Transcriptome dynamics during metamorphosis of imaginal discs into wings and thoracic dorsum in Apis mellifera castes

Author(s)

Miranda Soares, Michelle Prioli ^[1] ; Pinheiro, Daniel Guariz ^[2] ; de Paula Freitas, Flavia Cristina ^[3] ; Paulino Simoes, Zila Luz ^[4] ; Gentile Bitondi, Marcia Maria ^[4]

Affiliation

^[1] Univ Sao Paulo, Fac Med Ribeirao Preto, Dept Genet, Av Bandeirantes 3900, BR-14049900 Ribeirao Preto, SP - Brazil

^[2] Univ Estadual Paulista, Dept Tecnol, Fac Ciencias Agr & Vet, Jaboticabal, SP - Brazil

^[3] Fiocruz MS, Inst Carlos Chagas, Curitiba, Parana - Brazil

^[4] Univ Sao Paulo, Fac Filosofia Ciencias & Letras Ribeirao Preto, Dept Biol, Av Bandeirantes 3900, BR-14040901 Ribeirao Preto, SP - Brazil

• Document type: Journal article
• Source: BMC Genomics; v. 22, n. 1 OCT 22 2021.
• Web of Science Citations: 0

Abstract

Background Much of the complex anatomy of a holometabolous insect is built from disc-shaped epithelial structures found inside the larva, i.e., the imaginal discs, which undergo a rapid differentiation during metamorphosis. Imaginal discs-derived structures, like wings, are built through the action of genes under precise regulation. Results We analyzed 30 honeybee transcriptomes in the search for the gene expression needed for wings and thoracic dorsum construction from the larval wing discs primordia. Analyses were carried out before, during, and after the metamorphic molt and using worker and queen castes. Our RNA-seq libraries revealed 13,202 genes, representing 86.2% of the honeybee annotated genes. Gene Ontology analysis revealed functional terms that were caste-specific or shared by workers and queens. Genes expressed in wing discs and descendant structures showed differential expression profiles dynamics in premetamorphic, metamorphic and postmetamorphic developmental phases, and also between castes. At the metamorphic molt, when ecdysteroids peak, the wing buds of workers showed maximal gene upregulation comparatively to queens, thus underscoring differences in gene expression between castes at the height of the larval-pupal transition. Analysis of small RNA libraries of wing buds allowed us to build miRNA-mRNA interaction networks to predict the regulation of genes expressed during wing discs development. Conclusion Together, these data reveal gene expression dynamics leading to wings and thoracic dorsum formation from the wing discs, besides highlighting caste-specific differences during wing discs metamorphosis. (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: 12/12941-1 - Next-generation mRNA sequencing for high-throughput analysis of the metamorphosis in Apis mellifera castes
• Grantee: Michelle Prioli Miranda Soares
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• 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