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Galling impacts of the gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus trees vary with plant genotype

  • Yao Xiang
  • Wenfeng Guo
  • Si Shen
  • Xu Gao
  • Xiaoqiong LiEmail author
Original Research Article
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Abstract

Impacts of galling on the distributions of plant metabolites can vary greatly with plant genotype. In this study, two Eucalyptus genotypes with different resistance levels were chosen, and the levels of several primary and secondary metabolites, as well as phytohormones in galls and ungalled portions of galled leaves infested by the gall wasp Leptocybe invasa, and gall-free (control) leaves were compared. It was found that galls of both two plant genotypes accumulated higher concentrations of carbon, total phenolics, gibberellins (GA), and abscisic acid (ABA) but had lower chlorophyll content than ungalled portions. However, galls of highly susceptible genotype contained higher nitrogen (N), cytokinins (CK), GA, and chlorophyll content but lower C/N ratio, total phenolics, tannins, and ABA than less susceptible genotype. For both two genotypes, ABA in galls and ungalled portions increased compared with adjacent control leaves. CK and GA levels increased in galls but decreased in ungalled portions of highly susceptible genotype, compared with control leaves. For less susceptible genotype, CK levels increased in both galls and ungalled portions compared with control leaves, but higher levels of tannins, total phenolics, and GA were only detected in galls. Therefore, our study found insufficient evidence that the impact of galling on the distributions of these metabolites and phytohormones extended beyond the attacked leaves, because they varied greatly with plant genotype.

Keywords

Chlorophyll content Gall-inducing insect Nitrogen Nutrient sink Phenolic compound Phytohormone 

Notes

Acknowledgments

We gratefully acknowledge Baoming Wang from the Chinese Agriculture University for his assistance with phytohormone analysis. We would like to thank the Guangxi Zhuang Autonomous Region Forestry Research Institution for providing the seedlings of Eucalyptus trees. We also appreciate Professor Roy van Driesche for the language edits.

Funding information

This work was supported by the National Natural Science Foundation (31800423, 31660087) and the Natural Science Foundation of Guangxi Province (2018GXNSFBA281172).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abrahamson WG, Mccrea KD, Whitwell AJ, Vernieri LA (1991) The role of phenolics in goldenrod ball gall resistance and formation. Biochem Syst Ecol 19:615–622CrossRefGoogle Scholar
  2. Ananthakrishnan TN, Gopichandran R (1993) Chemical ecology in thrips-host plant interactions. Science Publishers, EnfieldGoogle Scholar
  3. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844PubMedCrossRefGoogle Scholar
  4. Bedetti CS, Modolo LV, Isaias RMDS (2014) The role of phenolics in the control of auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae). Biochem Syst Ecol 55:53–59CrossRefGoogle Scholar
  5. Bedetti CS, Braganca GP, Isaias RMDS (2017) Influence of auxin and phenolic accumulation on the patterns of cell differentiation in distinct gall morphotypes on Piptadenia gonoacantha (Fabaceae). Aust J Bot 65:411–420CrossRefGoogle Scholar
  6. Carneiro RGS, Isaias RMDS, Moreira ASFP, Oliveira DCD (2017) Reacquisition of new meristematic sites determines the development of a new organ, the Cecidomyiidae gall on Copaifera langsdorffii Desf. (Fabaceae). Front. Plant Sci 8:1622Google Scholar
  7. Dardeau F et al (2015) Effects of fertilisation on amino acid mobilisation by a plant-manipulating insect. Ecol Entomol 40:814–822CrossRefGoogle Scholar
  8. Dittrich-Schroeder G, Wingfield MJ, Hurley BP, Slippers B (2012) Diversity in Eucalyptus susceptibility to the gall-forming wasp Leptocybe invasa. Agric For Entomol 14:419–427CrossRefGoogle Scholar
  9. Dorchin N, Cramer MD, Hoffmann JH (2006) Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology 87:1781–1791PubMedCrossRefGoogle Scholar
  10. Dungey HS, Potts BM, Whitham TG, Li HF (2000) Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54:1938–1946PubMedCrossRefGoogle Scholar
  11. Erb M, Meldau S, Gregg AH (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259PubMedPubMedCentralCrossRefGoogle Scholar
  12. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19PubMedCrossRefGoogle Scholar
  13. Ferreira BG et al (2018) Antioxidant metabolism in galls due to the extended phenotypes of the associated organisms. PLoS One 13:e0205364PubMedPubMedCentralCrossRefGoogle Scholar
  14. Florentine SK, Raman A, Dhileepan K (2005) Effects of gall induction by Epiblema strenuana on gas exchange, nutrients, and energetics in Parthenium hysterophorus. Biocontrol 50:787–801CrossRefGoogle Scholar
  15. Formiga AT, Oliveira DCD, Ferreira BG, Magalhaes TA, de Castro AC, Wilson Fernandes G, Isaias RMDS (2013) The role of pectic composition of cell walls in the determination of the new shape-functional design in galls of Baccharis reticularia (Asteraceae). Protoplasma 250:899–908PubMedCrossRefGoogle Scholar
  16. Fritz RS, Nichols-Orians CM, Brunsfeld SJ (1994) Interspecific hybridization of plants and resistance to herbivores: hypotheses, genetics, and variable responses in a diverse herbivore community. Oecologia 97:106–117CrossRefGoogle Scholar
  17. Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annu Rev Ecol Syst 30:565–591CrossRefGoogle Scholar
  18. Giron D, Huguet E, Stone GN, Body M (2016) Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. J Insect Physiol 84:70–89CrossRefGoogle Scholar
  19. Hall CR, Carroll AR, Kitching RL (2017) A meta-analysis of the effects of galling insects on host plant secondary metabolites. Arthropod-Plant Inte 11:463–473CrossRefGoogle Scholar
  20. Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501PubMedCrossRefGoogle Scholar
  21. Hartley SE, Lawton JH (1992) Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. J Anim Ecol 61:113–119CrossRefGoogle Scholar
  22. Huang MY, Huang WD, Chou HM, Lin KH, Chen CC, Chen PJ, Chang YT, Yang CM (2014) Leaf-derived cecidomyiid galls are sinks in Machilus thunbergii (Lauraceae) leaves. Physiol Plant 152:475–485PubMedCrossRefGoogle Scholar
  23. Isaias RMDS, Ferreira BG, Alvarenga DRD, Barbosa LR, Salminen JP, Steinbauer MJ (2018) Functional compartmentalisation of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Austral Entomol 57:238–246CrossRefGoogle Scholar
  24. Kot I, Jakubczyk A, Karaś M, Złotek U (2017) Biochemical responses induced in galls of three Cynipidae species in oak trees. Bull Entomol Res 108:494–500PubMedCrossRefGoogle Scholar
  25. Larson KC (1998) The impact of two gall-forming arthropods on the photosynthetic rates of their hosts. Oecologia 115:161–166PubMedCrossRefGoogle Scholar
  26. Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:15–21PubMedCrossRefGoogle Scholar
  27. Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109:575–582PubMedCrossRefGoogle Scholar
  28. Li XQ, Liu YZ, Guo WF, Solanki MK, Yang ZD, Xiang Y, Ma ZC, Wen YG (2017) The gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) stimulates different chemical and phytohormone responses in two Eucalyptus varieties that vary in susceptibility to galling. Tree Physiol 37:1208–1217PubMedCrossRefGoogle Scholar
  29. Makkar HPS (2003) Quantification of tannins in tree and shrub foliage : a laboratory manual. Springer, New YorkCrossRefGoogle Scholar
  30. Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynth Res 46:467–472PubMedCrossRefGoogle Scholar
  31. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  32. Mendel Z, Protasov A, Fisher N, La Salle J (2004) Taxonomy and biology of Leptocybe invasa gen. & sp n. (Hymenoptera : Eulophidae), an invasive gall inducer on Eucalyptus. Aust J Entomol 43:101–113CrossRefGoogle Scholar
  33. Messina FJ, Richards JH, McArthur ED (1996) Variable responses of insects to hybrid versus parental sagebrush in common gardens. Oecologia 107:513–521PubMedCrossRefGoogle Scholar
  34. Meunier CL, Gundale MJ, Sanchez IS, Liess A (2016) Impact of nitrogen deposition on forest and lake food webs in nitrogen-limited environments. Glob Chang Biol 22:164–179PubMedCrossRefGoogle Scholar
  35. Motta LB, Kraus JE, Salatino A, Salatino MLF (2005) Distribution of metabolites in galled and non-galled foliar tissues of Tibouchina pulchra. Biochem Syst Ecol 33:971–981CrossRefGoogle Scholar
  36. Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci U S A 97:13184–13187PubMedPubMedCentralCrossRefGoogle Scholar
  37. Oates CN, Külheim C, Myburg AA, Slippers B, Naidoo S (2015) The transcriptome and terpene profile of Eucalyptus grandis reveals mechanisms of defense against the insect pest, Leptocybe invasa. Plant Cell Physiol 56:1418–1428PubMedCrossRefGoogle Scholar
  38. Oliveira DCD, Isaias RMDS (2010a) Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). S Afr J Bot 76:239–248CrossRefGoogle Scholar
  39. Oliveira DCD, Isaias RMDS (2010b) Cytological and histochemical gradients induced by a sucking insect in galls of Aspidosperma australe Arg. Muell (Apocynaceae). Plant Sci 178: 0–358CrossRefGoogle Scholar
  40. Oliveira DCD, Isaias RMDS, Moreira ASFP, Magalhães TA, Lemos-Filho JPD (2011) Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis? Plant Sci 180:489–495PubMedCrossRefGoogle Scholar
  41. Oliveira DCD, Isaias RMDS, Fernandes GW, Ferreira BG, Carneiro RGS, Fuzaro L (2016) Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J Insect Physiol 84:103–113PubMedCrossRefGoogle Scholar
  42. Oliveira DCD, Moreira ASFP, Isaias RMDS, Martini V, Rezende UC (2017) Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). Front Plant Sci 8:1249PubMedPubMedCentralCrossRefGoogle Scholar
  43. Paine TD, Steinbauer MJ, Lawson SA (2011) Native and exotic pests of Eucalyptus: a worldwide perspective. Annu Rev Entomol 56:181–201PubMedCrossRefGoogle Scholar
  44. Reis AR, Favarin JL, Malavolta E, Lavres Junior J, Moraes MF (2009) Photosynthesis, chlorophylls, and SPAD readings in coffee leaves in relation to nitrogen supply. Commun Soil Sci Plant Anal 40:1512–1528CrossRefGoogle Scholar
  45. Rocha S, Branco M, Boas LV, Almeida MH, Protasov A, Mendel Z (2013) Gall induction may benefit host plant: a case of a gall wasp and eucalyptus tree. Tree Physiol 33:388–397PubMedCrossRefGoogle Scholar
  46. Shivashankar S, Sumathi M, Ranganath HR (2012) Roles of reactive oxygen species and anti-oxidant systems in the resistance response of chayote fruit (Sechium edule) to melon fly Bactrocera cucurbitae (Coquillett). J Hortic Sci Biotechnol 87:391–397CrossRefGoogle Scholar
  47. SPSS Inc., 2013. SPSS for windows base system user’s guide, Release 22.0Google Scholar
  48. Straka JR, Hayward AR, Emery RJN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones. J Plant Interact 5:197–203CrossRefGoogle Scholar
  49. Sun TP (2011) The molecular mechanism and evolution of the GA–GID1–DELLA signaling module in plants. Curr Biol 21:338–345CrossRefGoogle Scholar
  50. Takei M, Yoshida S, Kawai T, Hasegawa M, Suzuki Y (2015) Adaptive significance of gall formation for a gall-inducing aphids on Japanese elm trees. J Insect Physiol 72:43–51PubMedCrossRefGoogle Scholar
  51. Tanaka Y, Okada K, Asami T, Suzuki Y (2013) Phytohormones in Japanese mugwort gall induction by a gall-inducing gall midge. Biosci Biotechnol Biochem 77:1942–1948PubMedCrossRefGoogle Scholar
  52. Tokuda M, Jikumaru Y, Matsukura K, Takebayashi Y, Kumashiro S, Matsumura M, Kamiya Y (2013) Phytohormones related to host plant manipulation by a gall-inducing leafhopper. PLoS One 8:e62350PubMedPubMedCentralCrossRefGoogle Scholar
  53. Tooker JF, De Moraes CM (2008) Gall insects and indirect plant defenses: a case of active manipulation? Plant Signal Behav 3:503–504PubMedPubMedCentralCrossRefGoogle Scholar
  54. Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod-Plant Interact 5:115–124CrossRefGoogle Scholar
  55. Tooker JF, Helms AM (2014) Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. J Chem Ecol 40:742–753CrossRefGoogle Scholar
  56. Wang H et al (2016) Gibberellic acid is selectively downregulated in response to aphid-induced gall formation. Acta Physiol Plant 38:214CrossRefGoogle Scholar
  57. Yamaguchi H, Tanaka H, Hasegawa M, Tokuda M, Asami T, Suzuki Y (2012) Phytohormones and willow gall induction by a gall-inducing sawfly. New Phytol 196:586–595PubMedCrossRefGoogle Scholar
  58. Yang H, Yang JP, Lv YM, He JJ (2014) SPAD values and nitrogen nutrition index for the evaluation of rice nitrogen status. Plant Prod Sci 17:81–92CrossRefGoogle Scholar
  59. Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, De Lucia EH (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci U S A 99:1088–1091PubMedPubMedCentralCrossRefGoogle Scholar
  60. Zhu F, Ren SX, Bl Q, Huang Z, Peng ZQ (2012) The abundance and population dynamics of Leptocybe invasa (Hymenoptera: Eulophidae) galls on Eucalyptus spp. in China. J Integr Agric 11:2116–2123CrossRefGoogle Scholar

Copyright information

© African Association of Insect Scientists 2019

Authors and Affiliations

  • Yao Xiang
    • 1
  • Wenfeng Guo
    • 2
  • Si Shen
    • 1
  • Xu Gao
    • 1
  • Xiaoqiong Li
    • 1
    • 3
    Email author
  1. 1.Guangxi Key Laboratory of Forest Ecology and Conservation, College of ForestryGuangxi UniversityNanningChina
  2. 2.Guangxi Crop Genetic Improvement and Biotechnology LaboratoryGuangxi Academy of Agricultural SciencesNanningChina
  3. 3.Guangxi Youyiguan Forest Ecosystem Research StationPingxiangChina

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