Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication

BMC Biology

Volumn 8, Issue , 2010, Pages

  Rapp, Ryan A ^a   Haigler, Candace H ^b   Flagel, Lex ^a,d   Hovav, Ran H ^c   Udall, Joshua A ^e   Wendel, Jonathan F ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c VOLCANI CENTER   (Israel)

^d DUKE UNIVERSITY   (United States)

^e BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GOSSYPIUM HIRSUTUM; GOSSYPIUM THURBERI;

ARTICLE; BIOLOGICAL MODEL; BREEDING; COTTON; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC SELECTION; GENETICS; METABOLISM; METHODOLOGY;

BREEDING; COTTON FIBER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GOSSYPIUM; MODELS, BIOLOGICAL; SELECTION, GENETIC;

EID: 78149432467     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-8-139     Document Type: Article

References (86)

1. Wendel JF, Cronn RC. Polyploidy and the evolutionary history of cotton. Advances in Agronomy 2003, 78:139-186.
2. Brubaker C, Wendel J. Reevaluating the origin of domesticated cotton (Gossypium hirsutum; Malvaceae) using nuclear restriction fragment length polymorphisms (RFLPs). Am J Botany 1994, 81:1309-1326.
3. Brubaker CL, Bourland FM, Wendel JF. The origin and domestication of cotton. Cotton; Origin, History, Technology and Production 1999, 3-31. New York: John Wiley and Sons, Smith C, Cothren J.
4. Wendel JF, Brubaker CL, Percival AE. Genetic diversity in Gossypium hirsutum and the origin of Upland cotton. Am J Botany 1992, 79:1291-1310.
5. Applequist WL, Cronn RC, Wendel JF. Comparative development of fiber in wild and cultivated cotton. Evol Devel 2001, 3:3-17.
6. Fryxell PA. The Natural History of The Cotton Tribe 1979, Texas: Texas A and M University Press.
7. Hutchinson JB. Intra-specific differentiation in Gossypium hirsutum. Heredity 1951, 5:161-193.
8. Cubas P, Lauter N, Doebley J, Coen E. The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 1999, 18(2):215-222. 10.1046/j.1365-313X.1999.00444.x, 10363373.
9. Burger JC, Chapman MA, Burke JM. Molecular insights into the evolution of crop plants. Am J Botany 2008, 95(2):113-122.
10. Burke JM, Burger JC, Chapman MA. Crop evolution: from genetics to genomics. Cur Opin Genet Devel 2007, 17(6):525-532.
11. Doebley JF, Gaut BS, Smith BD. The molecular genetics of crop domestication. Cell 2006, 127(7):1309-1321. 10.1016/j.cell.2006.12.006, 17190597.
12. Sweeney MT, Thomson MJ, Pfeil BE, McCouch S. Caught red-Handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 2006, 18(2):283-294. 10.1105/tpc.105.038430, 1356539, 16399804.
13. Clark RM, Wagler TN, Quijada P, Doebley JF. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nature Genetics 2006, 38:594-597. 10.1038/ng1784, 16642024.
14. Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF. The origin of the naked grains of maize. Nature 2005, 436:714-719. 10.1038/nature03863, 1464477, 16079849.
15. Dreher KA, Brown J, Saw RE, Callis J. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 2006, 18(3):699-714. 10.1105/tpc.105.039172, 1383644, 16489122.
16. Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu JP, Meller J, Elbert R, Alpert KB, Tanksley SD. fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 2000, 289(5476):85-88. 10.1126/science.289.5476.85, 10884229.
17. Chaudhary B, Hovav R, Flagel L, Mittler R, Wendel JF. Parallel expression evolution of oxidative stress-related genes in fiber from wild and domesticated diploid and polyploid cotton (Gossypium). BMC Genomics 2009, 10:378. 10.1186/1471-2164-10-378, 2907704, 19686594.
18. Hovav R, Udall JA, Hovav E, Rapp R, Flagel L. A majority of cotton genes are expressed in single-celled fiber. Planta 2008, 227:319-29. 10.1007/s00425-007-0619-7, 17849148.
19. Hovav R, Udall JA, Chaudhary B, Hovav E, Flagel L, Hu G, Wendel J. The evolution of spinable cotton fiber entailed natural selection for prolonged development and a novel metabolism. PLoS Genetics 2008, 4(2):e25. 10.1371/journal.pgen.0040025, 2222923, 18248099.
20. Chaudhary B, Hovav R, Rapp RA, Verma N, Udall JA, Wendel JF. Global analysis of gene expression in cotton fibers from wild and domesticated (Gossypium barbadense). Evol Devel 2008, 10(5):567-582.
21. Arpat AB, Waugh M, Sullivan JP, Gonzales M, Frisch D, Main D, Wood T, Leslie A, Wing RA, Wilkins TA. Functional genomics of cell elongation in developing cotton fibers. Plant Molec Biol 2004, 54(6):911-929.
22. Wilkins TA, Arpat AB. The cotton fiber transcriptome. Physiologia Plantarum 2005, 124:295-300.
23. Laan M, Pollard KS, Bryan J. A new partitioning around medoids algorithm. J Stat Comp Sim 2003, 73(8):575-584.
24. Tiwari SC, Wilkins TA. Cotton (Gossypium hirsutum) seed trichomes expand via a diffuse growing mechanism. Can J Botany 1995, 73(55):746-757.
25. Kim HJ, Triplett BA. Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiology 2001, 127(4):1361-1366. 10.1104/pp.010724, 1540163, 11743074.
26. Betancur L, Singh B, Rapp RA, Wendel JF, Marks MD, Roberts AW, Haigler CH. Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber. J Integrative Plant Biol 2010, 52:205-220.
27. Wang RL, Stec A, Hey J, Lukens L, Doebley JF. The limits of selection during maize domestication. Nature 1999, 398:236-239. 10.1038/18435, 10094045.
28. Stupar RM, Springer NM. Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 2006, 173(4):2199-2210. 10.1534/genetics.106.060699, 1569691, 16702414.
29. Lai Z, Kane NC, Zou Y, Rieseberg LH. Natural variation in gene expression between wild and weedy populations of Helianthus annuus. Genetics 2008, 179(4):1881-1890. 10.1534/genetics.108.091041, 2516066, 18689879.
30. Hegarty MJ, Barker GL, Brennan AC, Edwards KJ, Abbott RJ, Hiscock SJ. Extreme changes to gene expression associated with homoploid hybrid speciation. Molec Ecol 2009, 18(5):877-889.
31. Chelaifa H, Monnier A, Ainouche M. Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina × townsendii and Spartina anglica (Poaceae). New Phytol 2010, 186(1):161-174. 10.1111/j.1469-8137.2010.03179.x, 20149114.
32. Voelckel C, Heenan PB, Janssen B, Reichelt M, Ford K, Hofmann R, Lockhart PJ. Transcriptional and biochemical signatures of divergence in natural populations of two species of New Zealand alpine Pachycladon. Molec Ecol 2008, 17(21):4740-4753.
33. Demura T, Ye Z-H. Regulation of plant biomass production. Cur Opin Plant Biol 2010, 13:299-304.
34. Zhong R, Lee C, Ye Z-H. Evolutionary conservation of the transcriptional network regulating secondary wall biosynthesis. Trends Plant Sci 2010,
35. Haigler C, Singh B, Wang G, Zhang D. Genomics of cotton fiber secondary wall deposition and cellulose biogenesis. Genetics and Genomics of Cotton, Plant Genetics and Genomics: Crops and Models 3 2009, 385-417. New York: Springer, Patterson AH.
36. Paradez A, Wright A, Ehrhardt DW. Microtublule cortical array organization and plant cell morphogenesis. Cur Opin Plant Biol 2006, 9(6):571-578.
37. Zonia L, Munnik T. Life under pressure: hydrostatic pressure in cell growth and function. Trends Plant Sci 2007, 12(3):90-97. 10.1016/j.tplants.2007.01.006, 17293155.
38. Vidali L, Augustine RC, Kleinman KP, Bezanilla M. Profilin is essential for tip growth in the moss Physcomitrella patens. Plant Cell 2007, 19(11):3705-3722. 10.1105/tpc.107.053413, 2174871, 17981997.
39. Hussey PJ, Ketelaar T, Deeks M. Control of the actin cytoskeleton in plant cell growth. Ann Rev Plant Cell Biol 2006, 57:109-125.
40. Wang HY, Yu Y, Chen ZL, Xia GX. Functional characterization of Gossypium hirsutum profilin 1 gene (GhPFN1) in tobacco suspension cells. Characterization of in vivo functions of a cotton profilin gene. Planta 2005, 222(4):594-603. 10.1007/s00425-005-0005-2, 16001260.
41. Wang J, Wang HY, Zhao PM, Han LB, Jiao GL, Zheng YY, Huang SJ, Xia GX. Overexpression of a profilin (GhPFN2) promotes the progression of developmental phases in cotton fibers. Plant Cell Physiol 2010, 51(8):1276-1290. 10.1093/pcp/pcq086, 20558432.
42. Sullivan KF. Structure and utilization of tubulin isotypes. Ann Rev Cell Biol 1988, 4:687-716.
43. Meinert MC, Delmer DP. Changes in biochemical composition of the cell wall of the cotton fiber during development. Plant Physiol 1977, 59(6):1088-1097. 10.1104/pp.59.6.1088, 542513, 16660000.
44. Rose JK, Braam J, Fry SC, Nishitani K. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 2002, 43(12):1421-1435. 10.1093/pcp/pcf171, 12514239.
45. Singh B, Avci U, Eichler Inwood SE, Grimson MJ, Landgraf J, Mohnen D, Sorensen I, Wilkerson CG, Willats WG, Haigler CH. A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiol 2009, 150:684-699. 10.1104/pp.109.135459, 2689960, 19369592.
46. Singh B, Cheek HD, Haigler CH. A synthetic auxin (NAA) suppresses secondary wall cellulose synthesis and enhances elongation in cultured cotton fiber. Plant Cell Reporter 2009, 28(7):1023-1032.
47. Takahashi N, Nakazawa M, Shibata K, Yokota T, Ishikawa A, Suzuki K, Kawashima M, Ichikawa T, Shimada H, Matsui M. shk1-D, a dwarf Arabidopsis mutant caused by activation of the CYP72C1 gene, has altered brassinosteroid levels. Plant J 2005, 42:13-22. 10.1111/j.1365-313X.2005.02357.x, 15773850.
48. Thornton LE, Rupasinghe SG, Peng H, Schuler MA, Neff MM. Arabidopsis CYP72C1 is an atypical cytochrome P450 that inactivates brassinosteroids. Plant Molec Biol 2010, 74:167-181.
49. Sun Y, Veerabomma S, Abdel-Mageed HA, Fokar M, Asami T, Yoshida S, Allen RD. Brassinosteroid regulates fiber development on cultured cotton ovules. Plant Cell Physiol 2005, 46(8):1384-1391. 10.1093/pcp/pci150, 15958497.
50. Kurasawa K, Matsui A, Yokoyama R, Kuriyama T, Yoshizumi T, Matsui M, Suwabe K, Watanabe M, Nishitani K. The AtXTH28 gene, a xyloglucan endotransglucosylase/hydrolase, is involved in automatic self-pollination in Arabidopsis thaliana. Plant Cell Physiol 2009, 50(2):413-422. 10.1093/pcp/pcp003, 2642609, 19139039.
51. Miura K, Lee J, Miura T, Hasegawa PM. SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol 2010, 51(1):103-113. 10.1093/pcp/pcp171, 20007967.
52. Vasiliou V, Pappa A, Petersen DR. Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem-Biol Interact 2000, 129(1-2):1-19. 10.1016/S0009-2797(00)00211-8, 11154732.
53. Kotchoni SO, Kuhns C, Ditzer A, Kirch H, Bartels D. Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 2006, 29:1033-1048. 10.1111/j.1365-3040.2005.01458.x, 17080931.
54. Ishikawa T, Shigeoka S. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotech Bioch 2008, 72(5):1143-1154.
55. Narendra S, Venkataramani S, Shen GX, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H. The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 2006, 57(12):3033-3042. 10.1093/jxb/erl060, 16873450.
56. Edwards R, Dixona DP, Walbot V. Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 2000, 5(5):193-198. 10.1016/S1360-1385(00)01601-0, 10785664.
57. Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E, Schmidt UG. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 2006, 141(1):196-207. 10.1104/pp.106.079533, 1459324, 16581873.
58. Hoth S, Niedermeier M, Feuerstein A, Hornig J, Sauer N. An ABA-responsive element in the AtSUC1 promoter is involved in the regulation of AtSUC1 expression. Planta 2010, 232(4):911-923. 10.1007/s00425-010-1228-4, 20635094.
59. Ruan Y-L, Llewellyn DJ, Furbank RT, Chourey PS. The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered patterns of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton. J Exp Bot 2005, 56(413):977-984. 10.1093/jxb/eri091, 15710635.
60. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE. The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 2003, 132(2):821-829. 10.1104/pp.103.021428, 167022, 12805612.
61. Mahalingam R, Shah N, Scrymgeour A, Fedoroff N. Temporal evolution of the Arabidopsis oxidative stress response. Plant Molec Biol 2005, 57(5):709-730.
62. Briat JF, Ravet K, Arnaud N, Duc C, Boucherez J, Touraine B, Cellier F, Gaymard F. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Botany 2010, 105(5):811-822.
63. Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F. Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 2009, 57(3):400-412. 10.1111/j.1365-313X.2008.03698.x, 18826427.
64. Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A. The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 1999, 119(3):849-858. 10.1104/pp.119.3.849, 32100, 10069824.
65. Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP. Carbon partitioning to cellulose synthesis. Plant Molec Biol 2001, 47(1-2):29-51.
66. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci 1995, 92(20):9353-9357. 10.1073/pnas.92.20.9353, 40983, 7568131.
67. Salnikov VV, Grimson MJ, Seagull RW, Haigler C. Localization of sucrose synthase and callose in freeze-substituted secondary-wall-stage cotton fibers. Protoplasma 2003, 221(3-4):175-184.
68. Bieniawska Z, Barratt DHP, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM. Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 2007, 49(5):810-828. 10.1111/j.1365-313X.2006.03011.x, 17257168.
69. Rook F, Corke F, Baier M, Holman R, May AG, Bevan MW. Impaired sucrose induction 1 encodes a conserved plant-specific protein that couples carbohydrate availability to gene expression and plant growth. Plant J 2006, 46(6):1045-1058. 10.1111/j.1365-313X.2006.02765.x, 16805736.
70. Moinuddin SGA, Jourdes M, Laskar DD, Ki C, Cardenas CL, Kim KW, Zhang D, Davin LB, Lewis NG. Insights into lignin primary structure and deconstruction from Arabidopsis thaliana COMT (caffeic acid O-methyl transferase) mutant Atomt1. Org Biomol Chem 2010, 8(17):3928-3946. 10.1039/c004817h, 20652169.
71. Fan L, Shi WJ, Hu WR, Hao XY, Wang DM, Yuan H, Yan HY. Molecular and biochemical evidence for phenylpropanoid synthesis and presence of wall-linked phenolics in cotton fibers. J Integ Plant Biol 2009, 51(7):626-637.
72. Tuttle J, Idris A, Brown J, Haigler C, Robertson D. Geminivirus-mediated gene silencing from cotton leaf crumple virus is enhanced by low temperature in Gossypium hirsutum. Plant Physiol 2008, 148:41-50. 10.1104/pp.108.123869, 2528111, 18621976.
73. Taliercio EW, Boykin D. Analysis of gene expression in cotton fiber initials. BMC Plant Biol 2007, 7:22-35. 10.1186/1471-2229-7-22, 1906782, 17506877.
74. Wilkins TA, Smart LB. Isolation of RNA from plant tissue. A Laboratory Guide to RNA: solation, Analysis and Synthesis 1996, 21-41. New York: Wiley-Liss, Krieg PA.
75. Udall JA, Swanson JM, Haller K, Rapp RA, Sparks ME, Hatfield J, Yu YS, Wu YR, Dowd C, Arpat AB, et al. A global assembly of cotton ESTs. Genome Res 2006, 16(3):441-450. 10.1101/gr.4602906, 1415220, 16478941.
76. Senchina DS, Alvarez I, Cronn RC, Liu B, Rong JK, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF. Rate variation among nuclear genes and the age of polyploidy in Gossypium. Molec Biol Evol 2003, 20(4):633-643. 10.1093/molbev/msg065, 12679546.
77. Flagel L, Udall J, Nettleton D, Wendel J. Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 2008, 6(1):16. 10.1186/1741-7007-6-16, 2330141, 18416842.
78. Flagel LE, Wendel JF. Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytologist 186, 1:184-193.
79. Hovav R, Chaudhary B, Udall JA, Flagel L, Wendel JF. Parallel domestication, convergent evolution and duplicated gene recruitment in allopolyploid cotton. Genetics 2008, 179(3):1725-1733. 10.1534/genetics.108.089656, 2475765, 18562666.
80. Hovav R, Udall JA, Chaudhary B, Rapp R, Flagel L, Wendel JF. Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant. Proc Natl Acad Sci 2008, 105(16):6191-6195. 10.1073/pnas.0711569105, 2329682, 18420816.
81. Velleman PF, Hoaglin DC. The ABCs of Exploratory Data Analysis 1981, California: Duxbury Press.
82. Tukey JW. Exploratory Data Analysis 1977, Massachussetts: Addison-Wesley.
83. Team RDC R: A Language and Environment For Statistical Computing 2007, Vienna: R Foundation for Statistical Computing, Team RDC.
84. Littell RC, Milliken GA, Stroup WW, Wolfinger RD. SAS System For Mixed Models 1996, North Carolina: SAS Institute.
85. Storey JD, Tibshirani R. SAM thresholding and false discovery rates for detecting differential gene expression in DNA microarrays. The Analysis of Gene Expression Data: Methods and Software 2003, 272-290. New York: Springer, Parmigiani G, Garrett ES, Irizarry RA, Zeger SL.
86. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676. 10.1093/bioinformatics/bti610, 16081474.