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Developmental anatomy and immunocytochemistry reveal the neo-ontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae)

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The temporal balance between hyperplasia and hypertrophy, and the new functions of different cell lineages led to cell transformations in a centrifugal gradient that determines the gall globoid shape.

Abstract

Plant galls develop by the redifferentiation of new cell types originated from those of the host plants, with new functional and structural designs related to the composition of cell walls and cell contents. Variations in cell wall composition have just started to be explored with the perspective of gall development, and are herein related to the histochemical gradients previously detected on Psidium myrtoides galls. Young and mature leaves of P. myrtoides and galls of Nothotrioza myrtoidis at different developmental stages were analysed using anatomical, cytometrical and immunocytochemical approaches. The gall parenchyma presents transformations in the size and shape of the cells in distinct tissue layers, and variations of pectin and protein domains in cell walls. The temporal balance between tissue hyperplasia and cell hypertrophy, and the new functions of different cell lineages led to cell transformations in a centrifugal gradient, which determines the globoid shape of the gall. The distribution of cell wall epitopes affected cell wall flexibility and rigidity, towards gall maturation. By senescence, it provided functional stability for the outer cortical parenchyma. The detection of the demethylesterified homogalacturonans (HGAs) denoted the activity of the pectin methylesterases (PMEs) during the senescent phase, and was a novel time-based detection linked to the increased rigidity of the cell walls, and to the gall opening. Current investigation firstly reports the influence of immunocytochemistry of plant cell walls over the development of leaf tissues, determining their neo-ontogenesis towards a new phenotype, i.e., the globoid gall morphotype.

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Acknowledgments

We thank Fundação de Apoio à Pesquisa do Estado de Minas Gerais (FAPEMIG—APQ- 00901-11), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—Grant Number 307007/2012-2), and Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA—Project: “Manejo e biodiversidade de Psylloidea associados ao sistema integração lavoura-pecuária-floresta e à citricultura no Brasil”, number 02.12.01.028.00.00) for the financial support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We also thank Centro de Aquisição e Processamento de Imagens (CAPI-ICB/UFMG) for the analyses in confocal microscopy, and Dr. G. W. Fernandes, Dr. J. E. Kraus and Dr. M. Inbar for comments on the manuscript.

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The authors declare that they have no conflict of interest.

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  1. Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida Antônio Carlos, 6627, Pampulha, Belo Horizonte, Minas Gerais, 31270-901, Brazil

    Renê G. S. Carneiro & Rosy M. S. Isaias

  2. Instituto de Biologia, Universidade Federal de Uberlândia, Bloco 2D sala 28, Campus Umuarama, Uberlândia, Minas Gerais, 38400-902, Brazil

    Denis C. Oliveira

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  1. Renê G. S. Carneiro
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Correspondence to Rosy M. S. Isaias.

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Communicated by Xian Sheng Zhang.

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Carneiro, R.G.S., Oliveira, D.C. & Isaias, R.M.S. 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, 2093–2106 (2014). https://doi.org/10.1007/s00299-014-1683-7

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