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Efficacy of Trichoderma longibrachiatum in the control of Heterodera avenae

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Abstract

Trichoderma longibrachiatum can be used for the control of Heterodera avenae in crops, but the effectiveness and possible mechanisms are unknown. Here we determined the efficacy and the mechanism responsible for the nematode control in spring wheat (Triticum aestivum L.). Wheat seedlings inoculated with T. longibrachiatum at the concentrations from 1.5 × 104 to 1.5 × 108 spores ml−1 significantly increased plant height, root length, and plant biomass; decreased H. avenae infection in both rhizospheric soil and roots; and enhanced chlorophyll content, root activity, and the specific activities of resistance-related enzymes (peroxidase, polyphenol oxidase and phenylalanine ammonia lyase), compared to the control. Those reactions occurred soon after T. longibrachiatum inoculation and the effect reached the maximum 7–9 days after inoculation. Promoting competitive plant growth and inducing enzyme-trigged resistance serve as the main mechanism responsible for T. longibrachiatum against H. avenae. T. longibrachiatum can be considered an effective biocontrol agent against H. avenae in wheat.

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References

  • Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915

    Article  CAS  PubMed  Google Scholar 

  • Alessandro V, Gabriella C, Ivana C, Dalia A, Giancarlo P (2012) Evaluation of Trichoderma harzianum strain T22 as biological control agent of Calonectria pauciramosa. BioControl 57:687–696

    Article  Google Scholar 

  • Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295

    Google Scholar 

  • Bourne JM, Kerry BR, De Leij FAAM (1996) The importance of the host plant on the interaction between root-knot nematodes Meloidogyne spp. and the nematophagous fungus Pochonia chlamydosporia goddard. Biocontrol Sci Tech 6:539–548

    Article  Google Scholar 

  • Chen C, Belanger R, Benhamou N, Paulitz TC (2000) Defense enzymes induced in cucumber roots by treatment with plant growth promoting rhizobacteria (PGPR) and Phytium aphanidermatum. Physiol Mol Plant P 56:13–23

    Article  CAS  Google Scholar 

  • De la Peña E, Echeverría SR, van der Putten HH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840

    Article  PubMed  Google Scholar 

  • De Leij FAAM, Kerry BR (1993) Pochonia chlamydosporia biological control agent for Meloidogyne incognita and M. haplain pot and microplot tests. Nematogogica 39:115–126

    Article  Google Scholar 

  • Dinham B (2003) Growing vegetables in developing countries for local urban populations and export markets: problems confronting small-scale producers. Pest Manag Sci 59:575–582

    Article  CAS  PubMed  Google Scholar 

  • Elad Y (2000) Trichoderma harzianum T39 preparation for biocontrol of plant diseases control of Botrytis cinerea, Sclerotinia sclerotiorum and Cladosporium fulvum. Biocontrol Sci Tech 10:499–507

    Article  Google Scholar 

  • Elad Y, Zimmand G, Zaqs Y, Zuriel S, Chet I (1993) Use of Trichoderma harzianum in combination or alternation with fungicides to control cucumber grey mould (Botrytis cinerea) under commercial greenhouse conditions. Plant Pathol 42:324–332

    Article  CAS  Google Scholar 

  • Evans HC, Holmes KA, Thomas KA (2003) Mycobiota of an indigenous Theobroma species (Sterculiaceae) in Ecuador: assessing its potential for biological control of cocoa diseases. Mycol Prog 2:149–160

    Article  Google Scholar 

  • Ferraz S, de Freitas LG (2004) Use of antagonistic plants and natural products. In: Chen ZX, Chen SY, Dickson DW (eds) Nematology–advances and prospectives. Nematode management and utilization, 2nd edn. CABI Publishing, Cambridge, UK, pp 931–958

    Chapter  Google Scholar 

  • Han Y, Wang Y, Bi JL, Yang XQ, Huang Y, Zhao X, Hu Y, Cai QN (2009) Constitutive and induced activities of defense-related enzymes in aphid resistant and aphid susceptible cultivars of wheat. J Chem Ecol 35:176–182

    Article  CAS  PubMed  Google Scholar 

  • Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathol 96:190–194

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    Article  Google Scholar 

  • Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathol 90:248–252

    Article  CAS  Google Scholar 

  • Khan A, Williams KL, Nevalainen HKM (2004) Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biol Control 31:346–352

    Article  CAS  Google Scholar 

  • Li HL, Yuan HX, Sun JW, Fu B, Nian GL, Hou XS, Xing XP, Sun BJ (2010) First record of the cereal cyst nematode Heterodera filipjevi in China. Plant Dis 94:1505

    Article  Google Scholar 

  • Li ZJ, Xie XY, Zhang SQ, Liang YC (2011) Negative effects of oxytetracycline on wheat (Triticum aestivum L.) growth, root activity, photosynthesis, and chlorophyll contents. Agric Sci Chi 10:1545–1553

    Article  CAS  Google Scholar 

  • Long HB, Peng H, Huang WK, Wang GF, Gao BL, Moens M, Peng DL (2012) Identification and molecular characterization of a new β-1, 4-endoglucanase gene (Ha-eng-1a) in the cereal cyst nematode Heterodera avenae. Eur J Plant Pathol 134:391–400

    Article  CAS  Google Scholar 

  • Maciá-Vicente JG, Rosso LC, Ciancio A, Jansson HB, Lopez-Llorca LV (2009) Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: effects on plant growth and disease. Ann Appl Biol 155:391–401

    Article  Google Scholar 

  • Manzanilla-Lopez RH, Kenneth E, Bridge J (2004) Plant diseases caused by nematodes. In: Chen ZX, Chen SY, Dickson DW (eds) Nematology advances and perspectives. Nematode management and utilization, 2nd edn. CAB International, Wallingford, UK, pp 646–647

    Google Scholar 

  • Manzanilla-López RH, Esteves I, Powers SJ, Kerry BR (2011) Effects of crop plants on abundance of Pochonia chlamydosporia and other fungal parasites of root-knot and potato cyst nematodes. Ann Appl Biol 159:118–129

    Article  Google Scholar 

  • Meira BE, Edna S, Yitzhak S (2006) Nematicidal activity of Chrysanthemum coronarium. Eur J Plant Pathol 114:427–433

    Article  Google Scholar 

  • Monfort E, Lopez-Llorca LV, Jansson HB, Salinas J, Park JO, Sivasithamparam K (2005) Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root rot. Soil Biol Biochem 37:1229–1235

    Article  CAS  Google Scholar 

  • Nicol JM, Rivoal R (2008) Global knowledge and its application for the integrated control and management of nematodes of wheat. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, Dordrecht, The Netherlands, pp 251–252

    Google Scholar 

  • Nicol J, Rivoal R, Taylor S, Zaharieva M (2003) Global importance of cyst (Heterodera spp.) and lesion nematodes (Pratylenchus spp.) on cereals: distribution, yield loss, use of host resistance and integration of molecular tools. Nematol Monogr Perspect 2:1–19

    Google Scholar 

  • Nicol J, Io E, Lu I, Bolat N, Rivoal R (2007) The global importance of the cereal cyst nematode (Heterodera spp.) on wheat and international approaches to its control. Commun Agric Appl Biol Sci 72:677–686

    CAS  PubMed  Google Scholar 

  • Orth B, Frei R, Itin PH, Rinaldi MG, Speck B, Gratwohl A, Widmer AF (1996) Outbreak of invasive mycoses caused by Paecilomyces lilacinus from a contaminated skin lotion. Ann Intern Med 125:799–806

    Article  CAS  PubMed  Google Scholar 

  • Papavizas GC (1985) Trichoderma and Gliocladium: biology, ecology and the potential for biocontrol. Ann Rev Phytopathol 23:23–54

    Article  Google Scholar 

  • Peng DL, Nicol JM, Li HM, Hou SY, Li HX, Chen SL, Ma P, Li HL, Riley IT (2009) Current knowledge of cereal cyst nematode (Heterodera avenae) on wheat in China. In: Riley IT, Nicol JM, Dababat AA (eds) Cereal cyst nematodes: status, research and outlook. CMMITY, Ankara, Turkey, pp 29–34

    Google Scholar 

  • Persmark L, Jansson HB (1997) Nematophagous fungi in the rhizosphere of agricultural crops. FEMS Microbiol Ecol 22:303–312

    Article  CAS  Google Scholar 

  • Rivoal R, Cook R, Evaan K (1993) Plant parasitic nematodes in temperate agriculture. CAB International, Wallingford, UK

    Google Scholar 

  • Sahebani N, Hadavi N (2008) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Soil Biol Biochem 40:2016–2020

    Article  CAS  Google Scholar 

  • Sharon E, Bar-Eyal M, Chet I, Herrera-Estrella A, Kleifeld O, Spiegel Y (2001) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Am Phytopathol Soc 91:687–693

    Article  CAS  Google Scholar 

  • Sharon E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels GJ, Spiegel Y (2007) Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118:247–258

    Article  Google Scholar 

  • Siddiqui Z, Akhtar MS (2008) Synergistic effects of antagonistic fungi and a plant growth promoting rhizobacterium, an arbuscular mycorrhizal fungus, or composted cow manure on populations of Meloydogyne incognita and growth of tomato. Biocontrol Sci Tech 18:279–290

    Article  Google Scholar 

  • Siddiqui IA, Amer-Zareen M, Zaki MJ, Shaukat SS (2001) Use of Trichoderma species in the control of Meloidogyne javanica root knot nematode in okra and mungbean. Pak J Biol Sci 4:846–848

    Article  Google Scholar 

  • Smiley RW, Whittaker RG, Gourlie JA, Easley SA, Ingham RE (2005) Plant-parasitic nematodes associated with reduced wheat yield in Oregon: Heterodera avenae. J Nematol 37:297–307

    PubMed Central  PubMed  Google Scholar 

  • Sorribas FJ, Ornat C, Galeano M, Verdejo-Lucas S (2003) Evaluation of a native and introduced isolate of Pochonia chlamydosporia against Meloidogyne javanica. Biocontrol Sci Tech 13:707–714

    Article  Google Scholar 

  • UNEP (2000) Methyl bromide alternatives for North African and Southern European countries. In: Proceedings from the Workshop on Methyl Bromide Alternatives for North African and Southern European Countries, United Nations Environment Programme, Rome, Italy, pp 8–10

  • Vu TT, Hauschild R, Sikora RA (2006) Fusarium oxysporum endophytes induced systemic resistance against Radopholus similis on banana. Nematology 8:847–852

    Article  Google Scholar 

  • Zhang FG, Yuan J, Yang XM, Cui YQ, Chen LH, Ran W, Shen QR (2013) Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368:433–444

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by Plant Protection Department of Gansu Agricultural University; Key Laboratory of Grassland Ecosystems, the Ministry of Education of China; Sino-U.S. Centers for Grazingland Ecosystems Sustainability; Gansu Hall of Province Farming Herd Biology Technology and Project of Education Department of Gansu Province; Grassland ecological System of Ministry of Education Ministry Key Laboratory Project (CY-GG-2006-013); Gansu Hall of Province Farming Herd Biology Technology (GNSW-2009-04) and Project of Education Department of Gansu Province (042-03).

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Authors and Affiliations

  1. College of Grassland Science, Gansu Agricultural University, Lanzhou, 730070, China

    Shuwu Zhang & Bingliang Xu

  2. Agriculture and Agri-Food Canada, Swift Current, SK, S9H 3X2, Canada

    Yantai Gan

  3. Key Laboratory of Grassland Ecosystems, the Ministry of Education of China, Lanzhou, 730070, China

    Shuwu Zhang & Bingliang Xu

  4. Pratacultural Engineering Laboratory of Gansu Province, Lanzhou, 730070, China

    Shuwu Zhang & Bingliang Xu

  5. Sino-U.S. Centers for Grazingland Ecosystems Sustainability, Lanzhou, 730070, China

    Shuwu Zhang & Bingliang Xu

  6. Gansu Provincial Key Lab of Arid Land Crop Science, Lanzhou, 730070, China

    Yantai Gan

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  1. Shuwu Zhang
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  2. Yantai Gan
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Correspondence to Bingliang Xu.

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Zhang, S., Gan, Y. & Xu, B. Efficacy of Trichoderma longibrachiatum in the control of Heterodera avenae . BioControl 59, 319–331 (2014). https://doi.org/10.1007/s10526-014-9566-y

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