Abstract
Alternaria alternata is a necrotrophic fungus that may cause severe losses. To further elucidate the resistance mechanisms, we investigated the impacts of increasing biotic stress, or severity levels (5%, 25% and 50%), due to A. alternata infection on two tobacco cultivars with varying resistance levels. Under severe stress, the photosynthetic pigment, net photosynthetic rate (Pn), stomatal conductance (Gs) and stomatal limitation value (Ls) all decreased in both cultivars, whereas the intercellular CO2 concentration (Ci) exhibited an upward trend. Moreover, A. alternata caused adverse effects on PSII electron transport rate and chlorophyll a fluorescence parameters, including the maximal quantum yield of fluorescence (Fv/Fm), PSII potential efficiency (Fv/F0), PSII actual quantum yield (ΦPSII), photochemical quenching (qP) and non-photochemical quenching (NPQ), and ultimately decreased PSII photochemical activity. In addition, the contents of MDA, proline and total soluble sugar increased under stress. The adverse effect of A. alternata on the resistant cultivar was less harmful than the susceptible cultivar. We conclude that the reduction of photosynthesis is a result of non-stomatal limitations. However, the resistant cultivar has better self-protection of its photosynthetic system, improved light energy utilization ability and greater accumulation of osmotic regulation substances for mitigating the damage on cellular membranes. These attributes may account for the resistance to A. alternata.
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References
Allen DJ, Ort DR (2001) Impact of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science 6:36–42
Babita M, Maheswari M, Rao LM, Shanker AK, Rao DG (2010) Osmotic adjustment, drought tolerance and yield in castor (Ricinus communis L.) hybrids. Environmental and Experimental Botany 69:243–249
Bai LP, Sui FG, Ge TD, Sun ZH, Lu YY, Zhou GS (2006) Effect of soil drought stress on leaf water status, membrane permeability and enzymatic antioxidant system of maize. Pedosphere 16:326–332
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205–207
Ben-asher J, Tsuyuki I, Bravdo BA, Sagih M (2006) Irrigation of grapevines with saline water: I. Leaf area index, stomatal conductance, transpiration and photosynthesis. Agricultural Water Management 83:13–21
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31:491–543
Calatayud A (2007) Chlorophyll a fluorescence as indicator of atmospheric pollutant effects. Toxicological and Environmental Chemistry 89:627–639
Campos KF, Carvalho-De K, Souza-De FS, Marur CJ, Pereira LFP, Vieira LGE (2011) Drought tolerance and antioxidant enzymatic activity in transgenic ‘Swingle’ citrumelo plants over-accumulating proline. Environmental and Experimental Botany 72:242–250
Cheng DD, Zhang ZS, Sun XB, Zhao M, Sun GY, Chow WS (2016) Photoinhibition and photoinhibition-like damage to the photosynthetic apparatus in tobacco leaves induced by pseudomonas syringae pv. Tabaci under light and dark conditions. BMC Plant Biology 16:29
Demmig-Adams B, Adams-III WW, Baker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98:253–264
Dhinsa RS, Plumb-Dhindsa PP, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32:93–101
Ding L, Wang KJ, Jiang GM, Li YG, Jiang CD, Liu MZ, Niu SL, Peng Y (2006) Diurnal variation of gas exchange, chlorophyll fluorescence and xanthophylls cycle components of maize hybrids released in different years. Photosynthetica 44:26–31
Doodson JK, Manners JG, Myers A (1965) Some effects of yellow rust (Puccinia striformis) on 14Carbon assimilation and translocation in wheat. Journal of Experimental Botany 16:304–317
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28:350–356
Efeoğlu B, Ekmekci Y, Cicek N (2009) Physiological responses of three maize cultivars to drought stress and recovery. South African Journal of Botany 75:34–42
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33:317–345
Hao LM, Liang HG, Wang ZL, Liu XM (1999) Effects of water stress and rewatering on turnover and gene expression of photosystem II reaction center polypeptide D1 in Zea mays. Functional Plant Biology 26:375–378
Kim YM, Bouras N, Kav NNV, Strelkov SE (2010) Inhibition of photosynthesis and modification of the wheat leaf proteome by Ptr ToxB: a host-specific toxin from the fungal pathogen Pyrenophora tritici-repentis. Proteomics 10:2911–2926
Kooten O, Snel JFH (1990) The use of chlorophyll nomenclature in plant stress physiology. Photosynthesis Research 25:147–150
Liven A (1964) Photosynthesis in healthy and rust-infected plants. Plant Physiology 39:614–621
Lloyd HL (1972) Therapeutic effect of kinetin on tobacco alternariosis. Nature New Biology 240:94–96
Lu CM, Qiu NW, Wang BS, Zhang JH (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystemII to heat stress in halophyte Suaeda salsa. Journal of Experimental Botany 54:851–860
Lucas GB (1975) Diseases of tobacco (3rd). Harold E Parker & Sons Printer, Raleigh, pp 273–276
Massacci A, Nabiv SM, Pietrosanti L, Nematov SK, Chernikova TN, Thor K, Leipner J (2008) Response of photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiology and Biochemistry 46:189–195
Mo YL, Yang RP, Liu LH, Gu XR, Yang XZ, Wang YQ, Li H (2016) Growth, photosynthesis and adaptive responses of wild and domesticated watermelon genotypes to drought stress and subsequent re-watering. Plant Growth Regulation 79:229–241
Nielsen DC, Vigil MF, Benjamin JG (2009) The variable response of dry land corn yield to soil water content at planting. Agricultural Water Management 96:330–336
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60:324–349
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA)-Bioenergetics 975:384–394
Price CA, Cushman JC, Mendiola-Morgenthaler LR, Reardon EM (1987) Isolation of plastids in density gradients of percoll and other silica sols. Methods in Enzymology 148:157–179
Rahoutei J, García-Luque I, Barón M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiologia Plantarum 110:286–292
Rapacz M (2007) Chlorophy a fluorescence transient during freezing and recovery in winter wheat. Photosynthetica 45:409–418
Reinero A, Beachy RN (1986) Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Molecular Biology 6:291–301
Reinero A, Beachy RN (1989) Reduced photosystem II activity and accumulation of viral coat protein in chloroplasts of leaves infected with tobacco mosaic virus. Plant Physiology 89:111–116
Sakaki T, Kondo N, Sugahra K (1983) Breakdown of photosynthetic pigment and lipids in spinach leaves ozone fumigation: role of active oxygen. Physiologia Plantarum 59:28–34
Saneoka H, Nagasaka C, Hahn DT, Yang WJ, Premachandra GS, Joly RJ, Rhodes D (1995) Salt tolerance of glycinebetaine-deficient and-containing maize lines. Plant Physiology 107:631–638
Shafik J, Taha KH (1984) Chemical control of brown spot of tobacco in northern Iraq. Indian. Phytopathology 37:609–672
Shen X, Li HY, Jia QZ, Feng HQ, Li MQ, Liang HG (2008) Influence of wheat(Triticum aestivum L.)stripe rust infection on photosynthetic function and expression protein D1 of wheat leaves. Acta Ecologica Sinica 28:669–676
Shew HD, Lucas GB (1991) Compendium of tobacco disease. American Phytopathological. Society:148–156
Slavov S, Mayama S, Atanassov A (2004) Some aspects of epidemiology of Alternaria alteranata tobacco pathotype. Biotechnology & Biotechnological Equipment 18:85–89
Stavely JR, Main CE (1970) Influence of temperature and other factors on initiation of tobacco brown spot. Phytopathology 60:1591–1596
Thomas PW, Woodward FI, Quick WP (2004) Systemic irradiance signalling in tobacco. New Phytologist 161:193–198
Tripathy BC, Mohanty P (1980) Zinc-inhibited electron transport of photosynthesis in isolated barley chloroplasts. Plant Physiology 66:1174–1178
Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye JY, Mi HL (2006) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiology 141:465–474
Wang SQ, Li YL, Liu FL, Song HY, Shen JC (1997) JYH, a flue-cured tobacco germplasm with high resistance to brown spot disease. China Seed Industry 2:51–52
Yousifi N, Slama I, Ghnaya T, Savouré A, Abdelly C (2010) Effects of water deficit stress on growth, water relations and osmolyte accumulation in Medicago truncatula and M. laciniata populations. Comptes Rendus Biologies 333:205–213
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This work was financially supported by the Major Science and Technology Program from Guizhou Provincial Tobacco Company (201601), the Key Program of Henan Tobacco Industry Co., Ltd. (ZW2014003) and the Science and Technology Program of Zunyi Tobacco Company (201707).
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Yang, ZX., Yang, YF., Yu, SZ. et al. Photosynthetic, photochemical and osmotic regulation changes in tobacco resistant and susceptible to Alternaria alternata. Trop. plant pathol. 43, 413–421 (2018). https://doi.org/10.1007/s40858-018-0222-4
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DOI: https://doi.org/10.1007/s40858-018-0222-4