Improvement of drought tolerance in five different cultivars of Vicia faba with foliar application of ascorbic acid or silicon
Aim of study: To explore the role of ascorbic acid (AsA) or silicon (Si) in improving drought tolerance in five faba bean cultivars under irrigation water deficit (IWD).
Area of study: The experimental farm; 30° 36′ N, 32° 16′ E, Egypt.
Material and methods: Three drip irrigation regimes (WW, well-watered, 4000 m3 water ha-1; MD, moderate drought, 3000 m3 water ha-1; and SD, severe drought, 2000 m3 water ha-1) were applied to plants, which were sprayed 25, 40, and 55 days after sowing with 1.5 mM AsA or 2.0 mM Si vs distilled water as a control.
Main results: Drought negatively affected physiological attributes (photosynthetic pigments, gas exchange parameters, relative water content, membrane stability index, electrolyte leakage (EL), and lipid peroxidation), which restricted plant growth and yields, and stimulated alterations in both enzymatic and non-enzymatic antioxidant activities. However, AsA or Si application mitigated drought effects on physiological attributes, improving growth, yields and water use efficiency by raising antioxidant activities and suppressing lipid peroxidation and EL in stressful cultivars. The mitigating effects of AsA and Si were more pronounced under MD.Research highlights: ‘Nubaria-2’, ‘Giza-843’, and ‘Sakha-3’ were more tolerant than ‘Giza-716’ and ‘Sakha-4’, suggesting the use of AsA or Si to ameliorate the IWD effects on stressful cultivars. Certain physiological traits exhibited positive association with growth and seed yield, demonstrating their importance in enhancing seed yield under irrigation treatments.
Abid G, Hessini K, Aouida M, Aroua I, Baudoin JP, Muhovski Y, Mergeai G, Sassi K, Machraoui M, Souissi F, Jebara M, 2017. Agro-physiological and biochemical responses of faba bean (Vicia faba L. var. 'Minor') genotypes to water deficit stress. Biotechnol Agron Soc Environ 21 (2):146-159.
Agarie S, Hanaoka N, Ueno O, Miyazaki A, Kubota F, Agata W, Kaufman PB, 1998. Effects of silicon on tolerance to water deficit and heat stress in rice plants (Oryza sativa L.) monitored by electrolyte leakage. Plant Prod Sci 1: 96-103. https://doi.org/10.1626/pps.1.96
Akram NA, Shafiq F, Ashraf M, 2017. Ascorbic acid-A potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8: 613. https://doi.org/10.3389/fpls.2017.00613
Alghamdi S, Al‐Shameri M, Migdadi H, Ammar M, El‐Harty E, Khan M, Farooq M, 2015. Physiological and molecular characterization of faba bean (Vicia faba L.) genotypes for adaptation to drought stress. J Agron Crop Sci 201 (6): 401-409. https://doi.org/10.1111/jac.12110
Alzahrani Y, Kuşvuran A, Alharby HF, Kuşvuran S, Rady MM, 2018. The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicol Environ Saf 154: 187-196. https://doi.org/10.1016/j.ecoenv.2018.02.057
Amede T, Schubert S, 2003. Mechanisms of drought resistance in grain legumes I. Osmotic adjustment. Ethiop J Sci 26: 37-46. https://doi.org/10.4314/sinet.v26i1.18198
Anjum SA, Xie XY, Wang LC, Saleem MF, Man C, Lei W, 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6 (9): 2026-2032.
Asada K, 1999. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50: 601-639. https://doi.org/10.1146/annurev.arplant.50.1.601
Ashraf M, Foolad MR, 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp Bot 59: 206-216. https://doi.org/10.1016/j.envexpbot.2005.12.006
Ashraf M, Akram NA, 2009. Improving salinity tolerance of plants through conventional breeding and genetic engineering: An analytical comparison. Biotechnol Adv 27 (6): 744-752. https://doi.org/10.1016/j.biotechadv.2009.05.026
Aydinsakir K, Erdal S, Buyuktas D, Bastug R, Toker R, 2013. The influence of regular deficit irrigation applications on water use, yield, and quality components of two corn (Zea mays L.) genotypes. Agric Water Manag 128: 65-71. https://doi.org/10.1016/j.agwat.2013.06.013
Baghizadeh A, Ghorbanli A, Haj Mohammad RM, Mozafari H, 2009. Evaluation of interaction effect of drought stress with ascorbate and salicylic acid on some of physiological and biochemical parameters in okra (Hibiscus esculentus L.). Res J Biol Sci 4 (4): 380-387.
Bates LS, Waldren RP, Teare ID, 1973. Rapid determination of free proline for water stress studies. Plant Soil 39: 205-207. https://doi.org/10.1007/BF00018060
Bista D, Heckathorn S, Jayawardena D, Mishra S, Boldt J, 2018. Effects of drought on nutrient uptake and the levels of nutrient-uptake proteins in roots of drought-sensitive and-tolerant grasses. Planta 7 (2): 28. https://doi.org/10.3390/plants7020028
Blokhina O, Virolainen E, Fagerstedt KV, 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91: 179-194. https://doi.org/10.1093/aob/mcf118
Bowler C, Montagu VM, Inze D, 1992. Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43: 83-116. https://doi.org/10.1146/annurev.pp.43.060192.000503
Chance B, Maehly AC, 1955. Assay of catalase and peroxidase. Methods Enzymol 2: 764-775. https://doi.org/10.1016/S0076-6879(55)02300-8
Chaves MM, Flexas J, Pinheiro C, 2008. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot London 103 (4): 551-560. https://doi.org/10.1093/aob/mcn125
Chhogyel N, Kumar L, 2018. Climate change and potential impacts on agriculture in Bhutan: A discussion of pertinent issues. Agric Food Secur 7 (1): 79. https://doi.org/10.1186/s40066-018-0229-6
Conesa MR, de la Rosa JM, Fernández-Trujillo JP, Domingo R, Pérez-Pastor A, 2018. Deficit irrigation in commercial mandarin trees: water relations, yield and quality responses at harvest and after cold storage. Span J Agric Res 16 (3): e1201. https://doi.org/10.5424/sjar/2018163-12631
Conklin PL, 2001. Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24 (4): 383-394. https://doi.org/10.1046/j.1365-3040.2001.00686.x
Cornic G, Fresneau C, 2002. Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Ann Bot 89: 887-894. https://doi.org/10.1093/aob/mcf064
Coskun D, Britto DT, Huynh WQ, Kronzucker HJ, 2016. The role of silicon in higher plants under salinity and drought stress. Front Plant Sci 7: 1072. https://doi.org/10.3389/fpls.2016.01072
Crépon K, Marget P, Peyronnet C, Carrouee B, Arese P, Duc G, 2010. Nutritional value of faba bean (Vicia faba L.) seeds for feed and food. Field Crops Res 115 (3): 329-339. https://doi.org/10.1016/j.fcr.2009.09.016
Dai A, 2013. Increasing drought under global warming in observations and models. Nature Climate Change 3 (1): 52. https://doi.org/10.1038/nclimate1633
Dong B, Shi L, Shi C, Qiao Y, Liu M, Zhang Z, 2011. Grain yield and water use efficiency of two types of winter wheat cultivars under different water regimes. Agric Water Manage 99: 103-110. https://doi.org/10.1016/j.agwat.2011.07.013
Earl HJ, Davis RF, 2003. Effect of drought stress on leaf and whole canopy radiation use efficiency and yield of maize. Agron J 95 (3): 688-696. https://doi.org/10.2134/agronj2003.6880
El-Bassiouny HMS, Sadak MS, 2015. Impact of foliar application of ascorbic acid and α-tocopherol on antioxidant activity and some biochemical aspects of flax cultivars under salinity stress. Acta Biol Colomb 20 (2): 209-222.
Fadeels AA, 1962. Location and properties of chloroplasts and pigment determination in roots. Physiol Plant 15: 130-147. https://doi.org/10.1111/j.1399-3054.1962.tb07994.x
Fadzilla NM, Burdon RH, 1997. Salinity, oxidative stress and antioxidant responses in shoot cultures of rice. J Exp Bot 48: 325-331. https://doi.org/10.1093/jxb/48.2.325
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique K (2017) Drought stress in grain legumes during reproduction and grain filling. J Agron Crop Sci 203 (2): 81-102. https://doi.org/10.1111/jac.12169
Fielding JL, Hall JL, 1978. A biochemical and cytochemical study of peroxidase activity in roots of Pisum sativum. J Exp Bot 29: 969-981. https://doi.org/10.1093/jxb/29.4.969
Foyer CH, 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875. https://doi.org/10.1105/tpc.105.033589
Gadallah MAA, 1999. Effect of proline and glycine betaine on Vicia faba responses to salt stress. Biol Plant 42: 249-257.
Garg N, Manchanda G, 2009. ROS generation in plants: boon or bane? Plant Biosyst 143: 81-96. https://doi.org/10.1080/11263500802633626
Ghaffari H, Tadayon MR, Nadeem M, Razmjoo J, Cheema M, 2019. Foliage applications of jasmonic acid modulate the antioxidant defense under water deficit growth in sugar beet. Span J Agric Res 17 (4): e0805. https://doi.org/10.5424/sjar/2019174-15380
Gill SS, Tuteja N, 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48: 909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gong H, Chen K, Chen G, Wang S, Zhang C, 2003. Effects of silicon on growth of wheat under drought. J Plant Nutr 26 (5): 1055-1063. https://doi.org/10.1081/PLN-120020075
Heath RL, Packer L, 1968. Photo peroxidation isolated chloroplasts: kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198. https://doi.org/10.1016/0003-9861(68)90654-1
Huo Y, Wang M, Wei Y, Xia Z, 2016. Overexpression of the maize psbA gene enhances drought tolerance through regulating antioxidant system, photosynthetic capability, and stress defense gene expression in tobacco. Front Plant Sci 6: 1223. https://doi.org/10.3389/fpls.2015.01223
Irigoyen JJ, Emerich DW, Sanchez-Diaz M, 1992. Water stress induced changes in the concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Plant Physiol 8: 455-460.
Kabbadj A, Makoudi B, Mouradi M, Pauly N, Frendo P, Ghoulam C, 2017. Physiological and biochemical responses involved in water deficit tolerance of nitrogen-fixing Vicia faba. PloS one 12(12): e0190284. https://doi.org/10.1371/journal.pone.0190284
Kabir AH, Hossain MM, Khatun MA, Mandal A, Haider SA, 2016. Role of silicon counteracting cadmium toxicity in Alfalfa (Medicago sativa L.). Front Plant Sci 7: 11-17. https://doi.org/10.3389/fpls.2016.01117
Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N, 2005. Review: regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88: 424-438.
Köpke U, Nemecek T, 2010. Ecological services of faba bean. Field Crops Res 115 (3): 217-233. https://doi.org/10.1016/j.fcr.2009.10.012
Krouma A, 2010. Plant water relations and photosynthetic activity in three Tunisian chickpea (Cicer arietinum L.) genotypes subjected to drought. Turk J Agric For 34 (3): 257-264.
Kumar A, Prasad N, Sinha SK, 2015. Nutritional and antinutritional attributes of faba bean (Vicia faba L.) germplasms growing in Bihar, India. Physiol Molec Biol Plants 21 (1): 159-162. https://doi.org/10.1007/s12298-014-0270-2
Kusvuran S, Kiran S, Ellialtioglu SS, 2016. Antioxidant enzyme activities and abiotic stress tolerance relationship in vegetable crops. In: Abiotic and biotic stress in plants - Recent advances and future perspectives, Chapter 21, pp: 481-506; Shanker, Arun K. (Ed.). Intech, Chitra Shanker. https://doi.org/10.5772/62235
Latif M, Akram NA, Ashraf M, 2016. Regulation of some biochemical attributes in drought-stressed cauliflower (Brassica oleracea L.) by seed pre-treatment with ascorbic acid. J Hort Sci Biotechnol 91: 129-137. https://doi.org/10.1080/14620316.2015.1117226
Li J, Li X, Yang QH, Luo Y, Gong XW, Zhang WL, Hu YG, Yang TY, Dong KJ, Feng BL, 2019. Proteomic changes in the grains of foxtail millet (Setaria italica (L.) Beau) under drought stress. Span J Agric Res 17 (2): e0802. https://doi.org/10.5424/sjar/2019172-14300
Li P, Zhang Y, Wu X, Liu Y, 2018. Drought stress impact on leaf proteome variations of faba bean (Vicia faba L.) in the Qinghai-Tibet Plateau of China. 3Biotech 8 (2): 110. https://doi.org/10.1007/s13205-018-1088-3
Link W, Abdelmula AA, Kittlitz EV, Bruns S, Riemer H, Stelling D, 1999. Genotypic variation for drought tolerance in Vicia faba. Plant Breed 118: 477-483. https://doi.org/10.1046/j.1439-0523.1999.00412.x
Mateos-Naranjo E, Andrades-Moreno L, Davy AJ, 2013. Silicon alleviates deleterious effects of high salinity on the halophytic grass Spartina densiflora. Plant Physiol Biochem 63: 115-121. https://doi.org/10.1016/j.plaphy.2012.11.015
Maxwell K, Johnson GN, 2000. Chlorophyll fluorescence-A practical guide. J Exp Bot 51 (345): 659-668. https://doi.org/10.1093/jexbot/51.345.659
Merwad AMA, Desoky EM, Rady MM, 2018. Response of water deficit-stressed Vigna unguiculata performances to silicon, proline or methionine foliar application. Sci Hortic 228: 132-144. https://doi.org/10.1016/j.scienta.2017.10.008
Ming DF, Pei ZF, Naeem MS, Gong HJ, Zhou WJ, 2012. Silicon alleviates PEG‐induced water‐deficit stress in upland rice seedlings by enhancing osmotic adjustment. J Agron Crop Sci 198 (1): 14-26. https://doi.org/10.1111/j.1439-037X.2011.00486.x
Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SS, 2008. 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 31 (12): 1791-1802. https://doi.org/10.1111/j.1365-3040.2008.01882.x
Mukhtar A, Akram NA, Aisha R, Shafiq S, Ashraf M, 2016. Foliar applied ascorbic acid enhances antioxidative potential and drought tolerance in cauliflower (Brassica oleracea L. var. Botrytis). Agrochimica 60: 100-113.
Murata N, Takahashi S, 2008. How do environmental stresses accelerate photoinhibition? Trends Plant Sci 4: 178-182. https://doi.org/10.1016/j.tplants.2008.01.005
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI, 2007. Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767: 414-421. https://doi.org/10.1016/j.bbabio.2006.11.019
Nabe H, Funabiki R, Kashino Y, Koike H, Satoh K, 2007. Responses to desiccation stress in bryophytes and an important role of dithiothreitol-insensitive non-photochemical quenching against photoinhibition in dehydrated states. Plant Cell Physiol 48: 1548-1557. https://doi.org/10.1093/pcp/pcm124
Osman AS, Rady MM, 2012. Ameliorative effects of sulphur and humic acid on the growth, antioxidant levels, and yields of pea (Pisum sativum L.) plants grown in reclaimed saline soil. J Hortic Sci Biotechnol 87 (6): 626-632. https://doi.org/10.1080/14620316.2012.11512922
Ouzounidou G, Giannakoula A, Ilias I, Zamanidis P, 2016. Alleviation of drought and salinity stresses on growth, physiology, biochemistry and quality of two Cucumis sativus L. cultivars by Si application. Braz J Bot 39 (2): 531-539. https://doi.org/10.1007/s40415-016-0274-y
Pala M, Armstrong E, Johansen C, 2000. The role of legumes in sustainable cereal production in rainfed areas. Linking research marketing opportunities for pulses in the 21st century. In: Linking Research and Marketing Opportunities for Pulses in the 21st Century, Knight, R.(Ed.), Curr Plant Sci Biotechnol Agr Book Series 34: 323-334. https://doi.org/10.1007/978-94-011-4385-1_29
Papworth A, Maslin M, Randalls S, 2015. Is climate change the greatest threat to global health? Geogr J 181 (4): 413-422. https://doi.org/10.1111/geoj.12127
Parveen N, Ashraf M, 2010. Role of silicon in mitigating the adverse effects of salt stress on growth and photosynthetic attributes of two maize (Zea mays L.) cultivars grown hydroponically. Pak J Bot 42 (3): 1675-1684.
Pignocchi C, Foyer CH, 2003. Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 6 (4): 379-389. https://doi.org/10.1016/S1369-5266(03)00069-4
Qirat M, Shahbaz M, Perveen S, 2018. Beneficial role of foliar-applied proline on carrot (Daucus carota L.) under saline conditions. Pak J Bot 50 (5): 1735-1744.
Rady MM, 2011. Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci Hortic 129: 232-237. https://doi.org/10.1016/j.scienta.2011.03.035
Rady MM, Elrys AS, Abo El-Maati MF, Desoky EM, 2019. Interplaying roles of silicon and proline effectively improve salt and cadmium stress tolerance in Phaseolus vulgaris plant. Plant Physiol Biochem 139: 558-568. https://doi.org/10.1016/j.plaphy.2019.04.025
Rady MM, Hemida KA, 2016. Sequenced application of ascorbate-proline-glutathione improves salt tolerance in maize seedlings. Ecotoxicol Environ Saf 133: 252-259. https://doi.org/10.1016/j.ecoenv.2016.07.028
Ranjbarfordoei A, Samson R, Van Damme P, 2006. Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D.Webb] in response to salinity stress induced by NaCl. Photosynthetica 44 (4): 513-522. https://doi.org/10.1007/s11099-006-0064-z
Rao MV, Paliyath G, Ormrod DP, 1996. Ultraviolet-B radiation and ozone-induced biochemical changes in the antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110: 125-136. https://doi.org/10.1104/pp.110.1.125
Ray DK, West PC, Clark M, Gerber JS, Prishchepov AV, Chatterjee S, 2019. Climate change has likely already affected global food production. PloS one 14 (5): e0217148. https://doi.org/10.1371/journal.pone.0217148
Ribeiro T, Silva DAD, Esteves JADF, Azevedo CVG, Gonçalves JGR, Carbonell SAM, Chiorato AF, 2019. Evaluation of common bean genotypes for drought tolerance. Bragantia 78 (1): 1-11. https://doi.org/10.1590/1678-4499.2018002
Rios JJ, Martínez-Ballesta MC, Ruiz JM, Blasco B, Carvajal M, 2017. Silicon mediated improvement in plant salinity tolerance: the role of aquaporins. Front Plant Sci 8: 948. https://doi.org/10.3389/fpls.2017.00948
Saikia J, Sarma RK, Dhandia R, Yadav A, Bharali R, Gupta VK, Saikia R, 2018. Alleviation of drought stress in pulse crops with ACC deaminase producing rhizobacteria isolated from acidic soil of Northeast India. Sci Rep 8 (1): 3560. https://doi.org/10.1038/s41598-018-25174-5
Sairam RK, Rao KV, Srivastava GC, 2002. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163: 1037-1046. https://doi.org/10.1016/S0168-9452(02)00278-9
Schutzendubel A, Polle A, 2002. Plant responses to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot 53: 1351-1365. https://doi.org/10.1093/jexbot/53.372.1351
Seki M, Umezawa T, Urano K, Shinozaki K, 2007. Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10 (3): 296-302. https://doi.org/10.1016/j.pbi.2007.04.014
Semida WM, Hemida KA, Rady MM, 2018. Sequenced ascorbate-proline glutathione seed treatment elevates cadmium tolerance in cucumber transplants. Ecotoxicol Environ Saf 154: 171-179. https://doi.org/10.1016/j.ecoenv.2018.02.036
Sharma P, Jha AB, Dubey RS, Pessarakli M, 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012: 217037. https://doi.org/10.1155/2012/217037
Shi Y, Zhang Y, Han W, Feng R, Hu Y, Guo J, Gong H, 2016. Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Front Plant Sci 7: 196. https://doi.org/10.3389/fpls.2016.00196
Shirinbayan S, Khosravi H, Malakouti MJ, 2019. Alleviation of drought stress in maize (Zea mays) by inoculation with Azotobacter strains isolated from semi-arid regions. Appl Soil Ecol 133: 138-145. https://doi.org/10.1016/j.apsoil.2018.09.015
Siddiqui MH, Al-Khaishany MY, Al-Qutami MA, Al-Whaibi MH, Grover A, Ali HM, Al-Wahibi MS, Bukhari NA, 2015. Response of different genotypes of faba bean plant to drought stress. Int J Molec Sci 16: 10214-10227. https://doi.org/10.3390/ijms160510214
Siripornadulsil S, Traina S, Verma DS, Sayre RT, 2002. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14: 2837-2847. https://doi.org/10.1105/tpc.004853
Slabbert MM, Krüger GHJ, 2014. Antioxidant enzyme activity, proline accumulation, leaf area and cell membrane stability in water stressed Amaranthus leaves. S Afr J Bot 95: 123-128. https://doi.org/10.1016/j.sajb.2014.08.008
Thomas RL, Jen JJ, Morr CV, 1981. Changes in soluble and bound peroxidase, IAA oxidase during tomato fruit development. J Food Sci 47: 158-161. https://doi.org/10.1111/j.1365-2621.1982.tb11048.x
Vitória AP, Lea PJ, Azevedo RA, 2001. Antioxidant enzymes responses to cadmium in radish tissues. Phytochem 57: 710-710. https://doi.org/10.1016/S0031-9422(01)00130-3
Von Wettestein D, 1957. Chlorophyll-letale und der submikroskopische Formwechsel der Plastiden. Exp Cell Res 12: 427-506. https://doi.org/10.1016/0014-4827(57)90165-9
Wang Z, Li G, Sun H, Ma L, Guo Y, Zhao Z, Gao H, Mei L, 2018. Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves. Biology Open 7: bio035279. https://doi.org/10.1242/bio.035279
Weatherly PE, 1950. Studies in the water relations of cotton. 1. The field measurement of water deficits in leaves. New Phytol 49: 81-97. https://doi.org/10.1111/j.1469-8137.1950.tb05146.x
Wu ZZ, Ying YQ, Zhang YB, Bi YF, Wang AK, Du XH, 2018. Alleviation of drought stress in Phyllostachys edulis by N and P application. Sci Rep 8 (1): 228. https://doi.org/10.1038/s41598-017-18609-y
Yang SL, Lan SS, Gong M, 2009. Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166: 1694-1699. https://doi.org/10.1016/j.jplph.2009.04.006
Zhang W, Xie Z, Wang L, Li M, Lang D, Zhang X, 2017. Silicon alleviates salt and drought stress of Glycyrrhiza uralensis seedling by altering antioxidant metabolism and osmotic adjustment. J Plant Res 130 (3): 611-624. https://doi.org/10.1007/s10265-017-0927-3
Zhou S, Duursma RA, Medlyn BE, Kelly JWG, Prentice IC, 2013. How should we model plant responses to drought? An analysis of stomatal and nonstomatal responses to water stress. Agr Forest Meteorol 182-183: 204-214. https://doi.org/10.1016/j.agrformet.2013.05.009
© INIA. Manuscripts published are the property of the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, and quoting this source is a requirement for any partial or full reproduction.
SJAR is an Open Access Journal. All articles are distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the license CC-by must be expressly stated in this way when necessary.