Signatures of local adaptation to current and future climate in phenology-related genes in natural populations of Quercus robur.
Bud-burst phenology
Candidate genes
Forest tree
Genotype-environment association
Local adaptation
Sequence capture
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
19 Jan 2024
19 Jan 2024
Historique:
received:
27
02
2023
accepted:
12
12
2023
medline:
20
1
2024
pubmed:
20
1
2024
entrez:
19
1
2024
Statut:
epublish
Résumé
Local adaptation is a key evolutionary process that enhances the growth of plants in their native habitat compared to non-native habitats, resulting in patterns of adaptive genetic variation across the entire geographic range of the species. The study of population adaptation to local environments and predicting their response to future climate change is important because of climate change. Here, we explored the genetic diversity of candidate genes associated with bud burst in pedunculate oak individuals sampled from 6 populations in Poland. Single nucleotide polymorphism (SNP) diversity was assessed in 720 candidate genes using the sequence capture technique, yielding 18,799 SNPs. Using landscape genomic approaches, we identified 8 F The model revealed that pedunculate oak populations in the eastern part of the analyzed geographical region are the most sensitive to climate change. Our results might offer an initial evaluation of a potential management strategy for preserving the genetic diversity of pedunculate oak.
Sections du résumé
BACKGROUND
BACKGROUND
Local adaptation is a key evolutionary process that enhances the growth of plants in their native habitat compared to non-native habitats, resulting in patterns of adaptive genetic variation across the entire geographic range of the species. The study of population adaptation to local environments and predicting their response to future climate change is important because of climate change.
RESULTS
RESULTS
Here, we explored the genetic diversity of candidate genes associated with bud burst in pedunculate oak individuals sampled from 6 populations in Poland. Single nucleotide polymorphism (SNP) diversity was assessed in 720 candidate genes using the sequence capture technique, yielding 18,799 SNPs. Using landscape genomic approaches, we identified 8 F
CONCLUSIONS
CONCLUSIONS
The model revealed that pedunculate oak populations in the eastern part of the analyzed geographical region are the most sensitive to climate change. Our results might offer an initial evaluation of a potential management strategy for preserving the genetic diversity of pedunculate oak.
Identifiants
pubmed: 38243199
doi: 10.1186/s12864-023-09897-y
pii: 10.1186/s12864-023-09897-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
78Subventions
Organisme : Narodowe Centrum Nauki
ID : 2012/04/A/NZ9/00500
Organisme : Narodowe Centrum Nauki
ID : 2012/04/A/NZ9/00500
Organisme : Narodowe Centrum Nauki
ID : 2012/04/A/NZ9/00500
Organisme : Ministerstwo Edukacji i Nauki
ID : 008/RID/2018/19
Organisme : Ministerstwo Edukacji i Nauki
ID : 008/RID/2018/19
Organisme : Ministerstwo Edukacji i Nauki
ID : 008/RID/2018/19
Informations de copyright
© 2024. The Author(s).
Références
Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl. 2008;1(1):95–111.
pubmed: 25567494
pmcid: 3352395
doi: 10.1111/j.1752-4571.2007.00013.x
Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecol Lett. 2004;7(12):1225–41.
doi: 10.1111/j.1461-0248.2004.00684.x
Gonzalez-Martinez SC, Krutovsky KV, Neale DB. Forest-tree population genomics and adaptive evolution. New Phytol. 2006;170(2):227–38.
pubmed: 16608450
doi: 10.1111/j.1469-8137.2006.01686.x
de Villemereuil P, Gaggiotti OE, Mouterde M, Till-Bottraud I. Common garden experiments in the genomic era: new perspectives and opportunities. Heredity. 2016;116(3):249–54.
pubmed: 26486610
doi: 10.1038/hdy.2015.93
Alberto FJ, Aitken SN, Alia R, Gonzalez-Martinez SC, Hanninen H, Kremer A, Lefevre F, Lenormand T, Yeaman S, Whetten R, et al. Potential for evolutionary responses to climate change - evidence from tree populations. Glob Chang Biol. 2013;19(6):1645–61.
pubmed: 23505261
pmcid: 3664019
doi: 10.1111/gcb.12181
Savolainen O, Pyhäjärvi T, Knürr T. Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst. 2007;38(1):595–619.
doi: 10.1146/annurev.ecolsys.38.091206.095646
Aitken SN, Bemmels JB. Time to get moving: assisted gene flow of forest trees. Evol Appl. 2016;9(1):271–90.
pubmed: 27087852
doi: 10.1111/eva.12293
Bower AD, Aitken SN. Ecological genetics and seed transfer guidelines for Pinus albicaulis (Pinaceae). Am J Bot. 2008;95(1):66–76.
pubmed: 21632316
doi: 10.3732/ajb.95.1.66
Sork VL, Aitken SN, Dyer RJ, Eckert AJ, Legendre P, Neale DB. Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate. Tree Genet Genomes. 2013;9(4):901–11.
doi: 10.1007/s11295-013-0596-x
Rellstab C, Gugerli F, Eckert AJ, Hancock AM, Holderegger R. A practical guide to environmental association analysis in landscape genomics. Mol Ecol. 2015;24(17):4348–70.
pubmed: 26184487
doi: 10.1111/mec.13322
Storfer A, Patton A, Fraik AK. Navigating the interface between landscape genetics and landscape genomics. Front Genet. 2018;9:68.
pubmed: 29593776
pmcid: 5859105
doi: 10.3389/fgene.2018.00068
Fitzpatrick MC, Keller SR. Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation. Ecol Lett. 2015;18(1):1–16.
pubmed: 25270536
doi: 10.1111/ele.12376
Petit RJ, Carlson J, Curtu AL, Loustau M-L, Plomion C, González-Rodríguez A, Sork V, Ducousso A. Fagaceae trees as models to integrate ecology, evolution and genomics. New Phytol. 2013;197(2):369–71.
pubmed: 23253330
doi: 10.1111/nph.12089
Cannon CH, Brendel O, Deng M, Hipp AL, Kremer A, Kua C-S, Plomion C, Romero-Severson J, Sork VL. Gaining a global perspective on Fagaceae genomic diversification and adaptation. New Phytol. 2018;218(3):894–7.
pubmed: 29658637
doi: 10.1111/nph.15101
Cavender-Bares J. Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution. New Phytol. 2019;221(2):669–92.
pubmed: 30368821
doi: 10.1111/nph.15450
Leuschner C, Backes K, Hertel D, Schipka F, Schmitt U, Terborg O, Runge M. Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and wet years. For Ecol Manage. 2001;149(1):33–46.
doi: 10.1016/S0378-1127(00)00543-0
Gentilesca T, Camarero J, Colangelo M, Nolè A, Ripullone F. Drought-induced oak decline in the western Mediterranean region: an overview on current evidences, mechanisms and management options to improve forest resilience. iForest - Biogeosciences and Forestry. 2017;10(5):796–806.
doi: 10.3832/ifor2317-010
Alberto F, Bouffier L, Louvet JM, Lamy JB, Delzon S, Kremer A. Adaptive responses for seed and leaf phenology in natural populations of sessile oak along an altitudinal gradient. J Evol Biol. 2011;24(7):1442–54.
pubmed: 21507119
doi: 10.1111/j.1420-9101.2011.02277.x
Gugger PF, Cokus SJ, Sork VL. Association of transcriptome-wide sequence variation with climate gradients in valley oak (Quercus lobata). Tree Genet Genomes. 2016;12(2):15.
doi: 10.1007/s11295-016-0975-1
Homolka A, Schueler S, Burg K, Fluch S, Kremer A. Insights into drought adaptation of two European oak species revealed by nucleotide diversity of candidate genes. Tree Genet Genomes. 2013;9(5):1179–92.
doi: 10.1007/s11295-013-0627-7
Koehler K, Center A, Cavender-Bares J. Evidence for a freezing tolerance–growth rate trade-off in the live oaks (Quercus series Virentes) across the tropical–temperate divide. New Phytol. 2012;193(3):730–44.
pubmed: 22171967
doi: 10.1111/j.1469-8137.2011.03992.x
Ramírez-Valiente JA, Koehler K, Cavender-Bares J. Climatic origins predict variation in photoprotective leaf pigments in response to drought and low temperatures in live oaks (Quercus series Virentes). Tree Physiol. 2015;35(5):521–34.
pubmed: 25939867
doi: 10.1093/treephys/tpv032
Rellstab C, Zoller S, Walthert L, Lesur I, Pluess AR, Graf RE, Bodenes C, Sperisen C, Kremer A, Gugerli F. Signatures of local adaptation in candidate genes of oaks (Quercus spp.) with respect to present and future climatic conditions. Mol Ecol. 2016;25(23):5907–24.
pubmed: 27759957
doi: 10.1111/mec.13889
Sork VL. Gene flow and natural selection shape spatial patterns of genes in tree populations: implications for evolutionary processes and applications. Evol Appl. 2016;9(1):291–310.
pubmed: 27087853
doi: 10.1111/eva.12316
Pina-Martins F, Baptista J, Pappas G Jr, Paulo OS. New insights into adaptation and population structure of cork oak using genotyping by sequencing. Glob Chang Biol. 2019;25(1):337–50.
pubmed: 30358018
doi: 10.1111/gcb.14497
Riordan EC, Gugger PF, Ortego J, Smith C, Gaddis K, Thompson P, Sork VL. Association of genetic and phenotypic variability with geography and climate in three southern California oaks. Am J Bot. 2016;103(1):73–85.
pubmed: 26758886
doi: 10.3732/ajb.1500135
Gharehaghaji M, Minor ES, Ashley MV, Abraham ST, Koenig WD. Effects of landscape features on gene flow of valley oaks (Quercus lobata). Plant Ecol. 2017;218(4):487–99.
doi: 10.1007/s11258-017-0705-2
Sork VL, Squire K, Gugger PF, Steele SE, Levy ED, Eckert AJ. Landscape genomic analysis of candidate genes for climate adaptation in a California endemic oak, Quercus lobata. Am J Bot. 2016;103(1):33–46.
pubmed: 26744482
doi: 10.3732/ajb.1500162
Martins K, Gugger PF, Llanderal-Mendoza J, Gonzalez-Rodriguez A, Fitz-Gibbon ST, Zhao JL, Rodriguez-Correa H, Oyama K, Sork VL. Landscape genomics provides evidence of climate-associated genetic variation in Mexican populations of Quercus rugosa. Evol Appl. 2018;11(10):1842–58.
pubmed: 30459833
pmcid: 6231481
doi: 10.1111/eva.12684
Gugger PF, Fitz-Gibbon ST, Albarran-Lara A, Wright JW, Sork VL. Landscape genomics of Quercus lobata reveals genes involved in local climate adaptation at multiple spatial scales. Mol Ecol. 2021;30(2):406–23.
pubmed: 33179370
doi: 10.1111/mec.15731
Vanhove M, Pina-Martins F, Coelho AC, Branquinho C, Costa A, Batista D, Príncipe A, Sousa P, Henriques A, Marques I, et al. Using gradient Forest to predict climate response and adaptation in Cork oak. J Evol Biol. 2021;34(6):910–23.
pubmed: 33484040
doi: 10.1111/jeb.13765
Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen TH. From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can J Bot. 2003;81(12):1247–66.
doi: 10.1139/b03-141
Hänninen H, Tanino K. Tree seasonality in a warming climate. Trends Plant Sci. 2011;16(8):412–6.
pubmed: 21640632
doi: 10.1016/j.tplants.2011.05.001
Dantec CF, Vitasse Y, Bonhomme M, Louvet JM, Kremer A, Delzon S. Chilling and heat requirements for leaf unfolding in European beech and sessile oak populations at the southern limit of their distribution range. Int J Biometeorol. 2014;58(9):1853–64.
pubmed: 24452386
doi: 10.1007/s00484-014-0787-7
Olsen JE, Lee Y, Junttila O. Effect of alternating day and night temperature on short day-induced bud set and subsequent bud burst in long days in Norway spruce. Front Plant Sci. 2014;5:691.
pubmed: 25538722
pmcid: 4260492
doi: 10.3389/fpls.2014.00691
Memmott J, Craze PG, Waser NM, Price MV. Global warming and the disruption of plant–pollinator interactions. Ecol Lett. 2007;10(8):710–7.
pubmed: 17594426
doi: 10.1111/j.1461-0248.2007.01061.x
Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol. 2013;169:156–73.
doi: 10.1016/j.agrformet.2012.09.012
CaraDonna PJ, Iler AM, Inouye DW. Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci. 2014;111(13):4916–21.
pubmed: 24639544
pmcid: 3977233
doi: 10.1073/pnas.1323073111
Sakurai A, Takahashi K. Flowering phenology and reproduction of the Solidago virgaurea L. complex along an elevational gradient on Mt Norikura, central Japan. Plant Spec Biol. 2017;32(4):270–8.
doi: 10.1111/1442-1984.12153
Sampaio T, Branco M, Guichoux E, Petit RJ, Pereira JS, Varela MC, Almeida MH. Does the geography of cork oak origin influence budburst and leaf pest damage? For Ecol Manage. 2016;373:33–43.
doi: 10.1016/j.foreco.2016.04.019
Vitasse Y, Delzon S, Bresson CC, Michalet R, Kremer A. Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J For Res. 2009;39(7):1259–69.
doi: 10.1139/X09-054
Müller M, Seifert S, Finkeldey R. A candidate gene-based association study reveals SNPs significantly associated with bud burst in European beech (Fagus sylvatica L.). Tree Genet Genomes. 2015;11(6):1–13.
doi: 10.1007/s11295-015-0943-1
Muller M, Seifert S, Finkeldey R. Comparison and confirmation of SNP-bud burst associations in European beech populations in Germany. Tree Genet Genomes. 2017;13(3):59.
doi: 10.1007/s11295-017-1145-9
Derory J, Leger P, Garcia V, Schaeffer J, Hauser MT, Salin F, Luschnig C, Plomion C, Glossl J, Kremer A. Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol. 2006;170(4):723–38.
pubmed: 16684234
doi: 10.1111/j.1469-8137.2006.01721.x
Lesur I, Le Provost G, Bento P, Da Silva C, Leple JC, Murat F, Ueno S, Bartholome J, Lalanne C, Ehrenmann F, et al. The oak gene expression atlas: insights into Fagaceae genome evolution and the discovery of genes regulated during bud dormancy release. BMC Genomics. 2015;16(1):112.
pubmed: 25765701
pmcid: 4350297
doi: 10.1186/s12864-015-1331-9
Le Provost G, Lalanne C, Lesur I, Louvet J-M, Delzon S, Kremer A, Labadie K, Aury J-M, Da Silva C, Moritz T, et al. Oak stands along an elevation gradient have different molecular strategies for regulating bud phenology. BMC Plant Biol. 2023;23(1):108.
pubmed: 36814198
pmcid: 9948485
doi: 10.1186/s12870-023-04069-2
Derory J, Scotti-Saintagne C, Bertocchi E, Le Dantec L, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodenes C, Alberto F, et al. Contrasting relationships between the diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity. 2010;104(5):438–48.
pubmed: 19812610
doi: 10.1038/hdy.2009.134
Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, Gonzalez-Martinez SC, Neale DB. Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics. 2010;185(3):969–82.
pubmed: 20439779
pmcid: 2907212
doi: 10.1534/genetics.110.115543
Holliday JA, Ritland K, Aitken SN. Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). New Phytol. 2010;188(2):501–14.
pubmed: 20663060
doi: 10.1111/j.1469-8137.2010.03380.x
Neale DB, Savolainen O. Association genetics of complex traits in conifers. Trends Plant Sci. 2004;9(7):325–30.
pubmed: 15231277
doi: 10.1016/j.tplants.2004.05.006
Meger J, Ulaszewski B, Burczyk J. Genomic signatures of natural selection at phenology-related genes in a widely distributed tree species Fagus sylvatica L. BMC Genomics. 2021;22(1):583.
pubmed: 34332553
pmcid: 8325806
doi: 10.1186/s12864-021-07907-5
Plomion C, Aury JM, Amselem J, Leroy T, Murat F, Duplessis S, Faye S, Francillonne N, Labadie K, Le Provost G, et al. Oak genome reveals facets of long lifespan. Nat Plants. 2018;4(7):440–52.
pubmed: 29915331
pmcid: 6086335
doi: 10.1038/s41477-018-0172-3
Quang ND, Ikeda S, Harada K. Nucleotide variation in Quercus crispula Blume. Heredity. 2008;101(2):166–74.
pubmed: 18506204
doi: 10.1038/hdy.2008.42
Dering M, Lewandowski A, Ufnalski K, Kedzierska A. How far to the east was the migration of white oaks from the Iberian refugium? Silva Fennica. 2008;42(3):327.
doi: 10.14214/sf.240
Chmielewski M, Meyza K, Chybicki I, Dzialuk A, Litkowiec M, Burczyk J. Chloroplast microsatellites as a tool for phylogeographic studies: the case of white oaks in Poland. IForest - Biogeosciences Forestry. 2015;0(0):964–70.
Degen B, Yanbaev Y, Mader M, Ianbaev R, Bakhtina S, Schroeder H, Blanc-Jolivet C. Impact of gene flow and introgression on the range wide genetic structure of Quercus robur (L.) in Europe. Forests. 2021;12(10):1425.
doi: 10.3390/f12101425
De Mita S, Thuillet AC, Gay L, Ahmadi N, Manel S, Ronfort J, Vigouroux Y. Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol Ecol. 2013;22(5):1383–99.
pubmed: 23294205
doi: 10.1111/mec.12182
Lotterhos KE, Whitlock MC. The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Mol Ecol. 2015;24(5):1031–46.
pubmed: 25648189
doi: 10.1111/mec.13100
Heide OM. Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant. 1993;88(4):531–40.
pubmed: 28741760
doi: 10.1111/j.1399-3054.1993.tb01368.x
Saxe H, Cannell MGR, Johnsen Ø, Ryan MG, Vourlitis G. Tree and forest functioning in response to global warming. New Phytol. 2001;149(3):369–99.
pubmed: 33873342
doi: 10.1046/j.1469-8137.2001.00057.x
Caffarra A, Donnelly A. The ecological significance of phenology in four different tree species: effects of light and temperature on bud burst. Int J Biometeorol. 2011;55(5):711–21.
pubmed: 21113629
doi: 10.1007/s00484-010-0386-1
Strømme CB, Schmidt E, Olsen JE, Nybakken L. Climatic effects on bud break and frost tolerance in the northernmost populations of Beech (Fagus sylvatica) in Europe. Trees. 2019;33(1):79–89.
doi: 10.1007/s00468-018-1760-6
Cox K, Vanden Broeck A, Van Calster H, Mergeay J. Temperature-related natural selection in a wind-pollinated tree across regional and continental scales. Mol Ecol. 2011;20(13):2724–38.
pubmed: 21623981
doi: 10.1111/j.1365-294X.2011.05137.x
De Kort H, Vandepitte K, Bruun HH, Closset-Kopp D, Honnay O, Mergeay J. Landscape genomics and a common garden trial reveal adaptive differentiation to temperature across Europe in the tree species Alnus glutinosa. Mol Ecol. 2014;23(19):4709–21.
pubmed: 24860941
doi: 10.1111/mec.12813
Huang C-L, Chang C-T, Huang B-H, Chung J-D, Chen J-H, Chiang Y-C, Hwang S-Y. Genetic relationships and ecological divergence in Salix species and populations in Taiwan. Tree Genet Genomes. 2015;11(3):39.
doi: 10.1007/s11295-015-0862-1
Jaramillo-Correa J-P, Rodríguez-Quilón I, Grivet D, Lepoittevin C, Sebastiani F, Heuertz M, Garnier-Géré PH, Alía R, Plomion C, Vendramin GG, et al. Molecular proxies for climate maladaptation in a long-lived tree (Pinus pinaster Aiton, Pinaceae). Genetics. 2014;199(3):793–807.
pubmed: 25549630
pmcid: 4349072
doi: 10.1534/genetics.114.173252
Depardieu C, Gérardi S, Nadeau S, Parent GJ, Mackay J, Lenz P, Lamothe M, Girardin MP, Bousquet J, Isabel N: Connecting tree-ring phenotypes, genetic associations, and transcriptomics to decipher the genomic architecture of drought adaptation in a widespread conifer. Mol Ecol. 2021, n/a(n/a).
Eckert AJ, Maloney PE, Vogler DR, Jensen CE, Mix AD, Neale DB. Local adaptation at fine spatial scales: an example from sugar pine (Pinus lambertiana, Pinaceae). Tree Genet Genomes. 2015;11(3).
Estrella N, Menzel A, Kramer U, Behrendt H. Integration of flowering dates in phenology and pollen counts in aerobiology: analysis of their spatial and temporal coherence in Germany (1992–1999). Int J Biometeorol. 2006;51(1):49–59.
pubmed: 16832654
doi: 10.1007/s00484-006-0038-7
Archetti M, Richardson AD, O’Keefe J, Delpierre N. Predicting climate change impacts on the amount and duration of autumn colors in a New England forest. PLoS ONE. 2013;8(3):e57373.
pubmed: 23520468
pmcid: 3592872
doi: 10.1371/journal.pone.0057373
Delpierre N, Dufrêne E, Soudani K, Ulrich E, Cecchini S, Boé J, François C. Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agric For Meteorol. 2009;149(6):938–48.
doi: 10.1016/j.agrformet.2008.11.014
Gill AL, Gallinat AS, Sanders-DeMott R, Rigden AJ, Short Gianotti DJ, Mantooth JA, Templer PH. Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies. Ann Bot. 2015;116(6):875–88.
pubmed: 25968905
pmcid: 4640124
doi: 10.1093/aob/mcv055
Jeong S-J, Medvigy D. Macroscale prediction of autumn leaf coloration throughout the continental United States. Glob Ecol Biogeogr. 2014;23(11):1245–54.
doi: 10.1111/geb.12206
Hinckley TM, Dougherty PM, Lassoie JP, Roberts JE, Teskey RO. A Severe drought: impact on tree growth, phenology, net photosynthetic rate and water relations. Am Midl Nat. 1979;102(2):307–16.
doi: 10.2307/2424658
Alberto FJ, Derory J, Boury C, Frigerio JM, Zimmermann NE, Kremer A. Imprints of natural selection along environmental gradients in phenology-related genes of Quercus petraea. Genetics. 2013;195(2):495–512.
pubmed: 23934884
pmcid: 3781976
doi: 10.1534/genetics.113.153783
McKown AD, Klápště J, Guy RD, Geraldes A, Porth I, Hannemann J, Friedmann M, Muchero W, Tuskan GA, Ehlting J, et al. Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa. New Phytol. 2014;203(2):535–53.
pubmed: 24750093
doi: 10.1111/nph.12815
Singh RK, Svystun T, AlDahmash B, Jonsson AM, Bhalerao RP. Photoperiod- and temperature-mediated control of phenology in trees - a molecular perspective. New Phytol. 2017;213(2):511–24.
pubmed: 27901272
doi: 10.1111/nph.14346
Deans JD, Harvey FJ. Frost hardiness of 16 European provenances of sessile oak growing in Scotland. Forestry Int J Forest Res. 1996;69(1):5–11.
doi: 10.1093/forestry/69.1.5
Ducousso A, Guyon J, Krémer A. Latitudinal and altitudinal variation of bud burst in western populations of sessile oak (Quercus petraea (Matt) Liebl). Ann For Sci. 1996;53(2–3):775–82.
doi: 10.1051/forest:19960253
Jensen JS. Provenance Variation in Phenotypic Traits in Quercus robur and Quercus petraea in Danish Provenance Trials. Scand J For Res. 2000;15(3):297–308.
doi: 10.1080/028275800447922
Wise MJ, Tunnacliffe A. POPP the question: what do LEA proteins do? Trends Plant Sci. 2004;9(1):13–7.
pubmed: 14729214
doi: 10.1016/j.tplants.2003.10.012
Pukacka S, Wójkiewicz E. Carbohydrate metabolism in Norway maple and sycamore seeds in relation to desiccation tolerance. J Plant Physiol. 2002;159(3):273–9.
doi: 10.1078/0176-1617-00641
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 2002;29(4):417–26.
pubmed: 11846875
doi: 10.1046/j.0960-7412.2001.01227.x
Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM. HANABA TARANU Is a GATA transcription factor that regulates shoot apical meristem and flower development in arabidopsis[W]. Plant Cell. 2004;16(10):2586–600.
pubmed: 15367721
pmcid: 520957
doi: 10.1105/tpc.104.024869
Yordanov YS, Ma C, Strauss SH, Busov VB. EARLY BUD-BREAK 1 (<i>EBB1</i>) is a regulator of release from seasonal dormancy in poplar trees. Proc Natl Acad Sci. 2014;111(27):10001–6.
pubmed: 24951507
pmcid: 4103365
doi: 10.1073/pnas.1405621111
Wang SY, Jiao HJ, Faust M. Changes in metabolic enzyme activities during thidiazuron-induced lateral budbreak of apple. HortScience. 1991;26(2):171–3.
doi: 10.21273/HORTSCI.26.2.171
Manel S, Poncet BN, Legendre P, Gugerli F, Holderegger R. Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina. Mol Ecol. 2010;19(17):3824–35.
pubmed: 20723057
doi: 10.1111/j.1365-294X.2010.04716.x
Geburek T, Myking T. Evolutionary consequences of historic anthropogenic impacts on forest trees in Europe. For Ecol Manage. 2018;422:23–32.
doi: 10.1016/j.foreco.2018.03.055
Aitken SN, Whitlock MC. Assisted gene flow to facilitate local adaptation to climate change. Annu Rev Ecol Evol Syst. 2013;44(1):367.
doi: 10.1146/annurev-ecolsys-110512-135747
Buschbom J, Yanbaev Y, Degen B. Efficient long-distance gene flow into an isolated relict oak stand. J Hered. 2011;102(4):464–72.
pubmed: 21525180
doi: 10.1093/jhered/esr023
Sork VL, Davis FW, Westfall R, Flint A, Ikegami M, Wang H, Grivet D. Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Nee) in the face of climate change. Mol Ecol. 2010;19(17):3806–23.
pubmed: 20723054
doi: 10.1111/j.1365-294X.2010.04726.x
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25(15):1965–78.
doi: 10.1002/joc.1276
Hijmans RJ, Guarino L, Mathur P. DIVA-GIS Version 7.5. Manual. In. 2012.
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carre G, Marquez JRG, Gruber B, Lafourcade B, Leitao PJ, et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography. 2013;36(1):27–46.
doi: 10.1111/j.1600-0587.2012.07348.x
Kaur P, Gaikwad K. From genomes to GENE-omes: exome sequencing concept and applications in crop improvement. Front Plant Sci. 2017;8:2164.
pubmed: 29312405
pmcid: 5742236
doi: 10.3389/fpls.2017.02164
Carsjens C, Ngoc QN, Guzy J, Knutzen F, Meier IC, Muller M, Finkeldey R, Leuschner C, Polle A. Intra-specific variations in expression of stress-related genes in beech progenies are stronger than drought-induced responses. Tree Physiol. 2014;34(12):1348–61.
pubmed: 25430883
doi: 10.1093/treephys/tpu093
Street NR, Skogstrom O, Sjodin A, Tucker J, Rodriguez-Acosta M, Nilsson P, Jansson S, Taylor G. The genetics and genomics of the drought response in Populus. Plant J. 2006;48(3):321–41.
pubmed: 17005011
doi: 10.1111/j.1365-313X.2006.02864.x
Evans LM, Slavov GT, Rodgers-Melnick E, Martin J, Ranjan P, Muchero W, Brunner AM, Schackwitz W, Gunter L, Chen JG, et al. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nat Genet. 2014;46(10):1089–96.
pubmed: 25151358
doi: 10.1038/ng.3075
Chen J, Tsuda Y, Stocks M, Kallman T, Xu N, Karkkainen K, Huotari T, Semerikov VL, Vendramin GG, Lascoux M. Clinal variation at phenology-related genes in spruce: parallel evolution in FTL2 and Gigantea? Genetics. 2014;197(3):1025–38.
pubmed: 24814465
pmcid: 4096357
doi: 10.1534/genetics.114.163063
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.
doi: 10.14806/ej.17.1.200
Del Fabbro C, Scalabrin S, Morgante M, Giorgi FM. An Extensive evaluation of read trimming effects on illumina ngs data analysis. PLoS ONE. 2013;8(12):e85024.
pubmed: 24376861
pmcid: 3871669
doi: 10.1371/journal.pone.0085024
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60.
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. 2013. arXiv preprint arXiv:13033997.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9.
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–59.
pubmed: 10835412
pmcid: 1461096
doi: 10.1093/genetics/155.2.945
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8.
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611–20.
pubmed: 15969739
doi: 10.1111/j.1365-294X.2005.02553.x
Earl DA, Vonholdt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4(2):359–61.
doi: 10.1007/s12686-011-9548-7
Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics. 2008;180(2):977–93.
pubmed: 18780740
pmcid: 2567396
doi: 10.1534/genetics.108.092221
Storey JD. The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Stat. 2003;31(6):2013–35.
doi: 10.1214/aos/1074290335
Frichot E, Schoville SD, Bouchard G, Francois O. Testing for associations between loci and environmental gradients using latent factor mixed models. Mol Biol Evol. 2013;30(7):1687–99.
pubmed: 23543094
pmcid: 3684853
doi: 10.1093/molbev/mst063
Frichot E, François O. LEA: AnRpackage for landscape and ecological association studies. Methods Ecol Evol. 2015;6(8):925–9.
doi: 10.1111/2041-210X.12382
Ellis N, Smith SJ, Pitcher CR. Gradient forests: calculating importance gradients on physical predictors. Ecology. 2012;93(1):156–68.
pubmed: 22486096
doi: 10.1890/11-0252.1
Strobl C, Boulesteix A-L, Kneib T, Augustin T, Zeileis A. Conditional variable importance for random forests. BMC Bioinformatics. 2008;9(1):307.
pubmed: 18620558
pmcid: 2491635
doi: 10.1186/1471-2105-9-307
Gower JC: Statistical methods of comparing different multivariate analyses of the same data In: Mathematics in the archaeological and historical sciences. Edited by R. HF, G. KD, P. T. Edinburgh, UK: Edinburgh University Press; 1971: 138–149.
Dunne JP, Horowitz LW, Adcroft AJ, Ginoux P, Held IM, John JG, Krasting JP, Malyshev S, Naik V, Paulot F, et al. The GFDL earth system model version 41 (GFDL-ESM 41): overall coupled model description and simulation characteristics. J Adv Model Earth Syst. 2020;12(11):e2019MS002015.
doi: 10.1029/2019MS002015