Main Article Content
Abstract
Phytophthora capsici Leon. is the main pathogen that limits the production of peppers. In this study, the effects of 1 and 10 mM proline (Pro), prior to exposure of resistant (CM-334) and susceptible (SD-8) pepper seedlings to P. capsici, on some physiological parameters were investigated. A lower Pro concentration (1 mM) was found to be more effective than 10 mM Pro in increasing the stress tolerance of the CM-334 cultivar. Namely, in CM-334 cultivar, the highest chlorophyll a, chlorophyll b, carotenoid, glucose and fructose content and 1,1-diphenyl-2-picrylhydrazyl (DPPH) scavenging activity percentage were detected on the seventh day after application of 1 mM Pro + P. capsici, while the lowest malondialdehyde (MDA) amount was measured on the third day in the same treatment. The highest ferric reducing antioxidant power (FRAP) increase was determined on the seventh day in the 10 mM Pro + P. capsici application. The effects of the same Pro treatments on the SD-8 cultivar somewhat differed; the highest amounts of chlorophyll a, chlorophyll b, anthocyanins, fructose, total protein and endogenous Pro were detected on the seventh day in the 1 mM Pro + P. capsici application, while the lowest MDA amount was measured on the third day after the 10 mM Pro + P. capsici application, the highest DPPH % and FRAP values were detected on the seventh day with 10 mM Pro + P. capsici application.
Keywords
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References
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- Ashraf, M., Foolad, M.R., 2007: Roles of glycinebetaine and proline in improving plant abiotic stress tolerance. Environmental and Experimental Botany 59, 206–216.
- Blois, M.S., 1958: Antioxidant determinations by the use of a stable free radical. Nature 181 (4617), 1199–1200.
- Bates, L.S., Waldren, R.P., Teare, I.D., 1973: Rapid determination of free proline for water-stress studies. Plant and Soil 39(1), 205–207.
- Bradford, M.M., 1976: A rapid and sensitive method for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
- Claussen, W., 2005: Proline as a measure of stress in tomato plants. Plant Science, 168(1), 241 –248.
- Dawood, M.G., Taie, H.A.A., Nassar, R.M.A., Abdelhamid, M.T., Schmidhalter, U., 2014: The changes induced in the physiological, biochemical and anatomical characteristics of Vicia faba by the exogenous application of proline under seawater stress. South African Journal of Botany 93, 54–63.
- Devasagayam, T.P.A., Boloor, K.K., Ramasarma, T., 2003: Methods for estimating lipid peroxidation: an analysis of merits and demerits. Indian Journal of Biochemistry and Biophysics 40 (5), 300–308.
- Elewa, T.A., Sadak, M.S., Saad, A.M., 2017: Proline application improves physiological responses in quinoa plants under drought stress. Bioscience Research 14(1), 21–33.
- FAO, 2017: The statistical yearbook world food and agriculture. Retrieved September 15, 2020 from http://www.faostat.org
- Foster, J.M., Hausbeck, M. K., 2010: Resistance of pepper to Phytophthora crown, root, and fruit rot is affected by isolate virulence. Plant Disease 94(1), 24–30.
- Göçmen, M., 2006: Differential interactions of Phytophthora capsici isolates with pepper genotypes and characterization of resistance resources. PhD Thesis. University of Çukurova, Adana (in Turkish).
- Halhoul, M.N., Kleinberg, I., 1972: Differential determination of glucose and fructose yielding substances with anthrone. Analytical Biochemistry 50, 337–343.
- Hao, C., Xia, Z., Fan, R., Tan, L., Hu, L., Wu, B., Wu, H., 2016: De novo transcriptome sequencing of black pepper (Piper nigrum L.) and an analysis of genes involved in phenylpropanoid metabolism in response to Phytophthora capsici. BMC Genomics 17(1), 822.
- Hausbeck, M.K., Lamour, K.H., 2004: Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Disease 88(12), 1292–1303.
- Hayat, S., Hayat, Q., Alyemeni, M.N., Wani , A.S., Pichtel, J., Ahmad, A., 2012: Role of proline under changing environments. Plant Signaling and Behavior 7, 1456–1466.
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- Kavi Kishor, P.B., Hima Kumari, P., Sunita, M.S.L., Sreenivasulu, N., 2015: Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Frontiers in Plant Science, 6, 544.
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- Krishnan, V., Ahmad, S., Mahmood, M., 2015: Antioxidant potential in different parts and callus of Gynura procumbens and different parts of Gynura bicolor. BioMed Research International, 147909.
- Kurkela, S., Franck, M., Heino, P., Long, V., Palva, E.T., 1988: Cold induced gene expression in Arabidopsis thaliana L. Plant Cell Reports 7, 495–498.
- Landi, M., Pardossi, A., Remorini, D., Guidi, L., 2013: Antioxidant and photosynthetic response of a purple-leaved and a green-leaved cultivar of sweet basil (Ocimum basilicum) to boron excess. Environmental and Experimental Botany 85, 64–75.
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- Liang, X., Zhang, L., Natarajan, S.K., Becker, D.F., 2013: Proline mechanisms of stress survival. Antioxidants & Redox Signaling 19(9), 998–1011.
- Lichtenthaler, H.K., 1987: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
- Llave, C., 2016: Dynamic cross-talk between host primary metabolism and viruses during infections in plants. Current Opinion in Virology 19, 50–55.
- Mancinelli, A.L., Yang, C.P.H., Lindquist, P., Anderson, O.R., Rabino, I., 1975: Photocontrol of anthocyanin synthesis III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiology 55, 251–257.
- Mandal, K., Saravanan, R., Maiti, S., Kothari, I.L., 2009: Effect of downy mildew disease on photosynthesis and chlorophyll fluorescence in Plantago ovata Forsk. Journal of Plant Diseases and Protection 116(4), 164–168.
- McCready, R.M., Guggolz, J., Silviera, V., Owens, H.S., 1950: Determination of starch and amylose in vegetables. Analytical Chemistry 22(9), 1156–1158.
- Medeiros, L., Jaislanny, M., Medeiros De A Silva, M., Granja, C., Maria, M., De Souza E Silva Junior, G., Willadino, L., 2015: Effect of exogenous proline in two sugarcane genotypes grown in vitro under salt stress. Acta Biológica Colombiana 20(2), 57–63.
- Mirecki, R.M., Teramura, A.H., 1984: Effects of ultraviolet-B irradiance on soybean: V. The dependence of plant sensitivity on the photosynthetic photon flux density during and after leaf expansion. Plant Physiology 74(3), 475–480.
- Moustakas, M., Sperdouli, I., Kouna, T., Antonopoulou, C.I., Therios, I., 2011: Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regulation 65(2), 315–325.
- Nanjo, T., Fujita, M., Seki, M., Kato, T., Tabata, S., Shinozaki, K., 2003: Toxicity of Free Proline Revealed in an Arabidopsis T-DNA-Tagged Mutant Deficient in Proline Dehydrogenase. Plant and Cell Physiology 44(5), 541–548.
- Nounjan, N., Theerakulpisut, P., 2012: Effects of exogenous proline and trehalose on physiological responses in rice seedlings during salt-stress and after recovery. Plant, Soil and Environment 58(7), 309–315.
- Ortega, G., Palazon Espanol, C., Cuartero Zueco, J., 1991: Genetics of resistance to Phytophthora capsici in the pepper line ‘SCM-334’. Plant Breeding 107, 50–55.
- Porra, P.J., Thompson, W.A., Kriedemann, P.E., 1989: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls and a extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochemistry BiophysicsActa 975, 384–394.
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References
Abdelaal, K.A., Attia, K.A., Alamery, S.F., El-Afry, M.M., Ghazy, A.I., Tantawy, D.S., Hafez, Y.M., 2020: Exogenous application of proline and salicylic acid can mitigate the injurious impacts of drought stress on barley plants associated with physiological and histological characters. Sustainability 12(5), 1736.
Ashraf, M., Foolad, M.R., 2007: Roles of glycinebetaine and proline in improving plant abiotic stress tolerance. Environmental and Experimental Botany 59, 206–216.
Blois, M.S., 1958: Antioxidant determinations by the use of a stable free radical. Nature 181 (4617), 1199–1200.
Bates, L.S., Waldren, R.P., Teare, I.D., 1973: Rapid determination of free proline for water-stress studies. Plant and Soil 39(1), 205–207.
Bradford, M.M., 1976: A rapid and sensitive method for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
Claussen, W., 2005: Proline as a measure of stress in tomato plants. Plant Science, 168(1), 241 –248.
Dawood, M.G., Taie, H.A.A., Nassar, R.M.A., Abdelhamid, M.T., Schmidhalter, U., 2014: The changes induced in the physiological, biochemical and anatomical characteristics of Vicia faba by the exogenous application of proline under seawater stress. South African Journal of Botany 93, 54–63.
Devasagayam, T.P.A., Boloor, K.K., Ramasarma, T., 2003: Methods for estimating lipid peroxidation: an analysis of merits and demerits. Indian Journal of Biochemistry and Biophysics 40 (5), 300–308.
Elewa, T.A., Sadak, M.S., Saad, A.M., 2017: Proline application improves physiological responses in quinoa plants under drought stress. Bioscience Research 14(1), 21–33.
FAO, 2017: The statistical yearbook world food and agriculture. Retrieved September 15, 2020 from http://www.faostat.org
Foster, J.M., Hausbeck, M. K., 2010: Resistance of pepper to Phytophthora crown, root, and fruit rot is affected by isolate virulence. Plant Disease 94(1), 24–30.
Göçmen, M., 2006: Differential interactions of Phytophthora capsici isolates with pepper genotypes and characterization of resistance resources. PhD Thesis. University of Çukurova, Adana (in Turkish).
Halhoul, M.N., Kleinberg, I., 1972: Differential determination of glucose and fructose yielding substances with anthrone. Analytical Biochemistry 50, 337–343.
Hao, C., Xia, Z., Fan, R., Tan, L., Hu, L., Wu, B., Wu, H., 2016: De novo transcriptome sequencing of black pepper (Piper nigrum L.) and an analysis of genes involved in phenylpropanoid metabolism in response to Phytophthora capsici. BMC Genomics 17(1), 822.
Hausbeck, M.K., Lamour, K.H., 2004: Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Disease 88(12), 1292–1303.
Hayat, S., Hayat, Q., Alyemeni, M.N., Wani , A.S., Pichtel, J., Ahmad, A., 2012: Role of proline under changing environments. Plant Signaling and Behavior 7, 1456–1466.
Hayat, K., Khan, J., Khan, A., Ullah, S., Ali, S., Fu, Y., 2021: Ameliorative effects of exogenous Proline on photosynthetic attributes, nutrients uptake, and oxidative stresses under cadmium in Pigeon pea (Cajanus cajan L.). Plants 10(4), 796.
Hossain, M.A., Hoque, M.A., Burritt, D.J., Fujita, M., 2014: Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Ahmad, P. (ed.), Oxidative damage to plants, 477–522. Academic Press, San Diego.
Hoque Anamul, M.D., Okuma, E., Nakamara, Y., Shimoishi, Y., Murata, Y., 2008: Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. Journal of Plant Physiology 165, 813–824.
Huang, H., Ullah, F., Zhou, DX., Yi, M., Zhao, Y., 2019: Mechanisms of ROS regulation of plant development and stress responses. Frontiers in Plant Science 10, 800.
Jin, J.H., Zhang, H.X., Tan, J.Y., Yan, M.J., Li, D.W., Khan, A., Gong ZH., 2015: A new ethylene-responsive factor CaPTI1 gene in pepper (Capsicum annuum L.) involved in the regulation of defense response to Phytophthora capsici. Frontiers in Plant Science 6, 1217.
Jones, D.R., Graham, W.G., Ward, E.W.B., 1974: Compatible Interaction with Phytophthora capsici. Phytopathology 64, 1084–1090.
Kahraman, M., Sevim, G., Bor, M., 2019: The role of proline, glycinebetaine, and trehalose in stress-responsive gene expression. In: Hossain, M.A., Kumar, V., Burritt, J., Fujita, M., Makela, P.S.A. (eds.), In osmoprotectant-mediated abiotic stress tolerance in plants, 241 –256. Springer, Cham.
Kaushal, N., Gupta, K., Bhandhar, K., Kumar, S., Thakur, P., Nayyar, H., 2011: Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiology and Molecular Biology of Plants 17(3), 203–213
Kavi Kishor, P.B., Hima Kumari, P., Sunita, M.S.L., Sreenivasulu, N., 2015: Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Frontiers in Plant Science, 6, 544.
Kim, S., Park, J., Yeom, S. I, Kim, Y. M., Seo, E., Kim, K. T., et al., 2017: New reference genome sequences of hot pepper reveal the massive evaluation of plant disease-resistance gene by retroduplication. Genome Biology 18, 210.
Kim, S., Park, M., Yeom, S. I., Kim, Y. M., Lee, J. M., Lee, H. A., Choi, D., 2014: Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics 46(3), 270–278.
Koç, E., Üstün, A. S., İşlek, C., Arıcı, Y.K., 2011: Defence responses in leaves of resistant and susceptible pepper (Capsicum annuum L.) cultivars infected with different inoculum concentrations of Phytophthora capsici Leon. Scientia Horticulturae 128(4), 434–442.
Koç, E., 2017: Alleviation of Phytophthora capsici-induced oxidative stress by foliarly applied proline in Capsicum annuum L. Archives of Biological Sciences 69(4), 733–742.
Krishnan, V., Ahmad, S., Mahmood, M., 2015: Antioxidant potential in different parts and callus of Gynura procumbens and different parts of Gynura bicolor. BioMed Research International, 147909.
Kurkela, S., Franck, M., Heino, P., Long, V., Palva, E.T., 1988: Cold induced gene expression in Arabidopsis thaliana L. Plant Cell Reports 7, 495–498.
Landi, M., Pardossi, A., Remorini, D., Guidi, L., 2013: Antioxidant and photosynthetic response of a purple-leaved and a green-leaved cultivar of sweet basil (Ocimum basilicum) to boron excess. Environmental and Experimental Botany 85, 64–75.
Lehmann, S., Funck, D., Szabados, L., Rentsch, D., 2010: Proline metabolism and transport in plant development. Amino Acids 39(4), 949–962.
Liang, X., Zhang, L., Natarajan, S.K., Becker, D.F., 2013: Proline mechanisms of stress survival. Antioxidants & Redox Signaling 19(9), 998–1011.
Lichtenthaler, H.K., 1987: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Llave, C., 2016: Dynamic cross-talk between host primary metabolism and viruses during infections in plants. Current Opinion in Virology 19, 50–55.
Mancinelli, A.L., Yang, C.P.H., Lindquist, P., Anderson, O.R., Rabino, I., 1975: Photocontrol of anthocyanin synthesis III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiology 55, 251–257.
Mandal, K., Saravanan, R., Maiti, S., Kothari, I.L., 2009: Effect of downy mildew disease on photosynthesis and chlorophyll fluorescence in Plantago ovata Forsk. Journal of Plant Diseases and Protection 116(4), 164–168.
McCready, R.M., Guggolz, J., Silviera, V., Owens, H.S., 1950: Determination of starch and amylose in vegetables. Analytical Chemistry 22(9), 1156–1158.
Medeiros, L., Jaislanny, M., Medeiros De A Silva, M., Granja, C., Maria, M., De Souza E Silva Junior, G., Willadino, L., 2015: Effect of exogenous proline in two sugarcane genotypes grown in vitro under salt stress. Acta Biológica Colombiana 20(2), 57–63.
Mirecki, R.M., Teramura, A.H., 1984: Effects of ultraviolet-B irradiance on soybean: V. The dependence of plant sensitivity on the photosynthetic photon flux density during and after leaf expansion. Plant Physiology 74(3), 475–480.
Moustakas, M., Sperdouli, I., Kouna, T., Antonopoulou, C.I., Therios, I., 2011: Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regulation 65(2), 315–325.
Nanjo, T., Fujita, M., Seki, M., Kato, T., Tabata, S., Shinozaki, K., 2003: Toxicity of Free Proline Revealed in an Arabidopsis T-DNA-Tagged Mutant Deficient in Proline Dehydrogenase. Plant and Cell Physiology 44(5), 541–548.
Nounjan, N., Theerakulpisut, P., 2012: Effects of exogenous proline and trehalose on physiological responses in rice seedlings during salt-stress and after recovery. Plant, Soil and Environment 58(7), 309–315.
Ortega, G., Palazon Espanol, C., Cuartero Zueco, J., 1991: Genetics of resistance to Phytophthora capsici in the pepper line ‘SCM-334’. Plant Breeding 107, 50–55.
Porra, P.J., Thompson, W.A., Kriedemann, P.E., 1989: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls and a extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochemistry BiophysicsActa 975, 384–394.
Rabuma, T., Gupta, O. P., Chhokar, V., Yadav, M., 2021: Integrative RNA-Seq analysis of Capsicum annuum L.-Phytophthora capsici L. pathosystem reveals molecular cross-talk and activation of host defence response. bioRxiv. doi: https://doi.org/10.1101/2021.04.03.438323.
Ramel, F., Birtic, S., Cuiné, S., Triantaphylides, C., Ravanat, J. L., Havaux, M., 2012: Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology 158, 1267–1278.
Roychoudhury, A., Chakraborty, M., 2013: Biochemical and molecular basis of varietal difference in plant salt tolerance. Annual Research and Review in Biology 3, 422–454.
Santos-Sánchez, N.F., Salas-Coronado, R., Villanueva-Cañongo, C., Hernández-Carlos, B., 2019: Antioxidant compounds and their antioxidant mechanism. In: Shalaby, E. (ed.), Antioxidants, 1–28. IntechOpen, London.
Sharma, A., Kumar, V., Shahzad, B., Ramakrishnan, M., Sidhu, G.P.S., Bali, A.S., Handa, N., Kapoor, D., Yadav, P., Khanna, K., Bakshi, P., Rehman, A., Kohli, S.K., Khan, E.K., Parihar, R.D., Yuan, H., Thukral, A.K., Bhardwaj, R., Zheng, B., 2019: Photosynthetic response of plants under different abiotic stresses: a review. Journal of Plant Growth Regulation 39, 509–531.
Sharma, N., Prasad, M., 2017: An insight into plant-tomato leaf curl New Delhi virus interaction. Nucleus 60, 335–348.
Siddique, M.I., Lee, H.Y., Ro, N.Y., Han, K., Venkatesh, J., Solomon, A.M., Patil, A.S., Changkwian, A., Kwon, J.K., Kang, B.C., 2019: Identifying candidate genes for Phytophthora capsici resistance in pepper (Capsicum annuum) via genotyping-by-sequencing-based QTL mapping and genome-wide association study. Scientific Reports 9(1), 9962.
Subramanian, R., Subbramaniyan, P., Raj, V., 2013: Antioxidant activity of the stem bark of Shorea roxburghii and its silver reducing power. SpringerPlus 2(1), 28.
Trovato, M., Mattioli, R., Costantino, P., 2008: Multiple roles of proline in plant stress tolerance and development. Rendiconti Lincei 19(4), 325–346.
Van den Ende, W., Valluru, R., 2009: Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging?. Journal of Experimental Botany 60(1), 9–18.
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