Abstract
In addition to mediating photomorphogenesis, phytochromes are responsible for many abiotic stress responses, acting upon biochemical and molecular mechanisms of cell signaling. In this work, we measured the physiological and biochemical responses of phytochrome-mutant plants under water stress. In tomato (Solanum lycopersicum L.), the aurea mutant (au) is phytochrome-deficient and the high-pigment-1 mutant (hp1) has exaggerated light responses. We examined the effects of water withholding on water potential, leaf gas exchange, chlorophyll fluorescence, chloroplast pigment content and antioxidant enzyme activity in au and hp1 and their wild-type cultivar Micro-Tom (MT). Initial fluorescence and potential quantum efficiency of photosystem II (PSII) photochemistry were not affected by the treatment, but effective quantum yield of PSII, electron transport rate decreased and non-photochemical quenching increased significantly in MT. Under water withholding conditions, MT had higher malondialdehyde concentration than the mutants, but au had higher activities of catalase and ascorbate peroxidase compared to the other genotypes. The tolerance of mutants to the effects of water withholding may be explained by the higher activity of antioxidant enzymes in au and by a higher concentration of antioxidant compounds, such as carotenoids, in hp1.
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References
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175. doi:10.3109/07388550903524243
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta Bioenerg 1143: 113–134. doi:10.1016/0005-2728(93)90134-2
Auge GA, Rugnone ML, Cortés LE, González CV, Zarlavsky G, Boccalandro HE, Sánchez RA (2012) Phytochrome A increases tolerance to high evaporative demand. Physiol Plantarum 146:228–235. doi:10.1111/j.1399-3054.2012.01625.x
Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plantarum 104:280–292. doi:10.1034/j.1399-3054.1998.1040217.x
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Ann Rev Plant Biol 59:89–113. doi:10.1146/annurev.arplant.59.032607.092759
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621. doi:10.1093/jxb/erh196
Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plantarum 19:47–64. doi:10.1007/s11738-997-0022-9
Becker TW, Foyer C, Caboche M (1992) Light-regulated expression of the nitrate-reductase and nitrite-reductase genes in tomato and in the phytochrome-deficient aurea mutant of tomato. Planta 188:39–47. doi:10.1007/BF00198937
Benesová M, Holá D, Fischer L, Jedelský PL, Hnilicka F, Wilhelmová N, Rothová O, Kocová M, Procházková D, Honnerová J, Fridrichová L, Hnilicková H (2012) The physiology and proteomics of drought tolerance in maize: early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS One 7:e38017. doi:10.1371/journal.pone.0038017
Biehler K, Haupt S, Beckmann J, Fock H, Becker TW (1997) Simultaneous CO2- and 16O2/18O2-gas exchange and fluorescence measurements indicate differences in light energy dissipation between the wild type and the phytochrome-deficient aurea mutant of tomato during water stress. J Exp Bot 48:1439–1449. doi:10.1093/jxb/48.7.1439
Bilger W, Björkman O (1990) Role of xantophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185. doi:10.1007/BF00033159
Bilger W, Schreiber U, Bock M (1995) Determination of the quantum efficiency of photosystem II ana of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102:425–432. doi:10.1007/BF00341354
Boccalandro HE, Ploschuk EL, Yanovsky MJ, Sánchez RA, Gatz C, Casal JJ (2003) Increased phytochrome B alleviates density effects on tuber yield of field potato crops. Plant Physiol 133:1539–1546. doi:10.1104/pp.103.029579
Boccalandro HE, Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ (2009) Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis. Plant Physiol 150:1083–1092. doi:10.1104/pp.109.135509
Boggs JZ, Loewy K, Bibee K, Heschel MS (2010) Phytochromes influence stomatal conductance plasticity in Arabidopsis thaliana. Plant Growth Regul 60:77–81. doi:10.1007/s10725-009-9427-3
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Ann Rev Plant Physiol 29:345–378. doi:10.1146/annurev.pp.29.060178.002021
Carvalho RF, Aidar ST, Azevedo RA, Dodd IC, Peres LEP (2011a) Enhanced transpiration rate in the high pigment 1 tomato mutant and its physiological significance. Plant Biol 13:546–550. doi:10.1111/j.1438-8677.2010.00438.x
Carvalho RF, Campos ML, Azevedo RA (2011b) The role of phytochrome in stress tolerance. J Integr Plant Biol 53:920–929. doi:10.1111/j.1744-7909.2011.01081.x
Casal JJ, Ballaré CL, Tourn M, Sánchez RA (1994) Anatomy, growth and survival of a long-hypocotyl mutant of Cucumis sativus deficient in phytochrome B. Ann Bot 73:569–575. doi:10.1006/anbo.1994.1071
Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521. doi:10.1016/j.tplants.2007.10.001
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775
D’Amico-Damião V, Cruz FJR, Gavassi MA, Santos DMM, Melo HC, Carvalho RF (2015) Photomorphogenic modulation of water stress in tomato (Solanum lycopersicum L.): the role of phytochromes A, B1 and B2. J Hort Sci Biotechnol 90:25–30
Dias T, Melo HC, Alves FRR, Carvalho RF, Carneiro KS, Sousa CM (2015) Compostos fenólicos e capacidade antioxidante em frutos de tomateiros mutantes fotomorfogenéticos. Ciênc Rural 45:782–787. doi:10.1590/0103-8478cr20140098
Drumm H, Schopfer P (1974) Effect of phytochrome on development of catalase activity and isoenzyme pattern in mustard (Sinapis alba L.) seedlings. Planta 120:13–30. doi:10.1007/BF00388268
Eberhard S, Finazzi G, Wollman F (2008) The dynamics of photosynthesis. Ann Rev Genet 42:463–515. doi:10.1146/annurev.genet.42.110807.091452
Ehleringer J (1981) Leaf absorptances of Mohave and Sonoran desert plants. Oecologia 49:366–370
Genty B, Briantais J, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. doi:10.1016/S0304-4165(89)80016-9
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314. doi:10.1104/pp.59.2.309
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016
González CV, Ibarra SE, Piccoli PN, Botto JF, Boccalandro HE (2012) Phytochrome B increases drought tolerance by enhancing ABA sensitivity in Arabidopsis thaliana. Plant Cell Environ 35:1958–1968. doi:10.1111/j.1365-3040.2012.02529.x
Haupt-Herting S, Fock HP (2000) Exchange of oxygen and its role in energy dissipation during drought stress in tomato plants. Physiol Plantarum 110:489–495. doi:10.1111/j.1399-3054.2000.1100410.x
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. doi:10.1104/pp.84.2.450
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1
Hughes J (2010) Phytochrome three-dimensional structures and functions. Biochem Soc T 38:710–716. doi:10.1042/BST0380710
Jefferies RA (1994) Drought and chlorophyll fluorescence in field-grown potato (Solanum tuberosum). Physiol Plantarum 90:93–97. doi:10.1111/j.1399-3054.1994.tb02197.x
Jones DH (1984) Phenyalanine ammonia-lyase: regulation of its induction and its role in plant development. Phytochem 23:1349–1359. doi:10.1016/S0031-9422(00)80465-3
Kar M, Mishra D (1976) Catalase, peroxidase and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319. doi:10.1104/pp.57.2.315
Kendrick RE, Kerckhoffs LHJ, Van Tuinen A, Koornneef M (1997) Photomorphogenic mutants of tomato. Plant Cell Environ 20:746–751. doi:10.1046/j.1365-3040.1997.d01-109.x
Kilambi HV, Kumar R, Sharma R, Sreelakshmi Y (2013) Chromoplast-specific carotenoid-associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiol 161:2085–2101. doi:10.1104/pp.112.212191
Kraepiel Y, Rousselin P, Sotta B, Kerhoas L, Einhorn J, Caboche M, Miginiac E (1994) Analysis of phytochrome- and ABA-deficient mutants suggests that ABA degradation is controlled by light in Nicotiana plumbaginifolia. Plant J 6:665–672. doi:10.1046/j.1365-313X.1994.6050665.x
Laisk A, Loreto F (1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence. Plant Physiol 110:903–912
Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579. doi:10.1093/aob/mcn244
Li RH, Guo PG, Baum M, Grando S, Ceccarelli S (2006) Evaluation of chlorophyll content and fluorescence parameters as indicators of drought tolerance in barley. Agric Sci China 5:751–757. doi:10.1016/S1671-2927(06)60120-X
Lima ALS, Da Matta FM, Pinheiro HA, Totola MR, Loureiro ME (2002) Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions. Environ Exp Bot 47:239–247. doi:10.1016/S0098-8472(01)00130-7
Liu Y, Roof S, Ye Z, Barry C, Van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902. doi:10.1073/pnas.0400935101
Liu J, Zhang F, Zhou J, Chen F, Wang B, Xie X (2012) Phytochrome B control of total leaf area and stomatal density affects drought tolerance in rice. Plant Mol Biol 78:289–300. doi:10.1007/s11103-011-9860-3
López-Juez E, Nagatani A, Buurmeijer WF, Peters JL, Furuya M, Kendrick RE, Wesselius JC (1990) Response of light-grown wild-type and aurea-mutant tomato plants to end-of-day far-red light. J Photochem Photobiol B: Biol 4:391–405. doi:10.1016/1011-1344(90)85018-R
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. doi:10.1093/jxb/50.336.1199
Melo HC, Castro EM, Soares AM, Oliveira C, Ramos SJ (2009) Características fisiológicas de microtomateiros fitocromo-mutantes. Ciênc Agrotec 33:1213–1219. doi:10.1590/S1413-70542009000500003
Mishra KB, Iannacone R, Petrozza A, Mishra A, Armentano N, La Vecchia G, Trtílek M, Cellini F, Nedbal L (2012) Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Sci 182:79–86. doi:10.1016/j.plantsci.2011.03.022
Miyashita K, Tanakamaru S, Maitani T, Kimura K (2005) Recovery responses of photosynthesis, transpiration and stomatal conductance in kidney bean following drought stress. Environ Exp Bot 53:205–214. doi:10.1016/j.envexpbot.2004.03.015
Mohr H, Drumm H, Schmidt R, Steinitz B (1979) The effect of light pretreatments on phytochrome-mediated induction of anthocyanin and of phenyalanine ammonia-lyase. Planta 146:369–376. doi:10.1007/BF00387810
Monteiro CC, Rolão MB, Franco MR, Peters LP, Cia MC, Capaldi FR, Carvalho RF, Gratão PL, Rossi ML, Martinelli AP, Peters LEP, Azevedo RA (2012) Biochemical and histological characterization of tomato mutants. An Acad Bras Ciênc 84:573–585. doi:10.1590/S0001-37652012005000022
Mullineaux P, Ball L, Escobar C, Karpinska B, Creissen G, Karpinski S (2000) Are diverse signalling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy? Philos Trans R Soc London, Ser B 355:1531–1540. doi:10.1098/rstb.2000.0713
Muramoto T, Kami C, Kataoka H, Iwata N, Linley PJ, Mukougawa K, Yokota A, Kohchi T (2005) The tomato photomorphogenetic mutant aurea is deficient in phytochromobilin synthase for phytochrome chromophore biosynthesis. Plant Cell Physiol 46:661–665. doi:10.1093/pcp/pci062
Murshed R, Lopez-Lauri F, Sallanon H (2013) Effects of water stress on antioxidant systems and oxidative parameters in fruits of tomato (Solanum lycopersicum L. cv. Micro-Tom). Physiol Mol Biol Plants 19:363–378. doi:10.1007/s12298-013-0173-7
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Noctor G, Foyer CH (1998) Ascorbate and gluthatione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279. doi:10.1146/annurev.arplant.49.1.249
Ouedraogo M, Hubac C (1982) Effect of far red light on drought resistance of cotton. Plant Cell Physiol 23:1297–1303
Phimchan P, Chanthai S, Bosland PW, Techawongstien S (2014) Enzymatic changes in phenylalanine ammonia-lyase, cinnamic-4-hydroxylase, capsaicin synthase and peroxidase activities in Capsicum under drought stress. J Agric Food Chem 62:7057–7062. doi:10.1021/jf4051717
Pizarro L, Stange C (2009) Light-dependent regulation of carotenoid biosynthesis in plants. Cienc Investig Agrar 36:143–162. doi:10.4067/S0718-16202009000200001
Rahbarian R, Khavari-Nejad R, Ganjeali A, Bagheri A, Najafi F (2011) Drought stress effects on photosynthesis, chlorophyll fluorescence and water relations in tolerant and susceptible chickpea (Cicer arietinum L.) genotypes. Acta Biol Cracoviensia Ser Bot 53:47–56. doi:10.2478/v10182-011-0007-2
Rascher U, Liebig M, Lüttge U (2000) Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant, Cell Environ 23:1397–1405. doi:10.1046/j.1365-3040.2000.00650.x
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202. doi:10.1016/j.jplph.2004.01.013
Schittenhelm S, Menge-Hartmann U, Oldenburg E (2004) Photosynthesis, carbohydrate metabolism and yield of phytochrome-B-overexpressing potatoes under different light regimes. Crop Sci 44:131–143. doi:10.2135/cropsci2004.1310
Schopfer P (1977) Phytochrome control of enzymes. Annu Rev Plant Physiol 28:223–252. doi:10.1146/annurev.pp.28.060177.001255
Schöttler MA, Tóth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5:188. doi:10.3389/fpls.2014.00188
Sharma R, Sopory SK, Guha-Mukherjee S (1976) Phytochrome regulation of peroxidase activity in maize. Plant Sci Lett 6:69–75. doi:10.1016/0304-4211(76)90181-4
Siegel BZ (1993) Plant peroxidases: an organismic perspective. Plant Growth Regul 12:303–312. doi:10.1007/BF00027212
Silva FB, Costa AC, Alves RRP, Megguer CA (2014) Chlorophyll fluorescence as an indicator of cellular damage by glyphosate herbicide in Raphanus sativus L. plants. Am J Plant Sci 5:2509–2519. doi:10.4236/aips.2014.516265
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58. doi:10.1111/j.1469-8137.1993.tb03863.x
Sokolskaya SV, Sveshnikova NV, Kochetova GV, Solovchenko AE, Gostimski SA, Bashtanova OB (2003) Involvement of phytochrome in regulation of transpiration: red-/far red-induced responses in the chlorophyll-deficient mutant of pea. Func Plant Biol 30:1249–1259. doi:10.1104/pp.112.212191
Terry MJ, Kendrick RE (1996) The aurea and yellow-green-2 mutants of tomato are deficient in phytochrome chromophore synthesis. J Biol Chem 271:21681–21686. doi:10.1074/jbc.271.35.21681
Thomsen B, Drumm-Herrel H, Mohr H (1992) Control of the appearance of ascorbate peroxidase (EC 1.11.1.11) in mustard seedling cotyledons by phytochrome and photooxidative treatments. Planta 186:600–608. doi:10.1007/BF00198042
Toledo-Ortiz G, Huq E, Rodríguez-Concepción M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci USA 107:11626–11631. doi:10.1073/pnas.0914428107
Wang FF, Lian HL, Kang CY, Yang HQ (2010) Phytochrome B is involved in mediating red light-induced stomatal opening in Arabidopsis thaliana. Mol Plant 3:246–259. doi:10.1093/mp/ssp097
Wang ZX, Chen L, Ai J, Qin HY, Liu YX, Xu PL, Jiao ZQ, Zhao Y, Zhang QT (2012) Photosynthesis and activity of photosystem II in response to drought stress in Amur Grape (Vitis amurensis Rupr.). Photosynthetica 50:189–196. doi:10.1007/s11099-012-0023-9
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. doi:10.1016/S0176-1617(11)81192-2
Wellmann E, Schopfer P (1975) Phytochrome-mediated de novo synthesis of phenyalanine ammonia-lyase in cell suspension cultures of parsley. Plant Physiol 55:822–827. doi:10.1104/pp.55.5.822
Zhong HH, Young JC, Pease EA, Hangarter RP, McClung CR (1994) Interactions between light and the circadian clock in the regulation of CAT2 expression in Arabidopsis. Plant Physiol 104:889–898. doi:10.1104/pp.104.3.889
Zhong HH, Resnick AS, Straume M, McClung CR (1997) Effects of synergistic signaling by phytochrome A and cryptochrome1 on circadian clock-regulated catalase expression. Plant Cell 9:947–955. doi:10.1105/tpc.9.6.947
Zucker M (1965) Induction of phenylalanine deaminase by light and its relation to chlorogenic acid synthesis in potato tuber tissue. Plant Physiol 40:779–784. doi:10.1104/pp.40.5.779
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The first author would like to thank the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) for the Master’s Program Scholarship granted (Call 03/13).
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Alves, F.R.R., de Melo, H.C., Crispim-Filho, A.J. et al. Physiological and biochemical responses of photomorphogenic tomato mutants (cv. Micro-Tom) under water withholding. Acta Physiol Plant 38, 155 (2016). https://doi.org/10.1007/s11738-016-2169-8
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DOI: https://doi.org/10.1007/s11738-016-2169-8