Skip to main content
SpringerLink
Log in

Penicillium oxalicum directed systemic resistance in tomato against Alternaria alternata

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

Abstract

Enhanced yield of tomato has ever been an important issue due to its nutritional value and various dietary consumption forms. But, efficient yield increase can never be achieved without using environmentally safe means e.g. innate resistance. In present study, tomato innate antifungal resistance has been boosted up using Penicillium oxalicum, and then various aspects of resistance modulation have been explored in details. Two tomato varieties of differential antifungal resistance (Dinaar and Red Tara) were treated with six P. oxalicum strains which screened the best inducer strain (Pn 5); which remarkably controlled disease incidence (DI) of Alternaria alternata. Inducer was not only responsible for almost two times production of phenolics, alkaloids and terpenoids in Red Tara, but it also non-significantly triggered same biochemicals in Dinaar. Hemicellulose showed only 40 % increase in variety of least antifungal resistance. During quantification assays of peroxidase (POD), phenyl ammonia lyase and polyphenol oxidase, more or less the same doubling trend was recorded in susceptible variety, while only POD had significant enhancement in resistant variety under the influence of fungal inducer. It was also recorded that inducer not only modulated quantity of enzyme (glucanase), but its isozyme package was also altered. Colorimetric quantifications of lignin, cellulose and pectins proved that biotic inducer strengthened the physical structure of plant cells by increasing these contents from 30 to 120 %. The above investigation collectively comes with the recommendation of an efficient and environmentally safe inducer (P. oxalicum); which, can be used to control fungal pathogens.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdel-Kader MM, El-Mougy NS, El-Gamal NG, El-Mohamdy RS, Fatouh YO (2012) In vitro assay of some plant resistance inducers, essential oils and plant extracts on antagonistic ability of fungal bio-agents. J Appl Sci Res 8(3):1383–1391

    CAS  Google Scholar 

  • Ahmad A, Shafique S, Shafique S (2013) Cytological and physiological basis for tomato varietal resistance against Alternaria alternata. J Sci Food Agric 93:2315–2322. doi:10.1002/jsfa.6045

    Article  PubMed  CAS  Google Scholar 

  • Akhtar J, Gorham J, Qureshi RH (1994) Combined effect of salinity and hypoxia in wheat (Triticum aestivum L.) and wheat-Thynopyrum amphiploids. Plant Soil 166:47–54

    Article  CAS  Google Scholar 

  • Arvind V, Into L, Tuulikki S, Aarre H, Marja-Liisa R (2007) A simplified procedure for indole alkaloid extraction from Catharanthus roseus combined with a semi-synthetic production process for vinblastine. Molecules 12:1307–1315

    Article  Google Scholar 

  • Ashry NA, Mohamed HI (2011) Impact of secondary metabolites and related enzymes in flax resistance and or susceptibility to powdery mildew. WJAS 7(1):78–85

    CAS  Google Scholar 

  • Baloch AF (1994) Vegetable crops. Horticulture. National Book Foundation, Islamabad, pp 489–537

    Google Scholar 

  • Banerjee A, Datta JK, Mondal NK (2012) Biochemical changes in leaves of mustard under the influence of different fertilizers and cycocel. J Agric Technol 8(4):1397–1411

    CAS  Google Scholar 

  • Burrell MM, Rees TA (1974) Metabolism of phenylalanine and tyrosine in rice leaves infected by Pyricularia oryzae. Physiol Plant Pathol 4:497–508

    Article  CAS  Google Scholar 

  • Castro MS, Fontes W (2005) Plant defense and antimicrobial peptides. Protein Pept Lett 12:11–16

    Article  Google Scholar 

  • Chérif M, Arfaoui A, Rhaiem A (2007) Phenolic compounds and their role in bio-control and resistance of chickpea to fungal pathogenic attacks. Tunis J Plant Prot 2(1):7–21

    Google Scholar 

  • Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171–201

    Article  PubMed  CAS  Google Scholar 

  • De-Cal A, Pascual S, Larena I, Melgarejo P (1995) Biological control of Fusarium oxysporum f.sp lycopersici. Plant Pathol 44:909–917

    Article  Google Scholar 

  • Djonović S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145(3):875–889

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • El-Khallal SM (2007) Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (jasmonic acid and salicylic acid): 2-changes in the antioxidant enzymes, phenolic compounds and pathogen related-proteins. Aust J Basic Appl Sci 1(4):717–732

    CAS  Google Scholar 

  • EL-Morsy EM (1999) Microfungi isolated from the ectorhizosphere-rhizoplane zone of different halophytic plants from the red sea coast of Egypt. Mycologia 91:228–236

    Article  Google Scholar 

  • EL-Morsy EM, Serag MS, Zahran JAT, Rashed IG (2000) The occurrence of microfungi in the ectorhizosphere-rhizoplane zone of some selected macrophytes from the Nile delta of Egypt. Bull Fac Sci, Assiut University 2 (2-D): 15–26

  • Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, Lorenzo GD (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146(2):669–681

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Freeman BC, Beattie GA (2008) An overview of plant defenses against pathogens and herbivores. Plant Health Instr. doi:10.1094/PHI-I-2008-0226-01

    Google Scholar 

  • Ghosh R, Datta M, Purkayastha RP (2006) Intraspecific strains of Pythium aphanidermatum induced disease resistance in ginger and response of host proteins. Indian J Exp Biol 44:68–72

    PubMed  CAS  Google Scholar 

  • Guo XX, Zhao TY, Dong YD, Jiang S, Lu BL (2004) Transmission of dengue-2 virus by diapausing eggs of Aedes albopictus. Acta Entomol Sinica 47:424–428

    Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species––opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  PubMed  CAS  Google Scholar 

  • Hobson LA, Hartley FA, Ketcham DE (1979) Effects of variations in daylength and temperature on net rates of photosynthesis, dark respiration, and excretion by Isochrysis galbana Parke. Plant Physiol 63:947–951

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Johansson SM, Lundgren LN, Asiegbu FO (2004) Initial reactions in sapwood of Norway spruce and Scots pine after wounding and infection by Heterobasidion parviporum and H. annosum. Forest Pathol 34:197–210. doi:10.1111/j.1439-0329.2004.00358.x

    Article  Google Scholar 

  • Kempel A, Schmidt AK, Brand R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24(2):293–300. doi:10.1111/j.1365-2435.2009.01647.x

    Article  Google Scholar 

  • Kurabachew H, Wydra K (2010) Induction of defence related enzymes and gene expression after resistance induction by rhizobacteria and silicon against Ralstonia solanacearum in tomato (Solanum lycopersicum). Conference on international research on food security, natural resource management and rural development, ETH Zurich

  • Lawrence SD, Novak NG (2004) Maize genes induced by herbivory and volicitin. J Chem Ecol 30:2543–2557

    Article  PubMed  CAS  Google Scholar 

  • Linder M, Mattinen ML, Kontteli M, Lindeberg G, Stahlberg J, Drakenberg T, Reinikainen T, Pettersson G, Annila A (1995) Identification of functionally important amino acids in the cellulose-binding domain of Trichoderma reesei cellobiohydrolase I. Protein Sci 4:1056–1064

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce (Picea abies). Plant Physiol 132:1586–1599

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mayer AM, Harel E, Shaul RB (1965) Assay of catechol oxidase a critical comparison of methods. Phytochemistry 5:783–789

    Article  Google Scholar 

  • Miller B, Madilao LL, Ralph S, Bohlmann J (2005) Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in sitka spruce. Plant Physiol 137(1):369–382

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci 162:491–498

    Article  CAS  Google Scholar 

  • Mujica M, Granito M, Soto N (2009) Importance of the extraction method in the quantification of total phenolic compounds in Phaseolus vulgaris L. Interciencia Indexada en el Science Citation Index 34:650–654

    Google Scholar 

  • Mumm R, Posthumus MA, Dicke M (2008) Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ 31(4):575–585

    Article  PubMed  CAS  Google Scholar 

  • Putter J (1970) Peroxidasen In Methoden der enzymatischen Analysen. In: Bergmeyer H (ed) vol 1. Verlag Chemie, Weinheim

  • Quiroga M, Guerrero C, Botella MA, Barcelo A, Amaya I, Medina MI, Alfonso FJ, Forchetti MSD, Tigier H, Valpuesta V (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol 122:1119–1128

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Reglinski T, Dann E, Deverall B (2007) Integration of induced resistance in crop protection. In: Walters D, Newton A, Lyon G (eds) Induced resistance for plant defence. A sustainable approach to crop protection. Blackwell Publishing, Oxford, pp 201–228

    Chapter  Google Scholar 

  • Sempere F, Santamarina MP (2010) Study of the interactions between Penicillium oxalicum currie & thom and Alternaria alternata (FR.) Keissler. Braz J Microbiol 41(3):700–706

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43. doi:10.1146/annurev-phyto-073009-114450

    Article  PubMed  CAS  Google Scholar 

  • Van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Article  Google Scholar 

  • Vera J, Castro J, González A, Barrientos H, Matsuhiro B, Arce P, Zúñiga G, Moenne A (2011a) Long term protection against tobacco mosaic virus induced by the marine alga oligo-sulphated-galactan poly-Ga in tobacco plants. Mol Plant Pathol 12:437–447

    Article  PubMed  CAS  Google Scholar 

  • Vera J, Castro J, Gonzalez A, Moenne A (2011b) Seaweed polysaccharides and derived oligosaccharides stimulate defense responses and protection against pathogens in plants. Mar Drugs 12:2514–2525

    Article  CAS  Google Scholar 

  • Veronese P, Ruiz MT, Coca MA, Hernandez-Lopez A, Lee H, Ibeas JI, Damsz B, Pardo JM, Hasegawa PM, Bressan RA, Narasimhan ML (2003) In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiol 131(4):1580–1590

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Villalba-Mateos F, Rickauer M, Esquerré-Tugayé MT (1997) Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol Plant Microbe In 10:1045–1053

    Article  Google Scholar 

  • Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209

    Article  PubMed  CAS  Google Scholar 

  • Walters DR, Fountaine JM (2009) Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions. J Agr Sci 147:523–535

    Article  CAS  Google Scholar 

  • Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:1–8

    Article  Google Scholar 

  • Witzell J, Martin JA (2008) Phenolic metabolites in the resistance of northern forest trees to pathogens––past experiences and future prospects. Can J Forest Res 38:2711–2727

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Agricultural Sciences, University of the Punjab, Lahore, Pakistan

    Aqeel Ahmad, Sobiya Shafique, Shazia Shafique & Waheed Akram

Authors
  1. Aqeel Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sobiya Shafique
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shazia Shafique
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Waheed Akram
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aqeel Ahmad.

Additional information

Communicated by M. J. Reigosa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahmad, A., Shafique, S., Shafique, S. et al. Penicillium oxalicum directed systemic resistance in tomato against Alternaria alternata . Acta Physiol Plant 36, 1231–1240 (2014). https://doi.org/10.1007/s11738-014-1500-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1500-5

Keywords

Search

Navigation