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The relationship between resistance to tobacco brown spot and nitrogen metabolism in mature tobacco (Nicotiana tabacum) plants

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Abstract

Differences in nitrogen metabolism were analyzed in mature leaves of three tobacco cultivars with different levels of resistance to brown spot disease (Alternaria alternata) including one resistant (JYH) and two susceptible cultivars (NC89 and CBH). The results were as follows: All three cultivars had low levels of both total nitrogen and leaf tissue NH4 +; the activity of glutamine synthetase (GS) declined sharply in all cultivars, but that of JYH was significantly higher than that of NC89 and CBH; levels of NAD(H)-glutamate dehydrogenase (NAD(H)-GDH) activity in JYH increased until 75 days after germination, and then decreased. In contrast, NAD(H)-GDH activities in NC89 and CBH increased gradually at maturity; apoplastic NH4 + concentrations in the three cultivars gradually increased, but their apoplastic pHs and NH3 compensation points decreased, and these apoplastic parameters were significantly higher in NC89 and CBH than in JYH. These results indicated that the nitrogen metabolism in mature leaves differed remarkably among tobacco cultivars with different levels of resistance to brown spot disease. The resistant cultivar has a greater capacity to re-use nitrogen, while the susceptible cultivar loses more nitrogen via ammonia volatilization, which plays an important role in the initiation of tobacco brown spot. Our data suggest that the characteristics of leaf nitrogen metabolism of tobacco cultivars affect the level of resistance to tobacco brown spot.

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References

  • Agrios GN (1997) Plant pathology, 4th edn. Academic, San Diego

    Google Scholar 

  • Atkins PW (1990) Physical chemistry, 4th edn. Oxford University Press, Oxford

    Google Scholar 

  • Barbottin A, Lecomteb C, Bouchardc C, Jeuffroy MH (2005) Nitrogen remobilization during grain filling in wheat. Crop Sci 45:1141

    Article  Google Scholar 

  • Chen MX, Huang JL, Cui KH, Nie LX, Farooq S (2009) Genotypic variations and terms of NH3 volatilization in four rice (Oryza sativa L.) cultivars. Asian J Plant Sci 8:353–360

    Article  CAS  Google Scholar 

  • Cren M, Hirel B (1999) Glutamine synthetase in higher plants. Regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol 40:1187–1193

    Article  CAS  Google Scholar 

  • Duan WJ, Zhang XQ, Yang TZ, Dou XW, Chen TG, Li SJ, Jiang SJ, Huang YJ, Yin QY (2010) A novel role of ammonia in appressorium formation of Alternaria alternata (Fries) Keissler, a tobacco pathogenic fungus. J Plant Dis Protect 117:112–116

    Google Scholar 

  • Duan WJ, Yang TZ, Dai Y, Li DL, Zhang XQ, Liu HB, Li N, Wang CG (2012a) Stomatal NH3 compensation point and its metabolic regulation in senescence phenotypes of Nicotiana tabacum. Biol Plant 56:771–774

    Article  CAS  Google Scholar 

  • Duan WJ, Da Y, Yang TZ, Li DL, Li N, Wang CG (2012b) Ammonia-related metabolism of tobacco varieties differing in their susceptibility to Alternaria alternata. Russ J Plant Physiol 59:805–810

    Article  CAS  Google Scholar 

  • Dubois F, Brugière N, Sangwan RS, Hirel B (1996) Localization of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts shows organ- and cell-specific patterns of protein synthesis and gene expression. Plant Mol Biol 31:803–817

    Article  CAS  PubMed  Google Scholar 

  • Herrmann B, Mattsson M, Jones SK, Cellier P, Milford C, Sutton MA, Schjoerring JK, Neftel A, Road WM, Environmental N (2009) Vertical structure and diurnal variability of ammonia exchange potential within an intensively managed grass canopy. Biogeosciences 6:15–23

    Article  CAS  Google Scholar 

  • Hoffland E, Jeger MJ, Van Beusichem ML (2000) Effect of nitrogen supply rate on disease resistance in tomato depends on the pathogen. Plant Soil 218:239–247

    Article  CAS  Google Scholar 

  • Horneck D, Miller R (1998) Determination of total nitrogen in plant tissue. In: Karla Y (ed) Handbook of reference methods for plant analysis. CRC Press, Boca Raton

    Google Scholar 

  • Huber D, Watson R (1974) Nitrogen form and plant disease. Annu Rev Phytopathol 12:139–165

    Article  CAS  PubMed  Google Scholar 

  • Husted S, Schjoerring JK (1995) Apoplastic pH and ammonium concentration in leaves of Brassica napus L. Plant Physiol 109:1453–1460

    PubMed Central  CAS  PubMed  Google Scholar 

  • Husted S, Schjoerring JK (1996) Ammonia flux between oilseed rape plants and the atmosphere in response to changes in leaf temperature, light intensity and air humidity. Plant Physiol 112:67–74

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jin X, Zhao ZX, Li ZH, Chen RP, Xu TY, Xie YP, Xu L, Ou YJ, Xu FH (2008) Study on the relationship between the content of nitrogen and some biophysiological substances at topping and the occurrence of brown spot of tobacco applied with different amount of nitrogen. J Plant Nutr Fertil 14:940–946

    CAS  Google Scholar 

  • Kichey T, Heumez E, Pocholle D, Pageau K, Vanacker H, Dubois F, Le Gouis J, Hirel B (2006) Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytol 169:265–278

    Article  CAS  PubMed  Google Scholar 

  • Kramer-Haimovich H, Servi E, Katan T, Rollins J, Okon Y, Prusky D (2006) Effect of ammonia production by Colletotrichum gloeosporioides on pelB activation, pectate lyase secretion, and fruit pathogenicity. Appl Environ Microbiol 72:1034–1039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kumagai E, Araki T, Hamaoka N, Ueno O (2011) Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Ann Bot 108:1381–1386

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leleu O, Vuylsteker C (2004) Unusual regulatory nitrate reductase activity in cotyledons of Brassica napus seedlings: enhancement of nitrate reductase activity by ammonium supply. J Exp Bot 55:815–823

    Article  CAS  PubMed  Google Scholar 

  • Lloyd H (1972) Therapeutic effect of kinetin on tobacco alternariosis. Nature 240:94–96

    Article  CAS  Google Scholar 

  • Loubet B, Milford C, Hill PW, Tang YS, Cellier P, Sutton MA (2002) Seasonal variability of apoplastic NH4 + and pH in an intensively managed grassland. Plant Soil 238:97–110

    Article  CAS  Google Scholar 

  • Lucas GB (1975) Diseases of tobacco, 3rd edn. Biological Consulting Associates, Raleigh

    Google Scholar 

  • Masclaux-Daubresse C, Reisdorf-Cren M, Pageau K, Lelandais M, Grandjean O, Kronenberger J, Valadier MH, Feraud M, Jouglet T, Suzuki A (2006) Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol 140:444–456

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Massad RS, Loubet B, Tuzet A, Cellier P (2008) Relationship between ammonia stomatal compensation point and nitrogen metabolism in arable crops: current status of knowledge and potential modelling approaches. Environ Pollut 154:390–403

    Article  CAS  PubMed  Google Scholar 

  • Mattsson M, Hausler RE, Leegood RC, Lea PJ, Schjoerring JK (1997) Leaf atmosphere NH3 exchange in barley mutants with reduced activities of glutamine synthetase. Plant Physiol 114:1307–1312

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miflin BJ, Habash DZ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 370:979–987

    Article  Google Scholar 

  • Olea F, Pérez-García A, Cantón FR, Rivera ME, Cañas R, Avila C, Cazorla FM, Cánovas FM, De Vicente A (2004) Up-regulation and localization of asparagine synthetase in tomato leaves infected by the bacterial pathogen Pseudomonas syringae. Plant Cell Physiol 45:770–780

    Article  CAS  PubMed  Google Scholar 

  • Olesen JE, Jørgensen LN, Petersen J, Mortensen JV (2003) Effects of rates and timing of nitrogen fertilizer on disease control by fungicides in winter wheat. 2. Crop growth and disease development. J Agric Sci 140:15–29

    Article  CAS  Google Scholar 

  • Pageau K, Reisdorf-Cren M, Morot-Gaudry JF, Masclaux-Daubresse C (2006) The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive. J Exp Bot 57:547–557

    Article  CAS  PubMed  Google Scholar 

  • Pellier A-L, Laugé R, Veneault-Fourrey C, Langin T (2003) CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Mol Microbiol 48:639–655

    Article  CAS  PubMed  Google Scholar 

  • Prusky D, Lichter A (2008) Mechanisms modulating fungal attack in post-harvest pathogen interactions and their control. Eur J Plant Pathol 121:281–289

    Article  Google Scholar 

  • Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40:267–278

    Article  CAS  PubMed  Google Scholar 

  • Robert C, Bancal M-O, Ney B, Lannou C (2005) Wheat leaf photosynthesis loss due to leaf rust, with respect to lesion development and leaf nitrogen status. New Phytol 165:227–241

    Article  PubMed  Google Scholar 

  • Schjoerring JK, Mattsson M, Husted S (1998) Physiological parameters controlling plant-atmosphere ammonia exchange. Atmos Environ 32:491–498

    Article  CAS  Google Scholar 

  • Schjoerring JK, Husted S, Mack G, Nielsen KH, Finnemann J, Mattsson M (2000) Physiological regulation of plant-atmosphere ammonia exchange. Plant Soil 221:95–101

    Article  CAS  Google Scholar 

  • Shafik J, Taha K (1984) Chemical control of brown spot of tobacco in northern Iraq. Indian Phytopathol 37:669–672

    CAS  Google Scholar 

  • Shew HD, Lucas GB (eds) (1991) Compendium of tobacco diseases. American Phytopathological Society, St. Paul

    Google Scholar 

  • Skopelitis DS, Paranychianakis NV, Kouvarakis A, Spyros A, Stephanou EG, Roubelakis-Angelakis KA (2007) The isoenzyme 7 of tobacco NAD(H)-dependent glutamate dehydrogenase exhibits high deaminating and low aminating activities in vivo. Plant Physiol 145:1726–1734

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Solomon PS, Tan K-C, Oliver RP (2003) The nutrient supply of pathogenic fungi; a fertile field for study. Mol Plant Pathol 4:203–210

    Article  PubMed  Google Scholar 

  • Speer M, Kaiser WM (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiol 97:990–997

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sreeramamuthy CH, Arishukumar PH, Nageswararao CR (1996) Change in concentration of nitrogenous constituents in flue-cured tobacco leaf as affected by nitrogen fertilization in Vertisols. Tob Res 22:22–25

    Google Scholar 

  • Stavely JR, Main CE (1970) Influence of temperature and other factors on initiation of tobacco brown spot. Phytopathology 60:1591–1596

    Article  Google Scholar 

  • Stavely JR, Slana LJ (1971) Relation of leaf age to the reaction of tobacco to Alternaria alternata. Phytopathology 61:73–78

    Article  Google Scholar 

  • Talbot NJ, Mccafferty HRK, Ma M, Moore K, Hamer JE (1997) Nitrogen starvation of the rice blast fungus Magnaporthe grisea may act as an environmental clue for disease symptom expression. Physiol Mol Plant Pathol 50:179–195

    Article  CAS  Google Scholar 

  • Tavernier V, Cadiou S, Pageau K, Laugé R, Reisdorf-Cren M, Langin T, Masclaux-Daubresse C (2007) The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. J Exp Bot 58:3351–3360

    Article  CAS  PubMed  Google Scholar 

  • Tercé-Laforgue T, Mäck G, Hirel B (2004) New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum) plants grown under different nitrogen regimes. Physiol Plant 120:220–228

    Article  PubMed  Google Scholar 

  • Turano FJ, Dashner R, Upadhyaya A, Caldwell CR (1996) Purification of mitochondrial glutamate dehydrogenase from dark-grown soybean seedlings. Plant Physiol 112:1357–1364

    PubMed Central  CAS  PubMed  Google Scholar 

  • Walters DR, Bingham IJ (2007) Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control. Ann Appl Biol 151:307–324

    Article  CAS  Google Scholar 

  • Wang L, Pedas P, Eriksson D, Schjoerring JK (2013) Elevated atmospheric CO2 decreases the ammonia compensation point of barley plants. J Exp Bot 64:2713–2724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yao YX, Yu L, Cheng SY, Zhang Z (1995) Studies on relation between degree of brown spot on tobacco and the total amount of nitrogen in tobacco leaves. J Jilin Agric Univ 17:99–101

    Google Scholar 

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Acknowledgments

This work was financially supported by the special fund from Guizhou Provincial Tobacco Company (201230), the Key Special Program of China National Tobacco Corporation (TS-01-2011003) and the Program of China National Tobacco Corporation (110201002008).

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Correspondence to Tie-Zhao Yang.

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Section editor: Adalberto Café Filho

Zhi-Xiao Yang and Xiao-Quan Zhang contributed equally to this work.

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Yang, ZX., Zhang, XQ., Xue, G. et al. The relationship between resistance to tobacco brown spot and nitrogen metabolism in mature tobacco (Nicotiana tabacum) plants. Trop. plant pathol. 40, 219–226 (2015). https://doi.org/10.1007/s40858-015-0030-z

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