The effects of K+-deficiency on H2O2 dynamics and sucrose in tomato

https://doi.org/10.17221/103/2020-HORTSCICitation:

Zhao X.M., Zhang N., Liu X., Jiang J. (2021): The effects of K+-deficiency on H2O2 dynamics and sucrose in tomato. Hort. Sci. (Prague), 48: 90–97.

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Potassium (K+) deficiency inhibits the transport of photosynthetic products and causes severe crop yield losses. However, the underlying mechanisms are poorly understood. In this study, we used two tomato lines 081018 (K+-deficiency-sensitive) and 081034 (K+-deficiency-tolerant), showing tolerance to K+ deficiency to investigate the relationship between the H2O2 and sucrose in the tomato under K+-deficiency. The H2O2 accumulation was increased by the low K+ condition (0.5 mM) after 8 h in 081018. The enzymes related to the metabolism of H2O2 were decreased, and more malondialdehyde (MDA) was produced. After 24 h, the sucrose content had accumulated significantly in the leaves, however, it was deficient in the roots, and the expression level of the sucrose transporters (SUT1) was inhibited. In 081034, the activity of antioxidant enzymes was increased under K+-deficiency, and then the H2O2 subsequently returned to the control treatment (4 mM) levels and did not produce more MDA. The sucrose content was not significantly different from the control treatment after 24 h. The expression of SUT1 was not suppressed. These results suggested that the H2O2 dynamics played different roles in the two different strains. The transportation of sucrose was suppressed by the H2O2 from the leaf (source) to the root (sink) in 081018, and unrestricted by the advantageous reactive oxygen species dynamics capacity in 081034.

References:
Apel K., Hirt H. (2004): Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55: 373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
 
Cakmak I., Hengeler C., Marschner H. (1994a): Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. Journal of Experimental Botany, 45: 1245–1250. https://doi.org/10.1093/jxb/45.9.1245
 
Cakmak I., Hengeler C., Marschner H. (1994b): Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. Journal of Experimental Botany, 45: 1251–1257. https://doi.org/10.1093/jxb/45.9.1251
 
Chérel I., Lefoulon C., Boeglin M., Sentenac H. (2014): Molecular mechanisms involved in plant adaptation to low K+ availability. Journal of Experimental Botany, 65: 833–848. https://doi.org/10.1093/jxb/ert402
 
Couée I., Sulmon C., Gouesbet G., El Amrani (2006): Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. Journal of Experimental Botany, 57: 449–459. https://doi.org/10.1093/jxb/erj027
 
Gerardeaux E., Jordan-Meille L., Constantin J., Pellerin S., Dingkuhn M. (2010): Changes in plant morphology and dry matter partitioning caused by potassium deficiency in Gossypium hirsutum (L.). Environmental and Experimental Botany, 67: 451–459. https://doi.org/10.1016/j.envexpbot.2009.09.008
 
Hackel A., Schauer N., Carrari F., Fernie A., Grimm B., Kühn C. (2006): Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant Journal, 45:180–192. https://doi.org/10.1111/j.1365-313X.2005.02572.x
 
Hafsi C., Debez A., Abdelly C. (2014): Potassium deficiency in plants: effects and signaling cascades. Acta Physiologiae Plantarum, 36: 1055–1070. https://doi.org/10.1007/s11738-014-1491-2
 
Ho C., Tsay Y. (2010): Nitrate, ammonium, and potassium sensing and signaling. Current Opinion in Plant Biology, 13: 604–610. https://doi.org/10.1016/j.pbi.2010.08.005
 
Hu W., Yang J., Meng Y., Wang Y., Chen B., Zhao W., Oosterhuis D., Zhou Z. (2015): Potassium application affects carbohydrate metabolism in the leaf subtending the cotton (Gossypium hirsutum L.) boll and its relationship with boll biomass. Field Crop Research, 179: 120–131. https://doi.org/10.1016/j.fcr.2015.04.017
 
Huber S. (1984): Biochemical basis for effects of K-deficiency on assimilate export rate and accumulation of soluble sugars in soybean leaves. Plant Physiology, 76: 424–430. https://doi.org/10.1104/pp.76.2.424
 
Huber S., Israel D. (1982): Biochemical basis for partitioning of photosynthetically fixed carbon between starch and sucrose in soybean (Glycine max Merr.) leaves. Plant Physiology, 69: 691–696. https://doi.org/10.1104/pp.69.3.691
 
Lemoine R. (2000): Sucrose transporters in plants: update on function and structure. Biochimica et Biophysica Acta –Biomembranes, 1465: 246–262. https://doi.org/10.1016/S0005-2736(00)00142-5
 
Moustakas M., Sperdouli I., Kouna T., Antonopoulou C., Therios I. (2011): Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regulation, 65: 315–322. https://doi.org/10.1007/s10725-011-9604-z
 
Neill S., Desikan R., Hancock J. (2002): Hydrogen peroxide signalling. Current Opinion in Plant Biology, 5: 388–395. https://doi.org/10.1016/S1369-5266(02)00282-0
 
Osorio S., Ruan Y., Fernie A. (2014): An update on source-to-sink carbon partitioning in tomato. Frontiers in Plant Science, 5: 516.  https://doi.org/10.3389/fpls.2014.00516
 
Patterson B., Macrae E., Ferguson I. (1984): Estimation of hydrogen peroxide in plant extracts using titanium (iv). Analytical Biochemistry, 139: 487–492. https://doi.org/10.1016/0003-2697(84)90039-3
 
Quan L., Zhang B., Shi W., Li H. (2008): Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrative Plant Biology, 1: 2–18. https://doi.org/10.1111/j.1744-7909.2007.00599.x
 
Schmitt B., Stadler R., Sauer N. (2008): Immunolocalization of solanaceous SUT1 proteins in companion cells and xylem parenchyma: new perspectives for phloem loading and transport. Plant Physiology, 148: 187–199. https://doi.org/10.1104/pp.108.120410
 
Suzuki N., Koussevitzky S., Mittler R., Miller G. (2012): ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment, 35: 259–270.
 
Wang N., Hua H., Eneji A. (2012): Genotypic variations in photosynthetic and physiological adjustment to potassium deficiency in cotton (Gossypium hirsutum). Journal of Photochemistry and Photobiology Biology, 110: 1–8. https://doi.org/10.1016/j.jphotobiol.2012.02.002
 
Wang Y., Wu W. (2010): Plant sensing and signalling in response to K+-deficiency. Molecular Plant, 3: 280–287. https://doi.org/10.1093/mp/ssq006
 
Zhao X., Jiang J., Zhang Y. (2011): Different tomato strains growth and development affected by K+-deficiency stress. Jiangsu Agricultural Sciences, 39: 219–223. (in Chinese)
 
Zhao X., Liu Y., Liu X., Jiang J. (2018): Comparative transcriptome profiling of two tomato genotypes in response to potassium-deficiency stress. International Journal of Molecular Sciences, 19: 2402. https://doi.org/10.3390/ijms19082402
 
Apel K., Hirt H. (2004): Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55: 373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
 
Cakmak I., Hengeler C., Marschner H. (1994a): Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. Journal of Experimental Botany, 45: 1245–1250. https://doi.org/10.1093/jxb/45.9.1245
 
Cakmak I., Hengeler C., Marschner H. (1994b): Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. Journal of Experimental Botany, 45: 1251–1257. https://doi.org/10.1093/jxb/45.9.1251
 
Chérel I., Lefoulon C., Boeglin M., Sentenac H. (2014): Molecular mechanisms involved in plant adaptation to low K+ availability. Journal of Experimental Botany, 65: 833–848. https://doi.org/10.1093/jxb/ert402
 
Couée I., Sulmon C., Gouesbet G., El Amrani (2006): Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. Journal of Experimental Botany, 57: 449–459. https://doi.org/10.1093/jxb/erj027
 
Gerardeaux E., Jordan-Meille L., Constantin J., Pellerin S., Dingkuhn M. (2010): Changes in plant morphology and dry matter partitioning caused by potassium deficiency in Gossypium hirsutum (L.). Environmental and Experimental Botany, 67: 451–459. https://doi.org/10.1016/j.envexpbot.2009.09.008
 
Hackel A., Schauer N., Carrari F., Fernie A., Grimm B., Kühn C. (2006): Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant Journal, 45:180–192. https://doi.org/10.1111/j.1365-313X.2005.02572.x
 
Hafsi C., Debez A., Abdelly C. (2014): Potassium deficiency in plants: effects and signaling cascades. Acta Physiologiae Plantarum, 36: 1055–1070. https://doi.org/10.1007/s11738-014-1491-2
 
Ho C., Tsay Y. (2010): Nitrate, ammonium, and potassium sensing and signaling. Current Opinion in Plant Biology, 13: 604–610. https://doi.org/10.1016/j.pbi.2010.08.005
 
Hu W., Yang J., Meng Y., Wang Y., Chen B., Zhao W., Oosterhuis D., Zhou Z. (2015): Potassium application affects carbohydrate metabolism in the leaf subtending the cotton (Gossypium hirsutum L.) boll and its relationship with boll biomass. Field Crop Research, 179: 120–131. https://doi.org/10.1016/j.fcr.2015.04.017
 
Huber S. (1984): Biochemical basis for effects of K-deficiency on assimilate export rate and accumulation of soluble sugars in soybean leaves. Plant Physiology, 76: 424–430. https://doi.org/10.1104/pp.76.2.424
 
Huber S., Israel D. (1982): Biochemical basis for partitioning of photosynthetically fixed carbon between starch and sucrose in soybean (Glycine max Merr.) leaves. Plant Physiology, 69: 691–696. https://doi.org/10.1104/pp.69.3.691
 
Lemoine R. (2000): Sucrose transporters in plants: update on function and structure. Biochimica et Biophysica Acta –Biomembranes, 1465: 246–262. https://doi.org/10.1016/S0005-2736(00)00142-5
 
Moustakas M., Sperdouli I., Kouna T., Antonopoulou C., Therios I. (2011): Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regulation, 65: 315–322. https://doi.org/10.1007/s10725-011-9604-z
 
Neill S., Desikan R., Hancock J. (2002): Hydrogen peroxide signalling. Current Opinion in Plant Biology, 5: 388–395. https://doi.org/10.1016/S1369-5266(02)00282-0
 
Osorio S., Ruan Y., Fernie A. (2014): An update on source-to-sink carbon partitioning in tomato. Frontiers in Plant Science, 5: 516.  https://doi.org/10.3389/fpls.2014.00516
 
Patterson B., Macrae E., Ferguson I. (1984): Estimation of hydrogen peroxide in plant extracts using titanium (iv). Analytical Biochemistry, 139: 487–492. https://doi.org/10.1016/0003-2697(84)90039-3
 
Quan L., Zhang B., Shi W., Li H. (2008): Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrative Plant Biology, 1: 2–18. https://doi.org/10.1111/j.1744-7909.2007.00599.x
 
Schmitt B., Stadler R., Sauer N. (2008): Immunolocalization of solanaceous SUT1 proteins in companion cells and xylem parenchyma: new perspectives for phloem loading and transport. Plant Physiology, 148: 187–199. https://doi.org/10.1104/pp.108.120410
 
Suzuki N., Koussevitzky S., Mittler R., Miller G. (2012): ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment, 35: 259–270.
 
Wang N., Hua H., Eneji A. (2012): Genotypic variations in photosynthetic and physiological adjustment to potassium deficiency in cotton (Gossypium hirsutum). Journal of Photochemistry and Photobiology Biology, 110: 1–8. https://doi.org/10.1016/j.jphotobiol.2012.02.002
 
Wang Y., Wu W. (2010): Plant sensing and signalling in response to K+-deficiency. Molecular Plant, 3: 280–287. https://doi.org/10.1093/mp/ssq006
 
Zhao X., Jiang J., Zhang Y. (2011): Different tomato strains growth and development affected by K+-deficiency stress. Jiangsu Agricultural Sciences, 39: 219–223. (in Chinese)
 
Zhao X., Liu Y., Liu X., Jiang J. (2018): Comparative transcriptome profiling of two tomato genotypes in response to potassium-deficiency stress. International Journal of Molecular Sciences, 19: 2402. https://doi.org/10.3390/ijms19082402
 
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