Abstract
Plant response to drought is a complex phenomenon consisting of numerous metabolic pathways primarily based on water loss prevention and redox homeostasis maintenance. This study analyses the correlation of stomatal and non-stomatal carbon assimilation-limiting mechanisms with the strategies in antioxidant metabolism pathways and their connection with anatomical modifications in tomato leaves during long-term drought period lasting over 28 days. The results obtained in this research indicate that activation of stomatal closure was the first response to drought as stomatal pore was narrowed by 20% in day 15. The stomatal closing in early stress response was followed by decline in photosynthetic and transpiration rates even though the RUBISCO content has not been changed. Along with drought stress, both stomatal closure and RUBISCO content dramatically decreased leading to a decline in gas exchange parameters; thus, at the end of the experimental Queryperiod, the photosynthetic rate was reduced by 69% and transpiration rate by 80% in comparison with control plants. Superoxide dismutase and ascorbate peroxidase were induced in early stress response (as soon as after 15 days) with a constantly elevated activity during entire drought period. Terminal phase of drought induced the synthesis of new peroxidase isoform (MW ~ 49 kDa) which highly correlated with the phenolic acid contents. At the end of experimental period, the total phenol content of drought-treated plants was doubled as compared to control plants and this increase is correlated to elevated concentrations of hydroxybenzoic acid, ferulic acid, p-coumaric acid and caffeic acid. The progressive involvement of different antioxidant mechanisms over the drought period and their correlations with anatomical modifications and photosynthetic pigments protection was discussed in this paper.
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References
Abedi T, Pakniyat H (2010) Antioxidant enzymes changes in response to drought stress in ten cultivars of oilseed rape (Brassicanapus L.). Czech J Genet Plant Breed 46:27–34. https://doi.org/10.17221/67/2009-CJGPB
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76. https://doi.org/10.1016/j.plantsci.2012.07.014
Akashi K, Nishimura N, Ishida Y, Yokota A (2004) Potent hydroxyl radical-scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochem Biophys Res Commun 323:72–78. https://doi.org/10.1016/j.bbrc.2004.08.056
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Blödner C, Majcherczyk A, Kües U, Polle A (2007) Early drought-induced changes to the needle proteome of Norway spruce. Tree Physiol 27:1423–1431. https://doi.org/10.1093/treephys/27.10.1423
Bodner G, Nakhforoosh A, Kaul HP (2015) Management of crop water under drought: a review. Agron Sustain Dev 35:401–442. https://doi.org/10.1007/s13593-015-0283-4
Chai Q, Gan Y, Zhao C, Xu HL, Waskom RM, Niu Y, Siddique KH (2016) Regulated deficit irrigation for crop production under drought stress. A review. Agron Sustain Dev 36:3. https://doi.org/10.1007/s13593-015-0338-6
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Chen KM, Wang F, Wang YH, Chen T, Hu YX, Lin JX (2006) Anatomical and chemical characteristics of foliar vascular bundles in four reed ecotypes adapted to different habitats. Flora 201:555–569. https://doi.org/10.1016/j.flora.2005.12.003
Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture—not by affecting ATP synthesis. Trends Plant Sci 5:187–188. https://doi.org/10.1016/S1360-1385(00)01625-3
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Efeoğlu B, Ekmekci Y, Cicek N (2009) Physiological responses of three maize cultivars to drought stress and recovery. S Afr J Bot 75:34–42. https://doi.org/10.1016/j.sajb.2008.06.005
Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171. https://doi.org/10.1007/s00122-006-0218-1
Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189. https://doi.org/10.1093/aob/mcf027
Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, Medrano H (2006) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol 172:73–82. https://doi.org/10.1111/j.1469-8137.2006.01794.x
Flexas J, Diaz-Espejo A, Galmes J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298. https://doi.org/10.1111/j.1365-3040.2007.01700.x
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
Fu QS, Yang RC, Wang HS, Zhao B, Zhou CL, Ren S, Guo YD (2013) Leaf morphological and ultrastructural performance of eggplant (Solanummelongena L.) in response to water stress. Photosynthetica 51:109–114. https://doi.org/10.1007/s11099-013-0005-6
Garchery C, Gest N, Do PT, Alhagdow M, Baldet P, Menard G, Fernie AR (2013) A diminution in ascorbate oxidase activity affects carbon allocation and improves yield in tomato under water deficit. Plant Cell Environ 36:159–175. https://doi.org/10.1111/j.1365-3040.2012.02564.x
Gimenez C, Mitchell VJ, Lawlor DW (1992) Regulation of photosynthetic rate of two sunflower hybrids under water stress. Plant Physiol 98:516–524. https://doi.org/10.1104/pp.98.2.516
Gregorová Z, Kováčik J, Klejdus B, Maglovski M, Kuna R, Hauptvogel P, Matušíková I (2015) Drought-induced responses of physiology, metabolites, and PR proteins in Triticum aestivum. J Agric Food Chem 63:8125–8133. https://doi.org/10.1021/acs.jafc.5b02951
Guo YY, Yu HY, Yang MM, Kong DS, Zhang YJ (2018) Effect of drought stress on lipid peroxidation, osmotic adjustment and antioxidant enzyme activity of leaves and roots of Lyciumruthenicum Murr. Seedl Russ J Plant Physiol 65:244–250. https://doi.org/10.1134/S1021443718020127
Holm G (1954) Chlorophyll mutations in barley. Acta Agric Scand 4:457–471. https://doi.org/10.1080/00015125409439955
Hölttä T, Cochard H, Nikinmaa E, Mencuccini M (2009) Capacitive effect of cavitation in xylem conduits: results from a dynamic model. Plant Cell Environ 32:10–21. https://doi.org/10.1111/j.1365-3040.2008.01894.x
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 11:100–105
Kautz B, Noga G, Hunsche M (2015) PEG and drought cause distinct changes in biochemical, physiological and morphological parameters of apple seedlings. Acta Physiol Plant 37:162. https://doi.org/10.1007/s11738-015-1914-8
Kiani SP, Maury P, Sarrafi A, Grieu P (2008) QTL analysis of chlorophyll fluorescence parameters in sunflower (Helianthusannuus L.) under well-watered and water-stressed conditions. Plant Sci 175:565–573. https://doi.org/10.1016/j.plantsci.2008.06.002
Klunklin W, Savage G (2017) Effect on quality characteristics of tomatoes grown under well-watered and drought stress conditions. Foods 6(8):56. https://doi.org/10.3390/foods6080056
Kukavica B, Jovanovic SV (2004) Senescence-related changes in the antioxidant status of ginkgo and birch leaves during autumn yellowing. Physiol Plant 122:321–327. https://doi.org/10.1111/j.1399-3054.2004.00410.x
Kusvuran S, Dasgan HY (2017) Drought induced physiological and biochemical responses in Solanumlycopersicum genotypes differing to tolerance. Acta Sci Pol Hortorum Cultus 16:19–27. https://doi.org/10.24326/asphc.2017.6.2
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8:94. https://doi.org/10.3390/Fantiox8040094
Lee BR, Kim KY, Jung WJ, Avice JC, Ourry A, Kim TH (2007) Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifoliumrepens L.). J Exp Bot 58:1271–1279. https://doi.org/10.1093/jxb/erl280
Lehmann P, Or D (2015) Effects of stomata clustering on leaf gas exchange. New Phytol 207:1015–1025. https://doi.org/10.1111/nph.13442
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Ma Z, Cooper C, Kim HJ, Janick-Buckner D (2009) A study of rubisco through western blotting and tissue printing techniques. CBE Life Sci Educ 8:140–146. https://doi.org/10.1187/cbe.09-01-0003
Maroco JP, Rodrigues ML, Lopes C, Chaves MM (2002) Limitations to leaf photosynthesis in field-grown grapevine under drought—metabolic and modelling approaches. Funct Plant Biol 29:451–459. https://doi.org/10.1071/PP01040
Martinez V, Maestre TC, Rubio F, Girones-Vilapana A, Moreno DA, Mitler R, Rivero RM (2016) Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress. Front Plant Sci 7:1–17. https://doi.org/10.3389/fpls.2016.00838
Martin-StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecol Lett 20:1437–1447. https://doi.org/10.1111/ele.12851
Medrano H, Escalona JM, Bota J, Gulías J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot 89:895–905. https://doi.org/10.1093/aob/mcf079
Meisrimler CN, Buck F, Lüthje S (2014) Alterations in soluble Class III peroxidases of maize shoots by flooding stress. Proteomes 2:303–322. https://doi.org/10.3390/proteomes2030303
Nijsse J, Van der Heijden GWAM, Van Ieperen W, Keijzer CJ, Van Meeteren U (2001) Xylem hydraulic conductivity related to conduit dimensions along chrysanthemum stems. J Exp Bot 52:319–327. https://doi.org/10.1093/jexbot/52.355.319
Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer H (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850. https://doi.org/10.1093/aob/mcf096
Parry MA, Andralojc PJ, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Ann Bot 89:833–839. https://doi.org/10.1093/aob/mcf103
Pinheiro C, Chaves MM (2010) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882. https://doi.org/10.1093/jxb/erq340
Sam O, Jerez E, Dell'Amico J, Ruiz-Sanchez MC (2000) Water stress induced changes in anatomy of tomato leaf epidermes. Biol Plant 43:275–277. https://doi.org/10.1023/A:1002716629802
Sánchez-Rodríguez E, Rubio-Wilhelmi M, Cervilla LM, Blasco B, Rios JJ, Rosales MA, Ruiz JM (2010) Genotypic differences in some physiological parameters symptomatic for oxidative stress under moderate drought in tomato plants. Plant Sci 178:30–40. https://doi.org/10.1016/j.plantsci.2009.10.001
Sass JE (1940) Elements of botanical microtechnique. McGraw Hill Book Co., New York. https://doi.org/10.1038/148241b0
Scippa GS, Di Michele M, Onelli E, Patrignani G, Chiatante D, Bray EA (2004) The histone-like protein H1-S and the response of tomato leaves to water deficit. J Exp Bot 55:99–109. https://doi.org/10.1093/jxb/erh022
Sedigheh HG, Mortazavian M, Norouzian D, Atyabi M, Akbarzadeh A, Hasanpoor K, Ghorbani M (2011) Oxidative stress and leaf senescence. BMC Res Notes 4:477. https://doi.org/10.1186/1756-0500-4-477
Seminario A, Song L, Zulet A, Nguyen HT, González E, Larrainzar E (2017) Drought stress causes a reduction in the biosynthesis of ascorbic acid in soybean plants. Front Plant Sci 8:1042. https://doi.org/10.3389/fpls.2017.01042
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578. https://doi.org/10.3390/ijms160613561
Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. https://doi.org/10.1016/j.tplants.2008.01.005
Teisseire H, Guy V (2000) Copper-induced changes in antioxidant enzymes activities in fronds of duckweed (Lemna minor). Plant Sci 153:65–72. https://doi.org/10.1016/S0168-9452(99)00257-5
Ünyayar S, Keleş Y, Çekiç FÖ (2005) The antioxidative response of two tomato species with different drought tolerances as a result of drought and cadmium stress combinations. Plant, Soil Environ 51:57–64. https://doi.org/10.17221/3556-PSE
Vilagrosa A, Chirino E, Peguero-Pina JJ, Barigah TS, Cochard H, Gil-Pelegrin E (2012) Xylem cavitation and embolism in plants living in water-limited ecosystems. In: Aroca R (ed) Plant responses to drought stress, Springer, Berlin, pp 63–109. https://doi.org/10.1007/978-3-642-32653-0_3
Voelker SL, Lachenbruch B, Meinzer FC, Kitin P, Strauss SH (2011) Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival. Plant Cell Environ 34:655–668. https://doi.org/10.1111/j.1365-3040.2010.02270.x
Von Wettstein D (1957) Genetics and the submicroscopic cytology of plastids. Hereditas 43:303–317. https://doi.org/10.1111/j.1601-5223.1957.tb03440.x
Wang Y, Sperry JS, Venturas MD, Trugman AT, Love DM, Anderegg WR (2019) The stomatal response to rising CO2 concentration and drought is predicted by a hydraulic trait-based optimization model. Tree Physiol 39:1416–1427. https://doi.org/10.1093/treephys/tpz038
Zhao W, Sun Y, Kjelgren R, Liu X (2014) Response of stomatal density and bound gas exchange in leaves of maize to soil water deficit. Acta Physiol Plant 37:1704. https://doi.org/10.1007/s11738-014-1704-8
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This work was supported by the Government of Republic of Srpska, Ministry for Scientific and Technological Development, Higher Education and Information Society, Project no. 19/06-020/961-23/15. We hereby express our gratitude to court interpreter Mr. Mišo Milaković and Ms Tanja Grahovac for linguistic revision.
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Hasanagić, D., Koleška, I., Kojić, D. et al. Long term drought effects on tomato leaves: anatomical, gas exchange and antioxidant modifications. Acta Physiol Plant 42, 121 (2020). https://doi.org/10.1007/s11738-020-03114-z
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DOI: https://doi.org/10.1007/s11738-020-03114-z