Differential Expression of Two Cytosolic Ascorbate Peroxidase and Two Superoxide Dismutase Genes in Response to Abiotic Stress in Rice

Abstract

Abstract: Superoxide dismutase (SOD) and ascorbate peroxidase (APX) play central roles in the pathway for scavenging reactive oxygen species in plants, thereby contributing to the tolerance against abiotic stress. Here we report the responses of cytosolic SOD (cSOD; sodCc1 and sodCc2) and cytosolic APX (cAPX; OsAPX1 and OsAPX2) genes to oxidative and abiotic stress in rice. RNA blot analyses revealed that methyl viologen treatment caused a more prominent induction of cAPXs compared with cSODs, and hydrogen peroxide treatment induced the expression of cAPXs whereas cSODs were not affected. These results suggest that cAPXs play more important roles in defense against oxidative stress compared with cSODs. It is noted that cSODs and cAPXs showed coordinate response to abscisic acid treatment which induced both sodCc1 and OsAPX2. However, cSODs and cAPXs responded differentially to drought, salt and chilling stress, which indicates that cSOD and cAPX genes are expressed differentially in response to oxidative and abiotic stress in rice.Abstract: Superoxide dismutase (SOD) and ascorbate peroxidase (APX) play central roles in the pathway for scavenging reactive oxygen species in plants, thereby contributing to the tolerance against abiotic stresses. Here we report the responses of cytosolic SOD (cSOD; sodCc1 and sodCc2) and cytosolic APX (cAPX; OsAPx1 and OsAPx2) genes to oxidative and abiotic stresses in rice. RNA blot analyses revealed that methyl viologen treatment caused a more prominent induction of cAPXs compared with cSODs. Hydrogen peroxide treatment induced cAPXs whereas cSODs were not affected. These results suggest that cAPXs play more important roles in defense against oxidative stress compared with cSODs. It is noted that cSODs and cAPXs showed coordinate response to abscisic acid treatment by which sodCc1 and OsAPx2 were both induced. However, cSODs and cAPXs responded differentially to drought, salt, and chilling stresses, which indicates that cSOD and cAPX genes are expressed differentially in response to oxidative and abiotic stresses in rice.

Key words: ascorbate peroxidase, superoxide dismutase, reactive oxygen species, abiotic stress, rice

Shigeto MORITA, Shinya NAKATANI, Tomokazu KOSHIBA, Takehiro MASUMURA, Yasunari OGIHARA, Kunisuke TANAKA. Differential Expression of Two Cytosolic Ascorbate Peroxidase and Two Superoxide Dismutase Genes in Response to Abiotic Stress in Rice[J]. RICE SCIENCE.

References

Agrawal G K, Jwa N-S, Iwahashi H, Rakwal R. 2003. Importance of ascorbate peroxidases OsAPX1 and OsAPX2 in the rice pathogen response pathways and growth and reproduction revealed by their transcriptional profiling. Gene, 322: 93–103.
Asada K. 1999. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol, 50: 601–639.
Cakmak I, Marschner H. 1992. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol, 98: 1222–1227.
Chen W, Singh K B. 1999. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J, 19: 667–677.
Chirgwin J M, Przybyla A E, MacDonald R J, Rutter W J. 1979. Isolation of biologically active ribonucleic acid from sources
enriched in ribonuclease. Biochemistry, 18: 5294–5299.
Conklin P L, Last R L. 1995. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol, 109: 203–212.
Davletova S, Rizhsky L, Liang H, Zhong S, Oliver D J, Coutu J, Shulaev V, Schlauch K, Mittler R. 2005. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene
network of Arabidopsis. Plant Cell, 17: 268–281.
Finkelstein R R, Gampala S S, Rock C D. 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell, 14(Suppl): S15–S45.
Funatsuki H, Kurosaki H, Murakami T, Matsuba S, Kawaguchi K, Yumoto S, Sato Y. 2003. Deficiency of a cytosolic ascorbate peroxidase associated with chilling tolerance in soybean. Theor Appl Genet, 106: 494–502.
Garreton V, Carpinelli J, Jordana X, Holuigue L. 2002. The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol, 130: 1516–1526.
Guan L M, Zhao J, Scandalios J G. 2000. Cis-elements and trans- factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J, 22: 87–95.
Jiang M, Zhang J. 2002. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and upregulates the activities of antioxidant enzymes in maize leaves. J Exp Bot, 53: 2401–2410.
Kaminaka H, Morita S, Yokoi H, Masumura T, Tanaka K. 1997. Molecular cloning and characterization of a cDNA for plastidic copper/zinc-superoxide dismutase in rice (Oryza sativa L.). Plant Cell Physiol, 38: 65–69.
Kaminaka H, Morita S, Tokumoto M, Masumura T, Tanaka K. 1999a. Differential gene expressions of rice superoxide dismutase isoforms to oxidative and environmental stresses. Free Radical Res, 31(Suppl): S219–S225.
Kaminaka H, Morita S, Tokumoto M, Yokoyama H, Masumura T, Tanaka K. 1999b. Molecular cloning and characterization of a cDNA for an iron-superoxide dismutase in rice (Oryza sativa L.). Biosci Biotechnol Biochem, 63: 302–308.
Komatsu S, Muhammad A, Rakwal R. 1999. Separation and characterization of proteins from green and etiolated shoots of rice (Oryza sativa L.): Towards a rice proteome. Electrophoresis, 20: 630–636.
Koshiba T. 1993. Cytosolic ascorbate peroxydase in seedlings and leaves of maize (Zea mays). Plant Cell Physiol, 34: 713–721.
Lee S C, Kwon S Y, Kim S R. 2009. Ectopic expression of a cold-responsive CuZn superoxide dismutase gene, SodCc1, in transgenic rice (Oryza sativa L.). J Plant Biol, 52: 154–160.
Leung J, Giraudat J. 1998. Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol, 49: 199–222.
Lu Z, Takano T, Liu S. 2005. Purification and characterization of two ascorbate peroxidases of rice (Oryza sativa L.) expressed in Escherichia coli. Biotechnol Lett, 27: 63–67.
Lu Z, Liu D, Liu S. 2007. Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep, 26: 1909–1917.
Mishra N P, Mishra R K, Singhal G S. 1993. Changes in the activities of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiol, 102:
903–910.
Mittler R, Zilinskas B A. 1993. Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem, 212: 540–546.
Mittler R, Zilinskas B A. 1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J, 5: 397–405.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends Plant Sci, 9: 490–498.
Morita S, Kaminaka H, Yokoi H, Masumura T, Tanaka K. 1997. Cloning and characterization of cytosolic ascorbate peroxidase cDNA from rice (accession No. D45423). Plant Physiol, 113: 306.
Morita S, Kaminaka H, Masumura T, Tanaka K. 1999. Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; the involvement of hydrogen peroxide in oxidative stress signalling. Plant Cell Physiol, 40: 417–422.
Noctor G, Foyer C H. 1998. Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol, 49: 249–279.
Prasad T K, Anderson M D, Martin B A, Stewart C R. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell, 6: 65–74.
Rao M V, Paliyath G, Ormrod D P. 1996. Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol, 110: 125–136.
Sakamoto A, Ohsuga H, Tanaka K. 1992. Nucleotide sequences of two cDNA clones encoding different Cu/Zn-superoxide dismutases expressed in developing rice seed (Oryza sativa L.). Plant Mol Biol, 19: 323–327.
Sakamoto A, Nosaka Y, Tanaka K. 1993. Cloning and sequencing analysis of a complementary DNA for manganese-superoxide dismutase from rice (Oryza sativa L.). Plant Physiol, 103: 1477– 1478.
Sakamoto A, Okumura T, Kaminaka H, Sumi K, Tanaka K. 1995. Structure and differential response to abscisic acid of two promoters for the cytosolic copper/zinc-superoxide dismutase genes, SodCc1 and SodCc2, in rice protoplasts. FEBS Lett, 358: 62–66.
Sato Y, Antonio B A, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y. 2011. RiceXPro: A platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucl Acids Res, 39: D1141–D1148.
Sch?ner S, Krause G H. 1990. Protective systems against active oxygen speicies in spinach: Response to cold acclimation in excess light. Planta, 180: 383–389.
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta
Y, Yoshimura K. 2002. Regulation and function of peroxidase isoenzymes. J Exp Bot, 53: 1305–1319.
Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa K, Yokota A, Shigeoka S. 1998. Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett, 428: 47–51.
Shirzadegan M, Christie P, Seemann J R. 1991. An efficient method for isolation of RNA from tissue cultured plant cells. Nucl Acids Res, 19: 6055.
Teixeira F K, Menezes-Benavente L, Margis R, Margis-Pinheiro M. 2004. Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: Inferences from the rice genome. J Mol Evol, 59: 761–770.
Teixeira F K, Menezes-Benavente L, Galvao V C, Margis R, Margis- Pinheiro M. 2006. Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta, 224: 300–314.
Tsukamoto S, Morita S, Hirano E, Yokoi H, Masumura T, Tanaka K. 2005. A novel cis-element that is responsive to oxidative stress regulates three antioxidant defense genes in rice. Plant Physiol, 137: 317–327.

[1]	LI Qianlong, FENG Qi, WANG Heqin, KANG Yunhai, ZHANG Conghe, DU Ming, ZHANG Yunhu, WANG Hui, CHEN Jinjie, HAN Bin, FANG Yu, WANG Ahong. Genome-Wide Dissection of Quan 9311A Breeding Process and Application Advantages [J]. Rice Science, 2023, 30(6): 7-.
[2]	JI Dongling, XIAO Wenhui, SUN Zhiwei, LIU Lijun, GU Junfei, ZHANG Hao, Tom Matthew HARRISON, LIU Ke, WANG Zhiqin, WANG Weilu, YANG Jianchang. Translocation and Distribution of Carbon-Nitrogen in Relation to Rice Yield and Grain Quality as Affected by High Temperature at Early Panicle Initiation Stage [J]. Rice Science, 2023, 30(6): 12-.
[3]	Prathap V, Suresh KUMAR, Nand Lal MEENA, Chirag MAHESHWARI, Monika DALAL, Aruna TYAGI. Phosphorus Starvation Tolerance in Rice Through a Combined Physiological, Biochemical and Proteome Analysis [J]. Rice Science, 2023, 30(6): 8-.
[4]	Serena REGGI, Elisabetta ONELLI, Alessandra MOSCATELLI, Nadia STROPPA, Matteo Dell’ANNO, Kiril PERFANOV, Luciana ROSSI. Seed-Specific Expression of Apolipoprotein A-I_Milano Dimer in Rice Engineered Lines [J]. Rice Science, 2023, 30(6): 6-.
[5]	Sundus ZAFAR, XU Jianlong. Recent Advances to Enhance Nutritional Quality of Rice [J]. Rice Science, 2023, 30(6): 4-.
[6]	Kankunlanach KHAMPUANG, Nanthana CHAIWONG, Atilla YAZICI, Baris DEMIRER, Ismail CAKMAK, Chanakan PROM-U-THAI. Effect of Sulfur Fertilization on Productivity and Grain Zinc Yield of Rice Grown under Low and Adequate Soil Zinc Applications [J]. Rice Science, 2023, 30(6): 9-.
[7]	FAN Fengfeng, CAI Meng, LUO Xiong, LIU Manman, YUAN Huanran, CHENG Mingxing, Ayaz AHMAD, LI Nengwu, LI Shaoqing. Novel QTLs from Wild Rice Oryza longistaminata Confer Rice Strong Tolerance to High Temperature at Seedling Stage [J]. Rice Science, 2023, 30(6): 14-.
[8]	XIA Xiaodong, ZHANG Xiaobo, WANG Zhonghao, CHENG Benyi, Sun Huifeng, XU Xia, GONG Junyi, YANG Shihua, WU Jianli, SHI Yongfeng, XU Rugen. Mapping and Functional Analysis of LE Gene in a Lethal Etiolated Rice Mutant at Seedling Stage [J]. Rice Science, 2023, 30(6): 13-.
[9]	LIN Shaodan, YAO Yue, LI Jiayi, LI Xiaobin, MA Jie, WENG Haiyong, CHENG Zuxin, YE Dapeng. Application of UAV-Based Imaging and Deep Learning in Assessment of Rice Blast Resistance [J]. Rice Science, 2023, 30(6): 10-.
[10]	Md. Forshed DEWAN, Md. AHIDUZZAMAN, Md. Nahidul ISLAM, Habibul Bari SHOZIB. Potential Benefits of Bioactive Compounds of Traditional Rice Grown in South and South-East Asia: A Review [J]. Rice Science, 2023, 30(6): 5-.
[11]	Raja CHAKRABORTY, Pratap KALITA, Saikat SEN. Phenolic Profile, Antioxidant, Antihyperlipidemic and Cardiac Risk Preventive Effect of Chakhao Poireiton (A Pigmented Black Rice) in High-Fat High-Sugar induced Rats [J]. Rice Science, 2023, 30(6): 11-.
[12]	Jiang Changjie, Liang Zhengwei, Xie Xianzhi. Priming for Saline-Alkaline Tolerance in Rice: Current Knowledge and Future Challenges [J]. Rice Science, 2023, 30(5): 417-425.
[13]	Nazaratul Ashifa Abdullah Salim, Norlida Mat Daud, Julieta Griboff, Abdul Rahim Harun. Elemental Assessments in Paddy Soil for Geographical Traceability of Rice from Peninsular Malaysia [J]. Rice Science, 2023, 30(5): 486-498.
[14]	Ammara Latif, Sun Ying, Pu Cuixia, Noman Ali. Rice Curled Its Leaves Either Adaxially or Abaxially to Combat Drought Stress [J]. Rice Science, 2023, 30(5): 405-416.
[15]	Liu Qiao, Qiu Linlin, Hua Yangguang, Li Jing, Pang Bo, Zhai Yufeng, Wang Dekai. LHD3 Encoding a J-Domain Protein Controls Heading Date in Rice [J]. Rice Science, 2023, 30(5): 437-448.