Skip to main content

Advertisement

SpringerLink
Log in

Priming of Anti-Herbivore Defense in Tomato by Arbuscular Mycorrhizal Fungus and Involvement of the Jasmonate Pathway

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Mycorrhizas play a vital role in soil fertility, plant nutrition, and resistance to environmental stresses. However, mycorrhizal effects on plant resistance to herbivorous insects and the related mechanisms are poorly understood. This study evaluated effects of root colonization of tomato (Solanum lycopersicum Mill.) by arbuscular mycorrhizal fungi (AMF) Glomus mosseae on plant defense responses against a chewing caterpillar Helicoverpa arimigera. Mycorrhizal inoculation negatively affected larval performance. Real time RT-PCR analyses showed that mycorrhizal inoculation itself did not induce transcripts of most genes tested. However, insect feeding on AMF pre-inoculated plants resulted in much stronger defense response induction of four defense-related genes LOXD, AOC, PI-I, and PI-II in the leaves of tomato plants relative to non-inoculated plants. Four tomato genotypes: a wild-type (WT) plant, a jasmonic acid (JA) biosynthesis mutant (spr2), a JA-signaling perception mutant (jai1), and a JA-overexpressing 35S::PS plant were used to determine the role of the JA pathway in AMF-primed defense. Insect feeding on mycorrhizal 35S::PS plants led to higher induction of defense-related genes relative to WT plants. However, insect feeding on mycorrhizal spr2 and jai1 mutant plants did not induce transcripts of these genes. Bioassays showed that mycorrhizal inoculation on spr2 and jai1 mutants did not change plant resistance against H. arimigera. These results indicates that mycorrhizal colonization could prime systemic defense responses in tomato upon herbivore attack, and that the JA pathway is involved in defense priming by AMF.

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

Similar content being viewed by others

References

  • Bethlenfalvay GJ, Schüepp H (1994) Arbuscular mycorrhizas and agrosystem stability. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser Verlag, Basel, pp 117–131

    Chapter  Google Scholar 

  • Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838

    Article  PubMed  CAS  Google Scholar 

  • Cahill JF Jr, Elle E, Smith GR, Shore BH (2008) Disruption of a belowground mutualism alters interactions between plants and their floral visitors. Ecology 89:1791–1801

    Article  PubMed  Google Scholar 

  • Chellappan P, Christy SAA, Mahadevan A (2002) Multiplication of arbuscular mycorrhizal fungi on roots. In: Mukerji KG, Manoharachary C, Chamola BP (eds) Techniques in mycorrhizal studies. Kluwer Academic Publishers, Dordrecht, pp 285–297

    Chapter  Google Scholar 

  • Christensen SA, Nemchenko A, Borrego E, Murray I, Sobhy IS, Bosak L, Deblasio S, Erb M, Robert CA, Vaughn KA, Herrfurth C, Tumlinson J, Feussner I, Jackson D, Turlings TC, Engelberth J, Nansen C, Meeley R, Kolomiets MV (2013) The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J 74:59–73

    Article  PubMed  CAS  Google Scholar 

  • 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 (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071

    Article  PubMed  CAS  Google Scholar 

  • de Vos M, van Oosten VR, van Poecke RMP, van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux JP, van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937

    Article  PubMed  Google Scholar 

  • Douds DD, Millner P (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric Ecosyst Environ 74:77–93

    Article  Google Scholar 

  • Elsen A, Gervacio D, Swennen R, de Waele D (2008) AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256

    Article  PubMed  CAS  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785

    Article  PubMed  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  PubMed  CAS  Google Scholar 

  • Frost CJ, Appel HM, Carlson JE, de Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498

    Article  PubMed  Google Scholar 

  • Gange AC (1996) Reduction in vine weevil larval growth by mycorrhizal fungi. Mitt Biol Bund Forst 316:56–60

    Google Scholar 

  • Gange AC (2001) Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol 150:611–618

    Article  Google Scholar 

  • Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87

    Article  Google Scholar 

  • Gange AC, Brown VK, Sinclair GS (1994) Reduction of black vine weevil growth by vesicular-arbuscular mycorrhizal fungi. Entomol Exp Appl 70:115–119

    Article  Google Scholar 

  • Gange AC, Bower E, Brown VK (1999) Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120:123–131

    Article  Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    Article  PubMed  CAS  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  PubMed  CAS  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 8:101–110

    Article  Google Scholar 

  • Heil M, Silvabueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 140:5467–5472

    Article  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  PubMed  CAS  Google Scholar 

  • Howe GA, Ryan CA (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153:1411–1421

    PubMed  CAS  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91

    Article  PubMed  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292

    Article  PubMed  Google Scholar 

  • Kiefer E, Heller W, Ernst D (2000) A simple and efficient protocol for isolation of functional RNA from plant tissues rich in secondary metabolites. Plant Mol Biol Rep 18:33–39

    Google Scholar 

  • Kim J, Felton GW (2013) Priming of antiherbivore defensive responses in plants. Insect Sci 20:273–285

    Article  CAS  Google Scholar 

  • Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097

    Article  PubMed  Google Scholar 

  • León-Morcillo RJ, Angel J, Martín-Rodríguez, Vierheilig H, Ocampo JA, García-Garrido JM (2012) Late activation of the 9-oxylipin pathway during arbuscular mycorrhiza formation in tomato and its regulation by jasmonate signalling. J Exp Bot 63:545–3558

  • Li CY, Liu GH, Xu CC, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses 2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Verhage A, García-Andrade J, García JM, Azcon-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Gianinazzi S, Barea JM, Gianinazzi-Pearson V (eds) Mycorrhizas - functional processes and ecological impact. Springer- Verlag, Berlin Heidelberg, pp 123–135

    Chapter  Google Scholar 

  • Ramadan A, Muroi A, Arimura G (2011) Herbivore-induced maize volatiles serve as priming cues for resistance against post-attack by the specialist armyworm Mythimna separata. J Plant Interact 6:155–158

    Article  CAS  Google Scholar 

  • Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:854–863

    Article  PubMed  CAS  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  PubMed  CAS  Google Scholar 

  • Schaller F, Schaller A, Stintz A (2005) Biosynthesis and metabolism of jasmonates. J Plant Growth Regul 23:179–199

    Google Scholar 

  • Slaughter A, Daniela X, Flors V, Luna E, Hohn B, Mauch-Mani B (2012) Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20

    Article  CAS  Google Scholar 

  • Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5:e13324

    Article  PubMed  Google Scholar 

  • Song YY, Wang RL, Wei XC, Lu YJ, Wu GZ, Su YJ, Zeng RS (2011) Mechanism of tomato plants enhanced disease resistance against early blight primed by arbuscular mycorrhizal fungus Glomus versiforme. Chin J Appl Ecol 22:2316–2324 (in Chinese)

    CAS  Google Scholar 

  • Ton J, D’alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2006) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26

    Article  PubMed  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 365:69–72

    Google Scholar 

  • van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607

    Article  PubMed  Google Scholar 

  • van Wees SCM, van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  PubMed  Google Scholar 

  • Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562

    Article  PubMed  Google Scholar 

  • Waldbauer GP, Cohen RW, Friedman S (1984) An improved procedure for laboratory rearing of the corn earworm, Heliothis zea (Lepidoptera: Noctuidae). Great Lakes Entomol 17:113–118

    Google Scholar 

  • Wooley SC, Paine TD (2011) Infection by mycorrhizal fungi increases natural enemy abundance on tobacco (Nicotiana rustica). Environ Entomol 40:36–41

    Article  PubMed  Google Scholar 

  • Worrall D, Holroyd GH, Moore JP, Glowacz M, Croft P, Taylor JE, Paul ND, Roberts MR (2012) Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytol 193:770–778

    Article  PubMed  CAS  Google Scholar 

  • Zeng RS (2006) Disease resistance in plants through mycorrhizal fungi induced allelochemicals. In: Inderjit, Mukerji KG (eds) Allelochemicals: biological control of plant pathogens and diseases. Springer, Dordrecht, pp 181–192

    Chapter  Google Scholar 

  • Zvereva EL, Kozlov MV, Niemela P, Haukioja E (1997) Delayed induced resistance and increase in leaf fluctuating asymmetry as responses of Salix borealis to insect herbivory. Oecologia 109:368–373

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the National 973 Program of China (2011CB100400), National Natural Science Foundation of China (31070388, 31028018, 31100286), Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2010), Guangdong Natural Science Foundation of China (S2011040004336), China Postdoctoral Science Foundation (201104341, 20100480762), and Ph.D. Foundation of the Ministry of Education of China (20104404110004).

Author information

Authors and Affiliations

  1. State Key Laboratory of Conservation and Utilization of Subtropical Agro-bioresources, South China Agricultural University, Wushan, Guangzhou, 510642, China

    Yuan Yuan Song, Mao Ye, Rui Long Wang, Xiao Chen Wei, Shi Ming Luo & Ren Sen Zeng

  2. Key Laboratory of Tropical Agro-environment of Ministry of Agriculture of China, South China Agricultural University, Wushan, Guangzhou, 510642, China

    Yuan Yuan Song, Mao Ye, Rui Long Wang, Xiao Chen Wei, Shi Ming Luo & Ren Sen Zeng

  3. Institute of Genetics and Developmental Biology of the Chinese Academy of Sciences, Beijing, 100101, China

    Yuan Yuan Song & Chuan You Li

Authors
  1. Yuan Yuan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mao Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chuan You Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rui Long Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiao Chen Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shi Ming Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ren Sen Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ren Sen Zeng.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, Y.Y., Ye, M., Li, C.Y. et al. Priming of Anti-Herbivore Defense in Tomato by Arbuscular Mycorrhizal Fungus and Involvement of the Jasmonate Pathway. J Chem Ecol 39, 1036–1044 (2013). https://doi.org/10.1007/s10886-013-0312-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-013-0312-1

Keywords

Search

Navigation