Advertisement

Plant and Soil

, Volume 352, Issue 1–2, pp 233–241 | Cite as

Induction of metabolite organic compounds by mutualistic endophytic fungi to reduce the greenhouse whitefly Trialeurodes vaporariorum (Westwood) infection on tomato

  • Roy Donald Menjivar
  • Jose Alfonso Cabrera
  • Joachim Kranz
  • Richard Alexander Sikora
Regular Article

Abstract

Background and aims

Six mutualistic endophytic fungi that are known to colonize the endorhiza have shown biological control properties against plant-parasitic nematodes. In this study we aim to investigate the potential of these endophytic fungi to reduce the phloem-feeding insect Trialeurodes vaporariorum (Westwood) on tomato.

Methods

To determine the host plant choice of T. vaporariorum, the total number of insects present on each plant was counted daily for 10 days, and then the second leaf below the shoot apex were examined for its chlorophyll content index (CCI).To separate and quantify the active compounds produced in the tomato leaves, a reversed phase high liquid chromatography (RP-HPLC) analysis was performed.

Principle results

A greenhouse choice test showed that Trichoderma atroviride strain MT-20, T. atroviride strain S-2 and Fusarium oxysporum strain 162 (Fo162) reduced the number of greenhouse whiteflies fifty percent when compared to the untreated control during ten days after insect release. The highest level of biocontrol activity was attained with Fo162. The strains MT20, S-2, and Fo162 all demonstrated acropedal induction of resistance to the insects. The isolate Fusarium sp. strain Bonn-7 enhanced plant growth. The negative effect on insect attraction to the leaves of the endophyte treated plants was not associated with leaf altered chlorophyll content. RP-HPLC analysis revealed that inoculation of the fungus Fo162 induced a change in the accumulation of specific organic compounds in the tomato leaves that could be the cause of insect repellence.

Conclusions

This study demonstrated the high potential of mutualintic endophytic fungi, in particular of Fo162, to induce resistance in tomato against the phloemfeeding T. vaporariorum.

Keywords

Induced systemic resistance Metabolites Plant-insect interaction Acropedal 

Notes

Acknowledgements

The authors wish to thank the German Academic Exchange Service (DAAD, Bonn) for financial support of the primary author for doctoral research at the University of Bonn, Germany.

Supplementary material

11104_2011_991_MOESM1_ESM.doc (269 kb)
ESM 1 (DOC 269 kb)
11104_2011_991_MOESM2_ESM.doc (146 kb)
ESM 2 (DOC 146 kb)

References

  1. Ajlan AM, Potter DA (1991) Does immunization of cucumber against anthracnose by Colletotrichum lagenarium affect host suitability for arthropods? Entomol Exp Appl 58:83–91CrossRefGoogle Scholar
  2. Andersen RA, Hamilton-Kemp TR, Hildebrand DF, McCracken CT Jr, Collins RW, Fleming PD (1994) Structure-antifungal activity relationships among volatile C6 and C9 aliphatic aldehydes, ketones and alcohols. J Agr Food Chem 42:1563–1568CrossRefGoogle Scholar
  3. Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91–111PubMedGoogle Scholar
  4. Baldwin IT, Halitschke H, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant–insect interactions. Plant Biol 4:351–358Google Scholar
  5. Benhamou N (1996) Elicitor-induced plant defence pathways. Trends Plant Sci 1:233–240Google Scholar
  6. Benhamou N, Garand C (2001) Cytological analysis of defence related mechanisms induced in pea root tissues in response to colonization by nonpathogenic Fusarium oxysporum Fo47. Phytopathology 91:730–740PubMedCrossRefGoogle Scholar
  7. Bentz J, Reeves J, Barbosa P, Francis B (1995) Within-plant variation in nitrogen and sugar content of poinsettia and its effects on the oviposition pattern, survival, and development of Bemisia argentifolii (Homoptera: Aleyrodidae). Environ Entomol 24:271–277Google Scholar
  8. Byrne DN, Cohen AC, Draeger EA (1990) Water uptake from plant tissue by the egg pedicel of the greenhouse whitefy. Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae). Can J Zool 68:1193–1195CrossRefGoogle Scholar
  9. Cañizares Monteros CA (2003) Estudio sobre poblaciones de hongos endofíticos provenientes de suelos supresitos al nematodo barrenador Radopholus similis (Cobb) Thorne en plantaciones de plátano en la zona de Talamanca, Costa Rica. M.Sc. Thesis, CATIE, Turrialba, Costa RicaGoogle Scholar
  10. Cardoza YJ, Alborn HT, Tumlinson JH (2002) In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28:161–174PubMedCrossRefGoogle Scholar
  11. Chen J, McAuslane HJ, Carle RB, Webb SE (2004) Impact of Bemisia argentifolii (Homoptera: Auchenorrhyncha: Aleyrodidae) infestation and squash silver leaf disorder on zucchini yield and quality. J Econ Entomol 97:2083–2094PubMedCrossRefGoogle Scholar
  12. Cohen S, Antignus Y (1982) A noncirculative whitefly-borne virus affecting tomatoes in Israel. Phytoparasitica 10:101–109CrossRefGoogle Scholar
  13. Coombe PE (1981) Wavelength specific behaviour of the whitefly Trialeurodes vaporariorum (Homoptera: Aleyrodidae). J Comp Physiol 144:83–90CrossRefGoogle Scholar
  14. Coombe PE (1982) Visual behaviour of the greenhouse whitefly T. vaporariorum. Physiol Entomol 7:243–251CrossRefGoogle Scholar
  15. Dababat AA, Sikora RA (2007a) Influence of the mutualistic endophyte Fusarium oxysporum 162on Meloidogyne incognita attraction and invasion. Nematology 9:771–776CrossRefGoogle Scholar
  16. Dababat AA, Sikora RA (2007b) Importance of application time and inoculum density of Fusarium oxysporum 162 for biological control of Meloidogyne incognita on tomato. Nematropica 37:267–276Google Scholar
  17. Dababat AA, Sikora RA (2007c) Induced resistance by the mutualistic endophyte, Fusarium oxysporum strain 162, toward Meloidogyne incognita on tomato. Biocont Sci Technol 17:969–975CrossRefGoogle Scholar
  18. De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar induced nocturnal plant volatiles repel nonspecific females. Nature 410:577–580PubMedCrossRefGoogle Scholar
  19. Dicke M, van Poecke RMP, de Boer JG (2003) Inducible indirect defence of plants: from mechanisms to ecological functions. Basic Appl Ecol 4:27–42CrossRefGoogle Scholar
  20. Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902PubMedCrossRefGoogle Scholar
  21. Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem Physiol 32:3–37CrossRefGoogle Scholar
  22. Farmer EE, Almeras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378PubMedCrossRefGoogle Scholar
  23. Fransen JJ (1990) Natural enemies of whiteflies, fungi. In: Gerling D (ed) Whiteflies: their bionomics, pest status and management. Intercept, Andover, pp 187–210Google Scholar
  24. Gregg A (2008) Direct Defences in Plants and Their Induction by wounding and Insect Herbivores, p 7. In Schaller A. (Ed.), Induced Plant Resistance to Herbivore 2008. Springer Science Business Media B.V.Google Scholar
  25. Halitschke R, Schittko U, PohnertG BW, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717PubMedCrossRefGoogle Scholar
  26. Hallmann J, Sikora RA (1994a) Occurrence of planr parasitic nematode and nonpathogenic species of Fusarium in tomato plant in Kenia and their role as mutualistic synergists for biological control of root nematodes. Int J Pest Manag 40:321–325CrossRefGoogle Scholar
  27. Hallmann J, Sikora RA (1994b) Influence of Fusarium oxysporum a mutualistic fungal endophytic on Meloidogyne incognita of tomato. J Plant Dis Protect 101(5):475–481Google Scholar
  28. Hallmann J, Sikora RA (1996) Toxicity of fungal endophyte secondary metabolites to plant parasit nematodes and soil borne plant pathogenic fungi. Eur J Plant Pathol 102:155–162CrossRefGoogle Scholar
  29. Henneberry TJ, Toscano NC, Perring TM, Faust RM (1997) Preface. In: Henneberry TJ, Toscano NC, Perring TM, Faust RM (eds) Silverleaf Whitefly, 1997 supplement to the five-year national research and action plan: progress, review, technology transfer, and new research and action plan (1997–2001). USDA, ARS, Washington, DC, p. 2Google Scholar
  30. Henneberry TJ, Jech LF, Hendrix DL, Steele T (2000) Bemisia argentifolii (Homoptera: Aleyrodidae) honeydew and honeydew sugar relationships to sticky cotton. Southwest Entomol 25:1–14Google Scholar
  31. Hodges GS, Evans GA (2005) An identification guide to the whiteflies (Hemiptera: Aleyrodidae) of the Southeastern United States. Florida Entomologist 88(4):518–534CrossRefGoogle Scholar
  32. Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237Google Scholar
  33. Jauset AM, Sarasua MJ, Avilla J, Albajes R (1998) The impact of nitrogen fertilization of tomato on feeding site selection and oviposition by Trialeurodes vaporariorum. Entomol Exp Appl 86:175–182CrossRefGoogle Scholar
  34. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, 319 pGoogle Scholar
  35. Kessler A, Baldwin IT (2001) Defensive function of herbivoreinduced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  36. Le HTT, Padghamb JL, Sikora RA (2009) Biological control of the rice rootknot nematode Meloidogyne graminicola on rice, using endophytic and rhizosphere fungi. Int J Pest Manag 55:31–36CrossRefGoogle Scholar
  37. Mendoza A, Sikora A (2008) Biological control of Radopholus similis in banana by combined application of the mutualistic endophyte Fusarium oxysporum strain 162, the egg pathogen Paecilomyces lilacinus strain 251 and the antagonistic bacteria Bacillus firmus. Nematropica 37:203–213Google Scholar
  38. Meneses Hérnandez A (2003) Utilización de hongos específicos para el control biológico del nematodo barrenador Radopholus similis (Cobb). M.Sc. Thesis, CATIE, Turrialba, Costa RicaGoogle Scholar
  39. Merkx-Jacques M, Bede JC (2004) Caterpillar salivary enzymes: “eliciting” a response. Phytoprotection 85:33–37Google Scholar
  40. Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168PubMedCrossRefGoogle Scholar
  41. Niinemets U, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9:180–186PubMedCrossRefGoogle Scholar
  42. Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331PubMedCrossRefGoogle Scholar
  43. Pocasangre LE, Menjivar RD, zum Felde A, Riveros AS, Rosales FE, Sikora RA (2006) Hongos endofıticos como agentes biológicos de control de fitonematodos en banano. In: Proceedings of the XVII ACROBAT International Congress, vol. 1. Joinville, Santa Catarina, Brazil, pp 249–254Google Scholar
  44. Schmelz EA, Alborn HT, Tumlinson JH (2001) The influence of intact plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays. Planta 214:171–179PubMedCrossRefGoogle Scholar
  45. Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235CrossRefGoogle Scholar
  46. Turlings TCJ, Wackers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Carde RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 21–75CrossRefGoogle Scholar
  47. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253PubMedCrossRefGoogle Scholar
  48. Vaishampayan SM, Waldbauer GP, Kogan M (1975) Visual and olfactory responses in orientation to plants by the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Entomol Exp Appl 18:412–422CrossRefGoogle Scholar
  49. Van lenteren JC (2000) A greenhouse without pesticides: fact or fantasy? Crop Prot 29:375–384CrossRefGoogle Scholar
  50. van Poecke RMP, Dicke M (2004) Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biol 6:387–401PubMedCrossRefGoogle Scholar
  51. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci USA 98:8139–8144PubMedCrossRefGoogle Scholar
  52. Vernon RS, Gillespie DR (1990) Response of Frankliniella occidentalis (Thysanoptera: Thripidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) to fluorescent traps in a cucumber greenhouse. J Entomol Soc Br Columbia 87:38–41Google Scholar
  53. Vidal S (1996) Changes in suitability of tomato for whiteflies mediated by a non-pathogenic endophytic fungus. Entomol Exp Appl 80:272–274CrossRefGoogle Scholar
  54. Vu TT, Hauschild R, Sikora RA (2006) Fusarium oxysporum endophytes induced systemic resistance against Radopholus similis on banana. Nematology 8:847–852CrossRefGoogle Scholar
  55. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  56. Walters D, Heil M (2007) Cost and trade offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17CrossRefGoogle Scholar
  57. Yee WL, Toscano NC, Chu CC, Henneberry TJ, Nichols RL (1996) Bemisia argentifolii (Homoptera: Aleyrodidae) action thresholds and cotton photosynthesis. Environ Entomol 25:1267–1273Google Scholar
  58. Yee WL, Toscano NC, Hendrix DL, Henneberry TJ (1998) Effect of insecticide applications on Bemisia argentifolii (Homoptera: Aleyrodidae) densities and honeydew production. Environ Entomol 27:22–32Google Scholar
  59. zum Felde AKV (2002) Screening of Endophytic Fungi from Banana (Musa) for Antagonistic Effects towards the Burrowing Nematode, Radopholus similis (Cobb) Thorne. Thesis M. Sc. Bonn, Germany. Alemania. Universität BonnGoogle Scholar
  60. zum Felde A, Pocasangre LE, Cañizares Monteros CA, Sikora RA, Rosales FE, Riveros AS (2006) Effects of combined inoculations of endophytic fungi on biocontrol of the burrowing nematode (Radopholus similis) in banana. InfoMusa 15(1–2):12–18Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Roy Donald Menjivar
    • 1
  • Jose Alfonso Cabrera
    • 1
  • Joachim Kranz
    • 1
  • Richard Alexander Sikora
    • 1
  1. 1.Phytopathology and Nematology in Soil Ecosystems, Institute of Crop Science and Resource Conservation INRESUniversity of BonnBonnGermany

Personalised recommendations