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Hybridization and Adaptive Divergence in Oaks
Oliver Gailing and Jennifer Riehl
Published May 2016 International Oaks No. 27: 91–98
Abstract
Ecologically divergent, but hybridizing oaks provide a model to identify genomic regions and underlying genes that may be involved in adaptive species differences and reproductive isolation between species. Scoring of potentially neutral genomic and of genic microsatellites in two Red Oak species, Quercus rubra L. and Q. ellipsoidalis E.J. Hill, with different adaptations to drought revealed a set of candidate genes for stress tolerance and phenology. Thus, a trinucleotide microsatellite located in the coding sequence of a putative CONSTANS-like (COL) gene was nearly fixed on alternate alleles in the drought-tolerant Q. ellipsoidalis and in the drought-averse Q. rubra. Microsatellite size variation corresponded to size variation in a poly (E) repeat. In other studies, a Single Nucleotide Polymorphism in the same COL gene was associated with the timing of vegetative bud burst in Q. petraea (Matt.) Liebl. and variation in poly (E) repeat length in COL2B was associated with growth cessation in Populus tremula L. Next generation sequencing such as Restriction site associated DNA sequencing (RAD-seq) will be used for genome-wide outlier screens. With the availability of the whole genome sequence of Quercus robur L. chromosome-anchored high-density linkage maps can be used to compare the distribution of outlier genomic regions across oak species and to test for a co-location of Quantitative Trait Loci for adaptive species differences with outlier genomic regions.
Keywords
Quercus rubra, Quercus ellipsoidalis, speciation, candidate genes
References
Abadie, P., G. Roussel, B. Dencausse, C. Bonnet, E. Bertocchi, J.M. Louvet, A. Kremer, and P. Garnier-Gere. 2012. Strength, diversity and plasticity of postmating reproductive barriers between two hybridizing oak species (Quercus robur L. and Quercus petraea (Matt) Liebl.). Journal of Evolutionary Biology 25: 157-173.
Abrams, M.D. 1990. Adaptations and responses to drought in Quercus species of North America. Tree Physiology 7: 227-238.
Alberto, F.J., J. Derory, C. Boury, J.M. Frigerio, N.E. Zimmermann, and A. Kremer. 2013. Imprints of natural selection along environmental gradients in phenology-related genes of Quercus petraea. Genetics 195: 495-512.
Bodénès, C., E. Chancerel, O. Gailing, G.G. Vendramin, F. Bagnoli, J. Durand, P.G. Goicoechea, C. Soliani, F. Villani, C. Mattioni, H.P. Koelewijn, F. Murat, J. Salse, G. Roussel, C. Boury, F. Alberto, A. Kremer, and C. Plomion. 2012. Comparative mapping in the Fagaceae and beyond with EST-SSRs. Bmc Plant Biology 12.
Breda, N., H. Cochard, E. Dreyer, and A. Granier. 1993. Field comparison of transpiration, stomatal conductance and vulnerability to cavitation of Quercus petraea and Q. robur under water-stress. Annales des Sciences Forestières 50: 571-582.
Brendel, O., D. Le Thiec, C. Scotti-Saintagne, C. Bodénès, A. Kremer, and J.-M. Guehl. 2008. Quantitative Trait loci controlling water use efficiency and related traits in Quercus robur L. Tree Genetics and Genomes 4: 263-278.
Burns, R.M. and B.H. Honkala. 1990. Silvics of North America, Washington, DC.
Cavender-Bares, J., and A. Pahlich. 2009. Molecular, morphological and ecological niche differentiation of sympatric oak species, Quercus virginiana and Q. geminata (Fagaceae) American Journal of Botany 96: 1690-1702.
Cottam, W.P., J.M. Tucker, and F.S. Santamour Jr. 1982. Oak hybridization at the University of Utah. State Arboretum of Utah, University of Utah.
Curtu, A.L., O. Gailing, and R. Finkeldey. 2007. Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology 7: 218.
Curtu, A.L., O. Gailing, and R. Finkeldey. 2009. Patterns of contemporary hybridization inferred from paternity analysis in a four-oak-species forest. BMC Evolutionary Biology 9: 284.
de Heredia, U.L., M. Valbuena-Carabana, M. Cordoba, and L. Gil. 2009. Variation components in leaf morphology of recruits of two hybridising oaks Q. petraea (Matt.) Liebl. and Q. pyrenaica Willd. at small spatial scale. European Journal of Forest Research 128: 543-554.
de Leon, B. G.P., J.M. F. Zorrilla, V. Rubio, P. Dahiya, J. Paz-Ares, and A. Leyva. 2004. Interallelic complementation at the Arabidopsis CRE1 locus uncovers independent pathways for the proliferation of vascular initials and canonical cytokinin signalling. Plant Journal 38: 70-79.
Deng, W.W., C.Y. Liu, Y.X. Pei, X. Deng, L.F. Niu, and X.F. Cao. 2007. Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiology 143: 1660-1668.
Drost, D.R., S. Puranik, E. Novaes, C.R.D. B. Novaes, C. Dervinis, O. Gailing, and M. Kirst. 2015. Genetical genomics of Populus leaf shape variation. Bmc Plant Biology 15: 166.
Durand, J., C. Bodénès, E. Chancerel, J.-M. Frigero, G.G. Vendramin, F. Sebastiani, A. Buonamici, O. Gailing, H.-P. Koelewijn, F. Villani, C. Mattioni, M. Cherubini, P. G. Goicoechea, A. Herran, Z. Ikaran, C. Cabane, S. Ueno, A. de Daruvar, A. Kremer, and C. Plomion. 2010. A fast and cost-effective approach to develop and map EST-SSR markers: oak as a case study. BMC genomics 11: 570.
Evans, L.M., G.T. Slavov, E. Rodgers-Melnick, J. Martin, P. Ranjan, W. Muchero, A.M. Brunner, W. Schackwitz, L. Gunter, J.-G. Chen, G. Tuskan, and S. Difazio. 2014. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nature Genetics 46: 1089–1096.
Gailing, O. 2013. Differences in growth, survival and phenology in Quercus rubra and Q. ellipsoidalis seedlings. Dendrobiology 70: 71-79.
Gailing, O., R. Langenfeld-Heyser, A. Polle, and R. Finkeldey. 2008. Quantitative trait loci affecting stomatal density and growth in a Quercus robur progeny: implications for the adaptation to changing environments. Global Change Biology 14: 1934-1946.
Gerber, S., J. Chadoeuf, F. Gugerli, M. Lascoux, J. Buiteveld, J. Cottrell, A. Dounavi, S. Fineschi, L. L. Forrest, J. Fogelqvist, P. G. Goicoechea, J. S. Jensen, D. Salvini, G. G. Vendramin, and A. Kremer. 2014. High rates of gene flow by pollen and seed in oak populations across Europe. Plos One 9: e85130.
Goicoechea, P.G., A. Herran, J. Durand, C. Bodenes, C. Plomion, and A. Kremer. 2015. A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks. Heredity 114: 373-386.
Goicoechea, P.G., R J. Petit, and A. Kremer. 2012. Detecting the footprints of divergent selection in oaks with linked markers. Heredity 109: 361-371.
Guichoux, E., P. Garnier-Gere, L. Lagache, T. Lang, C. Boury, and R.J. Petit. 2013. Outlier loci highlight the direction of introgression in oaks. Molecular Ecology 22: 450-462.
Hardin, J.W. 1975. Hybridization and introgression in Quercus alba. Journal of the Arnold Arboretum 56: 336-363.
Hipp, A.L. and J.A. Weber. 2008. Taxonomy of Hill's oak (Quercus ellipsoidalis: Fagaceae): Evidence from AFLP data. Systematic Botany 33: 148-158.
Kremer, A., J L. Dupouey, J.D. Deans, J. Cottrell, U. Csaikl, R. Finkeldey, S. Espinel, J. Jensen, J. Kleinschmit, B. Van Dam, A. Ducousso, I. Forrest, U. Lopez de Heredia, A.J. Lowe, M. Tutkova, R.C. Munro, S. Steinhoff, and V. Badeau. 2002. Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science 59: 777-787.
Lepais, O. and S. Gerber. 2011. Reproductive patterns shape introgression dynamics and species succession within the European white oak complex. Evolution 65: 156-170.
Lepais, O., R.J. Petit, E. Guichoux, J.E. Lavabre, F. Alberto, A. Kremer, and S. Gerber. 2009. Species relative abundance and direction of introgression in oaks. Molecular Ecology 18: 2228-2242.
Lepoittevin, C., C. Bodénès, E. Chancerel, L. Villate, T. Lang, I. Lesur, C. Boury, F. Ehrenmann, D. Zelenica, A. Boland, C. Besse, P. Garnier-Géré, C. Plomion, and A. Kremer. 2015. Single-nucleotide polymorphism discovery and validation in high-density SNP array for genetic analysis in European white oaks. Molecular Ecology Resources 15: 1446-1459. doi: 10.1111/1755-0998.12407.
Lexer, C., A. Kremer, and R.J. Petit. 2006. Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Molecular Ecology 15: 2007-2012.
Lind-Riehl, J., A. Sullivan, and O. Gailing. 2014. Evidence for selection on a CONSTANS-like gene between two red oak species. Annals of Botany 113: 967-975.
Lind, J. and O. Gailing. 2013. Genetic structure of Quercus rubra L. and Q. ellipsoidalis E. J. Hill populations at gene-based EST-SSR and nuclear SSR markers. Tree Genetics & Genomes 31: 231-239.
Ma, X.F., D. Hall, K.R. St Onge, S. Jansson, and P.K. Ingvarsson. 2010. Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics 186: 1033-1044.
Manos, P.S., J.J. Doyle, and K.C. Nixon. 1999. Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Molecular Phylogenetics and Evolution 12: 333-349.
Mariette, S., J. Cottrell, U.M. Csaikl, P. Goikoechea, A.O. König, A.J. Lowe, B.C. Van Dam, T. Barreneche, C. Bodenes, R. Streiff, K. Burg, K. Groppe, R.C. Munro, H. Tabbener, and A. Kremer. 2002. Comparison of levels of genetic diversity detected with AFLP and microsatellite markers within and among mixed Q. petraea (Matt.) Liebl. and Q. robur L. stands. Silvae Genetica 51: 72-79.
Owusu, S.A., A.R. Sullivan, J.A. Weber, A.L. Hipp, and O. Gailing. 2015. Taxonomic relationships and gene flow in four North American Quercus species. Systematic Botany 40: 510-521.
Parelle, J., M. Zapater, C. Scotti-Saintagne, A. Kremer, Y. Jolivet, E. Dreyer, and O. Brendel. 2007. Quantitative trait loci of tolerance to waterlogging in a European oak (Quercus robur L.): physiological relevance and temporal effect patterns. Plant, Cell and Environment 30: 422-434.
Penaloza-Ramirez, J.M., A. Gonzalez-Rodriguez, L. Mendoza-Cuenca, H. Caron, A. Kremer, and K. Oyama. 2010. Interspecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico. Annals of Botany 105: 389-399.
Petit, R J., C. Bodénès, A. Ducousso, G. Roussel, and A. Kremer. 2003. Hybridization as a mechanism of invasion in oaks. New Phytologist 161: 151-164.
Plomion, C., J.-M. Aury, J. Amselem, T. Alaeitabar, V. Barbe, C. Belser, H. Bergès, C. Bodénès, N. Boudet, C. Boury, A. Canaguier, A. Couloux, C. Da Silva, S. Duplessis, F. Ehrenmann, B. Estrada-Mairey, S. Fouteau, N. Francillonne, C. Gaspin, C. Guichard, C. Klopp, K. Labadie, C. Lalanne, I. Le Clainche, J.-C. Leplé, G. Le Provost, T. Leroy, I. Lesur, F. Martin, J. Mercier, C. Michotey, F. Murat, F. Salin, D. Steinbach, P. Faivre-Rampant, P. Wincker, J. Salse, H. Quesneville, and A. Kremer. 2016. Decoding the oak genome: public release of sequence data, assembly, annotation and publication strategies. Molecular Ecology Resources 16:254-265. doi: 10.1111/1755-0998.12425
Saintagne, C., C. Bodenes, T. Barreneche, D. Pot, C. Plomion, and A. Kremer. 2004. Distribution of genomic regions differentiating oak species assessed by QTL detection. Heredity 92: 20-30.
Scotti-Saintagne, C., S. Mariette, I. Porth, P.G. Goicoechea, T. Barreneche, C. Bodenes, K. Burg, and A. Kremer. 2004. Genome scanning of interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea (Matt.) Liebl.). Genetics 168: 1615-1626.
Steinhoff, S. 1993. Results of species hybridization with Quercus robur L. and Quercus petraea (Matt) Liebl. Annales des Sciences Forestières 50: 137s-143s.
Steinhoff, S. 1998. Kontrollierte Kreuzungen zwischen Stiel- und Traubeneiche: Ergebnisse und Folgerungen. Allgemeine Forst- und Jagdzeitung 169: 163-168.
Sullivan, A.R., J.F. Lind, T.S. McCleary, J. Romero-Severson, and O. Gailing. 2013. Development and characterization of genomic and gene-based microsatellite markers in North American red oak species. Plant Molecular Biology Reporter 31: 231-239.
Tucker, J.M. 1990. Hybridization in California oaks. Fremontia 18: 13-19.
Tuskan, G.A., S. DiFazio, S. Jansson, J. Bohlmann, I. Grigoriev, U. Hellsten, N. Putnam, S. Ralph, S. Rombauts, A. Salamov, J. Schein, L. Sterck, A. Aerts, R.R. Bhalerao, R.P. Bhalerao, D. Blaudez, W. Boerjan, A. Brun, A. Brunner, V. Busov, M. Campbell, J. Carlson, M. Chalot, J. Chapman, G.L. Chen, D. Cooper, P.M. Coutinho, J. Couturier, S. Covert, Q. Cronk, R. Cunningham, J. Davis, S. Degroeve, A. Dejardin, C. Depamphilis, J. Detter, B. Dirks, I. Dubchak, S. Duplessis, J. Ehlting, B. Ellis, K. Gendler, D. Goodstein, M. Gribskov, J. Grimwood, A. Groover, L. Gunter, B. Hamberger, B. Heinze, Y. Helariutta, B. Henrissat, D. Holligan, R. Holt, W. Huang, N. Islam-Faridi, S. Jones, M. Jones-Rhoades, R. Jorgensen, C. Joshi, J. Kangasjarvi, J. Karlsson, C. Kelleher, R. Kirkpatrick, M. Kirst, A. Kohler, U. Kalluri, F. Larimer, J. Leebens-Mack, J C. Leple, P. Locascio, Y. Lou, S. Lucas, F. Martin, B. Montanini, C. Napoli, D.R. Nelson, C. Nelson, K. Nieminen, O. Nilsson, V. Pereda, G. Peter, R. Philippe, G. Pilate, A. Poliakov, J. Razumovskaya, P. Richardson, C. Rinaldi, K. Ritland, P. Rouze, D. Ryaboy, J. Schmutz, J. Schrader, B. Segerman, H. Shin, A. Siddiqui, F. Sterky, A. Terry, C.J. Tsai, E. Uberbacher, P. Unneberg, J. Vahala, K. Wall, S. Wessler, G. Yang, T. Yin, C. Douglas, M. Marra, G. Sandberg, Y. Van de Peer, and D. Rokhsar. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
Via, S. 2012. Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philosophical Transactions of the Royal Society B-Biological Sciences 367: 451-460.
Zeng, Y.F., W J. Liao, R.J. Petit, and D.Y. Zhang. 2010. Exploring species limits in two closely related Chinese oaks. Plos One 5: 15.
Zhang, R., A.L. Hipp, and O. Gailing. 2015. Sharing of chloroplast haplotypes among red oak species suggests interspecific gene flow between neighboring populations. Botany 93: 691-700.
Zhu, J., J.C. Jeong, Y. Zhu, I. Sokolchik, S. Miyazaki, J.K. Zhu, P.M. Hasegawa, H.J. Bohnert, H. Shi, D.J. Yun, and R.A. Bressan. 2008. Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proceedings of the National Academy of Sciences of the United States of America 105: 4945-4950.