All Title Author
Keywords Abstract

PLOS ONE  2013 

Egg Laying of Cabbage White Butterfly (Pieris brassicae) on Arabidopsis thaliana Affects Subsequent Performance of the Larvae

DOI: 10.1371/journal.pone.0059661

Full-Text   Cite this paper   Add to My Lib

Abstract:

Plant resistance to the feeding by herbivorous insects has recently been found to be positively or negatively influenced by prior egg deposition. Here we show how crucial it is to conduct experiments on plant responses to herbivory under conditions that simulate natural insect behaviour. We used a well-studied plant – herbivore system, Arabidopsis thaliana and the cabbage white butterfly Pieris brassicae, testing the effects of naturally laid eggs (rather than egg extracts) and allowing larvae to feed gregariously as they do naturally (rather than placing single larvae on plants). Under natural conditions, newly hatched larvae start feeding on their egg shells before they consume leaf tissue, but access to egg shells had no effect on subsequent larval performance in our experiments. However, young larvae feeding gregariously on leaves previously laden with eggs caused less feeding damage, gained less weight during the first 2 days, and suffered twice as high a mortality until pupation compared to larvae feeding on plants that had never had eggs. The concentration of the major anti-herbivore defences of A. thaliana, the glucosinolates, was not significantly increased by oviposition, but the amount of the most abundant member of this class, 4-methylsulfinylbutyl glucosinolate was 1.8-fold lower in larval-damaged leaves with prior egg deposition compared to damaged leaves that had never had eggs. There were also few significant changes in the transcript levels of glucosinolate metabolic genes, except that egg deposition suppressed the feeding-induced up-regulation of FMOGS-OX2, a gene encoding a flavin monooxygenase involved in the last step of 4-methylsulfinylbutyl glucosinolate biosynthesis. Hence, our study demonstrates that oviposition does increase A. thaliana resistance to feeding by subsequently hatching larvae, but this cannot be attributed simply to changes in glucosinolate content.

References

[1]  Dicke M, Bruin J (2001) Chemical information transfer between plants: back to the future. Biochem Syst Ecol 29: 981–994.
[2]  Choh Y, Takabayashi J (2004) Herbivore-induced extrafloral nectar production in lima bean plants enhanced by previous exposure to volatiles from infested conspecifics. J Chem Ecol 32: 2073–2077.
[3]  Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9: 813–817.
[4]  Frost CJ, Mescher MC, Carlson JE, de Moraes CM (2008) Plant defense priming against herbivores: Getting ready for a different battle. Plant Physiol 146: 818–824.
[5]  Galis I, Gaquerel E, Pandey SP, Baldwin IT (2009) Molecular mechanisms underlying plant memory in JA-mediated defence response. Plant Cell Environ 32: 617–627.
[6]  Arimura G-I, Shiojiri K, Karban R (2011) Acquired immunity to herbivory and allelopathy caused by airborne plant emissions. Phytochemistry 71: 1642–1649.
[7]  Petzold-Maxwell J, Wong S, Arellano C, Gould F (2011) Host plant direct defence against eggs of its specialist herbivore, Heliothis subflexa. Ecol Entomol 36: 700–708.
[8]  Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32: 1379–1397.
[9]  Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous arthropods? Biol Rev 85: 267–280.
[10]  Hilker M, Meiners T (2011) Plants and insect eggs: how do they affect each other? Phytochemistry 72: 1612–1623.
[11]  Tamiru A, Bruce TJA, Woodcock CM, Caulfield JC, Midega CAO, et al. (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14: 1075–1083.
[12]  Deshpande SA, Kainoh Y (2012) Herbivore egg deposition induces tea leaves to arrest the egg-larval parasitoid Ascogaster reticula. Entomol Exp Appl 144: 172–180.
[13]  Fatouros NE, Bukovinszkine'Kiss G, Kalkers LA, Soler Gamborena R, Dicke M, et al. (2005) Oviposition-induced plant cues: do they arrest Trichogramma wasps during host location. Entomol Exp Appl 115: 207–215.
[14]  Blenn B, Bandoly M, Küffner A, Otte T, Geiselhardt S, et al. (2012) Insect egg deposition induces indirect defense and epicuticular wax changes in Arabidopsis thaliana. J Chem Ecol 38: 882–892 DOI: 10.1007/s10886-012-0132-8.
[15]  Beyaert I, K?pke D, Stiller J, Hammerbacher A, Yoneya K, et al. (2012) Can insect egg deposition ?warn“ a plant of future feeding damage by herbivorous larvae? Proc R Soc B. 279: 101–108.
[16]  De Puysseleyr V, H?fte M, De Clercq P (2011) Ovipositing Orius laevigatus increase tomato resistance against Frankliniella occidentalis feeding by inducing the wound response. Arthropod Plant Interact 5: 71–80.
[17]  Kim J, Tooker JF, Luthe DS, De Moraes CM, Felton GW (2012) Insect eggs can enhance wound response in plants: A study system of tomato Solanum lycopersicum L. and Helicoverpa zea Boddie. PLoS ONE 7: e37420.
[18]  Bruessow F, Gouhier-Darimont G, Buchala A, Metraux JP, Reymond P (2010) Insect eggs suppress plant defence against chewing herbivores. Plant J 62: 876–885.
[19]  Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57: 303–333.
[20]  Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54: 57–83.
[21]  Textor S, Gershenzon J (2009) Herbivore induction of the glucosinolate–myrosinase defense system: major trends, biochemical bases and ecological significance. Phytochem Rev 8: 149–170.
[22]  Gigolashvili T, Berger B, Flügge UI (2009) Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana. Phytochem Rev 8: 3–13.
[23]  Burow M, Losansky A, Müller R, Plock A, Kliebenstein DJ, et al. (2009) The genetic basis of constitutive and herbivore-induced ESP-independent nitrile formation in Arabidopsis. Plant Physiol 149: 561–574.
[24]  Karban R, Baldwin IT (2002) Induced Responses to Herbivory. Chicago: The University of Chicago Press. 319 p.
[25]  Schaller A (2008) Induced Plant Resistance to Herbivory. Springer, 464 p.
[26]  Hansen BG, Kliebenstein DJ, Halkier BA (2007) Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 50: 902–910.
[27]  Li J, Hansen BG, Ober JA, Kliebenstein DJ, Halkier BA (2008) Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol 148: 1721–1733.
[28]  Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, et al. (2007) The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci U S A 104: 20427–20431.
[29]  Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, et al. (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci U S A 101: 4859–4864.
[30]  Mumm R, Burow M, Bukovinszkine'Kiss G, Kazantzidou E, Wittstock U, et al. (2008) Formation of simple nitriles upon glucosinolate hydrolysis affects direct and indirect defense against the specialist herbivore, Pieris rapae. J Chem Ecol 34: 1311–1321.
[31]  Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143: 784–800.
[32]  Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, et al. (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67: 2450–2462.
[33]  Davis CR, Gilbert N (1985) A comparative study of the egg-laying behavior and larval development of Pieris rapae L. and P. brassicae L. on the same host plants. Oecologia 67: 278–281.
[34]  Lucas-Barbosa D, van Loon JJA, Gols R, van Beek TA, Dicke M (2012) Reproductive escape: annual plant responds to butterfly eggs by accelerating seed production. Funct Ecol: doi: 10.1111/1365-2435.12004.
[35]  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 U S A 103: 5602–5607.
[36]  Burow M, Muller R, Gershenzon J, Wittstock U (2006) Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis. J Chem Ecol 32: 2333–2349.
[37]  Verwoerd TC, Dekker BMM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17: 2362.
[38]  Caldana C, Scheible WR, Mueller-Roeber B, Ruzicic S (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3: 7.
[39]  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2?ΔΔCT method. Methods 25: 402–408.

Full-Text

comments powered by Disqus