Could the Extended Phenotype Extend to the Cellular and Subcellular Levels in Insect-Induced Galls?

PLoS One. 2015 Jun 8;10(6):e0129331. doi: 10.1371/journal.pone.0129331. eCollection 2015.

Abstract

Neo-ontogenesis of plant galls involves redifferentiation of host plant tissues to express new phenotypes, when new cell properties are established via structural-functional remodeling. Herein, Psidium cattleianum leaves and Nothotrioza cattleiani galls are analyzed by developmental anatomy, cytometry and immunocytochemistry of cell walls. We address hypothesis-driven questions concerning the organogenesis of globoid galls in the association of P. cattleianum-N. cattleianum, and P. myrtoides-N. myrtoidis. These double co-generic systems represent good models for comparing final gall shapes and cell lineages functionalities under the perspective of convergent plant-dependent or divergent insect-induced characteristics. Gall induction, and growth and development are similar in both galls, but homologous cell lineages exhibit divergent degrees of cell hypertrophy and directions of elongation. Median cortical cells in P. cattleianum galls hypertrophy the most, while in P. myrtoides galls there is a centrifugal gradient of cell hypertrophy. Cortical cells in P. cattleianum galls tend to anisotropy, while P. myrtoidis galls have isotropically hypertrophied cells. Immunocytochemistry evidences the chemical identity and functional traits of cell lineages: epidermal cells walls have homogalacturonans (HGAs) and galactans, which confer rigidity to sites of enhanced cell division; oil gland cell walls have arabinogalactan proteins (AGPs) that help avoiding cell death; and parenchyma cell walls have HGAs, galactans and arabinans, which confer porosity. Variations in such chemical identities are related to specific sites of hypertrophy. Even though the double co-generic models have the same macroscopic phenotype, the globoid morphotype, current analyses indicate that the extended phenotype of N. cattleiani is substantiated by cellular and subcellular specificities.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anisotropy
  • Cell Shape
  • Cell Size
  • Cell Wall / metabolism
  • Immunohistochemistry
  • Insecta / physiology*
  • Phenotype
  • Plant Cells / metabolism*
  • Plant Leaves / metabolism
  • Plant Tumors / parasitology*
  • Psidium / metabolism
  • Subcellular Fractions / metabolism

Grants and funding

RGSC received scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BR - www.capes.gov.br). PP received scholarship from Fundação de Amparo a Pesquisa do Estado de Minas Gerais (BR - www.fapemig.br). RMSI received funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR - www.cnpq.br) (grant number 307007/2012-2). RGSC, PP and RMSI had financial support from Empresa Brasileira de Pesquisa Agropecuária (BR - www.embrapa.br) (grant number 02.12.01.028.00.00). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.