Anatomical, biochemical, and photosynthetic responses to recent allopolyploidy in glycine dolichocarpa (fabaceae)

American Journal of Botany

Volumn 99, Issue 1, 2012, Pages 55-67

  Coate, Jeremy E ^a   Luciano, Amelia K ^b   Seralathan, Vasu ^a   Minchew, Kevin J ^c   Owens, Tom G ^a   Doyle, Jeff J ^a  

^a Department of Obstetrics Gynecology   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE AT CHATTANOOGA   (United States)

Author keywords

Allopolyploidy; Fabaceae; Glycine dolichocarpa; Glycine syndetika; Glycine tomentella; Photosynthesis

Indexed keywords

CHLOROPHYLL; PLANT DNA;

ANATOMY; GENOTYPE; INTRASPECIFIC VARIATION; LEGUME; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; POLYPLOIDY; RECOMBINATION;

ARTICLE; CELL COUNT; CELL SIZE; CHIMERA; CHLOROPLAST; CYTOLOGY; ELECTRON TRANSPORT; FABACEAE; GENETIC SELECTION; GENETICS; GENOME SIZE; MESOPHYLL CELL; METABOLISM; PHENOTYPE; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT EPIDERMIS; PLANT LEAF; POLYPLOIDY; SPECIES DIFFERENCE;

CELL COUNT; CELL SIZE; CHIMERA; CHLOROPHYLL; CHLOROPLASTS; DNA, PLANT; ELECTRON TRANSPORT; FABACEAE; GENOME SIZE; MESOPHYLL CELLS; PHENOTYPE; PHOTOSYNTHESIS; PLANT EPIDERMIS; PLANT LEAVES; POLYPLOIDY; SELECTION, GENETIC; SPECIES SPECIFICITY;

FABACEAE; GLYCINE (ANGIOSPERM); GLYCINE DOLICHOCARPA; GLYCINE TOMENTELLA;

EID: 84858408588     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100465     Document Type: Article

References (78)

1. ALBERTIN, W., T. BALLIAU, P. BRABANT, A. M. CHEVRE, F. EBER, C. MALOSSE, and H. THIELLEMENT. 2006. Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173: 1101-1113.
2. ARUMUGANATHAN, K., and E. EARLE. 1991. Estimation of nuclear DNA content of plants by flow cytometry. Plant Molecular Biology Reporter 9: 229-241.
3. BEAULIEU, J. M., I. J. LEITCH, S. PATEL, A. PENDHARKAR, and C. A. KNIGHT. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist 179: 975-986.
4. BENNETT, M. D. 1987. Variation in genomic form in plants and its ecological implications. New Phytologist 106: 177-200.
5. BLANC, G., and K. H. WOLFE. 2004. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667-1678.
6. BOWERS, J. E., B. A. CHAPMAN, J. K. RONG, and A. H. PATERSON. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
7. BROWN, R., and P. RICKLESS. 1949. A new method for the study of cell division and cell extension with some preliminary observations on the effect of temperature and of nutrients. Proceedings of the Royal Society of London. Series B. Biological Sciences 136: 110-125.
8. BYRNE, M. C., C. J. NELSON, and D. D. RANDALL. 1981. Ploidy effects on anatomy and gas exchange of tall fescue leaves. Plant Physiology 68: 891-893.
9. CANNON, S. B., L. STERCK, S. ROMBAUTS, S. SATO, F. CHEUNG, J. GOUZY, X. WANG, ET AL. 2006. Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proceedings of the National Academy of Sciences, USA 103: 14959-14964.
10. CUI, L. Y., P. K. WALL, J. H. LEEBENS-MACK, B. G. LINDSAY, D. E. SOLTIS, J. J. DOYLE, P. S. SOLTIS, et al. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Research 16: 738-749.
11. DOLEZEL, J., J. GREILHUBER, and J. SUDA. 2007. Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols 2: 2233-2244.
12. DOYLE, J. J., J. L. DOYLE, and A. H. D. BROWN. 1999. Origins, colonization, and lineage recombination in a widespread perennial soybean polyploid complex. Proceedings of the National Academy of Sciences, USA 96: 10741-10745.
13. DOYLE, J. J., J. L. DOYLE, A. H. D. BROWN, and J. P. GRACE. 1990a. Multiple origins of polyploids in the Glycine tabacina complex inferred from chloroplast DNA polymorphism. Proceedings of the National Academy of Sciences, USA 87: 714-717.
14. DOYLE, J. J., J. L. DOYLE, J. P. GRACE, and A. H. D. BROWN. 1990b. Reproductively isolated polyploid races of Glycine tabacina (Leguminosae) had different chloroplast genome donors. Systematic Botany 15: 173-181.
15. DOYLE, J. J., J. L. D OYLE, A. H. D. B ROWN, and R. G. P ALMER. 2002. Genomes, multiple origins, and lineage recombination in the Glycine tomentella (Leguminosae) polyploid complex: Histone H3-D gene sequences. Evolution 56: 1388-1402.
16. DOYLE, J. J., J. L. DOYLE, J. T. RAUSCHER, and A. H. D. BROWN. 2003. Diploid and polyploid reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine). New Phytologist 161: 121-132.
17. DOYLE, J. J., J. L. DOYLE, J. T. RAUSCHER, and A. H. D. BROWN. 2004. Evolution of the perennial soybean polyploid complex (Glycine subgenus Glycine): A study of contrasts. Biological Journal of the Linnean Society 82: 583-597.
18. DOYLE J. J., L. E. FLAGEL, A. H. PATERSON, R. A. RAPP, D. E. SOLTIS, P. S. SOLTIS, and J. F. WENDEL. 2008. Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics 42: 443-461.
19. DUNSTONE, R., and L. EVANS. 1974. Role of changes in cell size in the evolution of wheat. Functional Plant Biology 1: 157-165.
20. ELLIS, J. R., and R. M. LEECH. 1985. Cell size and chloroplast size in relation to chloroplast replication in light-grown wheat leaves. Planta 165: 120-125.
21. GARRETT, M. K. 1978. Control of photorespiration at RuBP carboxylase/oxygenase level in ryegrass cultivars. Nature 274: 913-915.
22. HARBUT, R. M., J. A. SULLIVAN, and J. T. A. PROCTOR. 2010. Temperature affects dry matter production and net carbon exchange rate of lowerploidy Fragaria species and species hybrids. Canadian Journal of Plant Science 90: 885-892.
23. HEGARTY, M. J., G. L. BARKER, I. D. WILSON, R. J. ABBOTT, K. J. EDWARDS, and S. J. HISCOCK. 2006. Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Current Biology 16: 1652-1659.
24. Hull-Sanders, H. M., R. H. JOHNSON, H. A. OWEN, and G. A. MEYER. 2009. Effects of polyploidy on secondary chemistry, physiology, and performance of native and invasive genotypes of Solidago gigantea (Asteraceae). American Journal of Botany 96: 762-770.
25. JELLINGS, A. J., and R. M. LEECH. 1984. Anatomical variation in first leaves of nine Triticum genotypes, and its relationship to photosynthetic capacity. New Phytologist 96: 371-382.
26. JIAO, Y., N. J. WICKETT, S. A YYAMPALAYAM, A. S. CHANDERBALI, L. LANDHERR, P. E. RALPH, L. P. TOMSHO, ET AL. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
27. KAMINSKI, A., R. B. AUSTIN, M. A. FORD, and C. L. MORGAN. 1990. Flag leaf anatomy of Triticum and Aegilops species in relation to photosynthetic rate. Annals of Botany 66: 359-365.
28. KONDOROSI, E., F. ROUDIER, and E. GENDREAU. 2000. Plant cell-size control: Growing by ploidy? Current Opinion in Plant Biology 3: 488-492.
29. KRUEGER, R. W., and D. MILES. 1981. Photosynthesis in fescue: III. Rates of electron transport in a polyploid series of tall fescue plants. Plant Physiology 68: 1110-1114.
30. KUDO, N., and Y. KIMURA. 2002. Nuclear DNA enduduplication during petal development in cabbage: Relationship between ploidy levels and cell size. Journal of Experimental Botany 53: 1017-1023.
31. LEITCH, I. J., and M. D. BENNETT. 2004. Genome downsizing in polyploid plants. Biological Journal of the Linnean Society 82: 651-663.
32. LEVIN, D. A. 2003. The cytoplasmic factor in plant speciation. Systematic Botany 28: 5-11.
33. LEWIS, W. H. 1980. Polyploidy in species populations. In W. H. Lewis [ed.], Polyploidy: Biological relevance, 103-144. Plenum, New York, New York, USA.
34. LICHTENTHALER, H. K. 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In L. Packer and R. Douce [ed.], Methods in enzymology, vol. 148, 350-382. Academic Press, Waltham, Massachusetts, USA.
35. MAPLE, J., and S. G. MØLLER. 2007. Plastid division: Evolution, mechanism and complexity. Annals of Botany 99: 565-579.
36. MAXWELL, K., and G. N. JOHNSON. 2000. Chlorophyll fluorescence - A practical guide. Journal of Experimental Botany 51: 659-668.
37. MEADOWS, M. G. 1984. A batch assay using Calcofluor fluorescence to characterize cell wall regeneration in plant protoplasts. Analytical Biochemistry 141: 38-42.
38. MEARS, J. A. 1980. Chemistry of polyploids: A summary with comments on parthenium (Asteraceae-Ambrosiineae). In W. H. Lewis [ed.], Polyploidy: Biological relevance, 77-101. Plenum, New York, New York, USA.
39. MEIMBERG, H., K. J. RICE, N. F. MILAN, C. C. NJOKU, and J. K. MCKAY. 2009. Multiple origins promote the ecological amplitude of allopolyploid Aegilops (Poaceae). American Journal of Botany 96: 1262-1273.
40. MEYERS, L., and D. LEVIN. 2006. On the abundance of polyploids in flowering plants. Evolution 60: 1198-1206.
41. MEYERS, S. P., W. T. MOLIN, B. R. SELMAN, and L. E. SCHRADER. 1982a. Ploidy effects in isogenic populations of alfalfa: III. Chloroplast thylakoid-bound coupling factor 1 in protoplasts and leaves. Plant Physiology 70: 1715-1717.
42. MEYERS, S. P., S. L. NICHOLS, G. R. BAER, W. T. MOLIN, and L. E. SCHRADER. 1982b. Ploidy effects in isogenic populations of alfalfa: I. Ribulose- 1,5-bisphosphate carboxylase, soluble protein, chlorophyll, and DNA in leaves. Plant Physiology 70: 1704-1709.
43. MOLIN, W. T., S. P. MEYERS, G. R. BAER, and L. E. SCHRADER. 1982. Ploidy effects in isogenic populations of alfalfa: II. Photosynthesis, chloroplast number, ribulose-1,5-bisphosphate carboxylase, chlorophyll, and DNA in protoplasts. Plant Physiology 70: 1710-1714.
44. NI, Z., E. KIM, M. HA, E. LACKEY, J. LIU, Y. ZHANG, Q. SUN, and Z. J. CHEN. 2009. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457: 327-331.
45. NOTT, A., H. JUNG, S. KOUSSEVITZKY, and J. C HORY. 2006. Plastid-tonucleus retrograde signaling. Annual Review of Plant Biology 57: 739-759.
46. OTTO, S. P., and J. W HITTON. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437.
47. PANDIT, M. K., M. J. O. POCOCK, and W. E. KUNIN. 2011. Ploidy influences rarity and invasiveness in plants. Journal of Ecology 99: 1108-1115.
48. PETER, S., O. SPANG, P. MEDGYESY, and C. SCHÄFER. 1999. Consequences of intergeneric chloroplast transfers on photosynthesis and sensitivity to high light. Functional Plant Biology 26: 171-177.
49. PFEIL, B. E., L. A. CRAVEN, A. H. D. BROWN, B. G. MURRAY, and J. J. DOYLE. 2006. Three new species of northern Australian Glycine (Fabaceae, Phaseolae), G. gracei, G. montis-douglas and G. syndetika. Australian Systematic Botany 19: 245-258.
50. PFEIL, B. E., J. A. SCHLUETER, R. C. SHOEMAKER, and J. J. DOYLE. 2005. Placing paleopolyploidy in relation to taxon divergence: A phylogenetic analysis in legumes using 39 gene families. Systematic Biology 54: 441-454.
51. 2 exchange, leaf area and herbage yield of tetraploid and polyhaploid Festuca spp. Photosynthetica 22: 341-349.
52. PYKE, K. A. 1999. Plastid division and development. Plant Cell 11: 549-556.
53. PYKE, K. A., and R. M. LEECH. 1987. The control of chloroplast number in wheat mesophyll cells. Planta 170: 416-420.
54. RAMSEY, J. 2011. Polyploidy and ecological adaptation in wild yarrow. Proceedings of the National Academy of Sciences, USA 108: 7096-7101.
55. RAMSEY, J., and D. W. SCHEMSKE. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639.
56. REDINBAUGH, M. G., T. A. JONES, and Y. ZHANG. 2000. Ubiquity of the St chloroplast genome in St-containing Triticeae polyploids. Genome 43: 846-852.
57. SALMON, A., M. L. AINOUCHE, and J. F. WENDEL. 2005. Genetic and pigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Molecular Ecology 14: 1163-1175.
58. SCHLUETER, J. A., P. DIXON, C. GRANGER, D. G RANT, L. CLARK, J. J. DOYLE, and R. C. SHOEMAKER. 2004. Mining EST databases to resolve evolutionary events in major crop species. Genome 47: 868-876.
59. SCHRANZ, M. E., and T. Mitchell-Olds. 2006. Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell 18: 1152-1165.
60. SOLTIS, D. E., V. A. ALBERT, J. Leebens-Mack, C. D. BELL, A. H. PATERSON, C. ZHENG, D. SANKOFF, et al. 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96: 336-348.
61. SOLTIS, D. E., and P. S. SOLTIS. 1993. Molecular data and the dynamic nature of polyploidy. Critical Reviews in Plant Sciences 12: 243-273.
62. SOLTIS, D. E., and P. S. SOLTIS. 1999. Polyploidy: Recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348-352.
63. SOLTIS, D. E., P. S. SOLTIS, and J. A. TATE. 2004. Advances in the study of polyploidy since plant speciation. New Phytologist 161: 173-191.
64. STEBBINS, G. L. 1971. Chromosomal evolution in higher plants. Edward Arnold, London, UK.
65. STERCK, L., S. ROMBAUTS, S. JANSSON, F. STERKY, P. ROUZE, and Y. van de PEER. 2005. EST data suggest that poplar is an ancient polyploid. New Phytologist 167: 165-170.
66. TAL, M. 1980. Physiology of polyploids. In W. H. Lewis [ed.], Polyploidy: Biological relevance, 61-75. Plenum, New York, New York, USA.
67. TANG, H., X. WANG, J. E. BOWERS, R. MING, M. ALAM, and A. H. PATERSON. 2008. Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Research 18: 1944-1954.
68. TATE, J. A., Z. NI, A. C. SCHEEN, J. KOH, C. A. GILBERT, D. LEFKOWITZ, Z. J. CHEN, ET AL. 2006. Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173: 1599-1611.
69. TIMKO, M. P., and A. C. VASCONCELOS. 1981. Euploidy in Ricinus: Euploidy effects on photosynthetic activity and content of chlorophyll proteins. Plant Physiology 67: 1084-1089.
70. TOWN, C. D., F. C HEUNG, R. MAITI, J. C RABTREE, B. J. HAAS, J. R. WORTMAN, E. E. HINE, ET AL. 2006. Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18: 1348-1359.
71. TUSKAN, G. A., S. DIFAZIO, S. JANSSON, J. BOHLMANN, I. GRIGORIEV, U. HELLSTEN, N. PUTNAM, ET AL. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
72. VYAS, P., M. S. BISHT, S. MIYAZAWA, S. YANO, K. NOGUCHI, I. TERASHIMA, and S. Funayama-Noguchi. 2007. Effects of polyploidy on photosynthetic properties and anatomy in leaves of Phlox drummondii. Functional Plant Biology 34: 673-682.
73. WANG, J., L. TIAN, H. S. LEE, N. E. WEI, H. JIANG, B. WATSON, A. MADLUNG, ET AL. 2006. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507-517.
74. WARNER, D. A., and G. E. EDWARDS. 1988. C 4 Photosynthesis and leaf anatomy in diploid and autotetraploid Pennisetum americanum Pearl Millet. Plant Science 56: 85-92.
75. WARNER, D. A., and G. E. EDWARDS. 1993. Effects of polyploidy on photosynthesis. Photosynthesis Research 35: 135-147.
76. WARNER, D. A., and G. E. EDWARDS. 1989. Effects of polyploidy on photosynthetic rates, photosynthetic enzymes, contents of DNA, chlorophyll, and sizes and numbers of photosynthetic cells in the C 4 dicot Atriplex confertifolia. Plant Physiology 91: 1143-1151.
77. WARNER, D. A., M. S. B. KU, and G. E. EDWARDS. 1987. Photosynthesis, leaf anatomy and cellular constituents in the polyploid C 4 pathway grass Panicum virgatum. Plant Physiology 84: 461-466.
78. ZHANG, Y., G. H. XU, X. Y. GUO, and L. J. FAN. 2005. Two ancient rounds of polyploidy in rice genome. Journal of Zhejiang University, Science, B 6: 87-90.