Drought Stress Adaptation in Norway Spruce and Related Genomics Work

  • Jaroslav KlápštěEmail author
  • Jonathan Lecoy
  • María del Rosario García-Gil
Part of the Compendium of Plant Genomes book series (CPG)


Ongoing climate change has resulted in more frequent occurrences of stress events including droughts. Global warming affects all living organisms, especially forest trees. Norway spruce has become the dominant forestation species in Central Europe thanks to historical directions in forest stands management. However, the species is more drought stress sensitive compared to others such as silver fir or European beech. Therefore, health and productivity of local forests may be jeopardized when prolonged drought periods become a common phenomenon. Nevertheless, moderate levels of genetic variability in response to drought stress have been identified, between provenances, as well as among individuals within provenances, and thus, in this respect, selection for genetically superior planting stock is worthwhile. Drought stress response is mainly driven by the flexibility in stomata closure to prevent further water loss as a direct reaction to intrinsic water potential change; stomatal closure is controlled through the phytohormone abscisic acid (ABA). The development of a more complex root system via root tips and root hairs elongation to improve soil water search, as well as presence of specific pit membrane structures (torus) between xylem tracheids, which limits the propagation of embolisms, serve as additional protective measures against drought stress in spruce. To better understand the genetic architecture of drought tolerance, several genome-wide approaches such as quantitative trait locus (QTL) mapping, gene expression profiling, or association studies have been implemented. QTL analyses suggest a positive relationship between stomatal conductance and water use efficiency and a favorable relationship with growth. Among many GWAS derived genetic associations, genes encoding proteins for phytohormones biosynthesis and signaling implicated in abiotic stress responses (such as ABA) were identified. These recent genomics studies suggest several key players in genetic resistance to drought in Norway spruce, intriguingly, also some candidates conserved across distantly related conifer species. We conclude by providing directions for future research into drought resistance under the pressing need to identify the best locally adapted planting stock for future climates.


Drought tolerance Gene expression GWAS Stress response mechanisms Genetic variability 


  1. Albert M, Schmidt M (2010) Climate-sensitive modelling of site-productivity relationships for Norway spruce (Picea abies (L.) Karst.) and common beech (Fagus sylvatica L.). For Ecol Manag 259:739–749Google Scholar
  2. Albert M, Nagel R-V, Nuske RS, Sutmöller J, Spellmann H (2017) Tree species selection in the face of drought risk – uncertainty in forest planning. Forests 8:363Google Scholar
  3. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH (Ted), Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010). A global overview of drougth and heat induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684Google Scholar
  4. Aranda I, Alia R, Ortega U, Dantas AK, Majada J (2010) Intra-specific variability in biomass partitioning and carbon isotopic discrimination under moderate drought stress in seedlings from four Pinus pinaster populations. Tree Genet Genomes 6:169–178Google Scholar
  5. Attia Z, Domec JC, Oren R, Way DA, Moshelion M (2015) Growth and physiological responses of isohydric and anisohydric poplars to drought. J Exp Bot 66:4373–4381PubMedPubMedCentralGoogle Scholar
  6. Ballester J, Rodó X, Giorgi F (2010) Future changes in Central Europe heat waves expected to mostly follow summer mean warming. Clim Dyn 35:1191–1205Google Scholar
  7. Batth R, Singh K, Kumari S, Mustafiz A (2017) Transcript profiling reveals the presence of abiotic stress and developmental stage specific ascorbate oxidase genes in plants. Front Plant Sci 8:198PubMedPubMedCentralGoogle Scholar
  8. Battipaglia G, Saurer M, Cherubini P, Siegwolf RTW, Cotrufo MF (2009) Tree rings indicate different drought resistance of a native (Abies alba Mill.) and a non-native (Picea abies (L.) Karst.) species co-occurring at a dry site in Southern Italy. For Ecol Manag 257:820–828Google Scholar
  9. Beniston M, Stephenson DB, Christensen OB, Ferro CAT, Frei C, Goyette S, Halsnaes K, Holt T, Jylhä K, Koffi B, Palutikof J, Schöll R, Semmler T, Woth K (2007) Future extreme events in European climate: an exploration of regional climate model projections. Clim Chang 81:71–95Google Scholar
  10. Blödner C, Skroppa T, Johnsen Ø, Polle A (2005). Freezing tolerance in two Norway spruce (Picea abies [L.] Karst.) progenies is physiologically correlated with drought tolerance. J Plant Physiol 162(5):549–558Google Scholar
  11. Boisvenue C, Running SW (2006) Impacts of climate change on natural forest productivity – evidence since the middle of the 20th century. Glob Chang Biol 12:862–882Google Scholar
  12. Brendel O, Pot D, Plomion C, Rozenberg P, Guehl J-M (2002) Genetic parameters and QTL analysis of δ13C and ring width in maritime pine. Plant Cell Environ 25(8):945–953Google Scholar
  13. Brini E, Fennell CJ, Fernandez-Serra M, Hribar-Lee B, Lukšič M, Dill KA (2017) How water’s properties are encoded in its molecular structure and energies. Chem Rev 117:12385–12414PubMedPubMedCentralGoogle Scholar
  14. Brodribb TJ, McAdam SAM (2013) Abscisic acid mediates a divergence in the drought response of two conifers. Plant Physiol 162:1370–1377PubMedPubMedCentralGoogle Scholar
  15. Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc Natl Acad Sci USA 111:14489–14493PubMedGoogle Scholar
  16. Burczyk J, Giertych M (1991) Response of Norway spruce (Picea abies (L.) Karst.) annual increments to drought for various provenances and locations. Silvae Genet 40:146–152Google Scholar
  17. Chakraborty D, Jandl R, Kapeller S, Schueler S (2019) Disentangling the role of climate and soil on tree growth and its interaction with seed origin. Sci Total Environ 654:393–401PubMedGoogle Scholar
  18. Chen J, Källman T, Ma X, Gyllenstrand N, Zaina G, Morgante M, Bousquet J, Eckert A, Wegrzyn J, Neale D, Lagercrantz U, Lascoux M (2012) Disentangling the roles of history and local selection in shaping clinal variation of allele frequencies and gene expression in Norway spruce (Picea abies). Genetics 191:865–881PubMedPubMedCentralGoogle Scholar
  19. Chen L, Huang J-G, Stadt KJ, Comeau PG, Zhai L, Dawson A, Ashraful Alam S (2017) Drought explains variation in the radial growth of white spruce in western Canada. Agric For Meteorol 233:133–142Google Scholar
  20. Chmura DJ, Guzicka M, McCulloh KA, Zytkowiak R (2016) Limited variation found among Norway spruce half-sib families in physical response to drought and resistance to embolism. Tree Physiol 36(2):252–266PubMedGoogle Scholar
  21. Daszkowska-Golec A, Szarejko I (2013) Open or close the gate – stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138PubMedPubMedCentralGoogle Scholar
  22. de Miguel M, Cabezas J-A, de María N, Sánchez-Gómez D, Guevara M-A, Vélez M-D, Sáez-Laguna E, Díaz L-M, Mancha J-A, Barbero M-C, Collada C, Díaz-Sala C, Aranda I, Cervera M-T (2014). Genetic control of functional traits related to photosynthesis and water use efficiency in Pinus pinaster Ait. drought response: integration of genome annotation, allele association and QTL detection for candidate gene identification. BMC Genomics 15:464Google Scholar
  23. Ditmarova L, Kurjak D, Palmroth S, Kmet J, Strelcova K (2010) Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiol 30:205–213PubMedGoogle Scholar
  24. Du M, Ding G, Cai Q (2018) The transcriptomic response of Pinus massoniana to drought stress. Forests 9(6):326Google Scholar
  25. Dubos C, Le Provost G, Pot D, Salin F, Lalane C, Madur D et al (2003) Identification and characterization of water-stress-responsive genes in hydroponically grown maritime pine (Pinus pinaster) seedlings. Tree Physiol 23:169–179PubMedGoogle Scholar
  26. Dulamsuren C, Abilova SB, Bektayeva M, Eldarov M, Schuldt B, Leuschner C, Hauck M (2018). Hydraulic architecture and vulnerability to drought-induced embolism in southern boreal tree species of Inner Asia. Tree Physiol tpy116,
  27. Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, Gonzalez-Martinez SC, Neale DB (2010). Patterns of population structure and environmental associations to aridity across the range of Loblolly pine (Pinus taeda L., Pinaceae). Genetics 185(3):969–982Google Scholar
  28. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Ann Rev Plant Physiol 33:317–345Google Scholar
  29. Fox H, Doron-Faigenboim A, Kelly G, Bourstein R, Attia Z, Zhou J, Moshe Y, Moshelion M, David-Schwartz R (2018) Transcriptome analysis of Pinus halepensis under drought stress and during recovery. Tree Physiol 38(3):423–441PubMedGoogle Scholar
  30. Gazol A, Camarero JJ, Anderegg WRL, Vicente-Serrano SM (2016) Impacts of droughts on the growth resilience of Northern Hemisphere forests. Glob Ecol Biogeogr. Scholar
  31. Gehring CA, Sthultz CM, Flores-Renteria L, Whipple AV, Whitham TG (2017) Tree genetics defines fungal partner communities that may confer drought tolerance. Proc Natl Acad Sci USA 114:11169–11174PubMedGoogle Scholar
  32. George J-P, Schueler S, Karanitsch-Ackerl S, Mayer K, Klumpp RT, Grabner M (2015) Inter- and intra-specific variation in drought sensitivity in Abies spec, and its relation to wood density and growth traits. Agric For Meteorol 214–215:430–443PubMedPubMedCentralGoogle Scholar
  33. González-Martínez SC, Krutovsky KV, Neale DB (2006) Forest-tree population genomics and adaptive evolution. New Phytol 170(2):227–238Google Scholar
  34. Haas JC, Vergara A, Hurry V, Street NR (2019). Candidate regulators and target genes of drought stress in needles and roots of Norway spruce.
  35. Hammond WM, Adams HD (2019). Dying on time: traits influencing the dynamics of tree mortality risk from drought. Tree Physiol 00:tzp050Google Scholar
  36. Hartmann H, Ziegler W, Trumbore S (2013) Lethal drought leads to reduction in non-structural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427Google Scholar
  37. Heinimann HR (2010) A concept in adaptive ecosystem management – an engineering perspective. For Ecol Manag 259:848–856Google Scholar
  38. Kapeller S, Lexer MJ, Geburek T, Hiebl J, Schueler S (2012) Intraspecific variation in climate response of Norway spruce in the eastern Alpine range: selecting appropriate provenances for future climate. For Ecol Manag 271:46–57Google Scholar
  39. Kellomaki S, Peltola H, Nuutinen T, Korhonen KT, Strandman H (2008) Sensitivity of managed boreal forests in Finland to climate change, with implications to adaptive management. Philos Trans R Soc B 363:2341–2351Google Scholar
  40. Klisz M, Buras A, Sass-Klaassen U, Puchalka R, Koprowski M, Ukalska J (2019) Limitations at the limits? Diminishing of genetic effects in Norway spruce provenance trials. Front Plant Sci 10:306. Scholar
  41. Kohler M, Sohn J, Nagele G, Bauhus J (2010). Can drought tolerance of Norway spruce (Picea abies (L.) Karst.) be increased through thinning? Eur J For Res 129(6):1109–1118Google Scholar
  42. Körner C (2019) No need for pipes when the well is dry – a comment on hydraulic failure in trees. Tree Physiol 39:695–700PubMedGoogle Scholar
  43. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316PubMedGoogle Scholar
  44. Lauder JD, Moran EV, Hart SC (2019). Fight or flight? Potential tradeoffs between drought defense and reproduction in conifers. Tree Physiol 00:tpz031Google Scholar
  45. Laur J, Hacke UG (2014) Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling. New Phytol 203:388–400PubMedGoogle Scholar
  46. Le Provost G, Domergue F, Lalanne C, Campos PR, Grosbois A, Bert D, Meredieu C, Danjon F, Plomion C, Gion J-M (2013) Soil water stress affects both cuticular wax content and cuticle-related gene expression in young saplings of maritime pine (Pinus pinaster Ait). BMC Plant Biol 13:95PubMedPubMedCentralGoogle Scholar
  47. Levesque M, Saurer M, Siegwolf R, Eilmann B, Brang P, Bugmann H, Rigling A (2013) Drought response of five conniver species under contrasting water availability suggests high vulnerability of Norway spruces and European larch. Glob Chang Biol 19:3184–3199PubMedGoogle Scholar
  48. Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manag 259:698–709Google Scholar
  49. López de Herdia U, Váyquez-Poletti JL (2016) RNA-seq analysis in forest tree species: bioinformatic problems and solutions. Tree Genet Genomes 12:30Google Scholar
  50. Lu P, Biron P, Bréda N, Granier A (1995) Water relations of adult Norway spruce (Picea abies (L) Karst) under soil drought in the Vosges mountains: water potential, stomatal conductance and transpiration. Ann For Sci 52:117–129Google Scholar
  51. Ma F, Xu TT, Ji MF, Zhao CM (2014). Differential drought tolerance in tree populations from contrasting environments. AoB Plants 6:plu069.
  52. MacAllister S, Mencuccini M, Sommer U, Engel J, Hudson A, Salmon Y, Dexter KG (2019). Drought-induced mortality in Scots pine: opening the metabolic black box. Tree Physiol 00:tpz049Google Scholar
  53. Marguerit E, Bouffier L, Chancerel E, Costa P, Lagane F, Guehl J-M, Plomion C, Brendel O (2014) The genetics of water-use efficiency and its relation to growth in maritime pine. J Exp Bot 65(17):4757–4768PubMedPubMedCentralGoogle Scholar
  54. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braveman MS, Chen Y-J, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, He Ho C, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim J-B, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedPubMedCentralGoogle Scholar
  55. Miles C, Wayne M (2008) Quantitative trait locus (QTL) analysis. Nat Educ 1(1):208Google Scholar
  56. Mayr S, Gruber A, Bauer H (2003) Repeated freeze-thaw cycles induce embolism in drought stressed conifers (Norway spruce, stone pine). Planta 217:436–441PubMedGoogle Scholar
  57. Montwé D, Spiecker H, Hamann A (2014) An experimentally controlled extreme drought in a Norway spruce forest reveals fast hydraulic response and subsequent recovery of growth rates. Trees 28:891Google Scholar
  58. Moran E, Lauder J, Musser C, Stathos A, Shu M (2017) The genetics of drought tolerance in conifers. New Phytol 216(4):1034–1048PubMedGoogle Scholar
  59. Morgan JM (1984) Osmoregulation and water stress in higher plants. Ann Rev Plant Physiol 35:299–319Google Scholar
  60. Mottonen M, Aphalo PJ, Lehto T (2001) Role of boron in drought resistance in Norway spruce (Picea abies) seedlings. Tree Physiol 21:673–681PubMedGoogle Scholar
  61. Myers-Smith IH, Myers JH (2018). Comment on “Precipitation drives global variation in natural selection”. Science 359(6375):eaan5028.
  62. Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9(7):325–330PubMedGoogle Scholar
  63. Neale DB, Kremer A (2011) Forest tree genomics: Growing resources and applications. Nat Rev Genet 12(2):111–122PubMedGoogle Scholar
  64. Neuman M, Mues V, Moreno A, Hasenauer H, Seidl R (2017) Climate variability drives recent tree mortality in Europe. Glob Chang Biol 23(11):4788–4797Google Scholar
  65. Nonami H, Boyer JS (1993) Direct demonstration of a growth-induced water potential gradients. Plant Physiol 102:13–19PubMedPubMedCentralGoogle Scholar
  66. Plomion C, Bartholomé J, Bouffier L, Brendel O, Cochard H, de Miguel M, Delzon S, Gion J-M, Gonzalez-Martinez SC, Guehl J-M, Lagraulet H, Le Provost G, Marguerit E, Porté A (2016) Understanding the genetic bases of adaptation to soil water deficit in trees through the examination of water use efficiency and cavitation resistance: maritime pine as case study. J Plant Hydraul 3:e008Google Scholar
  67. Rosner S, Klein A, Müller U, Karlsson B (2007) Hydraulic and mechanical properties of young Norway spruce clones related to growth and wood structure. Tree Physiol 27(8):1179–1188Google Scholar
  68. Rosner S, Svetlik J, Andreassen K, Borja I, Dalsgaard L, Evans R, Karlsson B, Tollefsrud MM, Solberg S (2013) Wood density as a screening trait for drought sensitivity in Norway spruce. Can J For Res 44(2):154–161Google Scholar
  69. Ruehr NK, Grote R, Mayr S, Arneth A (2019). Beyond the extreme: recovery of carbon and water relations in woody plants following heat and drought stress. Tree Physiol 00:tpz032Google Scholar
  70. Saibo NJM, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623PubMedGoogle Scholar
  71. Salmon Y, Dietrich L, Sevanto S, Hölttä T, Dannoura M, Epron D (2019) Drought impacts on tree phloem: from cell-level responses to ecological significance. Tree Physiol 39:173–191PubMedGoogle Scholar
  72. Savi T, Casolo V, Dal Borgo A, Rosner S, Torboli V, Stenni B, Bertoncin P, Martllos S, Pallavicini A, Nardini A (2019). Drought-induced dieback of Pinus nigra: a tale of hydraulic failure and carbon starvation. Conserv Physiol 7(1):coz012Google Scholar
  73. Schaefer C, Grams TEE, Rotzer T, Feldermann A, Pretzsch H (2017) Drought stress reaction of growth and Δ13 C in tree rings of European beech and Norway spruce in monospecific versus mixed stands along precipitation gradient. Forests 8(6):177. Scholar
  74. Serra-Maluquer X, Mencuccini M, Martinez-Vilalta J (2018) Changes in tree resistance, recovery and resilience across three successive extreme droughts in the northeast Iberian Peninsula. Oecologia 187:343–354PubMedGoogle Scholar
  75. Sheffield J, Wood EF (2008) Projected changes in drought occurrence under future global warming from multi-model, multi-scenario, IPCC AR4 simulations. Clim Dyn 31:79–105Google Scholar
  76. Siepielski AM, Morrissey MB, Buoro M, Carlson SM, Caruso CM, Clegg SM, Coulson T, DiBattista J, Gotanda KM, Francis CD, Hereford J, Kingsolver JG, Augustine KE, Kruuk LE, Martin RA, Sheldon BC, Sletvold N, Svensson EI, Wade MJ, MacColl AD (2017) Precipitation drives global variation in natural selection. Science 355(6328):959–962PubMedGoogle Scholar
  77. Soloway AD, Amiro BD, Dunn AL, Wofsy SC (2017) Carbon neutral or a sink? Uncertainty caused by gap -filling long-term flux measurements for an old-growth boreal black spruce forest. Agr For Meteorol 233:110–121Google Scholar
  78. Sonesson J, Eriksson G (2010) Genetic variation in drought tolerance in Picea abies seedlings and its relationship to growth in controlled and filed experiments. Scand J For Res 18:7–18Google Scholar
  79. Speich MJR (2019). Quantifying and modeling water availability in temperate forests: a review of drought and aridity indices. iForest 12:1–16Google Scholar
  80. Stival Sena J, Giguère I, Rigault P, Bousquet J, Mackay J (2018) Expansion of the gene family in the Pinaceae is associated with considerable structural diversity and drought-responsive expression. Tree Physiol 38(3):442–456PubMedGoogle Scholar
  81. Swann ALS, Hoffman FM, Koven CD, Randerson JT (2016) Plant responses to increasing CO2 reduce estimates of climate impacts on drought severity. Proc Natl Acad Sci USA 113(36):10019–10024PubMedGoogle Scholar
  82. Taiz L, Zeiger E, Møller IM, Murphy A (2015). Plant physiology and development, 6th edn. Sinauer Associates, Inc.Google Scholar
  83. Tardieu F, Simonneau T, Muller B (2018) The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Ann Rev Plant Biol 69:733–759Google Scholar
  84. Thiele JC, Nuske RS, Ahrends B, Panferov O, Albert M, Staupendahl K, Junghans U, Jansen M, Saborowski J (2017) Climate change impact assessment – a simulation experiment with Norway spruce for a forest district in Central Europe. Ecol Model 346:30–47Google Scholar
  85. Tomasella M, Häberle K-H, Nardini A, Hesse B, Machlet A, Matyssek R (2017) Post-drought hydraulic recovery is accompanied by non-structural carbohydrate depletion in the stem wood of Norway spruce samplings. Sci Rep 7:14308PubMedPubMedCentralGoogle Scholar
  86. Trujillo-Moya C, George J-P, Fluch S, Geburek T, Grabner M, Karanitsch-Ackerl S, Konrad H, Mayer K, Sehr EM, Wischnitzki E, Schueler S (2018). Drought sensitivity of Norway spruce at the species’ warmest fringe: quantitative and molecular analysis reveals high genetic variation among and within provenances. G3-Genes Genomes Genet 8:1225–1245Google Scholar
  87. Tuberosa R (2012) Phenotyping for drought tolerance of crops in the genomics era. Front Physiol 3:347PubMedPubMedCentralGoogle Scholar
  88. Turtola S, Manninen A-M, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J Chem Ecol 29:1981–1995PubMedGoogle Scholar
  89. Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161PubMedPubMedCentralGoogle Scholar
  90. Vitali V, Buntgen U, Bauhus J (2017) Silver fir and Douglas fir are more tolerant to extreme droughts than Norway spruce in south-west Germany. Glob Chang Biol 23:5108–5119PubMedGoogle Scholar
  91. Wallin G, Karlsson PE, Selldén G, Ottosson S, Medin E-L, Pleijel H, Skärby L (2002) Impact of four years exposure to different levels of ozone, phosphorus and drought on chlorophyll, mineral nutrients, and stem volume of Norway spruce, Picea abies. Physiol Plant 114:192–206PubMedGoogle Scholar
  92. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697PubMedPubMedCentralGoogle Scholar
  93. Wolf JBW (2013) Principles of transcriptome analysis and gene expression quantification: an RNA-seq tutorial. Mol Ecol Res 13:559–572Google Scholar
  94. Woodall CW, Oswalt CM, Westfall JA, Perry CH, Nelson MD, Finley AO (2010) Selecting tree species for testing climate change migration hypotheses using forest inventory data. For Ecol Manag 259:778–785Google Scholar
  95. Zang C, Hartl-Meier C, Dittmar C, Rothe A, Menzel A (2014) Patterns of drought tolerance in major European temperate forest trees: climatic drivers and levels of variability. Glob Chang Biol 20(12):3767–3779PubMedGoogle Scholar
  96. Zawaski C, Busov VB (2014) Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. PLoS ONE 9(1):e86217PubMedPubMedCentralGoogle Scholar
  97. Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119Google Scholar

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© © Crown  2020

Authors and Affiliations

  • Jaroslav Klápště
    • 1
    Email author
  • Jonathan Lecoy
    • 2
  • María del Rosario García-Gil
    • 2
  1. 1.Scion (New Zealand Forest Research Institute Ltd.)RotoruaNew Zealand
  2. 2.Department of Forest Genetics and Plant PhysiologyUmeå Plant Science Centre, Swedish University of Agricultural SciencesUmeåSweden

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