Abstract
The gaseous pollutant Sulfur dioxide (SO2) impacts deleteriously on crop growth and development. To identify genes required for SO2 stress response in maize (Zea mays. L), one highly induced mRNA encoding a D1 protein of photosystem II (ZmpsbA) was isolated by mRNA differential display. Real-time PCR analysis indicated that the transcript levels of ZmpsbA were higher in leaves and were markedly up-regulated by SO2 stress. Overexpression of ZmpsbA enhanced SO2 stress tolerance in tobacco; showing much less damage upon SO2 exposure. The transgenic tobacco lines had higher proline accumulation, but lower levels of malondialdehyde when compared with the wild-type plants under SO2 stress. Further investigation showed that ZmpsbA transgenic plants displayed higher superoxide dismutase (SOD) and catalase (CAT) activities, increased SOD and CAT transcript levels, and decreased reactive oxygen species (ROS) accumulation under SO2 stress. Taken together, our results demonstrate that ZmpsbA confers SO2 stress tolerance in transgenic tobacco by reducing ROS accumulation and membrane damage through enhancing the antioxidant system. ZmpsbA might serve as a candidate gene in genetic improvement for environmental pollutants (SO2 and acid rain, etc.) tolerance engineering in crop plants.
Similar content being viewed by others
References
Able AJ, Guest DI, Sutherland MW (1998) Use of a new nitroblue tetrazolium -based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores. Plant Physiol 117:491–499
Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition–a historical perspective. Photosynth Res 76:343–370
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Agrawal M, Singh B, Rajput M, Marshall F, Bell JN (2003) Effect of air pollution on peri-urban agriculture: a case study. Environ Pollut 126:323–329
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Armbruster U, Zühlke J, Rengstl B, Kreller R, Makarenko E, Rühle T, Schünemann D, Jahns P, Weisshaar B, Nickelsen J, Leister D (2010) The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly. Plant Cell 22:3439–3460
Aro EM, McCaffery S, Anderson JM (1994) Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances. Plant Physiol 104:1033–1041
Baena-González E, Aro EM (2002) Biogenesis, assembly and turnover of photosystem II units. Philos Trans R Soc Lond B Biol Sci 357:1451–1459
Bates LS, Waldren RP, Tear ID (1973) Rapid determination of free proline for water- stress studies. Plant Soil 39:205–207
Bruce N, Perez-Padilla R, Albalak R (2000) Indoor air pollution in developing countries: a major environmental and public health challenge. Bull World Health Organ 78:1078–1092
Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J 50:696–709
Darrail NM (1989) The effect of air pollutants on physiological processes in plants. Plant Cell Environ 12:1–30
Demmig B, Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171:171–184
Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 86:421–431
Ferguson IB, Watkins CB, Harman JE (1983) Inhibition by calcium of senescence of detached cucumber cotyledons. Plant Physiol 71:182–186
Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314
Jain S, Kumar D, Jain M, Chaudhary P, Deswal R, Sarin NB (2012) Ectopic overexpression of a salt stress-induced pathogenesisrelated class 10 protein (PR10) gene from peanut (Arachis hypogaea L.) affords broad spectrum abiotic stress tolerance in transgenic tobacco. Plant Cell Tissue Organ Cult 109:19–31
Kim M, Christopher DA, Mullet JE (1993) Direct evidence for selective modulation of psbA, rpoA, rbcL and 16S RNA stability during barley chloroplast development. Plant Mol Biol 22:447–463
Klaff P, Gruissem W (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell 3:517–529
Klein RR, Mullet JE (1987) Control of gene expression during higher plant chloroplast biogenesis. Protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated barley seedlings. J Biol Chem 262:4341–4348
Klein RR, Mason HS, Mullet JE (1988) Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA, and rbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J Cell Biol 106:289–301
Leelavathi S, Bhardwaj A, Kumar S, Dass A, Pathak R, Pandey SS, Tripathy BC, Padmalatha KV, Dhandapani G, Kanakachari M, Solanke AU, Kumar PA, Cella R, Siva Reddy V (2011) Genome-wide transcriptome and proteome analyses of tobacco psaA and psbA deletion mutants. Plant Mol Biol 76:407–423
Livaka KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 25:402–408
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Meng Z, Zhang L (1992) Cytogenetic damage induced in human lymphocytes by sodium bisulfite. Mutat Res 298:63–69
Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749
Rintämaki E, Kettunen R, Aro EM (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centres. J Biol Chem 271:14870–14875
Shen Z, Ding M, Sun J, Deng S, Zhao R, Wang M, Ma X, Wang F, Zhang H, Qian Z, Hu Y, Yu R, Shen X, Chen S (2013) Overexpression of PeHSF mediates leaf ROS homeostasis in transgenic tobacco lines grown under salt stress conditions. Plant Cell Tissue Organ Cult 115:299–308
Soitama AJ, Zhou G, Clarke AK, Oquist G, Gustafsson P, Aro EM (1996) Over-production of the D1:2 protein makes synechococcus cells more tolerant to photoinhibition of photosystem II. Plant Mol Biol 30:467–478
Sun J, Li LS, Liu MQ, Wang MJ, Ding MQ, Deng SR, Lu CF, Zhou XY, Shen X, Zheng XJ, Chen SL (2010) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ Cult 103:205–215
Triolo L, Binazzi A, Cagnetti P, Carconi P, Correnti A, De Luca E, Di Bonito R, Grandoni G, Mastrantonio M, Rosa S, Schimberni M, Uccelli R, Zappa G (2008) Air pollution impact assessment on agro-ecosystem and human health characterization in the area surrounding the industrial settlement of Milazzo: a multidisciplinary approach. Environ Monit Assess 140:191–209
Tseng MJ, Liu CW, Yiu JC (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45:822–833
Xia Z, Sun K, Wang M, Wu K, Zhang H (2012) Overexpression of a maize sulfite oxidase gene in tobacco enhances tolerance to sulfite stress via sulfite oxidation and CAT-mediated H2O2 scavenging. PLoS One 7:e37383
Xia Z, Su X, Liu J, Wang M (2013) The RING-H2 finger gene 1 (RHF1) encodes an E3 ubiquitin ligase and participates in drought stress response in Nicotiana tabacum. Genetica 141:11–21
Xuan N, Jin Y, Zhang H, Xie Y, Liu Y, Wang G (2011) A putative maize zinc-finger protein gene, ZmAN13, participates in abiotic stress response. Plant Cell Tissue Organ Cult 107:101–112
Yang C, Deng W, Tang N, Wang X, Yan F, Lin D, Li Z (2013) Overexpression of ZmAFB2, the maize homologue of AFB2 gene, enhances salt tolerance in transgenic tobacco. Plant Cell Tissue Organ Cult 112:171–179
Yarmolinsky D, Brychkova G, Fluhr R, Sagi M (2013) Sulfite reductase protects plants against sulfite toxicity. Plant Physiol 161:725–743
Acknowledgments
This work was partially financially supported by the National Natural Science Foundation of China (No. 30971548).
Author information
Authors and Affiliations
Corresponding author
Additional information
Xinhong Su, Peng Zhou and Ran Wang have contributed equally to this work
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Su, X., Zhou, P., Wang, R. et al. Overexpression of the maize psbA gene enhances sulfur dioxide tolerance in transgenic tobacco. Plant Cell Tiss Organ Cult 120, 303–311 (2015). https://doi.org/10.1007/s11240-014-0607-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-014-0607-0