pp 1–16 | Cite as

Cytological attributes of storage tissues in nematode and eriophyid galls: pectin and hemicellulose functional insights

  • Bruno G. Ferreira
  • Gracielle P. Bragança
  • Rosy M. S. IsaiasEmail author
Original Article


Cell walls and protoplast may work together or distinctly in the establishment of the functional profiles of gall tissue compartments. This presumption is herein evaluated in three gall systems by immunocytochemical and ultrastructural analyses. The common storage tissues (CSTs) of leaf galls induced by Eriophyidae on Miconia ibaguensis leaves and by Ditylenchus gallaeformans on M. ibaguensis and M. albicans have rigid and porous cell walls due to their composition of pectins. Hemicelluloses in CST cell walls are scarcer when compared to the cell walls of the control leaves, being functionally compensated by rigid pectate gels. The typical nutritive tissues (TNTs) in galls induced by Ditylenchus gallaeformans are similar to promeristematic and secretory cells regarding their enriched cytoplasm, several mitochondria, and proplastids, as well as multivesicular and prolamellar bodies in cell membranes. The cytological features of the feeding cells of Eriophyidae galls indicate that they are not as metabolically active as the cells of the TNT in nematode galls. However, their cell wall composition suggests more plasticity and porosity than the cells of the TNT, which can compensate the less production of nutrients with more transport. The ultrastructural and immunocytochemical profiles of CST cells reveal functional similarities, which are independent of the taxa of the gall inducer or of the host plant. Despite their analogous functionalities, the protoplast and cell wall features of TNT cells of nematode galls and of the feeding cells of the Eriophyidae galls are distinct, and work out through different strategies toward keeping gall developmental site active.


Hemicelluloses Nutritive tissue Pectins Plant cell functionality Ultrastructure 


Author contributions

BGF and RMSI conceived and designed the research. BGF and GPB conducted the experiments. All authors analyzed the data, wrote and reviewed the manuscript, and read and approved the final version.

Funding information

This project is financially supported by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (process number APQ-02617-15). The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) also financially supported this study and provided posdoctoral grant to BGF (process number 171182/2017-0) and researcher grant to RMSI (process number 307011/2015-1).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2011) Plant cell walls: from chemistry to biology. Garland Science, New YorkGoogle Scholar
  2. Appezzato-Da-Glória B, Machado SR (2004) Ultrastructural analysis of in vitro direct and indirect organogenesis. Rev Bras Bot 27:429–437Google Scholar
  3. 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). Biochem Syst Ecol 55:53–59CrossRefGoogle Scholar
  4. Bozbuga R, Lilley CJ, Knox JP, Urwin PE (2018) Host-specific signatures of the cell wall changes induced by the plant parasitic nematode, Meloidogyne incognita. Sci Rep 8:17302CrossRefGoogle Scholar
  5. Bragança GP, Oliveira DC, Isaias RMS (2017) Compartmentalization of metabolites and enzymatic mediation in nutritive cell of Cecidomyiidae galls on Piper arboretum Aubl. (Piperaceae). J Plant Stud 6:11–22CrossRefGoogle Scholar
  6. 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, New York, pp 118–140Google Scholar
  7. Buckeridge MS, Santos HP, Tiné MAS (2000) Mobilisation of storage cell wall polysaccharides in seeds. Plant Physiol Biochem 38:141–156CrossRefGoogle Scholar
  8. Carneiro RGS, Isaias RMS (2015a) Cytological cycles and fates in Psidium myrtoides are altered towards new cell metabolism and functionalities by the galling activity of Nothotrioza myrtoidis. Protoplasma 252:637–646CrossRefGoogle Scholar
  9. Carneiro RGS, Isaias RMS (2015b) Gradients of metabolite accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking insects. AoB Plants 7:plv086CrossRefGoogle Scholar
  10. Carneiro RGS, Oliveira DC, Isaias RMS (2014) Developmental anatomy and immunocytochemistry reveal the neo-ontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae). Plant Cell Rep 33:2093–2106CrossRefGoogle Scholar
  11. Carneiro RGS, Pacheco P, Isaias RMS (2015) Could the extended phenotype extend to the cellular and subcellular levels in insect-induced galls? PLoS One 10(6):e0129331CrossRefGoogle Scholar
  12. Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:71–201CrossRefGoogle Scholar
  13. Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:204CrossRefGoogle Scholar
  14. Dropkin VH (1969) Cellular responses of plants to nematode infections. Annu Rev Phytopathol 7:101–122CrossRefGoogle Scholar
  15. Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function and development, 3rd edn. Wiley, HobokenCrossRefGoogle Scholar
  16. Fahn A (1979) Ultrastructure of nectaries in relation to nectar secretion. Am J Bot 66:977–985CrossRefGoogle Scholar
  17. Fahn A (1988) Secretory tissues in vascular plants. New Phytol 108:229–257CrossRefGoogle Scholar
  18. Ferreira BG, Isaias RMS (2013) Developmental stem anatomy and tissue redifferentiation induced by a galling Lepidoptera on Marcetia taxifolia (Melastomataceae). Botany 91:752–760CrossRefGoogle Scholar
  19. Ferreira BG, Isaias RMS (2014) Floral-like destiny induced by a galling Cecidomyiidae on the axillary buds of Marcetia taxifolia (Melastomataceae). Flora 209:391–400CrossRefGoogle Scholar
  20. Ferreira BG, Carneiro RGS, Isaias RMS (2015) Multivesicular bodies differentiate exclusively in nutritive fast-dividing cells in Marcetia taxifolia galls. Protoplasma 252:1275–1283CrossRefGoogle Scholar
  21. Ferreira BG, Álvarez R, Avritzer SC, Isaias RMS (2017a) Revisiting the histological patterns of storage tissues: beyond the limits of gall-inducing taxa. Botany 95:173–184CrossRefGoogle Scholar
  22. Ferreira BG, Avritzer SC, Isaias RMS (2017b) Totipotent nutritive cells and indeterminate growth in galls of Ditylenchus gallaeformans (Nematoda) on reproductive apices of Miconia. Flora 227:36–45CrossRefGoogle Scholar
  23. Ferreira BG, Oliveira DC, Moreira ASFP, Faria AP, Guedes LM, França MGC, Álvarez R, Isaias RMS (2018) Antioxidant metabolism in galls due to the extended phenotypes of the associated organisms. PLoS One 13:e0205364CrossRefGoogle Scholar
  24. Ferreira BG, Álvarez R, Bragança GP, Alvarenga DR, Pérez-Hidalgo N, Isaias RMS (2019a) Feeding and other gall facets: patterns and determinants in gall structure. Bot Rev 85:78–106. CrossRefGoogle Scholar
  25. Ferreira BG, Freitas MSC, Bragança GP, Moreira ASFP, Carneiro RGS, Isaias RMS (2019b) Enzyme-mediated metabolism in nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda: Anguinidae). Plant Biol.
  26. Formiga AT, Oliveira DC, Ferreira BG, Magalhães TA, Castro AC, Fernandes GW, Isaias RMS (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 250:899–908CrossRefGoogle Scholar
  27. Gao M, Showalter AM (1999) Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. Plant J 19:321–331CrossRefGoogle Scholar
  28. Gifford EM, Stewart KD (1967) Ultrastructure of the shoot apex of Chenopodium album and certain other seed plants. J Cell Biol 33:131–142CrossRefGoogle Scholar
  29. Isaias RMS, Ferreira BG, Alvarenga DR, Barbosa LR, Salminen J-P, Steinbauer MJ (2018) Functional compartmentalisation of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Aust Entomol 57:238–246CrossRefGoogle Scholar
  30. Jarvis MC (1984) Structure and properties of pectic gels in plant cell walls. Plant Cell Environ 7:153–164Google Scholar
  31. Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4) β-D-galactan. Plant Physiol 113:1405–1412CrossRefGoogle Scholar
  32. Jones L, Milne JF, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proceedings of the National Academy of Sciences 100:11783–11788.
  33. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138Google Scholar
  34. Kostoff D, Kendall J (1929) Studies on the structure and development of certain Cynipid galls. Biol Bull 56:402–458CrossRefGoogle Scholar
  35. Kraus JE, Arduin M (1997) Manual básico de métodos em Morfologia Vegetal. Editora da Universidade Federal Rural do Rio de Janeiro, SeropédicaGoogle Scholar
  36. Leroux O, Knox JP, Masschaele B, Bagniewska-Zadworna A, Marcus SE, Claeys M, Van Hoorebeke L, Viane RLL (2011) An extensin-rich matrix lines the carinal canals in Equisetum ramosissimum, which may function as water-conducting channels. Ann Bot 108(2):307–319. CrossRefGoogle Scholar
  37. Magalhães TA, Oliveira DC, Suzuki AYM, Isaias RMS (2014) Patterns of cell elongation in the determination of the final shape in galls of Baccharopelma dracunculifoliae (Psyllidae) on Baccharis dracunculifolia DC (Asteraceae). Protoplasma 251:747–753CrossRefGoogle Scholar
  38. Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan protein in plant development. Plant Physiol 122:3–9CrossRefGoogle Scholar
  39. Mani MS (1964) Ecology of plant galls. Dr. W Junk, The HagueCrossRefGoogle Scholar
  40. Marcus SE, Verhertbruggen Y, Herve C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WGT, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60CrossRefGoogle Scholar
  41. Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert A, Gilbert HJ, Willats WGT, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 61:191–203CrossRefGoogle Scholar
  42. Mastroberti AA, Mariath JEA (2008) Developmental of mucilage cells of Araucaria angustifolia (Araucariaceae). Protoplasma 232:233–245CrossRefGoogle Scholar
  43. McCann MC, Knox JP (2018) Plant cell wall biology: polysaccharides in architectural and developmental contexts. Ann Plant Rev 41:343–366CrossRefGoogle Scholar
  44. McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546CrossRefGoogle Scholar
  45. Meyer J (1987) Plant galls and gall inducers. Gebrüder Borntraeger, BerlinGoogle Scholar
  46. O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termacarphi Pty Ltd, MelbourneGoogle Scholar
  47. Oliveira DC, Isaias RMS (2010) Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). S Afr J Bot 76:239–248CrossRefGoogle Scholar
  48. 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 242:81–93CrossRefGoogle Scholar
  49. Oliveira DC, Carneiro RGS, Magalhães TA, Isaias RMS (2011a) Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae) Cecidomyiidae gall systems. Protoplasma 248:829–837CrossRefGoogle Scholar
  50. 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 180:489–495CrossRefGoogle Scholar
  51. Oliveira DC, Magalhães TA, Ferreira BG, Teixeira CT, Formiga AT, Fernandes GW, Isaias RMS (2014) Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. PLoS One 9:e94588CrossRefGoogle Scholar
  52. 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 84:103–113CrossRefGoogle Scholar
  53. Razem FA, Davis AR (1999) Anatomical and ultrastructural changes of the floral nectary of Pisum sativum L. during flower development. Protoplasma 206:57–72CrossRefGoogle Scholar
  54. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212Google Scholar
  55. Sabba RP, Lulai EC (2005) Immunocytological analysis of potato tuber periderm and changes in pectin and extensin epitopes associated with periderm maturation. J Am Soc Hortic Sci 130:936–942CrossRefGoogle Scholar
  56. Sala K, Malarz K, Barlow PW, Kurczyńska EU (2017) Distribution of some pectic and arabinogalactan protein epitopes during Solanum lycopersicum (L.) adventitious root development. BMC Plant Biology 17:25.
  57. Santos HP, Purgatto E, Mercier H, Buckeridge MS (2004) The control of storage xyloglucan mobilization in cotyledons of Hymenaea courbaril. Plant Physiol 135:287–299CrossRefGoogle Scholar
  58. Schindler TM, Bergfeld R, Van Cutsem P, von Sengbusch D, Schopfer P (1995) Distribution of pectins in cell walls of maize coleoptiles and evidence against their involvement in auxin-induced extension growth. Protoplasma 188:213–224CrossRefGoogle Scholar
  59. Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insects – nature’s most sophisticated herbivores. Basic Appl Ecol 6:407–411CrossRefGoogle Scholar
  60. Smallwood M, Yates EA, Willats WG, Martin H, Knox JP (1996) Immunochemical comparison of membrane associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459CrossRefGoogle Scholar
  61. Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522CrossRefGoogle Scholar
  62. 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 93:435–444CrossRefGoogle Scholar
  63. Thomas E, Konar RN, Street HE (1972) The fine structure of the embryogenic callus of Ranunculus sceleratus L. J Cell Sci 11:95–109Google Scholar
  64. 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 250:1363–1368Google Scholar
  65. Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862CrossRefGoogle Scholar
  66. Weischer B, Wyss U (1976) Feeding behaviour and pathogenicity of Xiphinema index on grapevine roots. Nematol 22:319–325CrossRefGoogle Scholar
  67. Willats WGT, Marcus SE, Knox JP (1998) Generation of monoclonal antibody specific to (1-5)-α-L-arabinan. Carbohydr Res 308:149–152CrossRefGoogle Scholar
  68. Willats WGT, Limberg G, Buchholt HC, Vanalebeeck GJ, Benen J, Christensen TMIE, Visser J, Voragen A, Mikkelsen JD, Knox JP (2000) Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defines oligossaccharides, polysaccharides, and enzymatic degradation. Carbohydr Res 327:309–320CrossRefGoogle Scholar
  69. Willats WG, McCartney L, Mackie W, Knox JP (2001a) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27CrossRefGoogle Scholar
  70. Willats WG, Orfila C, Limberg G, Buchholt HC, van Alebeek GJ, Voragen AG, Marcus SE, Christensen TM, Mikkelsen JD, Murray BS, Knox JP (2001b) Modulation of the degree and pattern of methylesterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem 276:19404–19413CrossRefGoogle Scholar
  71. Willats WGT, McCarney L, Steele-King CG, Marcus SE, Mort A, Huisman M, van Alebeek G-J, Schols HA, Voragen AGJ, Le Goff A, Bonnin E, Thibault J-F, Knox JP (2004) A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218:673–681CrossRefGoogle Scholar
  72. Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:169–175CrossRefGoogle Scholar
  73. Wyss U (1997) Root parasitic nematodes: an overview. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant-nematode interactions. Kluwer Academic Publishers, Dordrecht, pp 5–22CrossRefGoogle Scholar
  74. Yates EA, Valdor JF, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139CrossRefGoogle Scholar
  75. Zhao Q, Yuan S, Wang X, Zhang Y, Zhu H, Lu C (2008) Restoration of mature etiolated cucumber hypocotyl cell wall susceptibility to expansin by pretreatment with fungal pectinases and EGTA in vitro. Plant Physiol 147:1874–1885CrossRefGoogle Scholar
  76. Zykwinska AW, Ralet MCJ, Garnier CD, Thibault JFJ (2005) Evidence for in vitro binding of pectin side chains to cellulose. Plant Physiol 139:397–407CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Bruno G. Ferreira
    • 1
    • 2
  • Gracielle P. Bragança
    • 2
  • Rosy M. S. Isaias
    • 2
    Email author
  1. 1.Department of Botany, Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Department of BotanyUniversidade Federal de Minas GeraisBelo HorizonteBrazil

Personalised recommendations