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The redifferentiation of nutritive cells in galls induced by Lepidoptera on Tibouchina pulchra (Cham.) Cogn. reveals predefined patterns of plant development

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Abstract

Insect galls may present nutritive tissues with distinct cytological features related to the order of the gall inducer. Galling Lepidoptera larvae chew plant cells and induce the redifferentiation of parenchymatic cells into nutritive ones. The nutritive cells in the galls induced by a microlepidoptera on the leaves of Tibouchina pulchra (Cham.) Cogn. (Melastomataceae) are organelle-rich, with developed Golgi apparatus, endoplasmic reticulum, ribosomes, polyribosomes, mitochondria, plastids, and one great central or several fragmented vacuoles. The nonobservance of the nuclei in the nutritive cells deserves special attention, and confers a similarity between the nutritive cells and the vascular conductive ones. The great amount of rough endoplasmic reticulum, ribosomes, polyribosomes, and mitochondria is indicative of the high metabolic status of these cells. They are vascular cambium-like, with high protein synthesis and lipid storage. The proteins are essential to enzymatic metabolism, and secondarily, to larvae nutrition, similarly to the lipid droplets which confer energetic profile to these nutritive cells. The living enucleated cells receive mRNA from their neighbor ones, which may support the high metabolic profile of endoplasmic reticulum and ribosomes observed in galls. Thus, the nutritive cells are stimulated by the galling larvae activity, generating a new cell type, whose redifferentiation includes a mix of intrinsic and common plant pathways.

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References

  • Barnewall EC, De Clerck-Floate RA (2012) A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod-Plant Interactions 6:449–459. doi:10.1007/s11829-012-9193-4

    Article  Google Scholar 

  • Begnani CN (2001) Cloroplastos. In: Carvalho HF, Recco-Pimentel SM (eds) A Célula. Malone, Campinas, pp 187–198

    Google Scholar 

  • Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2010) Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Ann Bot 106(6):885–895. doi:10.1093/aob/mcq185

    Article  CAS  PubMed  Google Scholar 

  • Berlyn GP, Miksche JW (1976) Botanical microtechnique and cytochemistry. Iowa State, Ames

    Google Scholar 

  • Bertachini-Labello C, Carvalho HF (2001) Retículo endoplasmático. In: Carvalho HF, Recco-Pimentel SM (eds) A Célula. Malone, Campinas, pp 127–137

    Google Scholar 

  • Bertachini-Labello C, Dolder H, Carvalho HF (2001) Complexo de Golgi. In: Carvalho HF, Recco-Pimentel SM (eds) A Célula. Malone, Campinas, pp 138–148

    Google Scholar 

  • 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 118–137

    Google Scholar 

  • Carneiro MAA, Borges RAX, Araújo APA, Fernandes GW (2009) Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev Bras Entomol 53(4):570–592. doi:10.1590/s0085-56262009000400007

    Article  Google Scholar 

  • Chessen G, Fahn A (1988) Cell hypertrophy in stems of Pinus halepensis infested by Matsucoccus josephi. Protoplasma 143(2–3):111–117

    Article  Google Scholar 

  • Doering-Saad C, Newbury HJ, Couldridge CE, Bale JS, Pritchard J (2006) A phloem-enriched cDNA library from Ricinus: insights into phloem function. J Exp Bot 57(12):3183–3193. doi:10.1093/jxb/erl082

    Article  CAS  PubMed  Google Scholar 

  • Dreger-Jauffret F, Shorthouse JD (1992) Diversity of gall-inducing insects and their galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of Insect Induced-galls. Oxford University Press, Oxford, pp 60–86

    Google Scholar 

  • Evert RF (1977) Phloem structure and histochemistry. Ann Rev Pl Physiol 28:199–222

    Article  CAS  Google Scholar 

  • Evert RF, Bharati P, Deshpande P (1969) Electron microscope investigation of sieve-element ontogeny and structure in Ulmus americana. Protoplasma 68:403–432

    Article  Google Scholar 

  • Farrar JJ, Evert RF (1997) Seasonal changes in the ultrastructure of the vascular cambium of Robinia pseudoacacia. Trees 11:191–202

    Google Scholar 

  • Gomes L, Pimentel ER, Recco-Pimentel SM (2001) Ribossomos e a Síntese protéica. In: Carvalho HF, Recco-Pimentel SM (eds) A Célula. Malone, Campinas, pp 116–126

    Google Scholar 

  • Guellete BS, Benning UF, Hoffmann-Benning S (2012) Identification of lipids and lipid-binding proteins in phloem exudates from Arabidopsis thaliana. J Exp Bot 63(10):3603–3616. doi:10.1093/jxb/ers028

    Article  Google Scholar 

  • Heldt HW, Piechulla B (2011) Plant biochemistry. Academic, London

    Google Scholar 

  • Isaias RMS, Oliveira DC, Carneiro RGS (2011) Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae). Bot 89:581–592. doi:10.1139/b11-048

    Article  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. Mc-Graw-Hill Book, New York

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Kraus JE, Sousa HC, Resende MH, Castro NM, Vecchi C, Luque R (1998) Astra blue and basic fuchsin double staining of plant material. Biotechnic & Histohemistry 73:235–243

    Article  CAS  Google Scholar 

  • Lehninger AL, Nelson DL, Cox MM (1995) Princípios de Bioquímica. SARVIER, São Paulo

    Google Scholar 

  • Lev-Yadun S (2003) Stem cells in plants are differentiated too. Current Opinion in Plant Biology 4:93–100

    Google Scholar 

  • Lima ES, Magenta MAG, Kraus JE, Vecchi C, Martins SE (2000) Levantamento preliminar de galhas entomógenas ocorrentes em plantas da restinga de Bertioga (SP). Anais do V simpósio de ecossistemas brasileiros: Conservação 3:39–46

    Google Scholar 

  • Maffei ME, Mithofer A, Boland W (2007) Before gene expression: early events in plant-insect interaction. Trends Plant Sci 12:310–316. doi:10.1016/j.tplants.2007.06.001

    Article  CAS  PubMed  Google Scholar 

  • Mani MS (1964) Ecology of plant galls. Dr. W Junk Publishers, The Hague

    Google Scholar 

  • Mani MS (1992) Introduction to cecidology. In: Shorthouse JD, Rohfritsch O (eds) Biology of Insect Induced-galls. Oxford University Press, Oxford, pp 3–7

    Google Scholar 

  • Mendonça MS Jr (2007) Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the Neotropics. Bol Soc Argent Bot 42(3–4):347–357

    Google Scholar 

  • Meyer J (1987) Plant galls and gall inducers. Gebrüder Bomtraeger, Berlin

    Google Scholar 

  • Meyer J, Maresquele HJ (1983) Anatomie des Galles. Gebrüder Bomtrager, Berlin

    Google Scholar 

  • Moura MZD, Soares GLG, Isaias RMS (2008) Species-especific changes in tissue morphogenesis induced by two arthropod leaf gallers in Lantana camara (Verbenaceae). Austr J Bot 56:153–160. doi:10.1071/BT07131

    Article  Google Scholar 

  • Occhioni P (1979) “Galhas”, “Cecídias” ou “Tumores vegetais” em plantas nativas da flora do Brasil. Leandra 8–9:5–35

    Google Scholar 

  • 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. doi:10.1016/j.plantsci.2010.02.002

    Article  Google Scholar 

  • Oliveira DC, Christiano JCS, Soares GLG, Isaias RMS (2006) Reações de defesas químicas e estruturais de Lonchocarpus mulherbergianus (Fabaceae) à ação do galhador Euphalerus ostreoides (Hemiptera: Psyllidae). Rev Bras Bot 29(4):657–667

    Article  CAS  Google Scholar 

  • Oliveira DC, Magalhães TA, Carneiro RGS, Alvim MN, Isaias RMS (2010) Do Cecidomyiidae galls of Aspidosperma spruceanum (Apocynaceae) fit the pre-established cytological and histochemical patterns? Protoplasma 242:81–93. doi:10.1007/s00709-010-0128-6

    Article  CAS  PubMed  Google Scholar 

  • Oliveira DC, Carneiro RGS, Magalhães TA, Isaias RMS (2011a) Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae)—Cecidomyiidae gall systems. Protoplasma 248:829–837. doi:10.1007/s00709-010-0258-x

    Article  CAS  PubMed  Google Scholar 

  • Oliveira DC, Isaias RMS, Moreira ASFP, Magalhães TA, Lemos-Filho JP (2011b) Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis? Plant Sci 180:489–495. doi:10.1016/j.plantsci.2010.11.005

    Article  PubMed  Google Scholar 

  • Pearse AGE (1968) Histochemistry: theoretical and applied, 3rd edn., v 1. JA Churchill Ltd., London

  • Pimentel E (2001) Mitocôndrias. In: Carvalho HF, Recco-Pimentel SM (eds) A Célula. Malone, Campinas, pp 160–171

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  Google Scholar 

  • Robbers JE, Speedie MK, Tyler VE (1996) Pharmacognosy and pharmacobiotechnology. Williams & Wilkins, Baltimore

    Google Scholar 

  • Rohfritsch O (1978) Three-dimensional study of cell organelles in the nutritive tissue of a gall (Liposthenes glechomae L. on Glechoma hederacea L.). Protoplasma 95:297–307

    Article  Google Scholar 

  • Rohfritsch O (1992) Patterns in gall development. In: Shorthouse JD, Rohfritsch O (eds) Biology of Insect Induced-galls. Oxford University Press, Oxford, pp 60–86

    Google Scholar 

  • Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187. doi:10.1111/j.1365-313X.2004.02199.x

    Article  CAS  PubMed  Google Scholar 

  • Sennerby-Forsse L (1986) Seasonal variation in the ultrastructure of the cambium in young stems of willow (Salix viminalis) in relation to phenology. Physiologia Plantarum 67:529–537

    Article  Google Scholar 

  • Shorthouse JD (1986) Significance of nutritive cells in insect galls. Proc Entomol Soc Washington 88:368–375

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Google Scholar 

  • Stone GN, Schonrögge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18(10):512–522. doi:10.1016/S0169-5347(03)00247-7

    Article  Google Scholar 

  • Tavares JS (1919) As cecídias do Brasil que se criam nas plantas da família Melastomataceae. Brotéria: Série Zoológica 15:18–40

    Google Scholar 

  • Tavares JS (1922) Cecidologia Brazileira. As restantes das Famílias. Brotéria: Série Zoológica 20:5–48

    Google Scholar 

  • Van Bel AJE, Ehlers K, Knoblauch M (2002) Sieve elements caught in the act. Trends Plant Sci 7(3):126–132. doi:10.1016/S1360-1385(01)02225-7

    Article  PubMed  Google Scholar 

  • Vecchi C (1999) Galha foliar em Tibouchina pulchra (Cham.) Cogn. (Melastomataceae) morfo-anatomia e ontogenia. Dissertation (Botânica). Universidade de São Paulo, São Paulo

    Google Scholar 

  • Vidal BC, Mello MLS (1987) Biologia celular. Atheneu, São Paulo, p 347

Download references

Acknowledgments

The authors thank CAPES, CNPq, and FAPEMIG for financial support and R.G.S. Carneiro for language revision.

Conflict of interest

The authors declare no conflict of interest in the manuscript entitled “The redifferentiaton of nutritive cells of galls induced by Lepidoptera on T. pulchra (Cham.) Cogn. reveals predefined patterns on plant development.”

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Authors and Affiliations

  1. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Matão 277, Travessa 14, P.O. Box 11461, 05422-970, Cidade Universitária, São Paulo, Brazil

    Claudia Vecchi & Nanuza Luiza Menezes

  2. Instituto de Biologia, Universidade Federal de Uberlândia (UFU), Campus Umuarama, 38400-902, P.O. Box 593, Uberlândia, Minas Gerais, Brazil

    Denis Coelho Oliveira

  3. Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais (UFMG), Av. Antônio Carlos 6627, Pampulha, P.O. Box 486, 31270-901, Belo Horizonte, Minas Gerais, Brazil

    Bruno Garcia Ferreira & Rosy Mary Santos Isaias

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  1. Claudia Vecchi
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  2. Nanuza Luiza Menezes
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Correspondence to Rosy Mary Santos Isaias.

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Vecchi, C., Menezes, N.L., Oliveira, D.C. et al. 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 (2013). https://doi.org/10.1007/s00709-013-0519-6

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