Advertisement

Trees

, Volume 31, Issue 5, pp 1479–1490 | Cite as

Biochemical responses to drought, at the seedling stage, of several Romanian Carpathian populations of Norway spruce (Picea abies L. Karst)

  • Sorin T. Schiop
  • Mohamad Al Hassan
  • Adriana F. Sestras
  • Monica Boscaiu
  • Radu E. Sestras
  • Oscar Vicente
Original Article
Part of the following topical collections:
  1. Drought Stress

Abstract

Key message

Norway spruce seedlings apparently showing a relatively higher tolerance to drought can be easily selected using a battery of biomarkers such as water content, chlorophyll, and proline levels in the needles, and could be eventually used as an initial screening method in reforestation programmes.

Abstract

Norway spruce is a native European coniferous species distributed from the Carpathian Mountains and the Alps to northern Scandinavia. In the coming decades, spruce forests will need to cope with increasing climate changes which are already threatening their natural habitats. To identify reliable water stress biomarkers in this species, which may be eventually used to select populations responding better to forecasted drought events, we studied the physiological responses to severe water stress treatments (6-week withholding irrigation in the greenhouse) of 1-year-old spruce seedlings originating from several locations in the Romanian Carpathian Mountains. Variations in the levels of the studied photosynthetic pigments, osmolytes, and non-enzymatic antioxidants were detected across the spruce populations. Several of the parameters determined in seedling needles, such as the decrease in water content (nearly 40% reduction in the most sensitive populations), the degradation of chlorophylls, or a low increase of proline levels (up to sevenfold increment in the most sensitive populations but no change in the most tolerant), could be employed as biomarkers for an early assessment of water stress at this stage. Furthermore, seedlings from two of the populations under study responded better to water stress than the other populations and also seemed to be the least affected by osmotic stress during seed germination. Therefore, the determination of these biochemical markers at early seedling stages could represent a useful tool for the initial screening of populations with relatively high tolerance to drought, warranting further research for their potential use in spruce reforestation programmes.

Keywords

Biomarkers Drought Norway spruce Reforestation Seedlings 

Notes

Acknowledgements

This work was partly carried out under the frame of the European Social Fund, Human Resources Development Operational Programme 2007–2013, Project No. POSDRU/159/1.5/S/132765. We thank the two unknown reviewers, whose useful comments helped us to considerably improve the manuscript.

Compliance with ethical standards

Conflict of interests

The authors declare no conflict of interests.

References

  1. Abdul-Baki AA, Anderson JD (1973) Relationship between decarboxilation of glutamic acid and vigour in soybean seed. Crop Sci 13:222–226Google Scholar
  2. Al Hassan M, Martínez Fuertes M, Ramos Sánchez FJ, Vicente O, Boscaiu M (2015) Effects of salt and water stress on plant growth and on accumulation of osmolytes and antioxidant compounds in cherry tomato. Not Bot Horti Agrobo 43:1–11. doi: 10.15835/nbha4319793 Google Scholar
  3. Al Hassan M, Chaura J, López-Gresa MP, Borsai O, Daniso E, Donat-Torres MP, Mayoral O, Vicente O, Boscaiu M (2016a) Native-invasive plants vs. halophytes in Mediterranean salt marshes: stress tolerance mechanisms in two related species. Front. Plant Sci 7:473. doi: 10.3389/fpls.2016.00473 Google Scholar
  4. Al Hassan M, López-Gresa MP, Boscaiu M, Vicente O (2016b) Stress tolerance mechanisms in Juncus: responses to salinity and drought in three Juncus species adapted to different natural environments. Funct Plant Biol 43:949–960CrossRefGoogle Scholar
  5. Al Hassan M, Morosan M, López-Gresa MP, Prohens J, Vicente O, Boscaiu M (2016c) Salinity-induced variation in biochemical markers provides insight into the mechanisms of salt tolerance in common (Phaseolus vulgaris) and runner (P. coccineus) beans. Int J Mol Sci 17:1582. doi: 10.3390/ijms17091582 CrossRefPubMedCentralGoogle Scholar
  6. Al Hassan M, Pacurar A, López-Gresa MP, Donat-Torres MP, Llinares JV, Boscaiu M, Vicente O (2016d) Effects of salt stress on three ecologically distinct Plantago species. PLoS One 11(8):e0160236. doi: 10.1371/journal.pone.0160236 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Al Hassan M, Chaura J, Donat-Torres MP, Boscaiu M, Vicente O (2017) Antioxidant responses under salinity and drought in three closely related wild monocots with different ecological optima. AoB Plants 9(2):plx009. doi: 10.1093/aobpla/plx009 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, 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 drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. doi: 10.1016/j.foreco.2009.09.001 CrossRefGoogle Scholar
  9. Alonso R, Elvira S, Castillo FJ, Gimeno BS (2001) Interactive effects of ozone and drought stress on pigments and activities of antioxidative enzymes in Pinus halepensis. Plant Cell Environ 24:905–916CrossRefGoogle Scholar
  10. Bartels D, Sunkar T (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  11. Bates LS, Waldren RP, Teare LD (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. doi: 10.1007/BF00018060 CrossRefGoogle Scholar
  12. Bautista I, Boscaiu M, Lidón A, Llinares JV, Lull C, Donat MP, Mayoral O, Vicente O (2016) Environmentally induced changes in antioxidant phenolic compounds levels in wild plants. Acta Physiol Plant 38:9. doi: 10.1007/s11738-015-2025-2 CrossRefGoogle Scholar
  13. Ben-Gal A, Borochov-Neori H, Yermiyahu U, Shani U (2009) Is osmotic potential a more appropriate property than electrical conductivity for evaluating whole-plant response to salinity? Environ Exp Bot 65:232–237CrossRefGoogle Scholar
  14. Bhaskaran S, Smith RH, Newton RJ (1985) Physiological changes in cultured Sorghum cells in response to induced water stress. Plant Physiol 79:266–269. doi: 10.1104/pp.79.1.266 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Blainski A, Lopes GC, de Mello JCP (2013) Application and analysis of the Folin Ciocalteu method for the determination of the total phenolic content from Limonium brasiliense L. Molecules 18:6852–6865. doi: 10.3390/molecules18066852 CrossRefPubMedGoogle Scholar
  16. Bolte A, Ammer C, Löf M, Madsen P, Nabuurs GJ, Schall P, Spathelf P, Rock J (2009) Adaptive forest management in central Europe: climate change impacts, strategies and integrative concept. Scand J For Res 24:473–482. doi: 10.1080/02827580903418224 CrossRefGoogle Scholar
  17. Bradshaw RHW, Holmqvist BH, Cowling SA, Sykes MT (2000) The effects of climate change on the distribution and management of Picea abies in southern Scandinavia. Can J For Res 30:1992–1998CrossRefGoogle Scholar
  18. Clancy KM, Wagner MR, Reich PB (1995) Ecophysiology and insect herbivory. In: Smith WK, Hinckley TM (eds) Ecophysiology of coniferous forests. Academic Press, San Diego, pp 125–180CrossRefGoogle Scholar
  19. Cuculeanu V, Tuinea P, Bălteanu D (2002) Climate change impacts in Romania: vulnerability and adaptation options. Geo J 57:203–209. doi: 10.1023/B:GEJO.0000003613.15101.d9 Google Scholar
  20. Cyr DR, Buxton GF, Webb DP, Dumbroff EB (1990) Accumulation of free amino acids in the shoots and roots of three northern conifers during drought. Tree Physiol 6:293–303. doi: 10.1093/treephys/6.3.293 CrossRefPubMedGoogle Scholar
  21. Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wotton BM (2001) Climate change and forest disturbances. BioScience 51:723–734CrossRefGoogle Scholar
  22. Ditmarová L, Kurjak D, Palmroth S, Kmet J, Strelcová K (2010) Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiol 30:205–213. doi: 10.1093/treephys/tpp116 CrossRefPubMedGoogle Scholar
  23. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. doi: 10.1021/ac60111a017 CrossRefGoogle Scholar
  24. EEA (2004) Projected temperature changes in Europe up to 2080. http://www.eea.europa.eu. Accessed 16 Aug 2016
  25. Ellis RH, Roberts EH (1981) The quantification of aging and survival in orthodox seeds. Seed Sci Technol 9:373–409Google Scholar
  26. EUFGIS (2011) Portal Gene reserve forests. European Commission under the Council Regulation (EC) No. 870/2004. http://www.portal.eufgis.org. Accessed 17 Jan 2016
  27. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212. doi: 10.1051/agro:2008021 CrossRefGoogle Scholar
  28. Gall R, Landolt W, Schleppi P, Michellod V, Bucher JB (2002) Water content and bark thickness of Norway spruce (Picea abies) stems: phloem water capacitance and xylem sap flow. Tree Physiol 22:613–623CrossRefPubMedGoogle Scholar
  29. Gil R, Boscaiu M, Lull C, Bautista I, Lidón A, Vicente O (2013) Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct Plant Biol 40:805–818Google Scholar
  30. Gilliam FS (2016) Forest ecosystems of temperate climatic regions: from ancient use to climate change. New Phytol 212:871–887. doi: 10.1111/nph.14255 CrossRefPubMedGoogle Scholar
  31. Green S, Ray D (2009) Potential impacts of drought and disease on forestry in Scotland. Forestry Commission Research Note. http://www.forestry.gov.uk/pdf/FCRN004.pdf/$FILE/FCRN004.pdf. Accessed 29 Aug 2016
  32. Grossnickle SC (2000) Ecophysiology of northern spruce species: the performance of planted seedlings. NRC Research Press, OttawaGoogle Scholar
  33. Guo J, Yang Y, Wang G, Yang L, Sun X (2010) Ecophysiological responses of Abies fabri seedlings to drought stress and nitrogen supply. Physiol Plant 139:335–347PubMedGoogle Scholar
  34. Hanewinkel M, Cullmann DA, Schelhaas MJ, Nabuurs GJ, Zimmermann NE (2013) Climate change may cause severe loss in the economic value of European forest land. Nat Clim Change 3:203–207. doi: 10.1038/nclimate1687 CrossRefGoogle Scholar
  35. Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271. doi: 10.1104/pp.110.161752 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hart SJ, Veblen TT, Eisenhart KS, Jarvis D, Kulakowski D (2014) Drought induces spruce beetle (Dendroctonus rufipennis) outbreaks across northwestern Colorado. Ecology 95:930–939. doi: 10.1890/13-0230.1 CrossRefPubMedGoogle Scholar
  37. Hernández Y, Alegre L, Munné-Bosch S (2004) Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol 24:1303–1311CrossRefPubMedGoogle Scholar
  38. Heuer B (2010) Role of proline in plant response to drought and salinity. In: Pessarakli M (ed) Handbook of plant and crop stress. CRC Press, Boca Raton, pp 213–238Google Scholar
  39. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438CrossRefPubMedGoogle Scholar
  40. Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105Google Scholar
  41. Jansson G, Danusevicius D, Grotehusman H, Kowalczyk J, Krajmerova D, Skroppa T, Wolf H (2013) Norway Spruce (Picea abies (L.) H. Karst. In: Pâques LE (ed) Forest tree breeding in Europe: current state-of-the art and perspectives. Springer, Dordrecht, pp 123–176CrossRefGoogle Scholar
  42. Ježík M, Blaženec M, Letts MG, Ditmarová L, Sitková Z, Střelcová K (2014) Assessing seasonal drought stress response in Norway spruce (Picea abies (L.) Karst. by monitoring stem circumference and sap flow. Ecohydrology. doi: 10.1002/eco.1536 Google Scholar
  43. Jiménez S, Dridi J, Gutierrez D, Moret D, Irigoyen JJ, Moreno MA, Gogorcena Y (2013) Physiological, biochemical and molecular responses in four Prunus rootstocks submitted to drought stress. Tree Physiol 33:1061–1075CrossRefPubMedGoogle Scholar
  44. Kahle HP, Unseld R, Spiecker H (2005) Forest ecosystems in a changing environment: growth patterns as indicators for stability of Norway spruce within and beyond the limits of its natural range. In: Bohn U, Hettwer C, Gollub G (eds) Application and analysis of the map of the natural vegetation of Europe. Bundesamt für Naturschutz, Bonn, pp 399–409Google Scholar
  45. Kantar M, Lucas SJ, Budak H (2011) Drought stress: molecular genetics and genomics approaches. Adv Bot Res 57:445–493CrossRefGoogle Scholar
  46. Kazda M (2005) Results from the SUSTMAN Project (EU Framework 5, QLK5-CT-2002-00851). http://www.sustman.de. Accessed 30 Aug 2016
  47. Kivimäenpää M, Sutinen S, Karlsson PE, Selldén G (2003) Cell structural changes in the needles of Norway spruce exposed to long-term ozone and drought. Ann Bot 92:779–793. doi: 10.1093/aob/mcg202 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kolström M, Lindner M, Vilén T, Maroschek M, Seidl R, Lexer MJ, Netherer S, Kremer A, Delzon S, Barbati A, Marchetti M, Corona P (2011) Reviewing the science and implementation of climate change adaptation measures in European forestry. Forests 2:961–982. doi: 10.3390/f2040961 CrossRefGoogle Scholar
  49. Kravka M, Krejzar T, Cermak J (1999) Water content in stem wood of large pine and spruce trees in natural forests in central Sweden. Agric For Meteorol 98–99:555–562CrossRefGoogle Scholar
  50. Lei Y, Yin C, Li C (2006) Differences in some morphological, physiological and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiol Plant 127:182–191CrossRefGoogle Scholar
  51. Lévesque M (2013) Drought response of five conifers along an ecological gradient in Central Europe: a multiproxydendroecological analysis. Dissertation, ETH ZurichGoogle Scholar
  52. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. doi: 10.1042/bst0110591 CrossRefGoogle Scholar
  53. Lindner M (2000) Developing adaptive forest management strategies to cope with climate change. Tree Physiol 20:299–307CrossRefGoogle Scholar
  54. Maaten-Theunissen M, Kahle HP, Maaten E (2013) Drought sensitivity of Norway spruce is higher than that of silver fir along an altitudinal gradient in south western Germany. Ann For Sci 70:185–193. doi: 10.1007/s13595-012-0241-0 CrossRefGoogle Scholar
  55. Marshall JG, Rutledge RG, Blumwald E, Dumbroff EB (2000) Reduction in turgid water volume in jack pine, white spruce and black spruce in response to drought and paclobutrazol. Tree Physiol 20:701–707CrossRefPubMedGoogle Scholar
  56. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. doi: 10.1111/j.1469-8137.2008.02436.x CrossRefPubMedGoogle Scholar
  57. Mejnartowicz L, Lewandowski A (2007) Biochemical genetics. In: Mark GT, Adam B, Wladyslaw B (eds) Biology and ecology of Norway spruce. Forestry sciences. Springer, Dordrecht, pp 147–155Google Scholar
  58. Miron MS, Sumalan RL (2015) Physiological responses of Norway spruce (Picea abies [L.] Karst) seedlings to drought and overheating stress conditions. JHFB 19:146–151Google Scholar
  59. Mitchell AF (1972) Conifers in the British Isles: a descriptive handbook. Forestry Commission Booklet No. 33, HMSO, LondonGoogle Scholar
  60. Modrzynski J (2007) Ecology. In: Tjoelker MG, Boratynski A, Bugala W (eds) Biology and ecology of Norway spruce. Springer, Dordrecht, pp 195–220CrossRefGoogle Scholar
  61. Montwe 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 28:891–900. doi: 10.1007/s00468-014-1002-5 CrossRefGoogle Scholar
  62. Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 35:299–319CrossRefGoogle Scholar
  63. Munné-Bosch S, Peñuelas J (2004) Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Sci 166:1105–1110CrossRefGoogle Scholar
  64. Munns R, Termaat A (1986) Whole-plant responses to salinity. Aust J Plant Physiol 13:143–160CrossRefGoogle Scholar
  65. Pardo-Domènech LL, Tifrea A, Grigore MN, Boscaiu M, Vicente O (2015) Proline and glycine betaine accumulation in two succulent halophytes under natural and experimental conditions. Plant Biosyst 150:904–915CrossRefGoogle Scholar
  66. Patel JA, Vora AB (1985) Free proline accumulation in drought-stressed plants. Plant Soil 84:427–429. doi: 10.1007/BF02275480 CrossRefGoogle Scholar
  67. Popović M, Šuštar V, Gričar J, Štraus I, Torkar G, Kraigher H, de Marco A (2016) Identification of environmental stress biomarkers in seedlings of European beech (Fagus sylvatica) and Scots pine (Pinus sylvestris). Can J For Res 46:58–66CrossRefGoogle Scholar
  68. Radu S, Contescu L, Herta I, Burza E, Rosca T (1994) Pepiniere- Metode şi procedee pentru cultura în pepinieră a principalelor specii forestiere şi ornamentale. Institutul de Cercetări şi Amenajări Silvice, BucureştiGoogle Scholar
  69. Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731. doi: 10.4161/psb.6.11.17613 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rasband WS (1997–2012) ImageJ. US National Institutes of Health, Bethesda, Maryland. http://rsb.info.nih.gov/ij/. Accessed on 23 Jan 2016
  71. Saura-Mas S, Lloret F (2007) Leaf and shoot water content and leaf dry matter content of Mediterranean woody species with different post-fire regenerative strategies. Ann Bot 99:545–554. doi: 10.1093/aob/mcl284 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Schiop ST, Al Hassan M, Sestras AF, Boscaiu M, Sestras RE, Vicente O (2015) Identification of salt stress biomarkers in Romanian Carpathian populations of Picea abies (L.) Karst. PLoS One 10(8):e0135419. doi: 10.1371/journal.pone.0135419 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS One 7(6):e38554. doi: 10.1371/journal.pone.0038554 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Spiecker H (2000) Growth of Norway spruce (Picea abies [L.] Karst.) under changing environmental conditions in Europe. In: Klimo E, Hager H, Kulhavy J (eds) Spruce monocultures in Central Europe—problems and prospects, vol 33. European Forest Institute Proceedings, pp 11–26Google Scholar
  75. Sudachkova NE, Milyutina IL, Semenova GP (2002) Influence of water deficit on contents of carbohydrates and nitrogenous compounds in Pinus sylvestris L. and Larix sibirica Ledeb. tissues. Eur J For Res 4:1–11Google Scholar
  76. Tan W, Blake TJ, Boyle TJB (1992) Drought tolerance in faster- and slower-growing black spruce (Picea mariana) progenies: II. Osmotic adjustment and changes of soluble carbohydrates and amino acids under osmotic stress. Physiol Plant 85:645–651. doi: 10.1111/j.1399-3054.1992.tb04767.x CrossRefGoogle Scholar
  77. Toldi O, Tuba Z, Scott P (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci 176:187–199. doi: 10.1016/j.plantsci.2008.10.002 CrossRefGoogle Scholar
  78. Walker XJ, Mack MC, Johnstone JF (2015) Stable carbon isotope analysis reveals widespread drought stress in boreal black spruce forests. Glob Chang Biol 21:3102–3113. doi: 10.1111/gcb.12893 CrossRefPubMedGoogle Scholar
  79. Yang Y, Yao Y, Zhang X (2010) Comparison of growth and physiological responses to severe drought between two altitudinal Hippophae rhamnoides populations. Silva Fenn 44:603–614Google Scholar
  80. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559CrossRefGoogle Scholar
  81. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar
  82. Zrig A, Ben Mohamed H, Tounekti T, Ennajeh M, Valero D, Khemira H (2015) A comparative study of salt tolerance of three almond rootstocks: contribution of organic and inorganic solutes to osmotic adjustment. J Agric Sci Technol 17:675–689Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Sorin T. Schiop
    • 1
    • 2
  • Mohamad Al Hassan
    • 2
    • 5
  • Adriana F. Sestras
    • 1
  • Monica Boscaiu
    • 3
  • Radu E. Sestras
    • 4
  • Oscar Vicente
    • 2
  1. 1.Department of Forestry, Faculty of HorticultureUniversity of Agricultural Sciences and Veterinary MedicineCluj-NapocaRomania
  2. 2.Institute of Plant Molecular and Cellular Biology (IBMCP, UPV-CSIC)Universitat Politècnica de ValènciaValenciaSpain
  3. 3.Mediterranean Agroforest Institute (IAM, UPV)Universitat Politècnica de ValènciaValenciaSpain
  4. 4.Department of Horticulture and Landscaping, Faculty of HorticultureUniversity of Agricultural Sciences and Veterinary MedicineCluj-NapocaRomania
  5. 5.The New Zealand Institute for Plant & Food Research Ltd.AucklandNew Zealand

Personalised recommendations