Skip to main content
SpringerLink
Log in

Nutrition supply affects the activity of pathogenesis-related β-1,3-glucanases and chitinases in wheat

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Nitrogen (N) is an essential mineral for plants and both its deficiency and excess causes serious problems in agriculture. As stress-inducible defense is costly, N conditions likely affect the trade-off between the growth and defense. Previous studies identified a few defense-related enzymes dependent on N nutrition. Chitinases (EC 3.2.1.14) and glucanases (EC 3.2.1.39) are typical plant defense enzymes belonging to the group of pathogenesis-related (PR) proteins with multiple functions in plants. Since a comprehensive study on the impact of N nutrition on their activity is missing, we studied their profiles and activities at isoforms level in wheat plants grown hydroponically at N doses corresponding to limited (0, 0.75 and 5.25 mM N), optimal N (7.5 mM N) as well as excess (15, 30 and 35 mM N) N supply in the form of nitrate. Our results show that several isoforms of both enzymes in wheat leaves and/or shoots clearly depended on N supply, while their activities rather depended on organ type. Furthermore, glucanases and chitinases appeared to be regulated in an opposite way. The activities of particular chitinases and glucanases correlated with a proline content that has multiple functions in plants. Proline typically accumulated with increasing the N supply when certain excessive N doses induced the gene for proline synthase (P5CS) in shoots and that for ornithine aminotransferase (OAT) in roots. This work points to a N-dependent activity of several defense-related compounds suggesting the possibly of altered plant defense potential under various N regimes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamec L (2002) Leaf absorption of mineral nutrients in carnivorous plants stimulates root nutrient uptake. New Phytol 155:89–100

    Article  CAS  Google Scholar 

  • Avice JC, Le Dily F, Goulas E, Noquet C, Meuriot F, Volenec JJ, Cunningham SM, Sors TG, Dhont C, Castonguay Y, Nadeau P, Bélanger G, Chalifour FP, Ourry A (2003) Vegetative storage proteins in overwintering storage organs of forage legumes: roles and regulation. Can J Bot 81:1198–1212

    Article  CAS  Google Scholar 

  • Békésiová I, Nap JP, Mlynárová L (1999) Isolation of high quality DNA and RNA from leaves of the carnivorous plant Drosera rotundifolia. Plant Mol Biol Rep 17:269–277

    Article  Google Scholar 

  • Chandna R, Ahmad A (2015) Nitrogen stress-induced alterations in the leaf proteome of two wheat varieties grown at different nitrogen levels. Physiol Mol Biol Plants 21:19–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Fuchigami LH (2000) Rubisco activation state decreases with increasing nitrogen content in apple leaves. J Exp Bot 51:1687–1694

    Article  CAS  PubMed  Google Scholar 

  • Cramer MD, Lewis OAM (1993) The Influence of Nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) Plants. Ann Bot 72:359–365

    Article  CAS  Google Scholar 

  • Dietrich R, Ploss K, Heil M (2004) Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant Cell Environ 27:896–906

    Article  CAS  Google Scholar 

  • Gálusová T, Rybanský Ľ, Mészáros P, Spieß N, Piršelová B, Kuna R, Libantová J, Moravčíková J, Hauptvogel P, Matušiková I (2014) Variable responses of soybean chitinases to arsenic and cadmium stress at the whole plant level. Plant Growth Regul 76:147–155

    Article  Google Scholar 

  • Gojon A, Gaymard F (2010) Keeping nitrate in the roots: an unexpected requirement for cadmium tolerance in plants. J Mol Cell Biol 2:299–301

    Article  CAS  PubMed  Google Scholar 

  • Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol 10:37–49

    Article  CAS  PubMed  Google Scholar 

  • Gregorová Z, Kováčik J, Klejdus B, Maglovski M, Kuna R, Hauptvogel P, Matušíková I (2015) Drought-induced responses of physiology, metabolites, and PR proteins in Triticum aestivum. J Agric Food Chem 63:8125–8133

    Article  PubMed  Google Scholar 

  • Hakeem KR, Chandna R, Ahmad A, Qureshi MI, Iqbal M (2012) Proteomic analysis for low and high nitrogen-responsive proteins in the leaves of rice genotypes grown at three nitrogen levels. Appl Biochem Biotechnol 168:834–850

    Article  CAS  PubMed  Google Scholar 

  • Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937

    Article  PubMed  Google Scholar 

  • Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81:802–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karabal E, Yucel M, Oktem HA (2003) Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Sci 164:925–933

    Article  CAS  Google Scholar 

  • Kasprzewska A (2003) Plant chitinases: regulation and function. Cell Mol Biol Lett 8:809–824

    CAS  PubMed  Google Scholar 

  • Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865

    Article  PubMed  Google Scholar 

  • Konno H, Yamasaki Y, Sugimoto M, Takeda K (2008) Differential changes in cell wall matrix polysaccharides and glycoside-hydrolyzing enzymes in developing wheat seedlings differing in drought tolerance. J Plant Physiol 165:745–754

    Article  CAS  PubMed  Google Scholar 

  • Konotop Y, Mészáros P, Spieß N, Mistríková V, Piršelová B, Libantová J, Moravčíková J, Taran N, Hauptvogel P, Matušíková I (2012) Defense responses of soybean roots during exposure to cadmium, excess of nitrogen supply and combinations of these stressors. Mol Biol Rep 39:10077–10087

    Article  CAS  PubMed  Google Scholar 

  • Libantová J, Kämäräinen T, Moravčíková J, Matušíková I, Salaj J (2009) Detection of chitinolytic enzymes with different substrate specificity in tissues of intact sundew (Drosera rotundifolia L.): chitinases in sundew tissues. Mol Biol Rep 36:851–856

    Article  PubMed  Google Scholar 

  • Lichtenthaler H, Wellburn A (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Malagoli P, Le Deunf E (2014a) An updated model for nitrate uptake modelling in plants. I. Functional component: cross-combination of flow-force interpretation of nitrate uptake isotherms, and environmental and in planta regulation of nitrate influx. Ann Bot 113:991–1005

    Article  PubMed  PubMed Central  Google Scholar 

  • Malagoli P, Le Deunf E (2014b) An updated model for nitrate uptake modelling in plants. II. Assessment of active root involvement in nitrate uptake based on integrated root system age: measured versus modelled outputs. Ann Bot 113:1007–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Márquez AJ, Betti M, García-Calderón M, Pal’ove-Balang P, Díaz P, Monza J (2005) Nitrate assimilation in Lotus japonicus. J Exp Bot 56:1741–1749

    Article  PubMed  Google Scholar 

  • Mészáros P, Rybanský A, Hauptvogel P, Kuna R, Libantová J, Moravčíková J, Piršelová B, Tirpáková A, Matušíková I (2013) Cultivar-specific kinetics of chitinase induction in soybean roots during exposure to arsenic. Mol Biol Rep 40:2127–2138

    Article  PubMed  Google Scholar 

  • Mészáros P, Rybanský Ľ, Spieß N, Socha P, Kuna R, Libantová J, Moravčíková J, Piršelová B, Hauptvogel P, Matušíková I (2014) Plant chitinase responses to different metal-type stresses reveal specificity. Plant Cell Rep 33:1789–1799

    Article  PubMed  Google Scholar 

  • Migocka M, Warzybok A, Papierniak A, Kłobus G (2013) NO3 −/H+ antiport in the tonoplast of cucumber root cells is stimulated by nitrate supply: evidence for a reversible nitrate-induced phosphorylation of vacuolar NO3 −/H+ antiport. PLoS One 8:e73972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller G (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Pan SQ, Ye XS, Kuc J (1991) A technique for detection of chitinase, beta-1,3-glucanase, and protein patterns after a single separation using polyacrylamide-gel electrophoresis or isolelectrofocusing. Phytopathology 81:970–974

    Article  CAS  Google Scholar 

  • Petruzzelli L, Kunz C, Waldvogel R, Meins F Jr, Leubner-Metzger G (1999) Distinct ethylene- and tissue-specific regulation of β-1,3-glucanases and chitinases during pea seed germination. Planta 209:195–201

    Article  CAS  PubMed  Google Scholar 

  • Piršelová B, Matušíková I (2013) Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiol Plantarum 35:635–644

    Article  Google Scholar 

  • Saltzmann KD, Giovanini MP, Zheng C, Williams CE (2008) Virulent hessian fly larvae manipulate the free amino acid content of host wheat plants. J Chem Ecol 34:1401–1410

  • Sánchez E, López-Lefebre LR, García PC, Rivero RM, Ruiz JM, Romero L (2001) Proline metabolism in response to highest nitrogen dosages in green bean plants (Phaseolus vulgaris L. cv. Strike). J Plant Physiol 158:593–598

    Article  Google Scholar 

  • Shavrukov Y, Bowner J, Langridge P, Tester M (2006) Screening for sodium exclusion in wheat and barley. Proceedings of the 13th Australian Society of Agronomy, Perth. The Regional Institute Ltd. Publishing Web. Available from http://www.regional.org.au/au/asa/2006/concurrent/environment/4581_shavrukoky.htm

  • Smakowska E, Kong J, Busch W, Belkhadir Y (2016) Organ specific regulation of growth-defense tradeoffs by plants. Curr Opin Plant Biol 29:129–137

    Article  CAS  PubMed  Google Scholar 

  • Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book 8:e0140

    Article  PubMed  PubMed Central  Google Scholar 

  • Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17

    Article  CAS  Google Scholar 

  • Wang Y, Mi G, Chen F, Zhang J, Zhang F (2004) Response of root morphology to nitrate supply and its contribution to nitrogen accumulation in maize. J Plant Nutr 27:2189–2202

    Article  CAS  Google Scholar 

  • Wang YH, Feng Y, Xu NY, Chen BL, Ma RH, Zhou ZG (2009) Response of the enzymes to nitrogen applications in cotton fiber (Gossypium hirsutum L.) and their relationships with fiber strength. Sci China C Life Sci 52:1065–1072

    Article  CAS  PubMed  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012a) Uptake, allocation and signalling of nitrate. Trends Plant Sci 17:458–467

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Peng F, Yang L, Li M, Zhang S (2012b) Expression of genes involved in nitrate signaling and metabolism in peach roots in response to elevated levels of nitrate. Plant Mol Biol Rep 30:1450–1460

    Article  CAS  Google Scholar 

  • Wei H, Yordanov YS, Georgieva T, Li X, Busov V (2013) Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks. New Phytol 200:483–497

    Article  CAS  PubMed  Google Scholar 

  • Wu CT, Bradford KJ (2003) Class I chitinase and βa-1,3-glucanase are differentially regulated by wounding, methyl jasmonate, ethylene and gibberellin in tomato seeds and leaves. Plant Physiol 133:263–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang GB, Yi HY, Gong JM (2014) The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation. Plant Cell 26:3984–3998

  • Zur I, Gołebiowska G, Dubas E, Golemiec E, Matušíková I, Libantová J, Moravčíková J (2013) β-1,3-glucanase and chitinase activities in winter triticales during cold hardening and subsequent infection by Microdochium nivale. Biologia (Poland) 68:241–248

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financed by the Slovak Research and Development Agency under contract number APVV-15-0051 and UGA VIII/31/2015. This study was partly supported (to LA) by the Long-term research development project No. RVO 67985939 by the Czech Academy of Sciences and Agentúra na Podporu Výskumu a Vývoja (Grant No. 0197-10). Sincere thanks are due to Dr. Brian McMillan (Glasgow, Scotland, U.K.) for English correction.

Author information

Authors and Affiliations

  1. Institute of Plant Genetics and Biotechnology SAS, Akademická 2, 950 07, Nitra, Slovakia

    Marína Maglovski & Jana Moravčíková

  2. Department of Botany and Genetics, Faculty of Natural Sciences, Constantine the Philosopher University, Nábrežie mládeže 91, 949 74, Nitra, Slovakia

    Zuzana Gregorová & Patrik Mészáros

  3. Department of Mathematics, Faculty of Natural Sciences, Constantine the Philosopher University, Tr. A. Hlinku 1, 949 74, Nitra, Slovakia

    Ľubomír Rybanský

  4. National Agricultural and Food Centre—Research Institute of Plant Production, Bratislavská cesta 122, 921 68, Piešťany, Slovakia

    Pavol Hauptvogel

  5. Section of Plant Ecology, Institute of Botany of the Czech Academy of Sciences, Dukelská 135, 379 82, Třeboň, Czech Republic

    Lubomír Adamec

  6. Department of Ecochemistry and Radioecology, University of Ss. Cyril and Methodius, J. Herdu 2, 917 01, Trnava, Slovakia

    Ildikó Matušíková

Authors
  1. Marína Maglovski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zuzana Gregorová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ľubomír Rybanský
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrik Mészáros
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jana Moravčíková
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pavol Hauptvogel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lubomír Adamec
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ildikó Matušíková
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ildikó Matušíková.

Ethics declarations

Conflict of interest

The authors report no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10725_2016_222_MOESM1_ESM.pdf

Online resource 1: ESM_1.PDF Influence of different N concentrations in growth media (0-35 mM) on ratio of chlorophyll a/chlorophyll b (Chl a/b) (black symbols, bold letters), and the ratio of total pigment to total carotenoid content (Chl (a+b)/Car)(empty symbols, italics). Data in graphs are standardized average values with 95% confidential intervals (n = 5). Different letters indicate significance at P < 0.05. (PDF 187 KB)

10725_2016_222_MOESM2_ESM.pdf

Online resource 2: ESM_2.PDF Detected isoforms (arrows) of total (first columns), acidic and neutral (middle columns), basic and neutral (third columns) chitinases (a) and glucanases (b) in shoots and roots of wheat that were grown on media with 0-35 mM N. (PDF 233 KB)

Online resource 3: ESM_3.PDF Correlation coeficients for the parameters measured in wheat organs. (PDF 40 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maglovski, M., Gregorová, Z., Rybanský, Ľ. et al. Nutrition supply affects the activity of pathogenesis-related β-1,3-glucanases and chitinases in wheat. Plant Growth Regul 81, 443–453 (2017). https://doi.org/10.1007/s10725-016-0222-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-016-0222-7

Keywords

Search

Navigation