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Molecular genetic analysis of dormancy-related traits in poplars

Published online by Cambridge University Press:  20 January 2017

Glenn T. Howe
Affiliation:
Department of Forest Science, Oregon State University, Corvallis, OR 97331
Harvey D. Bradshaw
Affiliation:
College of Forest Resources, University of Washington, Seattle, WA 98195

Abstract

We studied the molecular genetics of dormancy-related traits in an F2 family of poplar (Populus) hybrids derived from a cross between a northern genotype of black cottonwood and a southern genotype of eastern cottonwood by mapping quantitative trait loci (QTLs) and candidate genes. Dormancy-related traits included timing of vegetative bud set, fall frost damage, chilling response, timing of vegetative bud flush, and winter survival under field conditions, as well as photoperiodic responses (timing of bud set and number of new leaves) in a warm greenhouse under either a uniform 8-h photoperiod or a naturally shortening photoperiod in the fall. QTL analyses were conducted using a linkage map consisting of AFLP, microsatellite, and candidate gene markers. The candidate genes were chosen because of their potential roles in either photoperiodic perception (PHYB1, PHYB2) or abscisic acid signal transduction (ABI1B, ABI1D, ABI3). Significant QTLs were detected for all dormancy-related traits, except for winter survival, which had a relatively low heritability compared with the other traits. Interestingly, half of the field bud set QTLs did not map near photoperiodic QTLs. This is consistent with the moderate genetic correlation between these traits (0.53 to 0.60) and suggests that genetic differences in photoperiodic responses play only a modest role in explaining genetic differences in the timing of bud set under field conditions. Except for ABI1D, each of the candidate genes tested mapped near one or more of the dormancy-related QTLs. We conclude that molecular markers and QTL analyses can be used to study the genetics of dormancy-related traits, to design more effective breeding programs, and to provide new insights into tree physiology.

Type
Research Article
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Abelson, P. H. 1991. Improved yields of biomass. Science 252:1469.Google Scholar
Aitken, S. N. and Adams, W. T. 1995. Screening for cold hardiness in coastal Douglas-fir. Pages 321324 In Potts, B. M., Borralho, N.M.G., Reid, J. B., Cromer, R. N., Tibbits, W. N., and Raymond, C. A., eds. Eucalypt Plantations: Improving Fiber Yield and Quality. Proceedings of the CRC/IUFRO Conference, Hobart, 19–24 February. Hobart, Australia: CRC for Temperate Hardwood Forestry.Google Scholar
Aitken, S. N. and Adams, W. T. 1997. Spring cold hardiness under strong genetic control in Oregon populations of Pseudotsuga menziesii var. menziesii . Can. J. For. Res. 27:17731780.Google Scholar
Aitken, S. N., Adams, W. T., Schermann, N., and Fuchigami, L. H. 1996. Family variation for fall cold hardiness in two Washington populations of coastal Douglas-fir (Pseudotsuga menziesii var. menziesii (Mirb.) Franco). For. Ecol. Manag. 80:187195.Google Scholar
Barros, R. S. and Neill, S. J. 1986. Periodicity of response to abscisic acid in lateral buds of willow (Salix viminalis L.). Planta 168:530535.Google Scholar
Billington, H. L. and Pelham, J. 1991. Genetic variation in the date of budburst in Scottish birch populations: implications for climate change. Funct. Ecol. 5:403409.Google Scholar
Binelli, G. and Bucci, G. A. 1994. Genetic linkage map of Picea abies Karst, based on RAPD markers, as a tool in population genetics. Theor. Appl. Genet. 88:283288.CrossRefGoogle ScholarPubMed
Borowska, B. and Powell, L. E. 1982. Abscisic acid relationships in dormancy of apple buds. Sci. Hortic. 18:111117.Google Scholar
Bradshaw, H. D. Jr. and Stettler, R. F. 1993. Molecular genetics of growth and development in Populus . I. Triploidy in hybrid poplars. Theor. Appl. Genet. 86:301307.CrossRefGoogle ScholarPubMed
Bradshaw, H. D. and Stettler, R. F. 1995. Molecular genetics of growth and development in Populus . IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics 139:963973.Google ScholarPubMed
Bradshaw, H. D., Villar, M., Watson, B. D., Otto, K. G., Stewart, S., and Stettler, R. F. 1994. Molecular genetics of growth and development in Populus . III. A genetic linkage map of a hybrid poplar composed of RFLP, STS, and RAPD markers. Theor. Appl. Genet. 89:167178.Google Scholar
Brissette, J. C. and Barnes, B. V. 1984. Comparisons of phenology and growth of Michigan and western North American sources of Populus tremuloides . Can. J. For. Res. 14:789793.Google Scholar
Byrne, M., Murrell, J. C., and Owen, J. V. 1997. Mapping of quantitative trait loci influencing frost tolerance in Eucalyptus nitens . Theor. Appl. Genet. 86:975979.CrossRefGoogle Scholar
Cai, Q., Guy, C. L., and Moore, G. A. 1994. Extension of the linkage map in Citrus using random amplified polymorphic DNA (RAPD) markers and RFLP mapping of cold-acclimation-responsive loci. Theor. Appl. Genet. 89:606614.CrossRefGoogle ScholarPubMed
Cathey, H. M. 1990. USDA plant hardiness zone map. USDA Agricultural Research Service Miscellaneous Publication No. 1475.Google Scholar
Chaparro, J. X., Werner, D. J., O’Malley, D., and Sederoff, R. R. 1994. Targeted mapping and linkage analysis of morphological isozyme, and RAPD markers in peach. Theor. Appl. Genet. 87:805815.Google Scholar
Charest, P. J., Devantier, Y., Jones, C., Sellmer, J. C., McCown, B. H., and Ellis, D. D. 1997. Direct gene transfer in poplar. Pages 6064 In Klopfenstein, N. B., Chun, Y. W., Kim, S. S., and Ahuja, M. R., eds. Micropropagation, Genetic Engineering, and Molecular Biology of Populus . USDA Forest Service General Technical Report RM-GTR-297.Google Scholar
Devey, M. E., Fiddler, T. A., Liu, B. H., Knapp, S. J., and Neale, D. B. 1994. An RFLP linkage map for loblolly pine based on a three-generation outbred pedigree. Theor. Appl. Genet. 88:273278.Google Scholar
Doebley, J., Stec, A., and Hubbard, L. 1997. The evolution of apical dominance in maize. Nature 386:485488.Google Scholar
Dunlap, J. M. and Stettler, R. F. 1996. Genetic variation and productivity of Populus trichocarpa and its hybrids. IX. Phenology and Melampsora rust incidence of native black cottonwood clones from four river valleys in Washington. For. Ecol. Manag. 87:233256.CrossRefGoogle Scholar
Ekberg, I., Eriksson, G., and Weng, Y. 1985. Between- and within-population variation in growth rhythm and plant height in four Picea abies populations. Stud. For. Suec. No. 167, 14 pp.Google Scholar
Eriksson, G., Ekberg, I., Dormling, I., and Matern, B. 1978. Inheritance of bud-set and bud flushing in Picea Abies . Theor. Appl. Genet. 52:319.CrossRefGoogle ScholarPubMed
Ernst, S. G. and Fechner, G. H. 1981. Variation in rooting and juvenile growth phenology of narrowleaf cottonwood in Colorado. Pages 111118 in Proceedings of the North Central Tree Improvement Conference, Madison, WI.Google Scholar
Farmer, R. E. Jr. 1970. Genetic variation among open-pollinated progeny of eastern cottonwood. Silvae Genet. 19:149151.Google Scholar
Farmer, R. E. Jr. 1992. Eastern cottonwood goes to China, poplar become a major component of agroforestry systems. J. For. 90:2124.Google Scholar
Farmer, R. E. Jr. 1993. Latitudinal variation in height and phenology of balsam poplar. Silvae Genet. 42:148153.Google Scholar
Farmer, R. E. Jr. and Reinholt, R. W. 1986. Genetic variation in dormancy relations of balsam poplar along a latitudinal transect in northwestern Ontario. Silvae Genet. 35:3842.Google Scholar
Fillatti, J. J., Sellmer, J., McCown, B., Haissig, B., and Comai, L. 1987. Agrobacterium mediated transformation and regeneration of Populus . Mol. Gen. Genet. 206:192199.Google Scholar
Finkelstein, R. 1994. Maternal effects govern variable dominance of two abscisic acid response mutations in Arabidopsis thaliana . Plant Physiol. 105:12031208.CrossRefGoogle ScholarPubMed
Fjellstrom, R. G. and Parfitt, D. E. 1994. RFLP inheritance and linkage in walnut. Theor. Appl. Genet. 89:665670.Google Scholar
Frary, A., Nesbitt, T. C., Grandillo, S., et al. 2000. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:8588.Google Scholar
Frewen, B. E., Chen, T.H.H., Howe, G., Davis, J., Rohde, A., Boerjan, W., and Bradshaw, H. D. Jr. 2000. QTL and candidate gene mapping of bud set and bud flush in Populus . Genetics 154:837845.Google Scholar
Fridman, E., Pleban, T., and Zamir, D. 2000. A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc. Natl. Acad. Sci. USA 97:47184723.Google Scholar
Fuchigami, L. H., Weiser, C. J., and Evert, D. R. 1971. Induction of cold acclimation in Cornus stolonifera Michx. Plant Physiol. 47:98103.Google Scholar
Giraudat, J., Hauge, B. M., Valon, C., Smalle, J., Parcy, F., and Goodman, H. M. 1992. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:12511261.Google Scholar
Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A.R., Vartanian, N., and Giraudat, J. 1999. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:18971909.Google Scholar
Grattapaglia, D. and Sederoff, R. 1994. Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:11211137.Google Scholar
Håbjørg, A. 1972. Effects of photoperiod and temperature on growth and development of three latitudinal and three altitudinal populations of Betula pubescens Ehrh. Meld Nor. Landbrukshøgsk. 51:127.Google Scholar
Han, K. H., Gordon, M. P., and Strauss, S. H. 1996. Cellular and molecular biology of Agrobacterium-mediated transformation of plants and its application to genetic engineering of Populus. Pages 201222 In Stettler, R. F., Bradshaw, H. D. Jr., Heilman, P. E., and Hinckley, T. M., eds. Biology of Populus and Its Implications for Management and Conservation. Ottawa, Canada: NRC Press.Google Scholar
Hauagge, R. and Cummins, J. N. 1991. Genetics of length of dormancy period in Malus vegetative buds. J. Am. Soc. Hortic. Sci. 116:121126.Google Scholar
Hemmat, M., Weeden, N. F., Manganaris, A. G., and Lawson, D. M. 1994. Molecular marker linkage map for apple. J. Hered. 85:411.Google Scholar
Howe, G. T., Bucciaglia, P. A., Hackett, W. P., Furnier, G. R., Cordonnier-Pratt, M., and Gardner, G. 1998. Evidence that the phytochrome gene family in black cottonwood has one PHYA locus and two PHYB loci but lacks members of the PHYC/F and PHYE subfamilies. Mol. Biol. Evol. 15:160175.Google Scholar
Howe, G. T., Davis, J., Frewen, B., Saruul, P., Jeknić, Z., Bradshaw, H. D. Jr., and Chen, T.H.H. 1999. Physiological and genetic approaches to studying endodormancy-related traits in Populus . Hortscience 34:11741184.Google Scholar
Howe, G. T., Gardner, G., Hackett, W. P., and Furnier, G. R. 1996. Phytochrome control of short-day-induced bud set in black cottonwood. Physiol. Plant 97:95103.Google Scholar
Howe, G. T., Hackett, W. P., Furnier, G. R., and Klevorn, R. E. 1995. Photoperiodic responses of a northern and southern ecotype of black cottonwood. Physiol. Plant 93:695708.Google Scholar
Howe, G. T., Saruul, P., Davis, J., and Chen, T.H.H. 2000. Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplars. Theor. Appl. Genet. 101:632642.CrossRefGoogle Scholar
Jeknić, Z. and Chen, T.H.H. 1999. Changes in protein profiles of poplar tissues during the induction of bud dormancy by short-day photoperiods. Plant Cell Physiol. 40:2535.CrossRefGoogle Scholar
Jian, L. C., Li, P. H., Sun, L. H., and Chen, T.H.H. 1997. Alterations in ultrastructure and subcellular localization of Ca2+ in poplar apical bud cells during the induction of dormancy. J. Exp. Bot. 48:11951207.Google Scholar
Johansen, L. G., Oden, P. C., and Junttila, O. 1986. Abscisic acid and cessation of apical growth in Salix pentandra . Physiol. Plant 66:409412.CrossRefGoogle Scholar
Junttila, O. and Kaurin, A. 1983. Climatic control of apical growth cessation in latitudinal ecotypes of Salix pentandra L. Pages 8391 In Kaurin, N. A., Junttila, O., and Nilsen, J., eds. Plant Production in the North. Tromso, Norway: Norwegian University Press.Google Scholar
Kaul, S., Koo, H. L., Jenkins, J., et al. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana . Nature 408:796815.Google Scholar
Knapp, S. J., Holloway, J. L., Bridges, W. C., and Liu, B. H. 1995. Mapping dominant markers using F2 matings. Theor. Appl. Genet. 91:7481.Google Scholar
Koornneef, M., Reuling, G., and Karssen, C. M. 1984. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana . Physiol. Plant 61:377383.Google Scholar
Kuser, J. E. and Ching, K. K. 1980. Provenance variation in phenology and cold hardiness of western hemlock seedlings. For. Sci. 26:463470.Google Scholar
Lander, E. S., Green, P., Abrahamson, J., Barlow, A., and Daly, M. J. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174181.CrossRefGoogle ScholarPubMed
Lang, G. A. 1987. Dormancy: a new universal terminology. Hortscience 22:817820.Google Scholar
Larson, P. R. 1972. Putting basic research into practice. Pages 1723 In Proceedings of the Technical Session. Appleton, WI: American Pulp Association.Google Scholar
Lawson, D. M., Hemmat, M., and Weeden, N. F. 1995. The use of molecular markers to analyze the inheritance of morphological and developmental traits in apple. J. Am. Soc. Hortic. Sci. 120:532537.CrossRefGoogle Scholar
Lenton, J. R., Perry, V. M., and Saunders, P. F. 1972. Endogenous abscisic acid in relation to photoperiodically induced bud dormancy. Planta 106:1322.Google Scholar
Leung, J., Bouvier-Durand, M., Morris, P. C., Guerrier, D., Chefdor, F., and Giraudat, J. 1994. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:14481452.Google Scholar
Li, P., and Adams, W. T. 1993. Genetic control of bud phenology in pole-size trees and seedlings of coastal Douglas-fir. Can. J. For. Res. 23:10431051.Google Scholar
Linvill, D. E. 1990. Calculating chilling hours and chill units from daily maximum and minimum temperature observations. Hortscience 25:1416.CrossRefGoogle Scholar
Liu, Z. and Furnier, G. R. 1993. Inheritance and linkage of allozymes and RFLPs in trembling aspen. J. Hered. 84:419424.CrossRefGoogle Scholar
Meyer, K., Leube, M., and Grill, E. 1994. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana . Science 264:14521455.Google Scholar
Mikola, J. 1982. Bud-set phenology as an indicator of climatic adaptation of Scots pine in Finland. Silva Fenn. 16:178184.Google Scholar
Nelson, C. D., Kubisiak, T. L., Stine, M., and Nance, W. L. 1994. A genetic linkage map of longleaf pine (Pinus palustris Mill) based on random amplified polymorphic DNAs. J. Hered. 85:433439.Google Scholar
Nelson, C. D., Nance, W. L., and Doudrick, R. L. 1993. A partial genetic linkage map of slash pine (Pinus elliottii Engelm var. elliottii) based on random amplified polymorphic DNAs. Theor. Appl. Genet. 87:145151.CrossRefGoogle ScholarPubMed
Oppenheimer, C. H. and Slor, E. 1968. Breeding of apples for a subtropical climate. II. Analysis of two F2 and nine backcross populations. Theor. Appl. Genet. 38:97102.Google Scholar
Ott, J. 1985. Analysis of Human Genetic Linkage. Baltimore, MD: Johns Hopkins University Press, p. 233.Google Scholar
Pauley, S. S. and Perry, T. O. 1954. Ecotypic variation in the photoperiodic response in Populus . J. Arnold Arbor. 35:167188.Google Scholar
Powell, L. E. 1982. Shoot growth in woody plants and possible participation of abscisic acid. Pages 363372 In Wareing, P. F., ed. Plant Growth Substances. New York: Academic Press.Google Scholar
Rehfeldt, G. E. 1983. Genetic variability with Douglas-fir populations: implications for tree improvement. Silvae Genet. 32:914.Google Scholar
Rehfeldt, G. E. 1992a. Breeding strategies for Larix occidentalis: adaptations to the biotic and abiotic environment in relation to improving growth. Can. J. For. Res. 22:513.Google Scholar
Rehfeldt, G. E. 1992b. Early selection in Pinus ponderosa: compromises between growth potential and growth rhythm in developing breeding strategies. For. Sci. 38:661677.Google Scholar
Riemenschneider, D. E., McMahon, B. G., and Ostry, M. E. 1992. Use of selection indices to increase tree height and to control damaging agents in 2-year-old balsam poplar. Can. J. For. Res. 22:561567.CrossRefGoogle Scholar
Riemenschneider, D. E., McMahon, B. G., and Ostry, M. E. 1994. Population-dependent selection strategies needed for 2-year-old black cottonwood clones. Can. J. For. Res. 24:17041710.Google Scholar
Rinne, P., Saarelainen, A., and Juntilla, O. 1994. Growth cessation and bud dormancy in relation to ABA level in seedlings and coppice shoots of Betula pubescens as affected by short photoperiod, water stress and chilling. Physiol. Plant 90:451458.Google Scholar
Rodriguez, A. J., Sherman, W. B., Scorza, R., Wisniewski, M., and Okie, W. R. 1994. ‘Evergreen’ peach, its inheritance and dormant behavior. J. Am. Soc. Hortic. Sci. 119:789792.Google Scholar
Rohde, A., Ardiles-Diaz, W., van Montagu, M., and Boerjan, W. 1998. Isolation and expression analysis of an ABSCISIC ACID-INSENSITIVE 3 (ABI3) homologue from Populus trichocarpa . J. Exp. Bot. 49:10591060.Google Scholar
Sheen, J. 1998. Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc. Natl. Acad. Sci. USA 95:975980.Google Scholar
Sorensen, F. C. 1983. Relationship between logarithms of chilling period and germination or bud flush rate is linear for many tree species. For. Sci. 29:237240.Google Scholar
Stettler, R. F., Bradshaw, H. D. Jr., and Zsuffa, L. 1992. The role of genetic improvement in short rotation forestry. Pages 185191 In Mitchell, C. P., Ford-Robertson, J. B., Hinkley, T., and Sennerby-Forsse, L., eds. London: Elsevier Applied Science.Google Scholar
Stettler, R. F., Fenn, R. C., Heilman, P. E., and Stanton, B. J. 1988. Populus trichocarpa × Populus deltoides hybrids for short rotation culture: variation patterns and 4-year field performance. Can. J. For. Res. 18:745753.Google Scholar
Taylor, J. S. and Dumbroff, E. B. 1975. Bud, root and growth regulator activity in Acer saccharum during the dormant season. Can. J. Bot. 53:321331.Google Scholar
Thomas, B. R., MacDonald, S. E., and Dancik, B. P. 1997. Variance components, heritabilities and gain estimates for growth chamber and field performance of Populus tremuloides: growth parameters. Silvae Genet. 46:317326.Google Scholar
Thompson, M. M., Smith, D. C., and Burgess, J. E. 1985. Nondormant mutants in a temperate tree species, Corylus avellana L. Theor. Appl. Genet. 70:687692.Google Scholar
Weber, J. C., Stettler, R. F., and Heilman, P. E. 1985. Genetic variation and productivity of Populus trichocarpa and its hybrids. I. Morphology and phenology of 50 native clones. Can. J. For. Res. 15:376383.Google Scholar
Worrall, J. 1983. Temperature-bud-burst relationships in amabalis and subalpine fir provenance tests replicated at different elevations. Silvae Genet. 32:203209.Google Scholar
Wright, L. L., Graham, R. L., Turhollow, A. F., and English, B. C. 1992. The potential impacts of short-rotation woody crops on carbon conservation. Pages 123156 In Sampson, R. N. and Hair, D., eds. Forests and Global Change. Volume I: Opportunities for Increasing Forest Cover. American Forests. Washington, DC.Google Scholar
Zsuffa, L., Sennerby-Forsse, L., Weisgerber, H., and Hall, R. B. 1993. Strategies for clonal forestry with poplars, aspens, and willows. Pages 91119 In Ahuja, M. R. and Libby, W. J., eds. Clonal Forestry. II. Conservation and Application. Berlin: Springer-Verlag.Google Scholar