Skip to main content
Log in

Altered metabolomic profile of selected metabolites and improved resistance of Cicer arietinum (L.) against Meloidogyne incognita (Kofoid & White) Chitwood following seed soaking with salicylic acid, benzothiadiazole or nicotinic acid

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The seeds of chickpea Cicer arietinum (L.) were soaked in 0.00, 10.0 or 20.0 μg/mL of salicylic acid (SA), benzothiadiazole (BTH) or nicotinic acid (NA) solutions for 1 h. Treated seeds were sown in field and metabolite profiling of free reduced/oxidized glutathione (GSH/GSSG), SA, acetyl salicylic acid (ASA), jasmonic acid (JA), and chlorogenic acid (CGA) in chickpea crop was carried out at regular intervals (15, 30, 60, 90 and 120 days of sowing) using liquid chromatography (LC). These defense activators increased the levels of GSH, SA, and CGA in leaf; GSSG, ASA, and JA in root; and decreased the levels of GSSG and JA in leaf; GSH, SA, and CGA in root. In leaf, the biosynthesis of SA increased concomitantly with that of GSH. ASA and JA levels declined with increase of SA concentration. CGA biosynthesis increased with decline of JA level. In root, CGA and SA levels declined with increase of JA concentration. The SA level was directly related to CGA and inversely to ASA and JA concentrations. The CGA and SA concentrations increased with treatment dosage up to 120 days. The concentration of leaf GSSG was linked with JA level in root. Chickpea was a SA-rich crop. GSH in leaf was the key metabolite for SA and JA signaling. The reduction in root infection and reproduction of root-knot nematode (RKN), Meloidogyne incognita was highest in BTH followed by SA and NA treatments. This was attributed to increased biosynthesis of CGA. The study firstly linked GSH and SA metabolism enhancing CGA biosynthesis in chickpea. The increase in CGA improved resistance against RKN. Seed treatment at 10.0 µg/mL BTH 1 h before sowing is recommended as strategic management decision to contain RKN on chickpea.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ANOVA:

Analysis of variance

ASA:

Acetyl salicylic acid

BTH:

Benzothiadiazole

CGA:

Chlorogenic acid

GR:

Glutathion reductase

GSH/GSSG:

Reduced/oxidized glutathione

HQT:

Hydroxycinnamoyl CoA quinate transferase

ICS:

Isochorismate synthase

JA:

Jasmonic acid

LC:

Liquid chromatography

MANOVA:

Multivariate analysis of variance

NA:

Nicotinic acid

NPR:

Nonexpresser of pathogenesis-related protein

PCA:

Principal component analysis

RKN:

Root-knot nematode

ROS:

Reactive oxygen species

SA:

Salicylic acid

References

  • Bartoli CG, Casalongue C, Simontacchi M, Márquez-García B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88

    Article  CAS  Google Scholar 

  • Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, Navarre DA, Kaloshian I (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol Plant Microbe Interact 9:1205–1214

    Article  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63

    Article  CAS  PubMed  Google Scholar 

  • Chaouch S, Queval G, Vanderauwera S, Mhamdi A, Vandorpe M, Langlois-Meurinne M, Van Breusegem F, Saindrenan P, Noctor G (2010) Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiol 153:1692–1705

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cooper WR, Jia L, Goggin L (2005) Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. J Chem Ecol 31:1953–1967

    Article  CAS  PubMed  Google Scholar 

  • Daher Z, Recorbet G, Valot B, Robert F, Balliau T, Potin S, Schoefs B, Dumas-Gaudot E (2010) Proteomic analysis of Medicago truncatula root plastids. Proteomics 10:2123–2137

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661

    Article  CAS  PubMed  Google Scholar 

  • Gimenez-Ibanez S, Solano R (2013) Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Front Plant Sci 4:72

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamamouch N, Li C, Seo PJ, Park C, Davis EL (2010) Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol Pathol 12:355–364

    Article  Google Scholar 

  • Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Noctor G (2013) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid Redox Signal 18:2106–2121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Howles PA, Sewalt VJH, Paiva NL, Elkind Y, Bate NJ, Lamb C, Dixon RA (1996) Overexpression of l-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112:1617–1624

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hukkanen A, Kokko H, Buchala A, Häyrinen J, Kärenlampi S (2008) Benzothiadiazole affects the leaf proteome in arctic bramble (Rubus arcticus). Mol Plant Pathol 9:799–808

    Article  CAS  PubMed  Google Scholar 

  • Hung CL, Rohde RA (1973) Phenol accumulation related to resistance in tomato to infection by root knot and lesion nematodes. J Nematol 5:253–258

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20:293–305

    Article  CAS  PubMed  Google Scholar 

  • Jahangir M, Abdel-Farid IB, Kim HK, Choi YH, Verpoorte R (2009) Healthy and unhealthy plants: the effect of stress on the metabolism of Brassicaceae. Environ Exp Bot 67:23–33

    Article  CAS  Google Scholar 

  • Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648–651

    Article  CAS  PubMed  Google Scholar 

  • Mandal S, Mallick N, Mitra A (2009) Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiol Biochem 47:642–649

    Article  CAS  PubMed  Google Scholar 

  • Maughan S, Foyer CH (2006) Engineering and genetic approaches to modulating the glutathione network in plants. Physiol Plant 126:382–397

    Article  CAS  Google Scholar 

  • Meher HC, Gajbhiye VT, Singh G (2011) Salicylic acid-induced glutathione status in tomato crop and resistance to root-knot nematode, Meloidogyne incognita (Kofoid & White) Chitwood. J Xenobiotics 1:22–28

    Article  CAS  Google Scholar 

  • Meher HC, Gajbhiye VT, Singh G (2012) A liquid chromatography method for selected amino acids, coenzymes, growth regulators and vitamins from Cicer arietinum (L.) and Solanum lycopersicum (L.). J Assoc Off Anal Chem Int 95:1142–1152

    CAS  Google Scholar 

  • Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, Saindrenan P, Gouia H, Issakidis-Bourguet E, Renou JP et al (2010) Arabidopsis GLUTATHIONE REDUCTASE 1 plays a crucial role in leaf responses to intracellular H2O2 and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153:1144–1160

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Molinari S, Baser N (2010) Induction of resistance to root-knot nematodes by SAR elicitors in tomato. Crop Protec 29:1354–1355

    Article  CAS  Google Scholar 

  • Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–316

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nandi B, Kundu K, Banerjee N, Sinha Babu SP (2003) Salicylic acid-induced suppression of Meloidogyne incognita infestation of okra and cowpea. Nematology 5:747–752

    Article  CAS  Google Scholar 

  • Niggeweg R, Michael AJ, Martin C (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat Biotechnol 22:746–754

    Article  CAS  PubMed  Google Scholar 

  • Owen KJ, Green CD, Deverall BJA (2002) Benzothiadiazole applied to foliage reduces development and egg deposition by Meloidogyne spp. in glasshouse-grown grapevine roots. Australas Plant Pathol 31:47–53

    Article  Google Scholar 

  • Peña-Cortés H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128

    Article  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  • Rennenberg H (1997) Molecular approaches to glutathione biosynthesis. In: Cram WJ, De Kok LJ, Brunold C, Rennenberg H (eds) Sulfur metabolism in higher plants. Backhuys Publishers, Leiden, pp 59–70

    Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. PNAS 106:653–657

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Siller-Cepeda JH, Chen THH, Fuchigami LH (1991) High performance liquid chromatography analysis of reduced and oxidized glutathione in woody plant tissues. Plant Cell Physiol 32:1179–1185

    CAS  Google Scholar 

  • Takahashi H, Kanayama Y, Zheng MS, Kusano T, Hase S, Ikegami M, Shah J (2004) Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol 45:803–809

    Article  CAS  PubMed  Google Scholar 

  • Wachter A, Rausch T (2005) Regulation of glutathione (GSH) synthesis in plants: Novel insight from Arabidopsis. Landbauforschung Völkenrode, Special Issue 283:149–155

    CAS  Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–571

    Article  CAS  PubMed  Google Scholar 

  • Wubben MJE, Jin J, Baum TJ (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol Plant Microbe Interact 21:424–432

    Article  CAS  PubMed  Google Scholar 

  • Wuyts N, Lognay G, Swennen R, Waele DD (2006) Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 57:2825–2835

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919

    Article  CAS  PubMed  Google Scholar 

  • Zechmann B, Mauch F, Sticher L, Müller M (2008) Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 59:4017–4027

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao N, Guan J, Forouhar F, Tschaplinski TJ, Cheng Z-M, Tong L, Chen F (2009) Two poplar methyl salicylate esterases display comparable biochemical properties but divergent expression patterns. Phytochemistry 70:32–38

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the Director, Indian Agricultural Research Institute for providing facilities for this work and Dr. Suresh Walia, Division of Agricultural Chemicals and Drs. Krishan K. Kaushal, Anju Kamra, Division of Nematology, Indian Agricultural Research Institute, for their constructive contributions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hari C. Meher.

Additional information

Communicated by E. Kuzniak-Gebarowska.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meher, H.C., Gajbhiye, V.T., Singh, G. et al. Altered metabolomic profile of selected metabolites and improved resistance of Cicer arietinum (L.) against Meloidogyne incognita (Kofoid & White) Chitwood following seed soaking with salicylic acid, benzothiadiazole or nicotinic acid. Acta Physiol Plant 37, 140 (2015). https://doi.org/10.1007/s11738-015-1888-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-015-1888-6

Keywords

Navigation