Plant and Soil

, Volume 357, Issue 1–2, pp 245–257 | Cite as

Biochar mediates systemic response of strawberry to foliar fungal pathogens

  • Yael Meller Harel
  • Yigal Elad
  • Dalia Rav-David
  • Menachem Borenstein
  • Ran Shulchani
  • Beni Lew
  • Ellen R. Graber
Regular Article

Abstract

Background and Aims

Various biochars added to soil have been shown to improve plant performance. Moreover, a wood biochar was found to induce tomato and pepper plant systemic resistance to two foliar fungal pathogens. The aim of this study was to explore the ability of wood biochar and greenhouse waste biochar to induce systemic resistance in strawberry plants against Botrytis cinerea, Colletotrichum acutatum and Podosphaera apahanis, and to examine at the molecular level some of their impacts on plant defense mechanisms.

Methods

Disease development tests on plants grown on 1 or 3% biochar-amended potting mixture, and quantification of relative expression of 5 plant defense-related genes (FaPR1, Faolp2, Fra a3, Falox, and FaWRKY1) by real-time PCR were carried out.

Results

Biochar addition to the potting medium of strawberry plants suppressed diseases caused by the three fungi, which have very different infection strategies. This suggests that biochar stimulated a range of general defense pathways, as confirmed by results of qPCR study of defense-related gene expression. Furthermore, primed-state of defense-related gene expression was observed upon infection by B. cinerea and P. aphanis.

Conclusion

The ability of biochar amendment to promote transcriptional changes along different plant defense pathways probably contributes to its broad spectrum capacity for disease suppression.

Keywords

Biotic stress Induced systemic resistance Plant disease Priming Systemic acquired resistance Systemic resistance 

Abbreviations

qPCR

real time quantitative PCR

RT

reverse transcription

IR

induced resistance

ISR

induced systemic resistance

SAR

systemic acquired resistance

HR

hypersensitive reaction

PR

pathogenesis related proteins

SA

salicylic acid

PGPR

plant growth-promoting rhizobacteria

PGPF

plant growth-promoting fungi

ET

ethylene

JA

jasmonic acid

MeJA

methyl jasmonate

CW

biochar produced from citrus wood

GHW-450

biochar produced from greenhouse waste at 450°C

AUDPC

area under the disease progress curve

Ct

cycle threshold

References

  1. Asai H, Samson BK, Stephan HM, Songyikhangsuthor K, Homma K, Kiyono Y, Inoue Y, Shiraiwa T, Horie T (2009) Biochar amendment techniques for upland rice production in Northern Laos 1. Soil physical properties, leaf SPAD and grain yield. Field Crop Res 111:81–84CrossRefGoogle Scholar
  2. Asif MH, Dhawan P, Nath P (2000) A simple procedure for the isolation of high quality RNA from ripening banana fruit. Plant Mol Biol Rep 18:109–115CrossRefGoogle Scholar
  3. Atkinson CJ, Fitzgerald JD, Hipps NA (2010) Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil 337:1–18CrossRefGoogle Scholar
  4. Casado-Diaz A, Encinas-Villarejo S, de los Santos B, Schiliro E, Yubero-Serrano EM, Amil-Ruiz F, Pocovi MI, Pliego-Alfaro F, Dorado G, Rey M, Romero F, Munoz-Blanco J, Caballero JL (2006) Analysis of strawberry genes differentially expressed in response to Colletotrichum infection. Physiol Plant 128:633–650CrossRefGoogle Scholar
  5. Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B, Grp P-A-P (2006) Priming: Getting ready for battle. Mol Plant Microbe Interact 19:1062–1071PubMedCrossRefGoogle Scholar
  6. De Cal A, Redondo C, Sztejnberg A, Melgarejo P (2008) Biocontrol of powdery mildew by Penicillium oxalicum in open-field nurseries of strawberries. Biol Cont 47:103–107CrossRefGoogle Scholar
  7. Elad Y, Rav-David D, Meller Harel Y, Borenshtein M, Ben Kalifa H, Silber A, Graber ER (2010) Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology 100:913–921PubMedCrossRefGoogle Scholar
  8. Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, de Los Santos B, Romero F, Pliego-Alfaro F, Munoz-Blanco J, Caballero JL (2009) Evidence for a positive regulatory role of strawberry (Fragaria x ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. J Exp Bot 60:3043–3065PubMedCrossRefGoogle Scholar
  9. Foolad MR, Ntahimpera N, Christ BJ, Lin GY (2000) Comparison of field, greenhouse, and detached-leaflet evaluations of tomato germ plasm for early blight resistance. Plant Dis 84:967–972CrossRefGoogle Scholar
  10. Freeman S, Minz D, Kolesnik I, Barbul O, Zveibil A, Maymon M, Nitzani Y, Kirshner B, Rav-David D, Bilu A, Dag A, Shafir S, Elad Y (2004) Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. Eur J Plant Pathol 110:361–370CrossRefGoogle Scholar
  11. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedCrossRefGoogle Scholar
  12. Gomez-Gomez L, Rubio-Moraga A, Ahrazem O (2011) Molecular cloning and characterisation of a pathogenesis-related protein CsPR10 from Crocus sativus. Plant Biol 13:297–303PubMedCrossRefGoogle Scholar
  13. Graber ER, Meller Harel Y, Kolton M, Cytryn E, Silber A, Rav-David D, Tsechansky L, Borenshtein M, Elad Y (2010) Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant Soil 337:481–496CrossRefGoogle Scholar
  14. Hossain MK, Strezov V, Chan KY, Ziolkowski A, Nelson PF (2011) Influence of pyrolysis temperature on production and nutrient properties of wastewater sludge biochar. J Environ Manag 92:223–228CrossRefGoogle Scholar
  15. Hukkanen AT, Kokko HI, Buchala AJ, McDougall GJ, Stewart D, Karenlampi SO, Karjalainen RO (2007) Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries. J Agric Food Chem 55:1862–1870PubMedCrossRefGoogle Scholar
  16. Joyce DC, Terry LA (2000) Suppression of grey mould on strawberry fruit with the chemical plant activator acibenzolar. Pest Manag Sci 56:989–992CrossRefGoogle Scholar
  17. Kolton M, Meller Harel Y, Pasternak Z, Graber ER, Elad Y, Cytryn E (2011) Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl Environ Microbiol 77:4924–4930PubMedCrossRefGoogle Scholar
  18. Kravchuk Z, Vicedo B, Flors V, Camanes G, Gonzalez-Bosch C, Garcia-Agustin P (2011) Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea. J Plant Physiol 168:359–366PubMedCrossRefGoogle Scholar
  19. Kwon Y, Oh JE, Noh H, Hong SW, Bhoo SH, Lee H (2011) The ethylene signaling pathway has a negative impact on sucrose-induced anthocyanin accumulation in Arabidopsis. J Plant Res 124:193–200PubMedCrossRefGoogle Scholar
  20. Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota - A review. Soil Biol Biochem 43:1812–1836CrossRefGoogle Scholar
  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  22. Major J, Rondon M, Molina D, Riha SJ, Lehmann J (2010) Maize yield and nutrition during 4 years after biochar application to a Colombian savanna oxisol. Plant Soil 333:117–128CrossRefGoogle Scholar
  23. Meller Harel Y, Kolton M, Elad Y, Rav-David D, Cytryn E, Ezra D, Borenstein M, Shulchani R, Graber ER (2011) Induced systemic resistance in strawberry (Fragaria × ananassa) to powdery mildew using various control agents. IOBC/wprs Bull 71:47–51Google Scholar
  24. Moyano E, Encinas-Villarejo S, Lopez-Raez JA, Redondo-Nevado J, Blanco-Portales R, Bellido ML, Sanz C, Caballero JL, Munoz-Blanco J (2004) Comparative study between two strawberry pyruvate decarboxylase genes along fruit development and ripening, post-harvest and stress conditions. Plant Sci 166:835–845CrossRefGoogle Scholar
  25. Munoz C, Hoffmann T, Escobar NM, Ludemann F, Botella MA, Valpuesta V, Schwab W (2010) The strawberry fruit Fra a allergen functions in flavonoid biosynthesis. Mol Plant 3:113–124PubMedCrossRefGoogle Scholar
  26. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655PubMedCrossRefGoogle Scholar
  27. Pertot I, Zasso R, Amsalem L, Baldessari M, Angeli G, Elad Y (2008) Integrating biocontrol agents in strawberry powdery mildew control strategies in high tunnel growing systems. Crop Prot 27:622–631CrossRefGoogle Scholar
  28. Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, Leon-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, Van der Sluis I, Bakker PAHM, Van Loon LC (2001) Rhizobacteria-mediated induced systemic resistance: Triggering, signalling and expression. Eur J Plant Pathol 107:51–61CrossRefGoogle Scholar
  29. Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21PubMedCrossRefGoogle Scholar
  30. Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84PubMedCrossRefGoogle Scholar
  31. Silber A, Levkovitch I, Graber ER (2010) pH-dependent mineral release and surface properties of cornstraw biochar: agronomic implications. Environ Sci Technol 44:9318–9323PubMedCrossRefGoogle Scholar
  32. Swartzberg D, Kirshner B, Rav-David D, Elad Y, Granot D (2008) Botrytis cinerea induces senescence and is inhibited by autoregulated expression of the IPT gene. Eur J Plant Pathol 120:289–297CrossRefGoogle Scholar
  33. Uzoma KC, Inoue M, Andry H, Fujimaki H, Zahoor A, Nishihara E (2011) Effect of cow manure biochar on maize productivity under sandy soil condition. Soil Use Manag 27:205–212CrossRefGoogle Scholar
  34. Vaccari FP, Baronti S, Lugato E, Genesio L, Castaldi S, Fornasier F, Miglietta F (2011) Biochar as a strategy to sequester carbon and increase yield in durum wheat. Eur J Agron 34:231–238CrossRefGoogle Scholar
  35. Vallad GE, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934CrossRefGoogle Scholar
  36. Van der Ent S, Van Wees SC, Pieterse CM (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588PubMedCrossRefGoogle Scholar
  37. Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Path 55:85–97CrossRefGoogle Scholar
  38. Verhagen BWM, Glazebrook J, Zhu T, Chang HS, Van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant Microbe Interact 17:895–908PubMedCrossRefGoogle Scholar
  39. Vicedo B, Flors V, De La OLM, Finiti I, Kravchuk Z, Real MD, Garcia-Agustin P, Gonzalez-Bosch C (2009) Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol Plant Microbe Interact 22:1455–1465PubMedCrossRefGoogle Scholar
  40. Wu J, Khan AA, Shih CT, Shih DS (2001) Cloning and sequence determination of a gene encoding an osmotin-like protein from strawberry (Fragaria X ananassa Duch.). DNA Seq 12:447–453PubMedGoogle Scholar
  41. Zhang Y, Shih DS (2007) Isolation of an osmotin-like protein gene from strawberry and analysis of the response of this gene to abiotic stresses. J Plant Physiol 164:68–77PubMedCrossRefGoogle Scholar
  42. Zhao JP, Su XH (2010) Patterns of molecular evolution and predicted function in thaumatin-like proteins of Populus trichocarpa. Planta 232:949–962PubMedCrossRefGoogle Scholar
  43. Zimmerli L, Metraux JP, Mauch-Mani B (2001) beta-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol 126:517–523PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Yael Meller Harel
    • 1
  • Yigal Elad
    • 1
  • Dalia Rav-David
    • 1
  • Menachem Borenstein
    • 1
  • Ran Shulchani
    • 1
  • Beni Lew
    • 2
  • Ellen R. Graber
    • 3
  1. 1.Department of Plant Pathology and Weed Research, Institute of Plant Protection, The Volcani CenterAgricultural Research OrganizationBet DaganIsrael
  2. 2.Department of Growing, Production and Environmental Engineering, Institute of Agricultural Engineering, The Volcani CenterAgricultural Research OrganizationBet DaganIsrael
  3. 3.Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil, Water and Environmental Sciences, The Volcani CenterAgricultural Research OrganizationBet DaganIsrael

Personalised recommendations