, 149:81 | Cite as

Solar ultraviolet-B radiation alters the attractiveness of Arabidopsis plants to diamondback moths (Plutella xylostella L.): impacts on oviposition and involvement of the jasmonic acid pathway

  • Carla Caputo
  • Mariana Rutitzky
  • Carlos L. Ballaré
Plant Animal Interactions


Solar ultraviolet-B radiation (UV-B) can have large impacts on the interactions between plants and herbivorous insects. Several studies have documented effects of UV-B-induced changes in plant tissue quality on the feeding performance of insect larvae. In contrast, the effects of UV-B-induced plant responses on the behavior of adult insects have received little attention. We carried out a series of field and glasshouse experiments using the model plant Arabidopsis thaliana L. and the crucifer-specialist insect Plutella xylostella L. (diamondback moth) to investigate the effects of UV-B on natural herbivory and plant–insect interactions. Natural herbivory under field conditions was less severe on plants exposed to ambient UV-B than on plants grown under filters that attenuated the UV-B component of solar radiation. This reduced herbivory could not be accounted for by effects of UV-B on larval feeding preference and performance, as P. xylostella caterpillars did not respond to changes in plant quality induced by UV-B. In contrast, at the adult stage, the insects presented clear behavioral responses: P. xylostella moths deposited significantly more eggs on plants grown under attenuated UV-B levels than on plants exposed to ambient UV-B. The deterring effect of UV-B exposure on insect oviposition was absent in jar1-1, a mutant with impaired jasmonic acid (JA) sensitivity, but it was conserved in mutants with altered ethylene signaling. The jar1-1 mutant also presented reduced levels of UV-absorbing phenolic compounds than the other genotypes that we tested. Our results suggest that variations in UV-B exposure under natural conditions can have significant effects on insect herbivory by altering plant traits that female adults use as sources of information during the process of host selection for oviposition. These effects of natural UV-B on plant quality appear to be mediated by activation of signaling circuits in which the defense-related hormone JA plays a functional role.


Herbivory Induced defenses UV-B 



We thank Javier Moreno, Ana María Zima and Walter De Nicoló for field and laboratory assistance, and Miriam Izaguirre and two anonymous reviewers for useful comments on the manuscript. This work was financially supported by grants from ANPCyT, Consejo Nacional de Investigaciones Científicas y Técnicas, and Universidad de Buenos Aires.


  1. A.-H.-Mackerness SA, Surplus SL, Blake P, John CF, Buchannan-Wollaston V, Jordan BR, Thomas B (1999) Ultraviolet-B-induced stress and changes in gene expression in Arabidopsis thaliana: role of signalling pathways controlled by jasmonic acid, ethylene and reactive oxygen species. Plant Cell Environ 22:1413–1243CrossRefGoogle Scholar
  2. Ballaré CL (2003) Stress under the sun: spotlight on ultraviolet-B responses. Plant Physiol 132:1725–1727PubMedCrossRefGoogle Scholar
  3. Ballaré CL, Scopel AL, Stapleton AE, Yanovsky MJ (1996) Solar ultraviolet-B radiation affects seedling emergence, DNA integrity, plant morphology, growth rate, and attractiveness to herbivore insects in Datura ferox. Plant Physiol 112:161–170PubMedGoogle Scholar
  4. Ballaré CL, Rousseaux MC, Searles PS, Zaller JG, Giordano CV, Robson TM, Caldwell MM, Sala OE, Scopel AL (2001) Impacts of solar ultraviolet-B radiation on terrestrial ecosystems of Tierra del Fuego (southern Argentina). An overview of recent progress. J Photochem Photobiol B Biol 62:67–77CrossRefGoogle Scholar
  5. Bassman JH (2004) Ecosystem consequences of enhanced solar ultraviolet radiation: secondary plant metabolites as mediators of multiple trophic interactions in terrestrial plant communities. Photochem Photobiol 79:382–398PubMedCrossRefGoogle Scholar
  6. Beninger CW, Abou-Zaid MM (1997) Flavonol glycosides from four pine species that inhibit early instar gypsy moth (Lepidoptera: Lymantriidae) development. Biochem Syst Ecol 25:505–512CrossRefGoogle Scholar
  7. Caldwell MM (1971) Solar UV irradiation and the growth and development of higher plants. In: Giese AC (ed) Photophysiology, vol 6. Academic Press, New York, pp 131–177Google Scholar
  8. Caldwell MM, Ballaré CL, Bornman JF, Flint SD, Bjorn LO, Teramura AH, Kulandaivelu G, Tevini M (2003) Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors. Photochem Photobiol Sci 2:29–38PubMedCrossRefGoogle Scholar
  9. Cipollini DF, Redman AM (1999) Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J Chem Ecol 25:271–281CrossRefGoogle Scholar
  10. Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–296PubMedCrossRefGoogle Scholar
  11. De Moraes CM, Mark C, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580PubMedCrossRefGoogle Scholar
  12. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097PubMedCrossRefGoogle Scholar
  13. Franceschi VR, Krekling T, Christiansen E (2002) Application of methyl jasmonate on (Pinaceae) stems induces defense-related responses in phloem and xylem. Am J Bot 89:578–586CrossRefGoogle Scholar
  14. Grant Petersson J, Renwick JAA (1996) Effects of ultraviolet-B exposure of Arabidopsis thaliana on herbivory by two crucifer-feeding insects (Lepidoptera). Environ Entomol 25:135–142Google Scholar
  15. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504PubMedCrossRefGoogle Scholar
  16. Haribal M, Feeny P (2003) Combined roles of contact stimulant and deterrents in assessment of host-plant quality by ovipositing zebra swallowtail butterflies. J Chem Ecol 29:653–70PubMedCrossRefGoogle Scholar
  17. Hatcher P, Paul N (1994) The effect of elevated UV-B radiation on herbivory of pea by Autographa gamma. Entomol Exp Appl 71:227–233CrossRefGoogle Scholar
  18. Izaguirre MM, Scopel AL, Baldwin IT, Ballaré CL (2003) Convergent responses to stress. Solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora. Plant Physiol 132:1755–1767PubMedCrossRefGoogle Scholar
  19. Jordan BR (2002) Molecular response of plant cells to UV-B stress. Funct Plant Biol 29:909–916CrossRefGoogle Scholar
  20. Justus KA, Dosdall LM, Mitchell BK (2000) Oviposition by Plutella xylostella (Lepidoptera Plutellidae) and effects phylloplane waxiness. J Econ Entomol 93:1152–1159PubMedCrossRefGoogle Scholar
  21. Kelly MT, Curry JP (1991) The influence of phenolic compounds on the suitability of three Salix species as hosts for the willow beetle Phratora vulgatissima. Entomol Exp Appl 61:25–32CrossRefGoogle Scholar
  22. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328PubMedCrossRefGoogle Scholar
  23. Kliebenstein DJ (2004) Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana-tinged glasses. Plant Cell Environ 27:675–684CrossRefGoogle Scholar
  24. Krizek DT, Britz SJ, Mirecki RM (1998) Inhibitory effects of ambient levels of solar UV-A and UV-B radiation on growth of cv. New Red Fire lettuce. Physiol Plant 103:1–7CrossRefGoogle Scholar
  25. Liakoura V, Stefanou M, Manetas Y, Cholevas C, Karabourniotis G (1997) Trichome density and its UV-B protective potential are affected by shading and leaf position on the canopy. Environ Exp Bot 38:223–229CrossRefGoogle Scholar
  26. Lindroth RL, Hofmann RW, Campbell BD, McNabb WC, Hunt DY (2000) Population differences in Trifolium repens L. response to ultraviolet-B radiation foliar chemistry and consequences for two lepidopteran herbivores. Oecologia 122:20–28CrossRefGoogle Scholar
  27. Long LM, Patel HP, Cory WC, Stapleton AE (2003) The maize epicuticular wax layer provides UV protection. Funct Plant Biol 30:75–81CrossRefGoogle Scholar
  28. Mazza CA, Battista D, Zima A, Szwarcberg-Bracchitta M, Giordano CV, Acevedo A, Scopel AL, Ballaré CL (1999a) The effects of solar UV-B radiation on the growth and yield of barley are accompanied by increased DNA damage and antioxidant responses. Plant Cell Environ 22:61–67CrossRefGoogle Scholar
  29. Mazza CA, Zavala J, Scopel AL, Ballaré CL (1999b) Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications. Proc Natl Acad Sci USA 96:980–985CrossRefGoogle Scholar
  30. Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol 122:117–125PubMedCrossRefGoogle Scholar
  31. Mazza CA, Izaguirre MM, Zavala J, Scopel AL, Ballaré CL (2002) Insect perception of ambient ultraviolet-B radiation. Ecol Lett 5:722–726CrossRefGoogle Scholar
  32. McCloud ES, Berenbaum MR (1994) Stratospheric ozone depletion and plant–insect interactions: effects of UVB radiation on foliage quality of Citrus jambhiri for Trichoplusia ni. J Chem Ecol 20:525–539CrossRefGoogle Scholar
  33. Paul ND, Gwynn-Jones D (2003) Ecological roles of solar UV radiation: towards an integrated approach. Trends Ecol Evol 18:48–55CrossRefGoogle Scholar
  34. Qaderi MM, Reid DM (2005) Growth and physiological responses of canola (Brassica napus) to UV-B and CO2 under controlled environment conditions. Physiol Plant 125:247–259CrossRefGoogle Scholar
  35. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719PubMedCrossRefGoogle Scholar
  36. Richard S, Lapointe G, Rutledge RG, Séguin A (2000) Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol 41:982–987PubMedCrossRefGoogle Scholar
  37. Rousseaux MC, Ballaré CL, Scopel AL, Searles PS, Caldwell MM (1998) Solar ultraviolet-B radiation affects plant–insect interactions in a natural ecosystem of Tierra del Fuego (southern Argentina). Oecologia 116: 528–535CrossRefGoogle Scholar
  38. Rousseaux MC, Julkunen-Tiitto R, Searles PS, Scopel AL, Aphalo PJ, Ballaré CL (2004) Solar UV-B radiation affects leaf quality and insect herbivory in the southern beech tree Nothofagus antarctica. Oecologia 138:505–512PubMedCrossRefGoogle Scholar
  39. Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377PubMedCrossRefGoogle Scholar
  40. Simmond MSJ (2001) Importance of flavonoids in insect-plant interactions: feeding and oviposition. Phytochemistry 56:245–252CrossRefGoogle Scholar
  41. Stratmann JW (2003) Ultraviolet-B radiation co-opts defense signaling pathways. Trends Plant Sci 8:526–533PubMedCrossRefGoogle Scholar
  42. Stratmann JW, Stelmach BA, Weller EW, Ryan CA (2000) UVB/UVA radiation activates a 48 kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochem Photobiol 71:116–123PubMedCrossRefGoogle Scholar
  43. Tabashnik BE, Cushing NL, Johnson MW (1987) Diamondback moth (Lepidoptera: Plutellidae) resistance to insecticides in Hawaii: intra-island variation and cross-resistance. J Econ Entomol 80:1091–1099Google Scholar
  44. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  45. Zavala J, Scopel AL, Ballaré CL (2001) Effects of solar UV-B radiation on soybean crops: Impact on leaf herbivory by Anticarsia gemmatalis. Plant Ecol 156:121–130CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Carla Caputo
    • 1
  • Mariana Rutitzky
    • 1
  • Carlos L. Ballaré
    • 1
  1. 1.IFEVA Consejo Nacional de Investigaciones Científicas y Técnicas and Universidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations