Differences in physiological and biochemical responses to summer drought of Pinus nigra subsp. pallasiana and Pinus brutia in a natural mixed stand

Abstract

Understanding how tree species respond to drought in their natural environment is needed to predict forest adaptation and management practices under global environmental changes. This study was carried out to determine and compare physiological and biochemical responses to variations in environmental conditions during summer drought of mixed natural stands of Pinus nigra Arn. subsp. pallasiana (Lamb.) Holmboe and Pinus brutia Ten. Midday xylem water potential (Ψ_md), water relations, photosynthetic pigments, total soluble sugar and proline contents were investigated during the growing season. Ψ_md followed a similar seasonal trend in both species but P. nigra subsp. pallasiana had higher Ψ_md than P. brutia. The Ψ_md gradually decreased from June, reached its lowest value in August, and then increased again. Gradual decreases in the osmotic potential at turgor loss point (Ψ_пTLP) were observed during the summer. Generally, Ψ_пTLP was lower in P. brutia. Total soluble sugars decreased from April to June for P. brutia, then increased and stayed relatively constant August to October. Similar changes were found at lower values in P. nigra subsp. pallasiana. Prolin accumulation and photosynthetic pigments were higher in P. brutia. The results indicate that physiological and biochemical responses of both species against changing environmental conditions were in different degrees but followed similar trends. P. nigra subsp. pallasiana is more sensitive to summer drought than P. brutia in their natural environment.

Keywords

Pinus nigra subsp. pallasiana / Pinus brutia / Osmotic potential / Photosynthetic pigments / Soluble sugars / Proline / Summer drought

References

[1] Arnon DI. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol, 1949, 24(1): 1-15.

[2] Atalay İ, Efe R. Ecological attributes and distribution of Anatolian black pine [Pinus nigra Arnold. subsp. pallasiana Lamb. Holmboe] in Turkey. J Environ Biol, 2012, 33: 509-519.

[3] Bandurska H, Plachta M, Woszczyk M. Seasonal patterns of free proline and carbohydrate levels in cherry laurel (Prunus laurocerasus) and ivy (Hederea helix) leaves and resistance to freezing and water deficit. Dendrobiology, 2009, 62: 3-9.

[4] Bansal S, Germino MJ. Temporal variation of nonstructural carbohydrates in montane conifers: similarities and differences among developmental stages, species and environmental conditions. Tree Physiol, 2009, 29: 559-568.

[5] Barbaroux C, Bréda N, Dufrêne E. Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica). New Phytol, 2003, 157(3): 605-615.

[6] Basu S, Ramegowda V, Kumar A, Pereira A. Plant adaptation to drought stress. Research, 2016, 1554: 1-10.

[7] Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil, 1973, 39: 205-207.

[8] Blum A. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ, 2017, 40: 4-10.

[9] Boscaiu M, Mora E, Fola O, Scridon S, Llinares J, Vicente O. Osmolyte accumulation in xerophytes as a response to environmental stress. Bull UASVM Hortic, 2009, 66(1): 96-102.

[10] Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Zhang Y, Hao G. Water relations and hydraulic architecture in cerrado trees: adjustments to seasonal changes in water availability and evaporative demand. Braz J Plant Physiol, 2008, 20(3): 233-245.

[11] Buras A, Schunk C, Zeiträg C, Herrmann C, Kaiser L, Lemme H, Straub C, Taeger S, Gößwein S, Klemmt H, Menzel A. Are Scots pine forest edges particularly prone to drought-induced mortality?. Environ Res Lett, 2018, 13: 025001.

[12] Çolak AH, Odabaşı T. Silvikültürel Planlama, 2004, Istanbul: Istanbul University (in Turkish)

[13] Daoudi H, Derridj A, Hannachi L, Mevy JP. Growth, ectomycorrhization and biochemical parameters of Quercus suber L. seedlings under drought conditions. Afr J Biotechnol, 2016, 15(38): 2082-2090.

[14] Deligöz A. Seasonal changes in the physiological characteristics of Anatolian black pine and the effect on seedling quality. Turk J Agric For, 2011, 35: 23-30.

[15] Deligöz A, Bayar E. Variations in physiological and biochemical traits of drought-stressed Quercus cerris seedlings. Turk J For, 2017, 18(4): 269-274.

[16] Deligoz A, Gur M. Morphological, physiological and biochemical responses to drought stress of Stone pine (Pinus pinea L.) seedlings. Acta Physiol Plant, 2015, 37: 243.

[17] Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for the determination of sugars and related substances. Ann Chem, 1956, 28(3): 350-356.

[18] Elvira S, Alonso R, Castillo FJ, Gimeno BS. On the response of pigments and antioxidants of Pinus halepensis seedlings to mediterranean climatic factors and long-term ozone exposure. New Phytol, 1998, 138: 419-432.

[19] Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA. Plant drought stress: Effects, mechanisms and management. Agron Sustain Dev, 2009, 29(1): 185-212.

[20] Gao DH, Gao Q, Xu HY, Ma F, Zhao CM, Liu JQ. Physiological responses to gradual drought stress in the diploid hybrid Pinus densata and its two parental species. Trees, 2009 23 4 717

[21] Gruber A, Pirkebner D, Oberhuber W, Wieser G. Spatial and seasonal variations in mobile carbohydrates in Pinus cembra in the timberline ecotone of the central Austrian Alps. Eur J For Res, 2011, 130: 173-179.

[22] Hatfield JL, Prueger JH. Temperature extremes: Effect on plant growth and development. Weather Clim Extreme, 2015, 10: 4-10.

[23] Hernández EI, Vilagrosa A, Pausas JG, Bellot J. Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol, 2010, 207: 233-244.

[24] Hyyryläinen A, Rautio P, Turunen M, Huttunen S. Seasonal and inter-annual variation in the chlorophyll content of three co-existing sphagnum species exceeds the effect of solar UV reduction in a subarctic peatland. Springer Plus, 2015 4 1 478

[25] Jaiswal A, Singh NK, Shekhawat GS, Aktar M, Jaiswal JP. Proline biosynthesis and accumulation in plants: a review. ITAS, 2010, 2(4): 651-660.

[26] Kancheva R, Borisova D, Georgiev G. Chlorophyll assessment and stress detection from vegetation optical properties. Ecol Eng Environ Prot, 2014, 1: 34-43.

[27] Kandemir G, Önde S, Temel F, Kaya Z. Population variation in drought resistance and its relationship with adaptive and physiological seedling traits in Turkish red pine (Pinus brutia Ten.). Turk J Biol, 2017, 41: 256-267.

[28] Major JE, Johnsen KH. Shoot water relations of mature black spruce families displaying a genotype x environment ınteraction in growth rate. II. Temporal trends and response to varying soil water conditions. Tree Physiol, 1999, 19: 375-382.

[29] Mandre M, Tullus H, Klošeiko J. Partitioning of carbohydrates and biomass of needles in scots pine canopy. Z Naturforsch, 2002, 57: 296-302.

[30] Merchant A, Arndt SK, Rowell DM, Posch S, Callister A, Tausz M, Mark Adams A. Seasonal changes in carbohydrates, cyclitols, and water relations of 3 field grown Eucalyptus species from contrasting taxonomy on a common site. Ann For Sci, 2010 67 1 104

[31] Mildrexler D, Yang Z, Cohen WB, Bell DM. A forest vulnerability index based on drought and high temperatures. Proc SPIE, 2016, 173: 314-325.

[32] Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SSO. Leaf water relations during summer water deficit: differential responses in turgor maintenance and variation in leaf structure among different plant communities in south-western Australia. Plant Cell Environ, 2008, 31: 1791-1802.

[33] Naor A. Midday stem water potenial as a plant water stress ındicator for ırrigation scheduling in fruit trees. Acta Hortic, 2000, 537: 447-454.

[34] Oleksyn J, Zytkowiak R, Karolewski P, Reich PB, Tjoelker MG. Genetic and environmental control of seasonal carbohydrate dynamics in trees of diverse Pinus sylvestris populations. Tree Physiol, 2000, 20: 837-847.

[35] Pardos M, Jıménez MD, Aranda I, Puértolas J, Pardos JA. Water relations of cork oak (Quercus suber L.) seedlings in response to shading and moderate drought. Ann For Sci, 2005, 62: 377-384.

[36] Parker WC, Pallardy SG. Leaf and root osmotic adjustment in drought-stressed Quercus alba, Q. macrocarpa, and Q. stellata seedlings. Can J For Res, 1988, 18(1): 1-5.

[37] Raftoyannis Y, Radoglou K. Physiological responses of beech and sessile oak in a natural mixed stand during a dry summer. Ann Bot, 2002, 89: 723-730.

[38] Regier N, Streb S, Zeeman SC, Frey B. Seasonal changes in starch and sugar content of poplar (Populus deltoides × nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiol, 2010, 30: 979-987.

[39] Ritchie GA. Duryea ML, Thomas DL. Assessing seedling quality. Forest nursery manual: production of bareroot seedlings, 1984, Hague: Martinus Nijhoff/Dr W Junk 243 260

[40] Sala A, Piper F, Hoch G. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol, 2010, 186: 274-281.

[41] Sauceda JU, Rodriguez HG, Lozano RR, Silva IC, Meza MG, Larga L. Seasonal trends of chlorophylls a and b carotenoids in native trees and shrubs of Northeastern Mexico. J Biol Sci, 2008, 8(2): 258-267.

[42] Sheikh AQ, Pandit AK, Ganai BA. Seasonal variation in chlorophyll content of some selected plant species of Yousmarg grassland ecosystem. Asian J Plant Sci Res, 2017, 7(2): 33-36.

[43] Solomou AD, Proutsos ND, Karetsos G, Tsagari K. Effects of climate change on vegetation in Mediterranean forests: a review. Int J Environ Agric Biotech, 2017, 2: 240-247.

[44] Tognetti R, Raschi A, Jones MB. Seasonal patterns of tissue water relations in three Mediterranean shrubs co-occurring at a natural CO₂ spring. Plant Cell Environ, 2000, 23: 1341-1351.

[45] Tyree MT, Hammel HT. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot, 1972, 23: 267-282.

[46] Viljevac M, Dugalić K, Mihaljević I, Šimić D, Sudar R, Jurković Z, Lepeduš H. Chlorophyll content, photosynthetic efficiency and genetic markers in two sour cherry (Prunus cerasus L.) genotypes under drought stress. Acta Bot Croat, 2013, 72(2): 221-235.

[47] White AD, Turner CN, Galbraith HJ. Leaf water relations and stomal behavior of four allopatric Eucalyptus species planted in Mediterranean southwestern Australia. Tree Physiol, 2000, 20: 1157-1165.

[48] Zhang JX, Nguyen HT, Blum A. Genetic analysis of osmotic adjustment in crop plants. J Exp Bot, 1999, 50(332): 291-302.

[49] Zolfaghar S, Villalobos-Vega R, Cleverly J, Eamus D. Co-ordination among leaf water relations and xylem vulnerability to embolism of Eucalyptus trees growing along a depth-to-groundwater gradient. Tree Physiol, 2015, 35: 732-743.