Influence of auxin and phenolic accumulation on the patterns of cell differentiation in distinct gall morphotypes on Piptadenia gonoacantha (Fabaceae)
Cibele Souza Bedetti A , Gracielle Pereira Bragança A and Rosy Mary dos Santos Isaias A BA Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Caixa Postal 486, CEP31270-901, Belo Horizonte, Minas Gerais, Brazil.
B Corresponding author. Email: rosy@icb.ufmg.br
Australian Journal of Botany 65(5) 411-420 https://doi.org/10.1071/BT16257
Submitted: 16 December 2016 Accepted: 15 June 2017 Published: 10 August 2017
Abstract
The cascade of biochemical changes occurring at sites of gall development seems to involve a group of common metabolites in plants, namely, the phenolics. Phenolic accumulation has been commonly related to chemical defence, but their primary role seems to be the regulation of cell hypertrophy in galls. Such regulation implies phenolics–auxin (IAA) association at some cell re-differentiation sites, and determines final gall shapes. Herein, we investigated phenolic and auxin accumulation in four gall systems, grouped in two morphotypes, namely lenticular and globoid, induced on pinnulas of Piptadenia gonoacantha (Mart.) J.F.Macbr. Changes in the direction and type of cell expansion between non-galled pinnula and galls were also evaluated. Galling insects associated to lenticular and globoid gall morphotypes promoted changes in host plant cells, leading to the development of different cell sizes, different degrees of anisotropy, and different directions of cell expansion. The accumulation of IAA–phenolics compartmentalised on the basis of gall morphotype, i.e. in the cells of superior and lateral inferior cortices in the lenticular gall morphotypes, and throughout the outer cortex in the globoid gall morphotypes. The sites of accumulation of IAA and phenolics coincided with the most hypertrophied regions, influencing on the determination of the final gall shape.
Additional keywords: Cecidomyiidae galls, developmental anatomy, histochemistry.
References
Abrahamson WG, McCrea KD, Whitwell AJ, Vermieri LA (1991) The role of phenolics in goldenrod ball gall resistance and formation. Biochemical Systematics and Ecology 19, 615–622.| The role of phenolics in goldenrod ball gall resistance and formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhtVarsrg%3D&md5=2daa467a1c2bb92de7c26ad8eb83af48CAS |
Arduin M, Kraus JE (1995) Anatomia e ontogenia de galhas foliares de Piptadenia gonoacantha (Fabales, Mimosaceae). Boletim de Botânica da Universidade de São Paulo 14, 109–130.
Arduin M, Kraus JE, Montenegro G (1994) Morfologia e fenologia de galhas foliares de Piptadenia gonoacantha (Fabales, Mimosaceae). Revista Brasileira de Entomologia 38, 79–89.
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annual Review of Cell and Developmental Biology 21, 203–222.
| Anisotropic expansion of the plant cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlektbrO&md5=551e1da8dccaa996289c977751d533a6CAS |
Bedetti CS, Modolo LV, Isaias RMS (2014) The role of phenolics in the control of auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae). Biochemical Systematics and Ecology 55, 53–59.
| The role of phenolics in the control of auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOjs7vL&md5=ac46e8d6f183c9335139d49c74f1b123CAS |
Bragança GP, Oliveira DC, Isaias RM (2017) Compartmentalization of metabolites and enzymatic mediation in nutritive cells of cecidomyiidae galls on Piper arboreum Aubl. (Piperaceae). Journal of Plant Studies
| Compartmentalization of metabolites and enzymatic mediation in nutritive cells of cecidomyiidae galls on Piper arboreum Aubl. (Piperaceae).Crossref | GoogleScholarGoogle Scholar |
Bukatsch F (1972) Bermerkungen zur Doppelfärbung Astrablau–Safranin. Mikrokosmos 61, 255
Carlquist S (1982) The use of ethylenediamine in softening hard plant structures for paraffin sectioning. Stain Technology 57, 311–317.
| The use of ethylenediamine in softening hard plant structures for paraffin sectioning.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2FpsVahtg%3D%3D&md5=a2be027852bb6e19cd150b558699110aCAS |
Carneiro RGS, Oliveira DC, Isaias RMS (2014a) Developmental anatomy and immunocytochemistry reveal the neoontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae). Plant Cell Reports 33, 2093–2106.
| Developmental anatomy and immunocytochemistry reveal the neoontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFKmsr%2FN&md5=dead21da8007263b66762d004c1a989fCAS |
Carneiro RGS, Castro AC, Isaias RMS (2014b) Unique histochemical in a photosynthesis-deficient plant gall. South African Journal of Botany 92, 97–104.
| Unique histochemical in a photosynthesis-deficient plant gall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVertL4%3D&md5=cc645b88c24782159b3f1e13ecdc899fCAS |
Crowell EF, Gonneau M, Vernhettes S, Höfte H (2010) Regulation of anisotropic cell expansion in higher plants. Comptes Rendus Biologies 333, 320–324.
| Regulation of anisotropic cell expansion in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlCqsL8%3D&md5=3029dc8e545b71f9f9847eb3f5516535CAS |
Dias GG, Ferreira BG, Moreira GRP, Isaias RMS (2013) Developmental pathway from leaves to galls induced by a sap-feeding insect on Schinus polygamus (Cav.) Cabrera (Anacardiaceae). Anais da Academia Brasileira de Ciencias 85, 187–200.
| Developmental pathway from leaves to galls induced by a sap-feeding insect on Schinus polygamus (Cav.) Cabrera (Anacardiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFOmtL4%3D&md5=29079566ea48f24e48b3bcc32437e654CAS |
Fleury G, Ferreira BG, Soares GLG, Oliveira DC, Isaias RMS (2015) Elucidating the determination of the rosette galls induced by Pisphondylia brasiliensis Couri and Maia 1992 (Cecidomyiidae) on Guapira opposita (Nyctaginaceae). Australian Journal of Botany 63, 608–617.
| Elucidating the determination of the rosette galls induced by Pisphondylia brasiliensis Couri and Maia 1992 (Cecidomyiidae) on Guapira opposita (Nyctaginaceae).Crossref | GoogleScholarGoogle Scholar |
Formiga AT, Silveira FAO, Fernandes GW, Isaias RMS (2015) Phenotypic plasticity and similarity among gall morphotypes on a superhost, Baccharis reticularia (Asteraceae). Plant Biology 17, 512–521.
| Phenotypic plasticity and similarity among gall morphotypes on a superhost, Baccharis reticularia (Asteraceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M%2Fhslyguw%3D%3D&md5=db3cc4a149179e219e676165227bf342CAS |
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.
Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall former? Oecologia 113, 492–501.
| The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall former?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1czns1GgtQ%3D%3D&md5=6da79baf703349a7502e42d2b9fec9acCAS |
Hartley SE (1999) Are gall insects large rhizobia? Oikos 84, 333–342.
| Are gall insects large rhizobia?Crossref | GoogleScholarGoogle Scholar |
Hori K (1992) Insect secretions and their effect on plant growth, with special reference to hemipterans. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 157–170. (Oxford University Press: Oxford, UK)
Isaias RMS, Oliveira DC, Carneiro RGS (2011) Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae). Botany 89, 581–592.
| Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Isaias RMS, Carneiro RGS, Oliveira DC, Santos JC (2013) Illustrated and annoted checklist of Brazilian gall morphotypes. Neotropical Entomology 42, 230–239.
| Illustrated and annoted checklist of Brazilian gall morphotypes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sbgtVeguw%3D%3D&md5=c1f0cef47ae6815069885e534978d791CAS |
Isaias RMS, Oliveira DC, Carneiro RGS, Kraus JE (2014) Developmental anatomy of galls in the neotropics: arthopods stimuli versus host plant constraints. In ‘Neotropical insect galls’. (Eds GW Fernandes, JC Santos) pp. 15–34. (Springer: Heidelberg, Germany)
Isaias RMS, Oliveira DC, Moreira ASFP, Soares GLG, Carneiro RGS (2015) The imbalance of redox homeostasis in arthropod-induced plant galls: mechanisms of stress generation and dissipation. Biochimica et Biophysica Acta 1850, 1509–1517.
| The imbalance of redox homeostasis in arthropod-induced plant galls: mechanisms of stress generation and dissipation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsVOjs74%3D&md5=2277f6e00c282c408a7faa20215324dfCAS |
Johansen DA (1940) ‘Plant microtechnique.’ (McGraw-Hill Books: New York)
Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. The Journal of Cell Biology 27, 137–138.
Kraus JE, Arduin M (1997) ‘Manual básico de métodos em morfologia vegetal.’ (EDUR: Seropédica, Brazil)
Leopold AC, Plummer TH (1961) Auxin–phenol complexes. Plant Physiology 36, 589–592.
| Auxin–phenol complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3MXht1Gktrc%3D&md5=a5a914c96b844fdf14a641b9f1b6801bCAS |
Magalhães TA, Oliveira DC, Suzuki AYM, Isaias RMS (2014) Patterns of cell elongation in the determination of the final shape of Baccharopelma dracunculifoliae DC. (Psyllidae). Protoplasma 251, 747–753.
| Patterns of cell elongation in the determination of the final shape of Baccharopelma dracunculifoliae DC. (Psyllidae).Crossref | GoogleScholarGoogle Scholar |
Mani MS (1964) ‘Ecology of plant galls.’ (Dr. W. Junk: The Hague, Netherlands)
Mapes CC, Davies PJ (2001) Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytologist 151, 195–202.
| Indole-3-acetic acid and ball gall development on Solidago altissima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltFGrsr8%3D&md5=c33bbca3ef3ec43e5115c78ac9bed6b4CAS |
Oliveira DC, Isaias RMS (2009) Influence of leaflet age in anatomy and possible adaptive values of midrib gall of Copaifera langsdorffii (Fabaceae: Caesalpinoideae). Revista de Biologia Tropical 57, 293–302.
Oliveira DC, Isaias RMS (2010) Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). South African Journal of Botany 76, 239–248.
| Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Oliveira DC, Christiano JCS, Soares GLG, Isaias RMS (2006) Reações de defesas químicas e estruturais de Lonchocarpus muehlbergianus Hassl. (Fabaceae) à ação do galhador Euphalerus ostreoides Crawf. (Hemiptera: Psyllidae). Revista Brasileira de Botanica. Brazilian Journal of Botany 29, 657–667.
| Reações de defesas químicas e estruturais de Lonchocarpus muehlbergianus Hassl. (Fabaceae) à ação do galhador Euphalerus ostreoides Crawf. (Hemiptera: Psyllidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs12rtrk%3D&md5=8e868fd77fee84f0fdbb0f367e59b0b2CAS |
Paiva JGA, Fank-De-Carvalho SM, Magalhães MP, Graciano-Ribeiro D (2006) Verniz vitral incolor 500®: uma alternativa de meio de montagem economicamente viável. Acta Botanica Brasílica 20, 257–264.
| Verniz vitral incolor 500®: uma alternativa de meio de montagem economicamente viável.Crossref | GoogleScholarGoogle Scholar |
Rohfritsch O (1992) Patterns in gall development. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 60–86. (Oxford University Press: Oxford, UK)
Souza VC, Lorenzi H (2005) ‘Botânica sistemática: guia ilustrado para identificação das famílias de Angiospermas da flora brasileira, baseado em AGP II.’ (Instituto Plantarum de Estudos da Flora LTDA: São Paulo, Brazil)
Stone GN, Schonrögge K (2003) The adaptive significance of insect gall morphology. Trends in Ecology & Evolution 18, 512–522.
| The adaptive significance of insect gall morphology.Crossref | GoogleScholarGoogle Scholar |
Suzuki AYM, Bedetti CS, Isaias RMS (2015) Detection and distribution of cell growth regulators and cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae). Botany 93, 435–444.
| Detection and distribution of cell growth regulators and cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptFSms7k%3D&md5=29844f7932025e48bcdaafbc09994aadCAS |
Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species alterslevels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod–Plant Interactions 5, 115–124.
| Feeding by a gall-inducing caterpillar species alterslevels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems.Crossref | GoogleScholarGoogle Scholar |