Advertisement

Protoplasma

pp 1–9 | Cite as

How the activity of natural enemies changes the structure and metabolism of the nutritive tissue in galls? Evidence from the Palaeomystella oligophaga (Lepidoptera) -Macairea radula (Metastomataceae) system

  • Uiara C. Rezende
  • João Custódio F. Cardoso
  • Vinícius C. Kuster
  • Letícia A. Gonçalves
  • Denis C. OliveiraEmail author
Original Article
  • 79 Downloads

Abstract

Insect-induced galls usually develop nutritional cells, which they induce and consume directly, and any metabolic modification of those cells may reflect changes of the insect’s own metabolism. The system Palaeomystella oligophaga (Lepidoptera)Macairea radula (Melastomataceae) presents a series of natural enemies, including parasitoids and cecidophages that can function as a natural experiment, respectively removing the specific galling feeding stimulus and providing a nonspecific one. Considering that the process of induction and maintenance of gall tissues strictly depends on the constant specific stimulus of galling, question I:What kind of metabolic changes these different groups of natural enemies can promote in chemical and structural composition of these galls? II: How the specialized tissues are metabolically dependent on the constant specific stimulus of galling in latter stages of gall development? Galls without natural enemies, with parasitoids or cecidophages in larvae or pupae stages were analyzed through histochemistry and cytological profiles and all compared to galls in natural senescence state. The analysis revealed the accumulation of proteins and lipids in typical nutritive tissue and starch in the storage tissue, as well a high integrity of cellular organelles and membrane systems on galls with gallings in the larval stage. Both parasitoids and cecidophages stop galling feeding activities, which resulted in the paralysis of the stimulus that maintain the metabolism of gall tissues, leading to generalized collapse. We demonstrate that the development and metabolic maintenance of a typical nutritive tissue in these galls are completely dependent on constant larval stimulus.

Keywords

Enemy hypothesis Gall cytology Gall structure Histochemistry Metabolism and plant-insect interaction 

Notes

Acknowledgments

The authors are grateful for Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitóides (INCT/HYMPAR), Programa Ecológico de Longa Duração (PELD), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—DCO fellowship (PQ 307011/2015). They thank the Laboratório Multiusuário de Microscopia de Alta Resolução (LaBMic) for ultrastructural analysis, and the assistance in the histochemical processes provided by Ana Flávia de Melo Silva and Phabliny M. S. Bomfim.

Funding information

The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—finance code 001, financed this study in part.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Baker JR (1958) Note on the use of bromophenol blue for the histochemical recognition of protein. Q J Microsc Sci 99:459–460Google Scholar
  2. Barnewall EC, De Clerck-Floate RA (2012) A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod-Plant Int 6:449–459.  https://doi.org/10.1007/s11829-012-9193-4 CrossRefGoogle Scholar
  3. Barraco G, Sylvestre I, Collin M, Escoute J, Lartaud M, Verdeil JL, Engelmann F (2014) Histocytological analysis of yam (Dioscorea alata) shoot tips cryopreserved by encapsulation-dehydration. Protoplasma 251:177–189.  https://doi.org/10.1007/s00709013-0536-5 CrossRefGoogle Scholar
  4. Barrantes G, Sandoval L, Hanson P (2017) Cocoon web induced by Eruga telljohanni (Ichneumonidae: Pimplinae) in Leucauge sp. (Tetragnathidae). Arachnology 17:245–247.  https://doi.org/10.13156/arac.2017.17.5.245 CrossRefGoogle Scholar
  5. Bartlett L, Connor EF (2014) Exogenous phytohormones and the induction of plant galls by insects. Arthropod-Plant Int 8:339–348.  https://doi.org/10.1007/s11829-0149309-0 Google Scholar
  6. Becker VO, Adamski D (2008) Three new cicidogenous Paleomystela Fletcher (Lepidoptera, Coleophoridae, Momphinae) associated with Melastomataceae in Brazil. Rev Bras Entomol 52: 647-657. https://doi.org/10.1590/S0085-56262008000400017Google Scholar
  7. Bedetti CS, Ferreira BG, Castro NM, Isaias RMS (2013) The influence of parasitoidism on the anatomical and histochemical profiles of the host leaves in a galling Lepidoptera–Bauhinia ungulata system. Braz J Biosci 11:242–249.  https://doi.org/10.1093/aobpla/plv086 Google Scholar
  8. Bronner R (1992) The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect induced-galls. Oxford University Press, Oxford, pp 118–140Google Scholar
  9. Brundett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan red 7B or fluorol yellow 088 in polyethylene glycol–glycerol. Biotech Histochem 66:111–116.  https://doi.org/10.3109/10520299109110562 CrossRefGoogle Scholar
  10. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and Mol Biol of plants. Wiley, RockvilleGoogle Scholar
  11. Carneiro RGS, Isaias RMS, Moreira ASFP, Oliveira DC (2017) Reacquisition of new meristematic sites determines the development of a new organ, the Cecidomyiidae gall on Copaifera langsdorffii Desf. (Fabaceae). Front Plant Sci 8:1622.  https://doi.org/10.3389/fpls.2017.01622 CrossRefGoogle Scholar
  12. Ferreira BG, Avritzer SC, Isaias RMS (2017) Totipotent nutritive cells and indeterminate growth in galls of Ditylenchus gallaeformans (Nematoda) on reproductive apices of Miconia. Flora 227:36–45.  https://doi.org/10.1016/j.flora.2016.12.008 CrossRefGoogle Scholar
  13. Ferreira BG, Carneiro RGS, Isaias RMS (2015) Multivesicular bodies differentiate exclusively in nutritive fast-dividing cells in Marcetia taxifolia galls. Protoplasma 252:1275–1283.  https://doi.org/10.1007/s00709-015-0759-8 CrossRefGoogle Scholar
  14. Ferreira BG, Falcioni R, Guedes LM, Avritzer SC, Antunes WC, Souza LA, Isaias RM (2016) Preventing false negatives for histochemical detection of phenolics and lignins in PEG-embedded plant tissues. J Histochem Cytochem 65:105–116.  https://doi.org/10.1369/0022155416677035 CrossRefGoogle Scholar
  15. Ferreira BG, Isaias RMS (2013) Developmental stem anatomy and tissue redifferentiation induced by a galling Lepidoptera on Marcetia taxifolia (Melastomataceae). Botany 91:752–760.  https://doi.org/10.1139/cjb-2013-0125 CrossRefGoogle Scholar
  16. Ferreira BG, Teixeira CT, Isaias RMS (2014) Efficiency of the polyethylene-glycol (PEG) embedding medium for plant Histochemistry. J Histochem Cytochem 62:577–583.  https://doi.org/10.1369/0022155414538265 CrossRefGoogle Scholar
  17. Gan S (2007) Senescence processes in plants. Blackwell, OxfordCrossRefGoogle 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 hostplant. J Insect Physiol 84:70–89.  https://doi.org/10.1016/j.jinsphys.2015.12.009 CrossRefGoogle Scholar
  19. Hanson P, Nishida K (2014) Insect galls of Costa Rica and their parasitoids. In: Fernandes GW, Santos JC (eds) Neotropical insect galls. Springer, Dordrecht, pp 497–517Google Scholar
  20. Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall former? Oecologia 113:492–501CrossRefGoogle Scholar
  21. Isaias RMS, Carneiro RGS, Santos JC, Oliveira DC (2014) Gall morphotypes in the Neotropics and the need to standardize them. In: Fernandes GW, Santos JC (eds) Neotropical insect galls. Springer, Dordrecht.  https://doi.org/10.1007/978-94-017-8783-3_4 Google Scholar
  22. Johansen DA (1940) Plant microtechnique. McGraw- Hill, New YorkGoogle Scholar
  23. Karnovsky M (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138Google Scholar
  24. Katimils Y, Azmaz M (2015) Investigation on the inquilines (Hymenoptera: Cynipidae, Synergini) of oak galls from inner western Anatolia, Turkey. Turk J Zool 39:168–173CrossRefGoogle Scholar
  25. Kołodziejek I, Kozioł J, Wałęza M, Mostowska A (2003) Ultrastructure of mesophyll cells and pigment content in senescing leaves of maize and barley. J Plant Growth Regul 22:217–227.  https://doi.org/10.1007/s00344-002-0024-1 CrossRefGoogle Scholar
  26. Korenko S, Hamouzová K, Kysilková K, Kolářová M, Kloss TG, Takasuka K, Pekár S (2018) Divergence in host utilisation by two spider ectoparasitoids within the genus Eriostethus (Ichneumonidae, Pimplinae). Zool Anz 272:1–5.  https://doi.org/10.1016/j.jcz.2017.11.006 CrossRefGoogle Scholar
  27. Kraus JE, Arduin M (1997) Manual básico de métodos em morfologia vegetal. Edur, SeropédicaGoogle Scholar
  28. Lingua G, Sgorbati S, Citterio A, Fusconi A, Trotta A, Gnavi E, Berta G (1999) Arbuscular mycorrhizal colonization delays nucleus senescence in leek root cortical cells. New Phytol 141:161–169.  https://doi.org/10.1046/j.1469-8137.1999.00328.x CrossRefGoogle Scholar
  29. Mani MS (1964) The ecology of plant galls. Dr. Junk, The HagueCrossRefGoogle Scholar
  30. Mete Ö, Mergen YO (2017) The community components associated with two common rose gall wasps (Hymenoptera: Cynipidae: Diplolepidini) in Turkey. Turk J Zool 41:696–701.  https://doi.org/10.3906/zoo-1602-20 CrossRefGoogle Scholar
  31. Meyer J, Maresquelle HJ (1983) Anatomie des galles. Gerbrüder Borntrager, BerlinGoogle Scholar
  32. O'brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373.  https://doi.org/10.1007/BF01248568 CrossRefGoogle Scholar
  33. Oliveira DC, Carneiro RGS, Magalhães TA, Isaias RMS (2011) Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae) - Cecidomyiidae gall systems. Protoplasma 248:829–837.  https://doi.org/10.1007/s00709-010-0258-x CrossRefGoogle Scholar
  34. Oliveira DC, Isaias RMS (2010) Cytological and histochemical gradients induced by a sucking insect in galls of Aspidosperma australe Arg. Muell (Apocynaceae). Plant Sci 178:350–358.  https://doi.org/10.1016/j.plantsci.2010.02.002 CrossRefGoogle Scholar
  35. Oliveira DC, Isaias RMS, 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 84:103–113.  https://doi.org/10.1016/j.jinsphys.2015.11.012 CrossRefGoogle Scholar
  36. Oliveira DC, Moreira ASFP, Isaias RMS (2014) Functional gradients in insect gall tissues: studies on Neotropical host plants. In: Fernandes GW, Santos JC (eds) Neotropical insect galls. Springer, Netherlands, Dordrecht.  https://doi.org/10.1093/aobpla/plv086 Google Scholar
  37. Oliveira DC, Moreira ASFP, Isaias RMS, Martini VC, Rezende UC (2017) Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). Front Plant Sci 8:01249.  https://doi.org/10.3389/fpls.2017.01249 CrossRefGoogle Scholar
  38. Raman A (2007) Insect-induced plant galls of India: unresolved questions. Curr Sci 92:748–757Google Scholar
  39. Rohfritsch O (1992) Patterns in gall development. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls, vol 87. Oxford University Press, Oxford, p 101Google Scholar
  40. Sanver D, Hawkins BA (2000) Galls as habitats: the inquiline communities of insect galls. Basic Appl Ecol 1:3–11.  https://doi.org/10.1078/1439-1791-00001 CrossRefGoogle Scholar
  41. Schönrogge K, Harper LJ, Lichtenstein CP (2000) The protein content of tissues in cynipid galls (Hymenoptera: Cynipidae): similarities between cynipid galls and seeds. Plant Cell Environ 23:215–222.  https://doi.org/10.1046/j.1365-3040.2000.00543.x CrossRefGoogle Scholar
  42. Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insects – nature’s most sophisticated herbivores. Basic Appl Ecol 6:407–411.  https://doi.org/10.1016/j.baae.2005.07.001 CrossRefGoogle Scholar
  43. Steinbauer MJ, Burns AE, Hall A, Riegler M, Taylor GS (2014) Nutritional enhancement of leaves by a psyllid through senescence-like processes: insect manipulation or plant defence? Oecologia 176:1061–1074.  https://doi.org/10.1007/s00442-014-3087-3 CrossRefGoogle Scholar
  44. Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522.  https://doi.org/10.1016/S0169-5347(03)00247-7 CrossRefGoogle Scholar
  45. Sugiura S, Yamazaki K (2009) Gall-attacking behavior in phytophagous insects, with emphasis on Coleoptera and Lepidoptera. Terr Arthropod Rev 2:41–61.  https://doi.org/10.1163/187498309x435658 CrossRefGoogle Scholar
  46. Sugiura S, Yamazaki K, Osono T (2006) Consequences of gall tissues as a food resource for a tortricid moth attacking cecidomyiid galls. Can Entomol 138:390–398.  https://doi.org/10.4039/n05-001 CrossRefGoogle Scholar
  47. Thomas H, Stoddart JL (1980) Leaf senescence. Ann Rev Plant Physiol 31: 83-111.Google Scholar
  48. Van Hezewijk BH, Roland J (2003) Gall size determines the structure of the Rabdophaga strobiloides host–parasitoid community. Ecol Entomol 28:593603–593603.  https://doi.org/10.1046/j.1365-2311.2003.00553.x Google Scholar
  49. Vecchi C, Menezes NL, Oliveira DC, Ferreira BG, Isaias RMS (2013) The redifferentiation of nutritive cells in galls induced by Lepidoptera on Tibouchina pulchra (Cham.) Cogn. Reveals predefined patterns of plant development. Protoplasma 250:1363–1368.  https://doi.org/10.1007/s00709-013-0519-6 CrossRefGoogle Scholar
  50. White TC (2012) The inadequate environment: nitrogen and the abundance of animals. Springer Science & Business Media.  https://doi.org/10.1007/978-3-642-78299-2
  51. Shorthouse JD, Rohfritsch O (1992) Biology of insect-induced galls. New York, OxfordGoogle Scholar
  52. Zamora R, Gómez JM (1993) Vertebrate herbivores as predators of insect herbivores: an asymmetrical interaction mediated by size differences. Oikos 66:223–228.  https://doi.org/10.2307/3544808 CrossRefGoogle Scholar
  53. Zhang H, Guiguet A, Dubreuil G, Kisiala A, Andreas P, Emery RJ, Huguet E, Body M, Giron D (2017) Dynamics and origin of cytokinins involved in plant manipulation by a leaf-mining insect. Insect Sci 24:1065–1078.  https://doi.org/10.1111/1744-7917.12500 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Uiara C. Rezende
    • 1
  • João Custódio F. Cardoso
    • 1
  • Vinícius C. Kuster
    • 2
  • Letícia A. Gonçalves
    • 2
  • Denis C. Oliveira
    • 1
    Email author
  1. 1.Laboratório de Anatomia, Desenvolvimento Vegetal e Interações (LADEVI); Instituto de BiologiaUniversidade Federal de Uberlândia—UFUUberlândiaBrazil
  2. 2.Instituto de Ciências BiológicasUniversidade Federal de Goiás—UFG, Regional JataíJataíBrazil

Personalised recommendations