Symbiosis

, Volume 65, Issue 2, pp 65–74 | Cite as

Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect

  • Gitika Shrivastava
  • Bonnie H. Ownley
  • Robert M. Augé
  • Heather Toler
  • Mary Dee
  • Andrea Vu
  • Tobias G. Köllner
  • Feng Chen
Article

Abstract

Terpenoids serve as an important form of chemical defense for plants. A greenhouse study was conducted to investigate the effects of two types of beneficial fungi on the accumulation of terpenoids in tomato plants and on defense against herbivorous insects. Control tomato plants without any fungal inoculation constitutively made monoterpenes and sesquiterpenes. Inoculation by Rhizophagus intraradices (N.C. Schenck & G.S. Sm.) C. Walker & A. Schüßler, an arbuscular mycorrhizal fungus, and Beauveria bassiana (Bals.-Criv.) Vuill., an endophytic entomopathogenic fungus, individually or in combination, led to enhanced levels of monoterpenes and sesquiterpenes, which included new monoterpenes not found in the control plants. Herbivore feeding assays using beet armyworm (Spodoptera exigua Hübner) were performed to compare the levels of defense in tomato plants with or without fungal inoculation. Beet armyworm larvae fed on tomato plants inoculated by either or both types of fungi were found to gain significantly less weight than those fed on control non-inoculated plants. This suggests that fungus-inoculated tomato plants had a stronger defense response against beet armyworm than control plants, which may be partly attributed to the difference in the levels of terpenoids.

Keywords

Beauveria bassiana Chemical profiling Glomus/Rhizophagus intraradices Insect herbivory Spodoptera exigua 

Notes

Acknowledgments

This project was supported by the University of Tennessee Institute of Agriculture.

References

  1. Ahern JR, Whitney KD (2014) Sesquiterpene lactone stereochemistry influences herbivore resistance and plant fitness in the field. Ann Bot 113:731–740CrossRefPubMedCentralPubMedGoogle Scholar
  2. Aimé S, Alabouvette C, Steinberg C, Olivain C (2013) The endophytic strain Fusarium oxysporum Fo47: a good candidate for priming the defense responses in tomato roots. Mol Plant Microbe Interact 26:918–926CrossRefPubMedGoogle Scholar
  3. Akiyama K, Hayashi H (2002) Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots. Biosci Biotechnol Biochem 66:762–769CrossRefPubMedGoogle Scholar
  4. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  5. Augé RM, Saxton AM, Toler HD (2014) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24CrossRefPubMedGoogle Scholar
  6. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778CrossRefPubMedGoogle Scholar
  7. Bergougnoux V (2014) The history of tomato: from domestication to biopharming. Biotechnol Adv 32:170–189CrossRefPubMedGoogle Scholar
  8. Borowicz VA (2013) The impact of arbuscular mycorrhizal fungi on plant growth following herbivory: a search for pattern. Acta Oecol 52:1–9CrossRefGoogle Scholar
  9. Brewer MJ, Trumble JT, Alvarado-Rodriguezi B, Chaney WE (1990) Beet armyworm (Lepidoptera: Noctuidae) adult and larval susceptibility to three insecticides in managed habitats and relationship to laboratory selection for resistance. J Econ Entomol 83:2136–2146CrossRefGoogle Scholar
  10. Broughton S, Harrison J (2012) Evaluation of monitoring methods for thrips and the effect of trap colour and semiochemicals on sticky trap capture of thrips (Thysanoptera) and beneficial insects (Syrphidae, Hemerobiidae) in deciduous fruit trees in Western Australia. Crop Prot 42:156–163CrossRefGoogle Scholar
  11. Brunetti C, George RM, Tattini M, Field K, Davey MP (2013) Metabolomics in plant environmental physiology. J Exp Bot 64:4011–4020CrossRefPubMedGoogle Scholar
  12. Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defense-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592CrossRefPubMedGoogle Scholar
  13. Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2–9CrossRefGoogle Scholar
  14. Chen F, Al-Ahmad H, Joyce B, Zhao N, Köllner TG, Degenhardt J, Stewart CN (2009a) Within-plant distribution and emission of sesquiterpenes from Copaifera officinalis. Plant Physiol Biochem 47:1017–1023CrossRefPubMedGoogle Scholar
  15. Chen F, Liu CJ, Tschaplinski TJ, Zhao N (2009b) Genomics of secondary metabolism in Populus: interactions with biotic and abiotic environments. Crit Rev Plant Sci 28:375–392CrossRefGoogle Scholar
  16. Chen H, Stout MJ, Qian Q, Chen F (2012) Genetic, molecular and genomic basis of rice defense against insects. Crit Rev Plant Sci 31:74–91CrossRefGoogle Scholar
  17. Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany-Botanique 92:149–160CrossRefGoogle Scholar
  18. Faeth SH, Fagan WF (2002) Fungal endophyte: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42:360–368CrossRefPubMedGoogle Scholar
  19. Falara V, Akhtar TA, Nguyen TT, Spyropoulou EA, Bleeker PM, Schauvinhold I, Matsuba Y, Bonini ME, Schilmiller AL, Last RL, Schuurink RC, Pichersky E (2011) The tomato terpene synthase gene family. Plant Physiol 157:770–789CrossRefPubMedCentralPubMedGoogle Scholar
  20. Fester T, Hause B, Schmidt D, Halfmann K, Schmidt J, Wray V, Hause G, Strack D (2002) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol 43:256–265CrossRefPubMedGoogle Scholar
  21. Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker S (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843CrossRefPubMedCentralPubMedGoogle Scholar
  22. Forgy D (2012) Arbuscular mycorrhizal fungi can benefit heavy metal tolerance and phytoremediation. Nat Sci Educ 41:23–26Google Scholar
  23. Gange AC, Brown VK, Aplin DM (2003) Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol Lett 6:1051–1055CrossRefGoogle Scholar
  24. Gehring C, Bennett A (2009) Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environ Entomol 38:93–102CrossRefPubMedGoogle Scholar
  25. Gómez-Vidal S, Salinas J, Tena M, Lopez-Llorca LV (2009) Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi. Electrophoresis 30:2996–3005CrossRefPubMedGoogle Scholar
  26. Griffin MR (2007) Beauveria bassiana, a cotton endophyte with biocontrol activity against seedling disease. Dissertation, University of Tennessee, Knoxville, TennesseeGoogle Scholar
  27. Gualandi RJ, Augé RM, Kopsell DA, Ownley BH, Chen F, Toler HD, Dee MM, Gwinn KD (2014) Fungal mutualists enhance growth and phytochemical content in Echinacea purpurea. Symbiosis 63:111–121CrossRefGoogle Scholar
  28. Guerrieri E, Lingua G, Digilio MC, Massa N, Berta G (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29:753–756CrossRefGoogle Scholar
  29. Hare JD, Andreadis TG (1983) Variation in the susceptibility of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) when reared on different host plants to the fungal pathogen, Beauveria bassiana in the field and laboratory. Environ Entomol 12:1892–1897CrossRefGoogle Scholar
  30. Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6:643–654CrossRefGoogle Scholar
  31. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Ann Rev Entomol 54:323–342CrossRefGoogle Scholar
  32. Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110CrossRefPubMedGoogle Scholar
  33. Jung SC, Martínez-Medina A, López-Ráez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664CrossRefPubMedGoogle Scholar
  34. Kang JH, McRoberts J, Shi F, Moreno JE, Jones AD, Howe GA (2014) The flavonoid biosynthetic enzyme chalcone isomerase modulates terpenoid production in glandular trichomes of tomato. Plant Physiol 164:1161–1174CrossRefPubMedCentralPubMedGoogle Scholar
  35. Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097CrossRefPubMedGoogle Scholar
  36. Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecol Lett 8:61–69CrossRefGoogle Scholar
  37. Lawo NC, Weingart GJF, Schuhmacher R, Forneck A (2011) The volatile metabolome of grapevine roots: first insights into the metabolic response upon phylloxera attack. Plant Physiol Biochem 49:1059–1063CrossRefPubMedCentralPubMedGoogle Scholar
  38. Leitner M, Kaiser R, Hause B, Boland W, Mithöfer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101CrossRefPubMedCentralPubMedGoogle Scholar
  39. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544CrossRefPubMedGoogle Scholar
  40. Lucas JA (1999) Plant immunisation: from myth to SAR. Pestic Sci 55:193–196CrossRefGoogle Scholar
  41. Maya MA, Matsubara Y (2013) Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza 23:381–390CrossRefPubMedGoogle Scholar
  42. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 15:490–501Google Scholar
  43. Megido RC, Haubruge E, Verheggen FJ (2014) Pheromone-based management strategies to control the tomato leafminer, tuta absoluta (Lepidoptera: Gelechiidae): a review. Biotechnol Agron Soc Environ 17:475–482Google Scholar
  44. Migiro LN, Maniania NK, Chabi-Olaye A, Vandenberg J (2010) Pathogenicity of entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana (Hypocreales:Clavicipitaceae) isolates to the adult pea leafminer (Diptera: Agromyzidae) and prospects of an autoinoculation device for infection in the field. Environ Entomol 39:468–475CrossRefPubMedGoogle Scholar
  45. Murray M, Thompson W (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321CrossRefPubMedCentralPubMedGoogle Scholar
  46. Navia-Giné WG, Gomez SK, Yuan J, Chen F, Korth KL (2009) Insect-induced gene expression at the core of volatile terpene release in Medicago truncatula. Plant Signal Behav 4:639–641CrossRefPubMedCentralPubMedGoogle Scholar
  47. Onstad DW (2014) Insect resistance management: biology, economics, and prediction, 2nd edn. Elsevier, NYGoogle Scholar
  48. Ownley BH, Griffin MR (2012) Dual biological control of insect pests and plant pathogens with fungi in the order Hypocreales. In: Brar SK (ed) Biocontrol: management, processes, and challenges. Nova, Hauppauge, pp 133–152Google Scholar
  49. Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveria bassiana: endophytic colonization and plant disease control. J Invertebr Pathol 98:267–270CrossRefPubMedGoogle Scholar
  50. Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 55:113–128CrossRefGoogle Scholar
  51. Phillips JM, Hayman DS (1970) Improved procedure for clearing roots, and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  52. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51CrossRefPubMedGoogle Scholar
  53. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398CrossRefPubMedGoogle Scholar
  54. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534CrossRefPubMedGoogle Scholar
  55. Quesada-Moraga E, Muñoz-Ledesma F, Santiago-Álvarez C (2009) Systemic protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environ Entomol 38:723–730CrossRefPubMedGoogle Scholar
  56. Rapparini F, Llusia J, Penuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122CrossRefPubMedGoogle Scholar
  57. Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531CrossRefPubMedGoogle Scholar
  58. Reid ML, Purcell JRC (2011) Condition-dependent tolerance of monoterpenes in an insect herbivore. Arthropod Plant Interact 5:331–337CrossRefGoogle Scholar
  59. Ruiz-Lozano JM, Porcel R, Azcon C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044CrossRefPubMedGoogle Scholar
  60. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  61. Schausberger P, Peneder S, Jurschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26:441–449CrossRefGoogle Scholar
  62. Shrivastava G, Rogers M, Wszelaki A, Panthee DR, Chen F (2010) Plant volatiles-based insect pest management in organic farming. Crit Rev Plant Sci 29:123–133CrossRefGoogle Scholar
  63. Sivasundaram V, Rajendran L, Muthumeena K, Suresh S, Raguchander T, Samiyappan R (2008) Effect of talc-formulated entomopathogenic fungus Beauveria against leaffolder (Cnaphalocrosis medinalis) in rice. World J Microbiol Biotechnol 24:1123–1132CrossRefGoogle Scholar
  64. Smith SE, Read D (2008) Mycorrhizal symbiosis. Elsevier, AmsterdamGoogle Scholar
  65. Song YY, Ye M, Wang RL, Wei XC, Luo SM, Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol 39:1036–1044CrossRefPubMedGoogle Scholar
  66. Spyropoulou EA, Haring MA, Schuurink RC (2014) Expression of terpenoids 1, a glandular trichome-specific transcription factor from tomato that activates the terpene synthase 5 promoter. Plant Mol Biol 84:345–357CrossRefPubMedGoogle Scholar
  67. Stökl J, Brodmann J, Dafni A, Ayasse M, Hansson BS (2011) Smells like aphids: orchid flowers mimic aphid alarm pheromones to attract hoverflies for pollination. Proc R Soc B 278:1216–1222CrossRefPubMedCentralPubMedGoogle Scholar
  68. Toussaint JP, Kraml M, Nell M, Smith SE, Smith FA, Steinkellner S, Schmiderer C, Vierheilig H, Novak J (2008) Effect of Glomus mosseae on concentrations of rosmarinic and caffeic acids and essential oil compounds in basil inoculated with Fusarium oxysporum f. sp. basilica. Plant Pathol 57:1109–1116CrossRefGoogle Scholar
  69. Vannette RL, Hunter MD (2009) Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agric For Entomol 11:351–358CrossRefGoogle Scholar
  70. Vannette RL, Hunter MD, Rasmann S (2013) Arbuscular mycorrhizal fungi alter above-and below-ground chemical defense expression differentially among Asclepias species. Front Plant Sci 4:361CrossRefPubMedCentralPubMedGoogle Scholar
  71. Vey A, Hoagland RE, Butt TM (2001) Toxic metabolites of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CAB International, NY, pp 311–346CrossRefGoogle Scholar
  72. Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer M, Bally R, Moenne-Loccoz Y, Comte G (2012) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356:151–163CrossRefGoogle Scholar
  73. Walter MH, Fester T, Strack D (2000) Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the ‘yellow pigment’ and other apocarotenoids. Plant J 21:571–578CrossRefPubMedGoogle Scholar
  74. Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243–254CrossRefPubMedGoogle Scholar
  75. Wezel A, Casagrande M, Celette F, Vian JF, Ferrer A, Peigne J (2014) Agroecological practices for sustainable agriculture. A review. Agron Sustain Dev 34:1–20CrossRefGoogle Scholar
  76. Yuan JS, Köllner TG, Wiggins G, Grant J, Degenhardt J, Chen F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J 55:491–503CrossRefPubMedGoogle Scholar
  77. Zhao N, Wang GD, Norris A, Chen XL, Chen F (2013) Studying plant secondary metabolism in the age of genomics. Crit Rev Plant Sci 32:369–382CrossRefGoogle Scholar
  78. Zhu XC, Song FB, Xu HW (2010) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331:129–137CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Gitika Shrivastava
    • 1
  • Bonnie H. Ownley
    • 2
  • Robert M. Augé
    • 1
  • Heather Toler
    • 1
  • Mary Dee
    • 2
  • Andrea Vu
    • 2
  • Tobias G. Köllner
    • 3
  • Feng Chen
    • 1
  1. 1.Department of Plant SciencesUniversity of TennesseeKnoxvilleUSA
  2. 2.Department of Entomology and Plant PathologyUniversity of TennesseeKnoxvilleUSA
  3. 3.Department of BiochemistryMax Planck Institute for Chemical EcologyJenaGermany

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