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Positive effects of root-knot nematodes (Meloidogyne incognita) on nitrogen availability do not outweigh their negative effects on fitness in Nicotiana attenuata

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Abstract

Aims

Root herbivory incurs fitness costs, but herbivory by nematodes can additionally increase nutrient availability mediated by enhanced root exudation and soil microbial activity and change plant susceptibility to aboveground herbivores due to systemic changes in plant defence. We hypothesized that such positive indirect effects may outweigh the negative direct effects of root herbivory by nematodes on plant performance.

Methods

We tested the effects of transient (3 weeks) and continuous (11 weeks) belowground herbivory by root-knot nematodes (Meloidogyne incognita) on the biomass, nitrogen levels, and reproductive output of Nicotiana attenuata, and its interaction with a specialist aboveground herbivore (Manduca sexta) in a greenhouse study.

Results

Continuous nematode herbivory caused an increase in shoot biomass and enhanced nitrogen levels in roots, shoots and seeds, but reduced the reproductive output of N. attenuata. Short-term, transient nematode herbivory had no effects. Feeding by the aboveground herbivore reduced reproductive output and increased seed nitrogen content. Nicotine levels in leaves and the plant interaction with M. sexta were not influenced by nematode herbivory.

Conclusion

In summary, only continuous nematode herbivory indirectly increased nitrogen availability and caused resource sequestration to the shoots; however, this effect was not strong enough to outweigh the direct fitness costs of nematode herbivory.

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References

  • Baldwin IT (1988) Short-term damage-induced increases in tobacco alkaloids protect plants. Oecologia 75:367–370

    Article  Google Scholar 

  • Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco. J Chem Ecol 15:1661–1680

    Article  CAS  PubMed  Google Scholar 

  • Baldwin IT, Halitschke R, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant–insect interactions. Curr Opin Plant Biol 4:351–358

    Article  CAS  PubMed  Google Scholar 

  • Bardgett RD, Cook R, Yeates GW, Denton CS (1999) The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212:23–33

    Article  CAS  Google Scholar 

  • Castagnone-Sereno P, Danchin EGJ, Perfus-Barbeoch L, Abad P (2013) Diversity and evolution of root-knot nematodes, genus meloidogyne: new insights from the genomic era. Annu Rev Phytopathol 51:203–220

    Article  CAS  PubMed  Google Scholar 

  • Davis EL, Rich JR (1987) Nicotine content of tobacco roots and toxicity to Meloidogyne incognita. J Nematol 19:23–29

    PubMed Central  CAS  PubMed  Google Scholar 

  • Denton CS, Bardgett RD, Cook R, Hobbs PJ (1999) Low amounts of root herbivory positively influence the rhizosphere microbial community in a temperate grassland soil. Soil Biol Biochem 31:155–165

    Article  CAS  Google Scholar 

  • Johnson SN, Clark KE, Hartley SE, Jones TH, McKenzie SW, Koricheva J (2012) Aboveground-belowground herbivore interactions. Ecology 93:2208–2215

    Article  PubMed  Google Scholar 

  • Johnson SN, Mitchell C, McNicol JW, Thompson J, Karley AJ (2013) Downstairs drivers - root herbivores shape communities of above-ground herbivores and natural enemies via changes in plant nutrients. J Anim Ecol 82:1021–1030

    Article  PubMed  Google Scholar 

  • Kahl J, Siemens DH, Aerts RJ, Gabler R, Kuhnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342

    Article  CAS  PubMed  Google Scholar 

  • Keinänen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in nicotiana attenuata. J Agric Food Chem 49:3553–3558

    Article  PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008a) Constitutive and induced defences to herbivory in above- and belowground plant tissues. Ecology 89:392–402

    Article  PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Kessler A, Rehill BR, Sardanelli S, Denno RF (2008b) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851

    Article  PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008c) Effects of plant vascular architecture on aboveground–belowground-induced responses to foliar and root herbivores on Nicotiana tabacum. J Chem Ecol 34:1349–1359

    Article  CAS  PubMed  Google Scholar 

  • Kaplan I, Sardanelli S, Denno RF (2009) Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecol Entomol 34:262–270

    Article  Google Scholar 

  • Krügel T, Lim M, Gase K, Halitschke R, Baldwin IT (2002) Agrobacterium-mediated transformation of nicotiana attenuata, a model ecological expression system. Chemoecol 12:177–183

    Article  Google Scholar 

  • Mathur V, Ganta S, Raaijmakers CE, Reddy AS, Vet LEM, van Dam NM (2011) Temporal dynamics of herbivore-induced responses in Brassica juncea and their effect on generalist and specialist herbivores. Entomol Experiment Appl 139:215–225

    Article  Google Scholar 

  • McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in nicotiana sylvestris. Planta 203:430–435

    Article  CAS  Google Scholar 

  • Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831

    Article  PubMed Central  PubMed  Google Scholar 

  • Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why Bother? Oecologia 167:1–9

    Article  PubMed  Google Scholar 

  • Patil J, Miller AJ, Gaur HS (2013) Effect of nitrogen supply form on the invasion of rice roots by the root-knot nematode, meloidogyne graminicola. Nematology 15:483–492

    Article  CAS  Google Scholar 

  • Rasmann S, De Vos M, Castell 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 Central  CAS  PubMed  Google Scholar 

  • Sasser JN, Freckman DW (1987) A world perspective on nematology: the role of society. Pages 7–14 in. Vistas on Nematology. J.A. Veech and D.W. Dickson, eds. Society of nematologists, Hyattsville, MD, USA

  • Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci U S A 103:12935–12940

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soler R, Schaper SV, Bezemer TM, Cortersero AM, Hoffmeister TS, van der Putten WH, Vet LEM, Harvey JA (2009) Influence of presence and spatial arrangement of belowground insects on host-plant selection of aboveground insects: a field study. Ecol Entomol 34:339–345

    Article  Google Scholar 

  • Soler R, Erb M, Kaplan I (2013) Long distance root–shoot signalling in plant–insect community interactions. Trends Plant Sci 18:149–156

    Article  CAS  PubMed  Google Scholar 

  • Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine's defensive function in nature. PLoS Biol 2:e217

    Article  PubMed Central  PubMed  Google Scholar 

  • Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol Lett 10:499–511

    Article  PubMed  Google Scholar 

  • Thaler JS, Stout MJ, Karban R, Duffey S (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312–324

    Article  Google Scholar 

  • van Dam NM, Hadwich K, Baldwin IT (2000) Induced responses in nicotiana attenuata affect behavior and growth of the specialist herbivore manduca sexta. Oecologia 122:371–379

    Article  Google Scholar 

  • van Dam NM, Raaijmakers CE, van der Putten WH (2005) Root herbivory reduces growth and survival of the shoot feeding specialist pieris rapae on brassica nigra. Entomol Exp Appl 115:161–170

    Article  Google Scholar 

  • van Dam NM, Heil M (2011) Multitrophic interactions below and above ground: en route to the next level. J Ecol 99:77–88

    Article  Google Scholar 

  • Voelckel C, Krügel T, Gase K, Heidrich N, van Dam NM, Winz R, Baldwin IT (2001) Anti-sense expression of putrescine N-methyltransferase confirms defensive role of nicotine in nicotiana sylvestris against manduca sexta. Chemoecology 11:121–126

    Article  CAS  Google Scholar 

  • Wang M, Biere A, van der Putten WH, Bezemer TM (2014) Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance. Oecologia 175:187–198

    Article  PubMed  Google Scholar 

  • Wink M, Theile V (2002) Alkaloid tolerance in manduca sexta and phylogenetically related sphingids (Lepidoptera : sphingidae). Chemoecol 12:29–46

    Article  CAS  Google Scholar 

  • Winz RA, Baldwin IT (2001) Molecular interactions between the specialist herbivore manduca sexta (Lepidoptera, sphingidae) and its natural host nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol 125:2189–2202

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wondafrash M, van Dam NM, Tytgat TOG (2013) Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Front Plant Sci 4:87

    Article  PubMed Central  PubMed  Google Scholar 

  • Wurst S, van Dam NM, Monroy F, Biere A, van der Putten WH (2008) Intraspecific variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage. J Chem Ecol 34:1360–1367

    Article  CAS  PubMed  Google Scholar 

  • Yeates GW, Saggar S, Denton CS, Mercer CF (1998) Impact of clover cyst nematode (heterodera trifolii) infection on soil microbial activity in the rhizosphere of white clover (trifolium repens) – a pulse-labelling experiment. Nematologica 44:81–90

    Article  Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Baldwin IT (2004) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in nicotiana attenuata. Proc Natl Acad Sci U S A 101:1607–1612

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We wish to thank Anke Steppuhn and Michèle Bandoly for providing N. attenuata seeds and for their advice and help with nicotine measurements. The diligent technical assistance of Monika Fünning, Anne Plank and Cynthia Kienzle is also gratefully acknowledged. This study was funded by the Deutsche Forschungsgemeinschaft (Collaborative Research Centre 973 “Priming and Memory of Organismic Responses to Stress” – Project B3).

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  1. Collaborative Research Center (CRC) 973, Institute of Biology, Functional Biodiversity, Freie Universität Berlin, Königin-Luise-Str. 1-3, 14195, Berlin, Germany

    Caspar Schöning & Susanne Wurst

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  1. Caspar Schöning
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  2. Susanne Wurst
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Correspondence to Caspar Schöning.

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Responsible Editor: Juha Mikola.

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Schöning, C., Wurst, S. Positive effects of root-knot nematodes (Meloidogyne incognita) on nitrogen availability do not outweigh their negative effects on fitness in Nicotiana attenuata . Plant Soil 400, 381–390 (2016). https://doi.org/10.1007/s11104-015-2738-4

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