Genome duplication and the evolution of physiological responses to water stress.
Whole-genome multiplication, or polyploidy, is common in angiosperms and many species consist of multiple cytotypes that have different physiological tolerances. However, the relative importance of genome duplication vs post-duplication evolutionary change in causing differentiation between cytotypes is not known. We examined the water relations of Chamerion angustifolium, a herbaceous perennial in which diploid and tetraploid cytotypes occupy different niches. To differentiate between the effects of genome duplication and evolutionary changes that followed polyploidization, we compared extant diploids and tetraploids with experimentally synthesized neotetraploids. Tetraploids had 32% higher xylem hydraulic conductivity (K(H)) than neotetraploids and 87% higher K(H) than diploids, but vulnerability to water stress induced cavitation and gas exchange sensitivity to water potential did not differ among cytotypes. Nevertheless, tetraploids took 22% and 30% longer to wilt than neotetraploids and diploids. A simple hydraulic model suggested that tetraploids deplete soil moisture to a greater degree than neotetraploids and diploids before reaching leaf water potentials that cause stomatal closure. We conclude that the different physiological tolerances and distribution of diploid and tetraploid C. angustifolium are unlikely to be caused solely by genome duplication. The enhanced ability of tetraploids to survive water stress likely evolved after polyploidization.
Maherali
Hafiz
H
Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.
Walden
Alison E
AE
Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.
Husband
Brian C
BC
Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.
D005075:Biological Evolution; D004171:Diploidy; D018745:Genome, Plant; D029594:Onagraceae / Q000033:anatomy & histology / Q000235:genetics* / Q000502:physiology*; D010641:Phenotype; D011123:Polyploidy; D013312:Stress, Physiological; D014867:Water / Q000378:metabolism; D052584:Xylem / Q000033:anatomy & histology / Q000502:physiology
D014867:Water
Baack EJ, Stanton ML. 2005. Ecological factors influencing tetraploid speciation in snow buttercups (Ranunculus adoneus): niche differentiation and tetraploid establishment. Evolution 59: 1936-1944.
Baldwin JT. 1941. Galax: the genus and its chromosomes. Journal of Heredity 32: 249-254.
Bennett MD, Bhandol P, Leitch IJ. 2000. Nuclear DNA amounts in angiosperms and their modern uses - 807 new estimates. Annals of Botany 86: 859-909.
Blakeslee AF. 1941. Effect of induced polyploidy in plants. The American Naturalist 75: 117-135.
Brammel RA, Semple JC. 1990. The cytotaxonomy of Solidago nemoralis (Compositae: Asteraceae). Canadian Journal of Botany 68: 2065-2069.
Carroll AB, Pallardy SG, Galen C. 2001. Drought stress, plant water status, and floral trait expression in fire-weed, Epilobium angustifolium (Onagraceae). American Journal of Botany 88: 438-446.
Chen SL, Tang PS. 1945. Studies on colchicine-induced autotetraploid barley. III. Physiological studies. American Journal of Botany 32: 177-179.
Chiu ST, Ewers FW. 1993. The effect of segment length on conductance measurements in Lonicera fragrantissima. Journal of Experimental Botany 44: 175-181.
Cochard H. 2002. Xylem embolism and drought-induced stomatal closure in maize. Planta 215: 466-471.
Cui L, Wall PK, Leebens-Mack J, Lindsay BG, Soltis D, Doyle JJ, Soltis P, Carlson J, Arumuganathan A, Barakat A et al. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Research 16: 738-749.
Dart S, Kron P, Mable BK. 2004. Characterizing polyploidy in Arabidopsis lyrata using chromosome counts and flow cytometry. Canadian Journal of Botany 82: 185-197.
Davis SD, Sperry JS, Hacke UG. 1999. The relationship between xylem conduit diameter and cavitation caused by freeze-thaw events. American Journal of Botany 86: 1367-1372.
Ewers FW. 1985. Xylem structure and water conduction in conifer trees, dicot trees, and lianas. International Association of Wood Anatomists Bulletin 6: 309-317.
Fowler NL, Levin DA. 1984. Ecological constraints on the establishment of a novel polyploid in competition with its diploid progenitor. The American Naturalist 124: 703-711.
Fukuda I. 1967. The biosystematics of Achlys. Taxon 16: 308-316.
Garbutt K, Bazzaz FA. 1983. Leaf demography, flower production and biomass of diploid and tetraploid populations of Phlox drummondii Hook. on a soil moisture gradient. The New Phytologist 93: 129-141.
Grant V. 1981. Plant speciation, 2nd edn. New York, NY, USA: Columbia.
Hardy OJ, Vanderhoeven S, De Loose M, Meerts P. 2000. Ecological, morphological, and allozymic differentiation between diploid and tetraploid knapweeds (Centaurea jacea) from a contact zone in the Belgian Ardennes. The New Phytologist 146: 281-290.
Husband BC. 2000. Constraints on polyploidy evolution: a test of the minority cytotype exclusion principle. Proceedings of the Royal Society B: Biological Sciences 267: 217-233.
Husband BC, Sabara HA. 2004. Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium. The New Phytologist 161: 703-713.
Husband BC, Schemske DW. 2000. Ecological mechanisms of reproductive isolation between diploid and tetraploid Chamerion angustifolium. Journal of Ecology 88: 689-701.
Husband BC, Ozimec B, Martin SL, Pollock L. 2008. Mating consequences of polyploid evolution in flowering plants: current trends, and insights from synthetic polyploids. International Journal of Plant Science 169: 195-206.
Jarbeau JA, Ewers FW, Davis SD. 1995. The mechanism of water stress induced embolism in two species of chaparral shrubs. Plant, Cell & Environment 18: 189-196.
Levin DA. 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35-43.
Levin DA. 1983. Polyploidy and novelty in flowering plants. American Naturalist 122: 1-25.
Levin DA. 2002. The role of chromosomal change in plant evolution. New York, NY, USA: Oxford.
Lewis AM, Boose ER. 1995. Estimating volume flow rates through xylem conduits. American Journal of Botany 82: 1112-1116.
Lewis WH, Terrell EE. 1962. Chromosomal races in eastern North American species of Hedyotis (Houstonia). Rhodora 64: 313-323.
Li WL, Berlyn GP, Ashton PMS. 1996. Polyploids and their structural and physiological characters relative to water deficit in Betula papyrifera (Betulaceae). American Journal of Botany 83: 15-20.
Maherali H, DeLucia EH. 2000. Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiology 20: 859-867.
Maherali H, DeLucia EH. 2001. Influence of climate-driven shifts in biomass allocation on water transport and storage in ponderosa pine. Oecologia 129: 481-491.
Maherali H, DeLucia EH, Sipe TW. 1997. Hydraulic adjustment of maple saplings to canopy gap formation. Oecologia 112: 472-480.
Maherali H, Reid CD, Johnson HB, Polley HW, Jackson RB. 2002. Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant, Cell & Environment 25: 557-566.
Maherali H, Pockman WT, Jackson RB. 2004. Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85: 2184-2199.
Malone SR, Mayeux HS, Johnson HB, Polley HW. 1993. Stomatal density and aperture length in four plant species grown across a subambient CO2 gradient. American Journal of Botany 80: 1413-1418.
Martin SL. 2008. The significance of polyploidy for adaptation. PhD thesis, Guelph, ON, Canada: University of Guelph.
Martinez-Vilalta J, Pockman WT. 2002. The vulnerability to freezing-induced xylem cavitation of Larrea tridentata in the Chihuahuan desert. American Journal of Botany 89: 1916-1924.
Maseda PH, Fernandez RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. Journal of Experimental Botany 57: 3963-3977.
Masterson J. 1994. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421-424.
McDowell NG, Pockman WT, Allen C, Breshears D, Cobb N, Kolb T, Sperry JS, West A, Williams D, Yepez EA. 2008. Tansley review: mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? The New Phytologist 178: 719-739.
McKay JK, Bishop JG, Lin JZ, Sala A, Richards JH, Mitchell-Olds T. 2001. Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress. Proceedings of the Royal Society Series B: Biological Sciences 268: 1715-1721.
McKay JK, Richards JH, Mitchell-Olds T. 2003. Genetics of drought adaptation in Arabidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology 12: 1137-1151.
Mencuccini M. 2003. The ecological significance of long-distance water transport: short term regulation, long term acclimation and the hydraulic costs of stature across plant life forms. Plant, Cell & Environment 26: 163-182.
Mencuccini M, Grace J. 1995. Climate influences the leaf area-sapwood area relationship in Scots pine (Pinus sylvestris L.). Tree Physiology 15: 1-10.
Mosquin T. 1967. Evidence for autopolyploidy in Epilobium angustifolium (Onagraceae). Evolution 21: 713-719.
Otto SP, Whitton J. 2000. Polyploidy incidence and evolution. Annual Review of Genetics 34: 401-437.
Pammenter NW, Vander Willigen C. 1998. A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiology 18: 589-593.
Pockman WT, Sperry JS. 1997. Freezing-induced xylem cavitation and the northern limit of Larrea tridentata. Oecologia 109: 19-27.
Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639.
Rothera SL, Davy AJ. 1986. Polyploidy and habitat differentiation in Deschampsia caespitosa. The New Phytologist 10: 449-467.
Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57: 361-381.
Schaefer VG, Miksche JP. 1977. Microspectrophotometric determination of DNA per cell and polyploidy in Fraxinus americana L. Silvae Genetica 26: 184-192.
Sémon M, Wolfe KH. 2007. Consequences of genome duplication. Current Opinion in Genetics & Development 17: 505-512.
Sharma AK, Dey D. 1967. A comprehensive cytotaxonomic study on the family Chenopodiaceae. Journal of Cytology and Genetics 2: 114-127.
Sokal RR, Rohlf J. 1995. Biometry, 3rd edn. New York, NY, USA: W.H. Freeman.
Soltis DE, Soltis PS, Schmeske DW, Hancock JF, Thompson JN, Husband BC, Judd WS. 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56: 13-30.
Sperry JS, Hacke UG. 2004. Analysis of circular bordered pit function. I. Angiosperm vessels with homogeneous pit membranes. American Journal of Botany 91: 369-385.
Sperry JS, Saliendra NZ. 1994. Intra-and inter-plant variation in xylem cavitation in Betula occidentalis. Plant, Cell & Environment 17: 1233-1241.
Sperry JS, Donnelly JR, Tyree MT. 1988. A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11: 35-40.
Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of Northern Utah and Interior Alaska. Ecology 75: 1736-1752.
Sperry JS, Hacke UG, Wheeler JK. 2005. Comparative analysis of end wall resistance in xylem conduits. Plant, Cell & Environment 28: 456-465.
Stebbins GL. 1971. Chromosomal evolution in higher plants. London, UK: Edward Arnold Ltd.
Tichá I. 1982. Photosynthetic characteristics during ontogenesis of leaves. 7. Stomata density and sizes. Photosynthetica 16: 375-471.
Tyree MT, Ewers FW. 1991. The hydraulic architecture of trees and other woody plants. The New Phytologist 119: 345-360.
Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 19-38.
Tyree MT, Davis SD, Cochard H. 1994. Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? International Association of Wood Anatomists Journal 14: 335-360.
Watanabe K. 1986. The cytogeography of the genus Eupatorium (Compositae). A review. Plant Species Biology 1: 99-116.
Whitehead D, Edwards WRN, Jarvis PG. 1984. Relationships between conducting sapwood area, foliage area and permeability in mature Picea stichensis and Pinus contorta trees. Canadian Journal of Forest Research 14: 940-947.
Zimmermann MH. 1983. Xylem structure and the ascent of sap. New York, NY, USA: Springer.
Zwieniecki MA, Melcher PJ, Holbrook NM. 2001. Hydrogel control of hydraulic resistance in plants. Science 291: 1059-1062.