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Overexpression of the Arabidopsis vacuolar H+-pyrophosphatase AVP1 gene in rice plants improves grain yield under paddy field conditions

Published online by Cambridge University Press:  14 October 2013

Y. S. KIM ,
I. S. KIM ,
Y. H. CHOE ,
M. J. BAE ,
S. Y. SHIN ,
S. K. PARK ,
H. G. KANG ,
Y. H. KIM  and
H. S. YOON
Y. S. KIM
Affiliation:
Department of Biology, Kyungpook National University, Daegu 702-701, South Korea
I. S. KIM*
Affiliation:
Department of Biology, Kyungpook National University, Daegu 702-701, South Korea
Y. H. CHOE
Affiliation:
Department of Biology, Kyungpook National University, Daegu 702-701, South Korea
M. J. BAE
Affiliation:
Department of Biology, Kyungpook National University, Daegu 702-701, South Korea
S. Y. SHIN
Affiliation:
Department of Biology, Kyungpook National University, Daegu 702-701, South Korea
S. K. PARK
Affiliation:
School of Applied Biosciences, Kyungpook National University, Daegu 702-701, South Korea
H. G. KANG
Affiliation:
Subtropical Horticulture Research Institute, Jeju National University, Jeju 690-756, South Korea
Y. H. KIM
Affiliation:
National Institute of Crop Science, Rural Development Administration, Suwon 441-857, South Korea
H. S. YOON*
Affiliation:
Department of Biology, Kyungpook National University, Daegu 702-701, South Korea
*
*To whom all correspondence should be address. Email: [email protected]; [email protected]
*To whom all correspondence should be address. Email: [email protected]; [email protected]
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Summary

The Arabidopsis gene AVP1 encodes a vacuolar H+-translocating inorganic pyrophosphatase (enzyme classification (EC) 3.6.1.1) that functions as an electronic proton pump in the vacuolar membrane and affects growth development and the stress response in plants. The current study was conducted to evaluate the molecular properties of the Arabidopsis thaliana vacuolar H+-pyrophosphatase (AVP1) gene in rice (Oryza sativa L.). Incorporation and expression of the transgene was confirmed by semi-quantitative reverse-transcription polymerase chain reaction (RT-PCR) and quantitative real-time PCR. Expression of the AVP1 gene in transgenic rice plants (TRP1 and TRP2) resulted in a significantly enhanced tolerance to 5·8 g/l NaCl under greenhouse conditions when compared with the control wild-type (WT) rice plants. Augmented AVP1 expression in the transgenic rice plants (TRP) also affected total biomass and improved ion homoeostasis through increased accumulation of Na+ ions in whole tissues when compared with control WT rice plants under high salinity conditions. The photochemical yield (Fv/Fm) values of TRP were higher than those of the WT rice plants, even though the values decreased over time in both the WT and transgenic (TRP1 to TRP8) rice plants. Furthermore, rice grain yield and biomass of the TRP were at least 15% higher based on culm and root weights, and panicle and spikelet numbers when compared with those of the WT rice plants during the 2010 and 2010 growing seasons in South Korea. Thus, these results suggest that ectopic AVP1 expression conferred tolerance and stress resistance to genetically modified transgenic crop plants by improving cellular ion homoeostasis in response to saline conditions, which enhanced rice yield and biomass under natural conditions in paddy fields.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 152 , Issue 6 , December 2014 , pp. 941 - 953
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Ahmad, R., Kim, M. D., Back, K. H., Kim, H. S., Lee, H. S., Kwon, S. Y., Murata, N., Chung, W. I. & Kwak, S. S. (2008). Stress-induced expression of choline oxidase in potato plant chloroplasts confers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Reports 27, 687–698.Google Scholar
Apse, M. P., Aharon, G. S., Snedden, W. A. & Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis . Science 285, 1256–1258.Google Scholar
Apse, M. P., Sottosanto, J. B. & Blumwald, E. (2003). Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant Journal 36, 229–239.Google Scholar
Baisakh, N., RamanaRao, M. V., Rajasekaran, K., Subudhi, P., Janda, J., Galbraith, D., Vanier, C. & Pereira, A. (2012). Enhanced salt stress tolerance of rice plants expressing a vacuolar H+-ATPase subunit c1 (SaVHAc1) gene from the halophyte grass Spartina alterniflora Löisel. Plant Biotechnology Journal 10, 453–464.CrossRefGoogle ScholarPubMed
Bartels, D. & Sunkar, R. (2005). Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23–58.Google Scholar
Bhaskaran, S. & Savithramma, D. L. (2011). Co-expression of Pennisetum glaucum vacuolar Na+/H+ antiporter and Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic tomato. Journal of Experimental Botany 62, 5561–5570.Google Scholar
Christensen, A. H. & Quail, P. H. (1996). Ubiquitin promoter-based vectors for high levels of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Research 5, 213–218.Google Scholar
Ferreira, I. D., do Rosario, V. E. & Cravo, P. V. L. (2006). Real-time quantitative PCR with SYBR Green I detection for estimating copy numbers of nine drug resistance candidate genes in Plasmodium falciparum . Malaria Journal 5, 1. doi: 10.1186/1475-2875-5-1 Google Scholar
Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P., Alper, S. L. & Fink, G. R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1 can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences USA 96, 1480–1485.Google Scholar
Gaxiola, R. A., Li, J., Undurraga, S., Dang, L. M., Allen, G. J., Alper, S. L. & Fink, G. R. (2001). Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proceedings of the National Academy of Sciences USA 98, 11444–11449.Google Scholar
Gaxiola, R. A., Fink, G. R. & Hirschi, K. D. (2002). Genetic manipulation of vacuolar proton pumps and transporters. Plant Physiology 129, 967–973.CrossRefGoogle ScholarPubMed
Gaxiola, R. A., Sanchez, C. A., Paez-Valencia, J., Ayre, B. G. & Elser, J. J. (2012). Genetic manipulation of a ‘vacuolar’ H+-PPase: from salt tolerance to yield enhancement under phosphorus-deficient soils. Plant Physiology 159, 3–11.CrossRefGoogle ScholarPubMed
Gao, F., Gao, Q., Duan, X. G., Yue, G. D., Yang, A. F. & Zhang, J. R. (2006). Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. Journal of Experimental Botany 57, 3259–3270.Google Scholar
Golldack, D. & Dietz, K. J. (2001). Salt-induced expression of the vacuolar H+-ATPase in the common rice plant is developmentally controlled and tissue specific. Plant Physiology 125, 1643–1654.Google Scholar
Hasegawa, P. M., Bressan, R. A., Zhu, J. K. & Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.Google Scholar
Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant Journal 6, 271–282.Google Scholar
Ibrahim, M., Khan, S. A., Zafar, Y., Mansoor, S., Yusuf, A. & Mukhtar, Z. (2009). Expression of a full length Arabidopsis vacuolar H+-Pyrophosphatase (AVP1) gene in tobacco (Nicotiana tabbacum) to increase tolerance to drought and salt stresses. Journal of Phycology 1, 433–440.Google Scholar
Jeong, J. S., Kim, Y. S., Baek, K. H., Jung, H., Ha, S. H., Choi, Y. D., Kim, M. K., Reuzeau, C. & Kim, J. K. (2010). Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiology 153, 185–197.Google Scholar
Kang, H. G., Jeon, J. S., Lee, S. & An, G. (1998). Identification of class B and class C floral organ identity genes from rice plants. Plant Molecular Biology 38, 1021–1029.Google Scholar
Kim, S. R., Lee, S., Kang, H. G., Jeon, J. S., Kim, K. M. & An, G. (2003). A complete sequence of the pGA1611 binary vector. Journal of Plant Biology 46, 211–214.CrossRefGoogle Scholar
Kim, Y. S. & Kim, J. K. (2009). Rice transcription factor AP37 involved in grain yield increase under drought stress. Plant Signaling and Behavior 4, 735–736.Google Scholar
Kim, Y. S., Kim, I. S., Bae, M. J., Choe, Y. H., Kim, Y. H., Park, H. M., Kang, H. G. & Yoon, H. S. (2013). Homologous expression of cytosolic dehydroascorbate reductase increases grain yield and biomass under paddy field conditions in transgenic rice (Oryza sativa L. japonica). Planta 237, 1613–1625.Google Scholar
Klimyuk, V. I., Carroll, B. J., Thomas, C. M. & Jones, J. D. G. (1993). Alkali treatment for rapid preparation of plant material for reliable PCR analysis. Plant Journal 3, 493–494.Google Scholar
Lee, Y. P., Kim, S. H., Bang, J. W., Lee, H. S., Kwak, S. S. & Kwon, S. Y. (2007). Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. Plant Cell Reports 26, 591–598.Google Scholar
Leigh, R. A. (1997). Solute composition of vacuoles. Advances in Botanical Research 25, 171–194.Google Scholar
Li, J., Yang, H., Peer, W. A., Richter, G., Blakeslee, J., Bandyopadhyay, A., Titapiwantakun, B., Undurraga, S., Khodakovskaya, M., Richards, E. L., Krizek, B., Murphy, A. S., Gilroy, S. & Gaxiola, R. (2005). Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310, 121–125.Google Scholar
Li, Z., Baldwin, C. M., Hu, Q., Liu, H. & Luo, H. (2010). Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant Cell and Environment 33, 272–289.Google Scholar
Liu, H., Tang, R., Zhang, Y., Wang, C., Lv, Q., Gao, X., Li, W. & Zhang, H. (2010). AtNHX3 is a vacuolar K+/H+ antiporter required for low-potassium tolerance in Arabidopsis thaliana . Plant Cell and Environment 33, 1989–1999.Google Scholar
Lv, S., Zhang, K., Gao, Q., Lian, L., Song, Y. & Zhang, J. R. (2008). Overexpression of an H+-PPase from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant and Cell Physiology 49, 1150–1164.CrossRefGoogle ScholarPubMed
Maeshima, M. (2000). Vacuolar H+-pyrophosphatase. Biochimica et Biophysica Acta 1465, 37–51.Google Scholar
McElroy, D. & Brettell, R. I. S. (1994). Foreign gene expression in transgenic cereals. Trends in Biotechnology 12, 62–68.Google Scholar
McElroy, D., Zhang, W., Cao, J. & Wu, R. (1990). Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2, 163–171.Google Scholar
Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.Google Scholar
Nagai, T. & Makino, A. (2009). Differences between rice and wheat in temperature responses of photosynthesis and plant growth. Plant and Cell Physiology 50, 744–755.Google Scholar
Oh, S. J., Song, S. I., Kim, Y. S., Jang, H. J., Kim, S. Y., Kim, M., Kim, Y. K., Nahm, B. H. & Kim, J. K. (2005). Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiology 138, 341–351.Google Scholar
Oh, S. J., Kim, Y. S., Kwon, C. W., Park, H. K., Jeong, J. S. & Kim, J. K. (2009). Overexpression of transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiology 150, 1368–1379.CrossRefGoogle ScholarPubMed
Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A., Tanaka, A., Nakamura, T. & Hayakawa, T. (2002). Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Letters 532, 279–282.Google Scholar
Park, S., Li, J., Pittman, J. K., Berkowitz, G. A., Yang, H., Undurraga, S., Morris, J., Hirschi, K. D. & Gaxiola, R. A. (2005). Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proceedings of the National Academy of Sciences USA 102, 18830–18835.Google Scholar
Pasapula, V., Shen, G., Kuppu, S., Paez-Valencia, J., Mendoza, M., Hou, P., Chen, J., Qiu, X., Zhu, L., Zhang, X., Auld, D., Blumwald, E., Zhang, H., Gaxiola, R. & Payton, P. (2011). Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fiber yield in the field conditions. Plant Biotechnology Journal 9, 88–99.Google Scholar
Peng, S., Huang, J., Sheehy, J. E., Laza, R. C., Visperas, R. M., Zhong, X., Centeno, G. S., Khush, G. S. & Cassman, K. G. (2004). Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences USA 101, 9971–9975.Google Scholar
Pinheiro, H. A., Damatta, F. M., Chaves, A. R. M., Loureiro, M. E. & Ducatti, C. (2005). Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora . Annals of Botany 96, 101–108.CrossRefGoogle ScholarPubMed
Schumacher, K., Vafeados, D., Mccarthy, M., Sze, H., Wilkins, T. & Chory, J. (1999). The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development. Genes and Development 13, 3259–3270.Google Scholar
Sharp, R. E., Poroyko, V., Hejlek, L. G., Spollen, W. G., Springer, G. K., Bohnert, H. J. & Nguyen, H. T. (2004). Root growth maintenance during water deficits: physiology to functional genomics. Journal of Experimental Botany 55, 2343–2351.Google Scholar
Shi, H. Z., Lee, B. H., Wu, S. J. & Zhu, J. K. (2003). Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana . Nature Biotechnology 21, 81–85.Google Scholar
Singh, S. (2001). Growth, yield and biochemical response of rice genotypes to low light and high temperature-humidity stress. Oryza 37, 35–38.Google Scholar
Takeda, S. & Matsuoka, M. (2008). Genetic approaches to crop improvement: responding to environmental and population changes. Nature Reviews Genetics 9, 444–457.CrossRefGoogle ScholarPubMed
Tang, L., Kim, M. D., Yang, K. S., Kwon, S. Y., Kim, S. H., Kim, J. S., Yun, D. J., Kwak, S. S. & Lee, H. S. (2008). Enhanced tolerance of transgenic potato plants overexpressing nucleoside diphosphate kinase 2 against multiple environmental stresses. Transgenic Research 17, 705–715.Google Scholar
Verslues, P. E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J. & Zhu, J. K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant Journal 45, 523–539.Google Scholar
Wang, B., Lüttge, U. & Ratajczak, R. (2001). Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa . Journal of Experimental Botany 52, 2355–2365.Google Scholar
Yang, H., Knapp, J., Koirala, P., Rajagopal, D., Peer, W. A., Silbart, L. K., Murphy, A. & Gaxiola, R. A. (2007). Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type I H+-pyrophosphatase. Plant Biotechnology Journal 5, 735–745.Google Scholar
Zhao, F. Y., Zhang, X. J., Li, P. H., Zhao, Y. X. & Zhang, H. (2006). Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1 . Molecular Breeding 17, 341–353.Google Scholar
Zhang, J., Li, J., Wang, X. & Chen, J. (2011). OVP1, a vacuolar H+-translocating inorganic pyrophosphatase (V-PPase), overexpression improved rice cold tolerance. Plant Physiology and Biochemistry 49, 33–38.Google Scholar
Zhen, R. G., Kim, E. J. & Rea, P. A. (1994). Localization of cytosolically oriented maleimide-reactive domain of vacuolar H+-pyrophosphatase. Journal of Biological Chemistry 269, 23342–23350.Google Scholar
Zhen, R. G., Kim, E. J. & Rea, P. A. (1997). The molecular and biochemical basis of pyrophosphate-energized proton translocation at the vacuolar membrane. Advances in Botanical Research 25, 297–337.Google Scholar
Zhu, J. K. (2001). Plant salt tolerance. Trends in Plant Science 6, 66–71.Google Scholar