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

Author(s):Show less -

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]

Affiliation

^[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

• Document type: Journal article
• Source: PLoS One; v. 14, n. 3 MAR 14 2019.
• Web of Science Citations: 2

Abstract

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)

• FAPESP's process: 14/13136-0 - RNA-seq for characterization of the genes involved in the construction and differentiation of the insect exoskeleton using bees as a model
• Grantee: Marcia Maria Gentile Bitondi
• Support Opportunities: Regular Research Grants
• FAPESP's process: 11/03171-5 - Causal analysis of Apis mellifera development: regulatory genes and hierachical networks of gene expression in the specification of tissue and organs
• Grantee: Zilá Luz Paulino Simões
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 14/50265-3 - Distribution and metabolism of natural and synthetic xenobiotics: from the comprehension of reactional process to tissue imaging generation
• Grantee: Norberto Peporine Lopes
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants
• FAPESP's process: 12/24284-5 - Comparative approach of cuticular maturation heterochrony in social and solitary bees using RNA-Seq, hydrocarbons quantification and electron microscopy
• Grantee: Tiago Falcon Lopes
• Support Opportunities: Scholarships in Brazil - Doctorate