Abstract
We investigated the influence of 40 days of drought on growth, storage processes and primary photosynthetic processes in 3-month-old Scots pine and Norway spruce seedlings growing in perlite culture. Water stress significantly affected seedling water status, whereas absolute dry biomass growth was not substantially influenced. Water stress induced an increase in non-structural carbohydrate content (sugars, sugar alcohols, starch) in the aboveground part of pine seedlings in contrast to spruce seedlings. Due to the relatively low content of sugars and sugar alcohols in seedling organs, their expected contribution to osmotic potential changes was quite low. In contrast to biomass accumulation and storage, photosynthetic primary processes were substantially influenced by water shortage. In spruce seedlings, PSII was more sensitive to water stress than PSI. In particular, electron transport in PSI was stable under water stress despite the substantial decrease of electron transport in PSII. The increase in thermal energy dissipation due to enhancement of non-photochemical quenching (NPQ) was evident in both species under water stress. Simultaneously, the yields of non-regulated energy dissipation in PSII were decreased in pine seedlings under drought. A relationship between growth, photosynthetic activities and storage processes is analysed under weak water deficit.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ETC:
-
Electron transport chain
- NPQ:
-
Non-photochemical quenching
- NSC:
-
Non-structural carbohydrates
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- PTOX:
-
Plastoquinol terminal oxidases
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- WHC:
-
Water-holding capacity
References
Allakhverdiev SI (2011) Recent progress in the study of structure and function of photosystem II. J Photochem Photobiol B 104:1–8. https://doi.org/10.1016/j.jphotobiol.2011.03.010
Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinactivation: influence of a new phenolic compound. Biochemistry 36:4149–4154. https://doi.org/10.1021/bi962170n
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550. https://doi.org/10.1007/s11120-008-9331-0
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. https://doi.org/10.1146/annurev.arplant.50.1.601
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Bansal S, Germino MJ (2008) Carbon balance of conifer seedlings at timberline: relative changes in uptake, storage, and utilization. Oecologia 158:217. https://doi.org/10.1007/s00442-008-1145-4
Baquedano FJ, Castillo FJ (2006) Comparative ecophysiological effects of drought on seedlings of the Mediterranean water-saver Pinus halepensis and water-spenders Quercus coccifera and Quercus ilex. Trees 20:689. https://doi.org/10.1007/s00468-006-0084-0
Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998. https://doi.org/10.1104/pp.008250
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504. https://doi.org/10.1007/BF00402983
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 162:549–558. https://doi.org/10.1016/j.jplph.2004.09.005
Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644. https://doi.org/10.1051/forest:2006042
Brestic M, Zivcak M, Hauptvogel P, Misheva S, Kocheva K, Yang X, Allakhverdiev SI (2018) Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynth Res. https://doi.org/10.1007/s11120-018-0486-z
Deslauriers A, Beaulieu M, Balducci L, Giovannelli A, Gagnon MJ, Rossi S (2014) Impact of warming and drought on carbon balance related to wood formation in black spruce. Ann Bot 114:335–345. https://doi.org/10.1093/aob/mcu111
Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Ann Rev Plant Biol 65:667–687. https://doi.org/10.1146/annurev-arplant-050213-040054
Ditmarová Ľ, Kurjak D, Palmroth S, Kmeť J, Střelcová K (2009) Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiol 30:205–213. https://doi.org/10.1093/treephys/tpp116
Driever SM, Lawson T, Andralojc PJ, Raines CA, Parry MAJ (2014) Natural variation in photosynthetic capacity, growth, and yield in 64 field-grown wheat genotypes. J Exp Bot 65:4959–4973. https://doi.org/10.1093/jxb/eru253
Duan B, Lu Y, Yin C, Junttila O, Li C (2005) Physiological responses to drought and shade in two contrasting Picea asperata populations. Physiol Plant 124:476–484. https://doi.org/10.1111/j.1399-3054.2005.00535.x
Dulamsuren C, Hauck M, Bader M, Oyungerel S, Osokhjargal D, Nyambayar S, Leuschner C (2009) The different strategies of Pinus sylvestris and Larix sibirica to deal with summer drought in a northern Mongolian forest–steppe ecotone suggest a future superiority of pine in a warming climate. Can J For Res 39:2520–2528. https://doi.org/10.1139/X09-156
Enquist BJ, Kerkhoff AJ, Stark SC, Swenson NG, McCarthy MC, Price CA (2007) A general integrative model for scaling plant growth, carbon flux, and functional trait spectra. Nature 449:218. https://doi.org/10.1038/nature06061
Flexas J, Escalona JM, Evain S, Gulías J, Moya I, Osmond CB, Medrano H (2002) Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. Physiol Plant 114:231–240. https://doi.org/10.1034/j.1399-3054.2002.1140209.x
Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621. https://doi.org/10.1111/j.1365-3040.2007.01757.x
Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Gallé A (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193:70–84. https://doi.org/10.1016/j.plantsci.2012.05.009
Flexas J, Diaz-Espejo A, Gago J, Gallé A, Galmés J, Gulías J, Medrano H (2014) Photosynthetic limitations in Mediterranean plants: a review. Environ Exp Bot 103:12–23. https://doi.org/10.1016/j.envexpbot.2013.09.002
Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661. https://doi.org/10.1093/jxb/ers013
Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 year after a drought episode. New Phytol 190:750–759. https://doi.org/10.1111/j.1469-8137.2010.03628.x
Garcia-Forner N, Sala A, Biel C, Savé R, Martínez-Vilalta J (2016) Individual traits as determinants of time to death under extreme drought in Pinus sylvestris L. Tree Physiol 36:1196–1209. https://doi.org/10.1093/treephys/tpw040
Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114. https://doi.org/10.1007/s00425-003-1077-5
Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893. https://doi.org/10.1134/S1021443716050058
González L, González-Vilar M (2001) Determination of relative water content. In: Roger MJR (ed) Handbook of plant ecophysiology techniques, 1st edn. Springer, Dordrecht, pp 207–212. https://doi.org/10.1007/0-306-48057-3_14
Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849. https://doi.org/10.1111/j.1365-3040.2005.01333.x
Gruber A, Pirkebner D, Oberhuber W, Wieser G (2011) Spatial and seasonal variations in mobile carbohydrates in Pinus cembra in the timberline ecotone of the Central Austrian Alps. Eur J For Res 130:173–179. https://doi.org/10.1007/s10342-010-0419-7
Gururani MA, Venkatesh J, Tran L-SP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
Handa S, Bressan RA, Handa AK, Carpita NC, Hasegawa PM (1983) Solutes contributing to osmotic adjustment in cultured plant cells adapted to water stress. Plant Physiol 73:834–843. https://doi.org/10.1104/pp.73.3.834
Hartmann H, Ziegler W, Trumbore S (2013) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427. https://doi.org/10.1111/1365-2435.12046
Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081. https://doi.org/10.1046/j.0016-8025.2003.01032.x
Huang W, Fu P-L, Jiang Y-J, Zhang J-L, Zhang S-B, Hu H, Cao K-F (2013) Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest. Tree Physiol 33:211–220. https://doi.org/10.1093/treephys/tps132
Ivanov YV, Kartashov AV, Ivanova AI, Savochkin YV, Kuznetsov VV (2016) Effects of zinc on Scots pine (Pinus sylvestris L.) seedlings grown in hydroculture. Plant Physiol Biochem 102:1–9. https://doi.org/10.1016/j.plaphy.2016.02.014
Ivanov YV, Zlobin IE, Kartashov AV, Pashkovskiy PP, Kuznetsov VV (2018) Scale of physiological processes sensitivity to PEG-induced water stress in Scots pine seedlings. Russ J Plant Physiol. https://doi.org/10.1134/S1021443718040143
Jia H, Oguchi R, Hope AB, Barber J, Chow WS (2008) Differential effects of severe water stress on linear and cyclic electron fluxes through Photosystem I in spinach leaf discs in CO2-enriched air. Planta 228:803–812. https://doi.org/10.1007/s00425-008-0783-4
Jones RW, Storey R (1978) Salt stress and comparative physiology in the Gramineae. II. Glycinebetaine and proline accumulation in two salt-and water-stressed barley cultivars. Funct Plant Biol 5:817–829. https://doi.org/10.1071/PP9780817
Kartashov AV, Pashkovskiy PP, Ivanov YV, Ivanova AI, Savochkin YV (2014) Morphogenesis of Norway spruce and Scots pine seedlings assimilating organs under the influence of red and blue LED light. Tomsk State Univ J Biol 25:167–182. https://doi.org/10.17223/19988591/25/12
Keunen ELS, Peshev D, Vangronsveld J, Van Den Ende WIM, Cuypers ANN (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255. https://doi.org/10.1111/pce.12061
Kim JH, Kim SJ, Cho SH, Chow WS, Lee CH (2005) Photosystem I acceptor side limitation is a prerequisite for the reversible decrease in the maximum extent of P700 oxidation after short-term chilling in the light in four plant species with different chilling sensitivities. Physiol Plant 123:100–107. https://doi.org/10.1111/j.1399-3054.2005.00443.x
Klughammer C, Schreiber U (1994) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14
Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004. https://doi.org/10.1093/pcp/pcu033
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209. https://doi.org/10.1023/B:PRES.0000015391.99477.0d
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608. https://doi.org/10.1093/jxb/err460
Kreslavskii VD, Carpentier R, Klimov VV, Murata N, Allakhverdiev SI (2007) Molecular mechanisms for photosynthetic apparatus resistance to stress. Biol Membr 24:195–217
Kruger EL, Volin JC (2006) Reexamining the empirical relation between plant growth and leaf photosynthesis. Funct Plant Biol 33:421–429. https://doi.org/10.1071/FP05310
Li X, Schmid B, Wang F, Paine CT (2016) Net assimilation rate determines the growth rates of 14 species of subtropical forest trees. PloS ONE 11:e0150644. https://doi.org/10.1371/journal.pone.0150644
Linkosalo T, Heikkinen J, Pulkkinen P, Mäkipää R (2014) Fluorescence measurements show stronger cold inhibition of photosynthetic light reactions in Scots pine compared to Norway spruce as well as during spring compared to autumn. Front Plant Sci 5:264. https://doi.org/10.3389/fpls.2014.00264
Loewus FA, Murthy PP (2000) myo-Inositol metabolism in plants. Plant Sci 150:1–19. https://doi.org/10.1016/S0168-9452(99)00150-8
López R, Aranda I, Gil L (2009) Osmotic adjustment is a significant mechanism of drought resistance in Pinus pinaster and Pinus canariensis. For Syst 18:159–166. https://doi.org/10.5424/fs/2009182-01059
Lu C, Zhang J (1999) Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants. J Exp Bot 50:1199–1206. https://doi.org/10.1093/jxb/50.336.1199
Martı̀nez JP, Lutts S, Schanck A, Bajji M, Kinet JM (2004) Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L? J Plant Physiol 161:1041–1051. https://doi.org/10.1016/j.jplph.2003.12.009
Martínez-Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F (2016) Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol Monogr 86:495–516. https://doi.org/10.1002/ecm.1231
McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Hüner NP (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). BBA-Bioenergetics 1807:954–967. https://doi.org/10.1016/j.bbabio.2010.10.024
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. https://doi.org/10.1104/pp.110.170704
McGarvey RC, Martin TA, White TL (2004) Integrating within-crown variation in net photosynthesis in loblolly and slash pine families. Tree Physiol 24:1209–1220. https://doi.org/10.1093/treephys/24.11.1209
Miyake C, Miyata M, Shinzaki Y, Tomizawa KI (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637. https://doi.org/10.1093/pcp/pci067
Moya JL, Ros R, Picazo I (1993) Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth Res 36:75–80. https://doi.org/10.1007/BF00016271
Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729. https://doi.org/10.1093/jxb/erq438
Munekage Y, Hashimoto M, Miyake C, Tomizawa KI, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582. https://doi.org/10.1038/nature02598
Nguyen A, Lamant A (1988) Pinitol and myo-inositol accumulation in water-stressed seedlings of maritime pine. Phytochemistry 27:3423–3427. https://doi.org/10.1016/0031-9422(88)80742-8
Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR (2009) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J Exp Bot 60:2249–2270. https://doi.org/10.1093/jxb/erp036
Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594. https://doi.org/10.1093/emboj/20.20.5587
Oukarroum A, Schansker G, Strasser RJ (2009) Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plant 137:188–199. https://doi.org/10.1111/j.1399-3054.2009.01273.x
Peltier G, Cournac L (2002) Chlororespiration. Ann Rev Plant Biol 53:523–550. https://doi.org/10.1146/annurev.arplant.53.100301.135242
Piper FI, Fajardo A, Hoch G (2017) Single-provenance mature conifers show higher non-structural carbohydrate storage and reduced growth in a drier location. Tree Physiol 37:1001–1010. https://doi.org/10.1093/treephys/tpx061
Pollastrini M, Holland V, Brüggemann W, Bussotti F (2016) Chlorophyll a fluorescence analysis in forests. Ann di Bot 6:23–37. https://doi.org/10.4462/annbotrm-13257
Pravdin LF (1964) Sosna obyknovennaya. Izmenchivost’, vnutrividovaya sistematika i selekciya. Nauka, Moscow (In Russian)
Pravdin LF (1975) El’ evropeyskaya i el’ sibirskaya v SSSR. Nauka, Moscow (In Russian)
Quero JL, Villar R, Marañón T, Zamora R, Vega D, Sack L (2008) Relating leaf photosynthetic rate to whole-plant growth: drought and shade effects on seedlings of four Quercus species. Funct Plant Biol 35:725–737. https://doi.org/10.1071/FP08149
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62. https://doi.org/10.1007/BF00024185
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ 37:153–161. https://doi.org/10.1111/pce.12141
Shirao M, Kuroki S, Kaneko K, Kinjo Y, Tsuyama M, Förster B, Takahashi S, Badger MR (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54:1152–1163. https://doi.org/10.1093/pcp/pct066
Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS ONE 7:e38554. https://doi.org/10.1371/journal.pone.0038554
Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64. https://doi.org/10.1111/j.1399-3054.2010.01437.x
Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Von Korff M (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci USA 106:10348–10353. https://doi.org/10.1073/pnas.0903478106
Urban L, Aarrouf J, Bidel LP (2017) Assessing the effects of water deficit on photosynthesis using parameters derived from measurements of leaf gas exchange and of chlorophyll a fluorescence. Front Plant Sci 8:2068. https://doi.org/10.3389/fpls.2017.02068
Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546. https://doi.org/10.1007/s11120-013-9885-3
Zlobin IE, Ivanov YV, Kartashov AV, Kuznetsov VV (2018) Impact of drought stress induced by polyethylene glycol on growth, water relations and cell viability of Norway spruce seedlings. Environ Sci Pollut Res 25:8951–8962. https://doi.org/10.1007/s11356-017-1131-7
Acknowledgements
This work was supported by the Russian Science Foundation (Project No. 16-14-10224). We are grateful to Dr. Eugene A. Lysenko for assistance in obtaining data on chlorophyll fluorescence parameters. We are grateful to Prof. A.M. Nosov and Dr. D.V. Kochkin for their support and valuable advice regarding the analysis of sugars.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zlobin, I.E., Ivanov, Y.V., Kartashov, A.V. et al. Impact of weak water deficit on growth, photosynthetic primary processes and storage processes in pine and spruce seedlings. Photosynth Res 139, 307–323 (2019). https://doi.org/10.1007/s11120-018-0520-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-018-0520-1