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Distinctive Potassium-Accumulation Capability of Alligatorweed (Alternanthera philoxeroides) Links to High-Affinity Potassium Transport Facilitated by K+-Uptake Systems

Published online by Cambridge University Press:  20 January 2017

Zhi-zhong Song
Affiliation:
State Key Laboratory of Soil and Sustainable Agriculture (Institute of Soil Science, Chinese Academy of Sciences), Nanjing 210008, China
Yan-hua Su*
Affiliation:
State Key Laboratory of Soil and Sustainable Agriculture (Institute of Soil Science, Chinese Academy of Sciences), Nanjing 210008, China
*
Corresponding author's E-mail: yhsu@issas.ac.cn

Abstract

Alligatorweed is well known for its potassium (K+)-accumulating capabilities and its strong resistance to undesired growth conditions. The results of this study revealed properties of K+ accumulation and its contribution to drought stress in alligatorweed. In addition, we attempted to characterize the molecular mechanisms of K+ accumulation in this plant. Alligatorweed plants showed a consistent increase in biomass in response to external K+ concentrations, ranging from micromolar levels up to 50 mmol L−1; K+ was also accumulated accordingly in the plants. The stem was the most K+-accumulating organ, accumulating up to 13% of the K+. Moreover, this K+ superaccumulation caused improved resistance to drought stress. The apparent K+ uptake by the roots showed a typical high-affinity property, and the Michaelis constant increased at higher rates of plant K+ in the starting materials. Furthermore, three putative, K+-uptake transporter complementary DNAs (cDNAs) were isolated from alligatorweed (ApKUP1, ApKUP2, and ApKUP3, respectively) using degenerated primers and rapid amplification of cDNA end techniques. The expression of ApKUP1 and ApKUP3 was predominately localized to the leaves, whereas ApKUP2 was expressed throughout the entire plant. The expression of ApKUP1 and ApKUP3 was stimulated in the stems and roots when K+ was depleted from the external medium. Moreover, ApKUP3 expression was enhanced in the stem in response to abscisic acid treatment and drought stress. In conclusion, our findings provide further insight into the mechanisms of K+ accumulation linked to K+ uptake in alligatorweed.

Type
Physiology, Chemistry, and Biochemistry
Copyright
Copyright © Weed Science Society of America 

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Footnotes

current address: 71, East Beijing Rd. Nanjing 210008 China.

References

Literature Cited

Becker, D., Hoth, S., Ache, P., Wenkel, S., Roelfsema, M.R.G., Meyerhoff, O., Hartung, W., and Hedrich, R. 2003. Regulation of the ABA-sensitive Arabidopsis potassium channel gene GORK in response to water stress. FEBS Lett. 554:119126.Google Scholar
Benlloch-González, M., Arquero, O., Fournier, J. M., Barranco, D., and Benlloch, M. 2008. K+ starvation inhibits water-stress-induced stomatal closure. Plant Physiol. 165:623630.Google Scholar
Davies, C., Shin, R., Liu, W., Thomas, M. R., and Schachtman, D. P. 2006. Transporters expressed during grape berry (Vitis vinifera L.) development are associated with an increase in berry size and berry potassium accumulation. J. Exp. Bot. 57:32093216.Google Scholar
Desbrosses, G., Kopka, C., Ott, T., and Udvardi, M. K. 2004. Lotus japonicus LjKUP is induced late during nodule development and encodes a potassium transporter of the plasma membrane. Mol. Plant Microbe Interact. 17:789797.Google Scholar
Epstein, E., Rains, D. W., and Elzam, O. E. 1963. Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. U. S. A. 49:684692.Google Scholar
Fernando, M., Kulpa, J., Siddiqi, M. Y., and Glass, A. D. M. 1990. Potassium-dependent changes in the expression of membrane-associated proteins in barley roots, I: correlations with K+ (86Rb+) influx and root K+ concentration. Plant Physiol. 92:11281132.Google Scholar
Fu, H. H. and Luan, S. 1998. AtKUP1: a dual-affinity K+ transporter from Arabidopsis . Plant Cell 10:6373.Google Scholar
Garciadeblas, B., Benito, B., and Rodriguez-Navarro, A. 2002. Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa . Plant Mol. Biol. 50:623633.Google Scholar
Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thibaud, J. B., and Sentenac, H. 1998. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647655.Google Scholar
Gierth, M. and Mäser, P. 2007. Potassium transporters in plants—involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett. 581:23482356.Google Scholar
Glass, A.D.M. 1976. Regulation of potassium absorption in barley roots: an allosteric model. Plant Physiol. 58:3337.Google Scholar
Glass, A.D.M. 1983. The regulation of ion transport. Annu. Rev. Plant Physiol. 34:311326.Google Scholar
Hirsch, R. E., Lewis, B. D., Spalding, E. P., and Susaman, M. R. 1998. A role for the AKT1 potassium channel in plant nutrition. Science 280:918921.Google Scholar
Kochian, L. V. and Lucas, W. J. 1988. Potassium transport in roots. Pages 93178 in Callow, J. A., ed. Advances in Botanical Research, Vol 15. London, UK Academic.Google Scholar
Lebaudy, A., Véry, A. A., and Sentenac, H. 2007. K+ channel activity in plants: genes, regulations and functions. FEBS Lett. 581:23572366.Google Scholar
Li, M., Li, Y., Li, H., and Wu, G. 2011. Overexpression of AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. Tree Physiol. 31:349357.Google Scholar
Lu, R. K. 2000. Analytical Methods of Soil and Agricultural Chemistry. Beijing China Agricultural Science and Technology. Pp. 191196. [in Chinese].Google Scholar
Maathuis, F.J.M. and Amtmann, N. 1999. K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann. Bot. (Lond.) 84:123133.Google Scholar
Maathuis, F.J.M. and Sanders, D. 1996. Mechanisms of potassium absorption by higher plant roots. Physiol. Plant 96:158168.Google Scholar
Martinez-Cordero, M. A., Vicente, M., and Francisco, R. 2004. Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper. Plant Mol. Biol. 56:413421.Google Scholar
Mäser, P., Thomine, S., Schroeder, J. I., Ward, J. M., Hirschi, K., Sze, H., Talke, I. N., Amtmann, A., Maathuis, F.J.M., Sanders, D., Harper, J. F., Tchieu, J., Gribskov, M., Persans, M. W., Salt, D. E., Kim, S. A., and Guerinot, M. L. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis . Plant Physiol. 126:16461667.Google Scholar
Mian, A., Oomen, R. J., Isayenkov, S., Sentenac, H., Maathuis, F. J., and Véry, A. A. 2011. Over-expression of an Na+-and K+-permeable HKT transporter in barley improves salt tolerance. Plant J. 68:468479.Google Scholar
Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15:473497.Google Scholar
Nieves-Cordones, M., Martinez-Cordero, M. A., Martinez, V., and Rubio, F. 2007. An NH4 +-sensitive component dominates high-affinity K+ uptake in tomato plants. Plant Science 172:273280.Google Scholar
Peng, K. Q. and Hu, D. D. 1986. A kinetic study of potassium uptake by Alternanthera philoxeroides (Mart.) Griseb. Acta Phytophysiol. Sin. 12:187193. [in Chinese].Google Scholar
Rai, R. K., Singh, P., Shrivastava, A. K., and Suman, A. 2008. Modulation of low-temperature-induced biochemical changes in bud and root band zones of sugar cane sets by potassium, zinc, and Ethrel for improving sprouting. J. Agric. Food Chem. 56:1197611982.Google Scholar
Rubio, F., Santa-Maria, G. E., and Rodriguez-Navarro, A. 2000. Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol. Plant 109:3443.Google Scholar
Sambrook, J. and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual, Vol. 1, 3rd ed. Cold Spring Harbor, NY Cold Spring Harbor Laboratory.Google Scholar
Santa-Maria, G. E., Rubio, F., Dubcovsky, J., and Rodriguez-Navarro, A. 1997. The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:22812289.Google Scholar
Su, H., Golldack, D., Zhao, C. S., and Bohnert, H. J. 2002. The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol. 129:14821493.Google Scholar
Tiwari, H. S., Agarwal, R. M., and Bhatt, R. K. 1998. Photosynthesis, stomatal resistance and related characteristics as influenced by-potassium under normal water supply and water stress conditions in rice (Oryza sativa L.) Indian J. Plant Physiol 3:314316.Google Scholar
Vallejo, A. J., Peralta, M. L., and Santa-Maria, G. E. 2005. Expression of potassium-transporter coding genes, and kinetics of rubidium uptake, along a longitudinal root axis. Plant Cell Environ. 28:850862.Google Scholar
Véry, A. A. and Sentenac, H. 2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 54:575603.Google Scholar
Wang, Y. H., Garvin, D. F., and Kochian, L. V. 2002. Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol. 130:13611370.Google Scholar
Ward, J. M., Mäser, P., and Schroeder, J. I. 2009. Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71:5982.Google Scholar
Wolf, T., Heidelmann, T., and Marten, I. 2006. ABA regulation of K-permeable channels in maize subsidiary cells. Plant. Cell. Physiol. 47:13721380.Google Scholar
Xie, S. P. and Ni, J. S. 1987. A study of potassium absorption and compartmentation in roots of Alternanthera philoxeroides (Mart.) Griseb in comparison with soybean and sunflower seedlings. Acta Phytophysiol. Sin. 13:410417. [in Chinese].Google Scholar