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Exploring integument transcriptomes, cuticle ultrastructure, and cuticular hydrocarbons profiles in eusocial and solitary bee species displaying heterochronic adult cuticle maturation

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Autor(es):
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Falcon, Tiago [1, 2] ; Pinheiro, Daniel G. [3] ; Ferreira-Caliman, Maria Juliana [4] ; Turatti, Izabel C. C. [5] ; Pinto de Abreu, Fabiano C. [1] ; Galaschi-Teixeira, Juliana S. [4] ; Martins, Juliana R. [1] ; Elias-Neto, Moyses [4] ; Soares, Michelle P. M. [1] ; Laure, Marcela B. [1] ; Figueiredo, Vera L. C. [4] ; Lopes, Norberto Peporine [5] ; Simoes, Zila L. P. [4] ; Garofalo, Carlos A. [4] ; Bitondi, Marcia M. G. [4]
Número total de Autores: 15
Afiliação do(s) autor(es):
[1] Univ Sao Paulo, Dept Genet, Fac Med Ribeirao Preto, Ribeirao Preto - Brazil
[2] Hosp Clin Porto Alegre, Nucleo Bioinformat, Porto Alegre, RS - Brazil
[3] Univ Estadual Paulista, Fac Ciencias Agr & Vet, Dept Tecnol, Jaboticabal - Brazil
[4] Univ Sao Paulo, Dept Biol, Fac Filosofia Ciencias & Letras Ribeirao Preto, Ribeirao Preto - Brazil
[5] Univ Sao Paulo, Dept Fis & Quim, Fac Ciencias Farmaceut Ribeirao Preto, Ribeirao Preto - Brazil
Número total de Afiliações: 5
Tipo de documento: Artigo Científico
Fonte: PLoS One; v. 14, n. 3 MAR 14 2019.
Citações Web of Science: 2
Resumo

Differences in the timing of exoskeleton melanization and sclerotization are evident when comparing eusocial and solitary bees. This cuticular maturation heterochrony may be associated with life style, considering that eusocial bees remain protected inside the nest for many days after emergence, while the solitary bees immediately start outside activities. To address this issue, we characterized gene expression using large-scale RNA sequencing (RNA-seq), and quantified cuticular hydrocarbon (CHC) through gas chromatography-mass spectrometry in comparative studies of the integument (cuticle plus its underlying epidermis) of two eusocial and a solitary bee species. In addition, we used transmission electron microscopy (TEM) for studying the developing cuticle of these and other three bee species also differing in life style. We found 13,200, 55,209 and 30,161 transcript types in the integument of the eusocial Apis mellifera and Frieseomelitta varia, and the solitary Centris analis, respectively. In general, structural cuticle proteins and chitin-related genes were upregulated in pharate-adults and newly-emerged bees whereas transcripts for odorant binding proteins, cytochrome P450 and antioxidant proteins were overrepresented in foragers. Consistent with our hypothesis, a distance correlation analysis based on the differentially expressed genes suggested delayed cuticle maturation in A. mellifera in comparison to the solitary bee. However, this was not confirmed in the comparison with F. varia. The expression profiles of 27 of 119 genes displaying functional attributes related to cuticle formation/differentiation were positively correlated between A. mellifera and F. varia, and negatively or non-correlated with C. analis, suggesting roles in cuticular maturation heterochrony. However, we also found transcript profiles positively correlated between each one of the eusocial species and C. analis. Gene co-expression networks greatly differed between the bee species, but we identified common gene interactions exclusively between the eusocial species. Except for F. varia, the TEM analysis is consistent with cuticle development timing adapted to the social or solitary life style. In support to our hypothesis, the absolute quantities of n-alkanes and unsaturated CHCs were significantly higher in foragers than in the earlier developmental phases of the eusocial bees, but did not discriminate newly-emerged from foragers in C. analis. By highlighting differences in integument gene expression, cuticle ultrastructure, and CHC profiles between eusocial and solitary bees, our data provided insights into the process of heterochronic cuticle maturation associated to the way of life. (AU)

Processo FAPESP: 14/13136-0 - RNA-seq para caracterização da expressão gênica relacionada à construção e diferenciação do exoesqueleto de insetos utilizando abelhas como modelo
Beneficiário:Marcia Maria Gentile Bitondi
Modalidade de apoio: Auxílio à Pesquisa - Regular
Processo FAPESP: 11/03171-5 - Análise causal do desenvolvimento de Apis mellifera: genes reguladores e redes hierárquicas de expressão gênica na especificação de tecidos e órgãos
Beneficiário:Zilá Luz Paulino Simões
Modalidade de apoio: Auxílio à Pesquisa - Temático
Processo FAPESP: 14/50265-3 - Metabolismo e distribuição de xenobióticos naturais e sintéticos: da compreensão dos processos reacionais à geração de imagens teciduais
Beneficiário:Norberto Peporine Lopes
Modalidade de apoio: Auxílio à Pesquisa - Programa BIOTA - Temático
Processo FAPESP: 12/24284-5 - Abordagem comparativa da heterocronia da maturação cuticular em abelhas sociais e solitárias utilizando-se RNA-Seq, quantificação de hidrocarbonetos e microscopia eletrônica
Beneficiário:Tiago Falcon Lopes
Modalidade de apoio: Bolsas no Brasil - Doutorado