Plant ascorbate peroxidase: molecular phylogeny and role in oxidative stress
DOI:
https://doi.org/10.24193/subbbiol.2018.2.12Keywords:
antioxidative defense system, evolution, osmoprotectants, phylogenetic.Abstract
Oxidative stress appears as a condition in accumulation and detoxification of reactive oxygen species (ROS). ROS are oxygen-derived free radicals, generated predominantly in mitochondria, peroxisomes and chloroplasts, as natural byproducts of the normal cell aerobic metabolism. In spite of their damaging effect, ROS can act as secondary messengers in different cellular processes, including tolerance to environmental stress factors. To neutralize the harmful effects of ROS, plants have evolved enzymatic and non-enzymatic defense systems. In flowering plants, ascorbate peroxidase (APX) is present in eight isoenzyme forms and constitutes an important enzymatic component in scavenging the harmful hydrogen peroxide to water as part of ascorbate-glutathione cycle. APX proteins, their roles, in planta expression location and their phylogenetic relationships are presented in the current paper. The phylogenetic analysis performed with the maximum likelihood method which was established for 118 protein sequences of 45 flowering plants. Our phylogenetic analysis revealed diversification of ascorbate peroxidase in angiosperms, and indicates a close relationship of APX1 with APX2, APX3 with APX4 and APX5, and APX6 with sAPX and tAPX proteins. Evolutionary relationships of plant ascorbate peroxidase isoenzymes indicate the evolution of different plant species genome and their phylogenetic affiliation.
References
Alscher, R. G., Donahue, H., Cramer, C. L. (1997) Reactive oxygen species and antioxidants: relationships in green cells, Physiol. Plant., 100:224–233
Apel, K., Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant. Biol., 55:373–399
Arvind, P., Prasad, M. N. V. (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L: a free-floating freshwater macrophyte, Plant. Physiol. Biochem., 41:391-397
Begara-Morales, J. C., Sánchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pérez, C., López-Jaramillo, J., Padilla, M. N., Carreras, A., Corpas, F. J., Barroso, J. B. (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation, J. Exp. Bot., 65:527-538
Boo, Y. C., Yung J. (1999) Water deficit-induced oxidative stress and antioxidant defences in rice plants, J. Plant Physiol., 155:255-261
Campanella, J. J., Bitincka, L., Smalley, J. (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences, BMC bioinformatics 4:1-29
Chen, C., Dickman, M. B. (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii, Proc. Natl. Acad. Sci., 102:3459-3464
Desikan, R., A-H-Mackerness, S. S., Hancock, J. T., Neill, S. J. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress, Plant Physiol., 127:159–172
Elstner, E. F. (1991) Mechanisms of oxygen activation in different compartments of plant cells, In: Active Oxygen/Oxidative Stress in Plant Metabolics, Pelland, E.J., Steffen, K.L. (eds.), MD Rockville: American Society of Plant Physiologists, pp. 13-25
Foyer, C. H., Harbinson, J. (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Causes of photo-oxidative stress and amelioration of defense systems in plants, Foyer, C.H., Mullineaux, P.M. (eds.), CRC, Boca-Raton, pp. 1-42
Gill, S. S., Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Bioch., 48:909-930
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0, Syst. Bio., 59:307-321
Halliwell, B. (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life, Plant Physiol., 141:312–322
Han, C., Liu, Q., Yang, Y. (2009) Short-term effects of experimental warming and enhanced ultraviolet-B radiation on photosynthesis and antioxidant defense of Picea asperata seedlings, Plant Growth Regul., 58:153–162
Hefny, M., Abdel-Kader, D. Z. (2009) Antioxidant-enzyme system as selection criteria for salt tolerance in forage sorghum genotypes (Sorghum bicolor L. Moench). In: Salinity and Water Stress, Ashraf, M., Ozturk, M., Athar, H.R. (eds.), editors. The Netherlands: Springer, pp. 25-36
Heyno, E., Mary, V., Schopfer, P., Krieger-Liszkay, A. (2011) Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes, Planta, 234:35–45
Jimenez, A., Hernandez, J. A., del Rio, L. A., Sevilla, F. (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Phys., 114:275–284
Khan, N. A., Samiullah, Singh S., Nazar, R. (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress, J. Agron. Crop. Sci., 193:435-444
Klotz, L. O. (2002) Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen, Biol. Chem., 383:443–456
Kumar, S., Stecher, G., Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 33:1870-1874
Le, S. Q., Gascuel, O. (2008) An improved general amino acid replacement matrix, Mol. Biol. Evol., 25:1307-1320
Lefort, V., Longueville, J. E., Gascuel, O. (2017) SMS: Smart Model Selection in PhyML, Mol. Biol. Evol., 34:2422–2424
Madhusudhan, R., Ishikawa, T., Sawa, Y., Shigeoka, S., Shibata, H. (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells. Physiol. Plant., 117:550–557
Maheshwari, R., Dubey, R. S. (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings, Plant. Growth. Regul., 59:37–49
Malan, C., Gregling, M. M., Gressel, J. (1990) Correlation between CuZn superoxide dismutase and glutathione reductase and environmental and xenobiotic stress tolerance in maize inbreeds, Plant Sci., 69:157–166
McEntyre, J., Ostell, J. (2002) The NCBI handbook. Bethesda (MD): National Center for Biotechnology Information (US)
Mobin, M., Khan, N. A. (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress, J. Plant Physiol., 164:601-610
Nakano, Y., Asada, K. (1987) Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate depleted medium and reactivation by monodehydroascorbate radical, Plant Cell Physiol., 28:131–140
Navrot, N., Rouhier, N., Gelhaye, E., Jaquot, J. P. (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria, Physiol. Plant., 129: 185-195
Noctor, G., Foyer, C. H. (1998) Ascorbate and glutathione: keeping active oxygen under control, Annu. Rev. Plant. Biol., 49:249–279
Orvar, B. L., Ellis, B. E. (1997) Des plants de tabac transgéniques exprimant un ARN antisens pour ascorbate peroxydase cytosolique montrent une susceptibilité accrue aux blessures d’ozone [Transgenic tobacco plants expressing an antisense RNA to cytosolic ascorbate peroxidase show increased susceptibility to ozone injury]. L’usine J., 11:1297-1305
Sharma, P., Dubey, R. S. (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes, Plant Sci., 167:541–550
Sharma, P., Dubey, R. S. (2005a) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant, Journal of Plant Phys., 162:854-864
Sharma, P., Dubey, R. S. (2005b) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings, Plant Growth Regul., 46:209–221
Sharma, P., Dubey, R. S. (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum, Plant Cell Rep., 26:2027–2038
Sharma, P., Jha, B., Dubey, R. S., Pessarakli, M. (2012) Reactive Oxygen Species, Oxidative Damage, and Antioxidative Defense Mechanism in Plants under Stressful Conditions, J. Bot., doi:10.1155/2012/217037
Simonovicova, M., Tamás, L., Huttová, J., Mistrík, I. (2004) Effect of aluminium on oxidative stress related enzymes activities in barley roots, Biol. Plant., 48:261-266
Singh, S., Khan, N. A., Nazar, R., Anjum, N. A. (2008) Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress, American J. Plant Phys., 3:25-32
Srivastava, A. K., Bhargava. P., Rai, L. C. (2005) Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum, World J. Microbiol. Biotechnol., 22:1291-1298
Székely, G., Ábrahám, E., Cséplő, Á., Rigó, G., Zsigmond, L., Csiszár, J., Ayaydin, F., Strizhov, N., Jásik, J., Schmelzer, E., Koncz, C., Szabados, L. (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis, Plant J., 53:11-28
Tsugane, K., Kobayashi, K., Niwa, Y., Ohba, Y., Wada, K., Kobayashi, H. (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification, Plant Cell, 11:1195–1206
Wang, J., Zhang, H., Allen, R. D. (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress, Plant Cell Physiol., 40:725–732
Yan, J., Tsuichihara, N., Etoh, T., Iwai, S. (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening, Plant Cell Environ., 30:1320–1325
Yang, Y., Han, C., Liu, Q., Lin, B., Wang, J. (2008) Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings, Acta Physiol. Plant., 30:433-440
Yu, C. S., Lin, C. J., Hwang, J. K. (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions, Protein Science, 13:1402-1406
Yu, C. S., Chen, Y. C., Lu, C. H., Hwang, J. K. (2006) Prediction of protein subcellular localization, Proteins: Structure, Function and Bioinformatics, 64:643-651
Zhengiang, L., Liu, D., Shenkui, L. (2007) Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis, Plant Cell Rep., 26:1909-1917
Zlatev, Z. S., Lidon, F. C., Ramalho, J. C., Yordanov, I. T. (2006) Comparison of resistance to drought of three bean cultivars, Biol. Plant., 50:389-394.
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