M, Le Guillou S, Piegu B, Henry AM, Le Guilloux M, Damerval C, De Vienne D. 2007. Maize Sh2 gene is constrained by natural selection but escaped domestication. J Evol Biol. 20:503-516.
40. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
41. McVean G, Awadalla P, Fearnhead P. 2002. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231-1241.
42. Miller AJ, Schaal BA. 2006. Domestication and the distribution of genetic variation in wild and cultivated populations of the Mesoamerican fruit tree Spondias purpurea L. (Anacardiaceae). Mol Ecol. 15:1467-1480.
43. Myers AM, Morell MK, James MG, Ball SG. 2000. Recent progress toward understanding biosynthesis of the amylopectin crystal. J Plant Physiol. 122:989-997.
44. Nakamura Y. 1996. Some properties of starch debranching enzymes and their possible role in amylopectin biosynthesis. Plant Sci. 121:1-18.
45. Nakamura Y, Francisco PB, Hosaka Y, Sato A, Sawada T, Kubo A, Fujita N. 2005. Essential amino acids of starch synthase IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Mol Biol. 58:213-227.
46. Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan MD. 2006. Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173: 975-983.
47. Olsen KM, Purugganan MD. 2002. Molecular evidence on the origin and evolution of glutinous rice. Genetics 162:941-950.
48. Pan D, Nelson OE. 1984. A debranching enzyme efficiency in endosperms of the sugray-1 mutants of maize. Plant Physiol. 74:324-328.
49. Ramos-Onsins SE, Puerma E, Balana-Alcaide D, Salguero D, Aguade M. 2008. Multilocus analysis of variation using a large empirical data set: phenylpropanoid pathway genes in Arabi-dopsis thaliana. Mol Ecol. 17:1211-1223.
50. Rand DM, Kann LM. 1996. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol. 13:735-748.
51. Rausher MD, Miller RE, Tiffin P. 1999. Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway. Mol Biol Evol. 16:266-274.
52. Rozas J, Sànchez-DelBarrio JC, Messequer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497.
53. Sabeti PC, Reich DE, Higgins JM, et al. (17 co-authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837.
54. Sano Y. 1984. Differential regulation of waxy gene expression in rice endosperm. Theor Appl Genet. 68:467-473.
55. Smidansky ED, Martin JM, Hannah LC, Fischer AM, Giroux MJ. 2003. Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta 216:656-664.
56. Sokal RR, Rohlf FJ. 1995. Biometry: the principles and practice of statistics in biological research, 3rd ed. New York: W.H. Freeman and Co.
57. Souames SM, Bonnivard E, Bazin C, Higuet D. 2003. High mutation rate of TPE repeats: a microsatellite in the putative transposase of the hobo element in Drosophila melanogaster. Mol Biol Evol. 20:1826-1832.
58. Tajima F. 1983. Evolutionary relationship of DNA-sequences in finite populations. Genetics 105:437-460.
59. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
60. Tanaka N, Fujita N, Nishi A, Satoh H, Hosaka Y, Ugaki M, Kawasaki S, Nakamura Y. 2004. The structure of starch can be manipulated by changing the expression levels of starch branching enzyme llb in rice endosperm. Plant Biotech J. 2:507-516.
61. Umeda M, Ohtsubo H, Ohtsubo E. 1991. Diversification of the rice waxy gene by insertion of mobile DNA elements into introns. Jpn J Genet. 66:569-586.
62. Umemoto T, Yano M, Satoh H, Shomura A, Nakamura Y. 2002. Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor Appl Genet. 104:1-8.
63. Wang ZY, Zheng FQ, Shen GZ, Gao JP, Snustad DP, Li MG, Zhang JL, Hong MM. 1995. The amylose content in rice endosperm is related to the posttranscriptional regulation of the waxy gene. Plant J. 7:613-622.
64. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276.
65. Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES. 2002. Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA. 99:12959-12962.
66. Wong WSW, Nielsen R. 2004. Detecting selection in noncoding regions of nucleotide sequences. Genetics 167:949-958.
67. Wright SI, Charlesworth B. 2004. The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168:1071-1076.
68. Wright SI, Gaut BS. 2005. Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol. 22: 506-519.
69. Zhang ZC, Zhang SF, Yang JC, Zhang JH. 2008. Yield, grain quality and water use efficiency of rice under non-flooded mulching cultivation. Field Crops Res. 108:71-81.
70. Zhu Q, Zheng X, Luo J, Gaut BS, Ge S. 2007. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol Biol Evol. 24:875-888.