biologia plantarum

International journal on Plant Life established by Bohumil Nģmec in 1959

Biologia plantarum 62:579-587, 2018 | DOI: 10.1007/s10535-018-0791-6

Nitrogen metabolism-related enzymes in Mesembryanthemum crystallinum after Botrytis cinerea infection

E. Gajewska1,*, E. Surówka2, A. Kornas3, E. Ku¼niak1
1 Department of Plant Physiology and Biochemistry, Faculty of Biology and Environmental Protection, University of £ód¼, £ód¼, Poland
2 Institute of Plant Physiology, Polish Academy of Sciences, Kraków, Poland
3 Institute of Biology, Pedagogical University, Kraków, Poland

We compared C3 and CAM (crassulacean acid metabolism) states in Mesembryanthemum crystallinum, a facultative CAM species, with respect to the involvement of phosphoenolpyruvate carboxylase (PEPC) and nitrogen metabolismrelated enzymes in plant response to Botrytis cinerea infection. The enzyme activities were monitored both in pathogeninoculated 2nd leaf pair and non-inoculated 3rd leaf pair. The control activities of most studied enzymes were dependent on the mode of photosynthesis. Compared to C3 plants, those performing CAM exhibited higher PEPC, nitrate reductase (NR), and deaminating glutamate dehydrogenase (NAD-GDH) activities but lower glutamine synthetase (GS) and alanine aminotransferase (ALT) activities. Regardless of the mode of photosynthetic carbon assimilation, the plants responded to infection with enhancement of PEPC and inhibition of NR activities in the inoculated leaves. Whereas the activity of GS remained unaffected, those of all glutamate-yielding enzymes, namely ferredoxin-dependent glutamate synthase (Fd-GOGAT), aspartate aminotransferase (AST), ALT, and aminating glutamate dehydrogenase (NADHGDH) were altered after infection. However, the time-course and extent of the observed changes differed in C3 and CAM plants. In general, CAM plants responded to infection with an earlier increase in PEPC and Fd-GOGAT activities as well as later inhibition of NR activity. Contrary to C3 plants, in those performing CAM the activities of PEPC, Fd-GOGAT, NADH-GDH, and AST in the non-inoculated 3rd leaf pair were similarly influenced by infection as in leaves directly inoculated with the pathogen. This implies that the local infection induced an alteration of carbon/nitrogen status in healthy upper leaves. This reprogramming resulting from changes in PEPC and nitrogen metabolism-related enzymes was C3- and CAM-specific.

Keywords: crassulacean acid metabolism; glutamate dehydrogenase; grey mould; ice plant; nitrate reductase; phosphoenolpyruvate carboxylase
Subjects: nitrogen metabolism; CAM; glutamate dehydrogenase; nitrate reductase; PEPC; ice plant; grey mould

Received: November 7, 2016; Revised: October 31, 2017; Accepted: January 12, 2018; Published: September 1, 2018  Show citation

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Gajewska, E., Surówka, E., Kornas, A., & Ku¼niak, E. (2018). Nitrogen metabolism-related enzymes in Mesembryanthemum crystallinum after Botrytis cinerea infection. Biologia plantarum62(3), 579-587. doi: 10.1007/s10535-018-0791-6
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References

  1. Aubry, S., Brown, N.J., Hibberd, J.M.: The role of proteins in C(3) plants prior to their recruitment into the C(4) pathway. - J. exp. Bot. 62: 3049-3059, 2011. Go to original source...
  2. Bilgin, D.D., Zavala, J., Zhu, J., Clough, S.J., Or, D.R., DeLucia, E.H.: Biotic stress globally downregulates photosynthesis genes. - Plant Cell Environ. 33: 1597-1613, 2010. Go to original source...
  3. Bolton, M.D., Thomma, B.P.H.J.: The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. - Physiol. mol. Plant Pathol. 72: 104-110, 2008. Go to original source...
  4. Botrel, A., Kaiser, W.M.: Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. - Planta 201: 496-501, 1997. Go to original source...
  5. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  6. Cebeci, O., Kokturk, B., Ergen, N., Ozturk, L., Cakmak, I., Budak, H.: Differential expression of wheat transcriptomes in response to varying cadmium concentrations. - Biol. Plant. 52: 703-708, 2008. Go to original source...
  7. Champigny, M.L.: Integration of photosynthetic carbon and nitrogen metabolism in higher plants. - Photosynth. Res. 46: 117-127, 1995. Go to original source...
  8. Chang, Y.-M., Liu, W.-Y., Shih, A.C.-C., Shen, M.-N., Lu, C.-H., Lu, M.-Y.J., Yang, H.-W., Wang, T.-Y., Chen, S.C.-C., Chen, S.M., Li, W.-H., Ku, M.S.B.: Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. - Plant Physiol. 160: 165-177, 2012. Go to original source...
  9. Coruzzi, G.M., Zhou, L.: Carbon and nitrogen sensing and signaling in plants: emerging "matrix effects". - Curr. Opin. Plant Biol. 4: 247-253, 2001. Go to original source...
  10. Delgado-Alvarado, A., Walker, R.P., Leegood, R.C.: Phosphoenolpyruvate carboxykinase in developing pea seeds is associated with tissues involved in solute transport and is nitrogen-responsive. - Plant Cell Environ. 30: 225-235, 2007. Go to original source...
  11. Doubnerovį, V., Ry¹lavį, H.: What can enzymes of C4 photosynthesis do for C3 plants under stress? - Plant Sci. 180: 575-583, 2011. Go to original source...
  12. Foyer, C.H., Noctor, G.: Photosynthetic nitrogen assimilation: inter-pathway control and signaling. - In: Foyer, C.H., Noctor, G., (ed.): Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism, Advances in Photosynthesis and Respiration. Pp. 1-22. Kluwer Academic Publishers, Dordrecht 2002. Go to original source...
  13. Gabara, B., Ku¼niak, E., Sk³odowska, M., Surówka, E., Miszalski, Z.: Ultrastructural and metabolic modifications at the plant-pathogen interface in Mesembryanthemum crystallinum leaves infected by Botrytis cinerea. - Environ. exp. Bot. 77: 33-43, 2012. Go to original source...
  14. Gajewska, E., Niewiadomska, E., Tokarz, K., S³aba, M., Sk³odowska, M.: Nickel-induced changes in carbon metabolism in wheat shoots. - J. Plant Physiol. 170: 369-377, 2013. Go to original source...
  15. Gajewska, E., Sk³odowska, M.: Nickel-induced changes in nitrogen metabolism in wheat shoots. - J. Plant Physiol. 166: 1034-1044, 2009. Go to original source...
  16. Gao, S., Liu, K.-T., Chung, T.-W., Chen, F.: The effects of NaCl stress on Jatropha cotyledon growth and nitrogen metabolism. - J. Soil Sci. Plant Nutr. 13: 99-113, 2013. Go to original source...
  17. Gawronska, K., Niewiadomska, E.: Participation of citric acid and isocitric acid in the diurnal cycle of carboxylation and decarboxylation in the common ice plant. - Acta Physiol. Plant. 37: 61 doi:10.1007/s11738-015-1807-x, 2015. Go to original source...
  18. Ku¼niak, E., Gabara, B., Sk³odowska, M., Libik-Konieczny, M., Miszalski, Z.: Effects of NaCl on the response of the halophyte Mesembryanthemum crystallinum callus to Botrytis cinerea infection. - Biol. Plant. 55: 423-430, 2011. Go to original source...
  19. Ku¼niak, E., Ka¼mierczak, A., Wielanek, M., G³owacki, R., Kornas, A.: Involvement of salicylic acid, glutathione and protein S-thiolation in plant cell death-mediated defence response of Mesembryanthemum crystallinum against Botrytis cinerea. - Plant Physiol. Biochem. 63: 30-38, 2013. Go to original source...
  20. Ku¼niak, E., Kornas, A., Gabara, B., Ullrich, C., Sk³odowska, M., Miszalski, Z.: Interaction of Botrytis cinerea with the intermediate C3-CAM plant Mesembryanthemum crystallinum. - Environ. exp. Bot. 69: 137-147, 2010. Go to original source...
  21. Ku¼niak, E., Kornas, A., Ka¼mierczak, A., Rozp±dek, P., Nosek, M., Kocurek, M., Zellnig, G., Müller, M., Miszalski, Z.: Photosynthesis-related characteristics of the midrib and the interveinal lamina in leaves of C3-CAM intermediate plant Mesembryanthemum crystallinum. - Ann. Bot. 117: 1141-1151, 2016. Go to original source...
  22. Lea, P.J., Miflin, B.J.: Glutamate synthase and the synthesis of glutamate in plants. - Plant Physiol. Biochem. 41: 555-564, 2003. Go to original source...
  23. Leegood, R.C., Walker, R.P.: Regulation and roles of phosphoenolpyruvate carboxykinase in plants. - Arch. Biochem. Biophys. 414: 204-210, 2003. Go to original source...
  24. Libik-Konieczny, M., Surówka, E., Ku¼niak, E., Nosek, M., Miszalski, Z.: Photosynthetic metabolism influences the direction of changes in antioxidant system activity in Mesembryanthemum crystallinum leaves inoculated with Botrytis cinerea or Pseudomonas syringae. - J. Plant Physiol. 168: 1052-1059, 2011. Go to original source...
  25. Liu, G., Ji, Y., Bhuiyan, N.H., Pilot, G., Selvaraj, G., Zou, J., Wei, Y.: Amino acid homeostasis modulates salicylic acidassociated redox status and defense responses in Arabidopsis. - Plant Cell 22: 3845-3863, 2010. Go to original source...
  26. Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., Suzuki, A.: Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. - Ann. Bot. 105: 1141-1157, 2010. Go to original source...
  27. Miyashita, Y., Good, A.G.: NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation. - J. exp. Bot. 59: 667-680, 2008. Go to original source...
  28. Müller, C., Scheible, W., Stitt, M., Krapp, A.: Influence of malate and 2-oxoglutarate on the NIA transcript level and nitrate reductase activity in tobacco leaves. - Plant Cell Environ. 24: 191-203, 2001. Go to original source...
  29. Nunes-Nesi, A., Fernie, A.R., Stitt, M.: Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. - Mol. Plant 3: 973-996, 2010. Go to original source...
  30. Rojas, C.M., Senthil-Kumar, M., Tzin, V., Mysore, K.S.: Regulation of primary plant metabolism during plantpathogen interactions and its contribution to plant defense. - Front. Plant Sci. 5: 17. doi:10.3389/fpls.2014.00017, 2014. Go to original source...
  31. Ry¹lavį, H., Müller, K., Semorįdovį, ©., Synkovį, H., Čeųovskį, N.: Photosynthesis and activity of phosphoenolpyruvate carboxylase in Nicotiana tabacum L. leaves infected by Potato virus A and Potato virus Y. - Photosynthetica 41: 357-363, 2003. Go to original source...
  32. Sįnchez, R., Flores, A., Cejudo, F.J.: Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated polypeptides and are differentially expressed in response to drought and salt stress. - Planta 223: 901-909, 2006. Go to original source...
  33. Scharte, J., Schön, H., Weis, E.: Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. - Plant Cell Environ. 28: 1421-1435, 2005. Go to original source...
  34. Schultz, J.C., Appel, H.M., Ferrieri, A.P., Arnold, T.M.: Flexible resource allocation during plant defense responses. Front. Plant Sci. 4: 324, 2013. Go to original source...
  35. Seifi, H.S., Van Bockhaven, J., Angenon, G., Höfte, M.: Glutamate metabolism in plant disease and defense: friend or foe? - Mol. Plant Microbe Interact. 26: 475-485, 2013. Go to original source...
  36. Skopelitis, D.S., Paranychianakis, N.V., Paschalidis, K.A., Pliakonis, E.D., Delis, I.D., Yakoumakis, D.I., Kouvarakis, A., Papadakis, A.K., Stephanou, E.G., Roubelakis- Angelakis, K.A.: Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. - Plant Cell 18: 2767-2781, 2006. Go to original source...
  37. Snoeijers, S.S., Pérez-Garcķa, A., Joosten, M.H.A.J., De Wit, P.J.G.M.: The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. - Eur. J. Plant Pathol. 106: 493-506, 2000. Go to original source...
  38. Song, J.T., Lu, H., McDowell, J.M., Greenberg, J.T.: A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. - Plant J. 40: 200-212, 2004. Go to original source...
  39. Stewart, G.R., Rhodes, D.: Nitrogen metabolism of halophytes. - New Phytol. 80: 307-316, 1978. Go to original source...
  40. Sun, W., Huang, A., Sang, Y., Fu, Y., Yang, Z.: Carbonnitrogen interaction modulates plant growth and expression of metabolic genes in rice. - J. Plant Growth Regul. 32: 575-584, 2013. Go to original source...
  41. Vlot, A.C., Klessig, D.F., Park, S.-W.: Systemic acquired resistance: the elusive signal(s). - Curr. Opin. Plant Biol. 11: 436-442, 2008. Go to original source...
  42. Zeier, J.: New insights into the regulation of plant immunity by amino acid metabolic pathways. - Plant Cell Environ. 36: 2085-2103, 2013. Go to original source...