Transcription factors, chromatin proteins and the diversification of Hemiptera

Abstract

Availability of complete genomes provides a means to explore the evolution of enormous developmental, morphological, and behavioral diversity among insects. Hemipterans in particular show great diversity of both morphology and life history within a single order. To better understand the role of transcription regulators in the diversification of hemipterans, using sequence profile searches and hidden Markov models we computationally analyzed transcription factors (TFs) and chromatin proteins (CPs) in the recently available Rhodnius prolixus genome along with 13 other insect and 4 non-insect arthropod genomes. We generated a comprehensive collection of TFs and CPs across arthropods including 303 distinct types of domains in TFs and 139 in CPs. This, along with the availability of two hemipteran genomes, R. prolixus and Acyrthosiphon pisum, helped us identify possible determinants for their dramatic morphological and behavioral divergence. We identified five domain families (i.e. Pipsqueak, SAZ/MADF, THAP, FLYWCH and BED finger) as having undergone differential patterns of lineage-specific expansion in hemipterans or within hemipterans relative to other insects. These expansions appear to be at least in part driven by transposons, with the DNA-binding domains of transposases having provided the raw material for emergence of new TFs. Our analysis suggests that while R. prolixus probably retains a state closer to the ancestral hemipteran, A. pisum represents a highly derived state, with the emergence of asexual reproduction potentially favoring genome duplication and transposon expansion. Both hemipterans are predicted to possess active DNA methylation systems. However, in course of their divergence aphids seem to have expanded the ancestral hemipteran DNA methylation along with a distinctive linkage to the histone methylation system, as suggested by expansion of SET domain methylases, including those fused to methylated CpG recognition domains. Thus, differential use of DNA methylation and histone methylation might have played a role in emergence of polyphenism and cyclic parthenogenesis from the ancestral hemipteran.

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

“…Given the developmental roles of Pipsqueak TFs in Drosophila, these LSEs might have played some role in the morphological and behavioral diversification of hemipterans. Other predicted TF expansions were also found as resulting from proliferation of transposable elements (37). Other expansions related to development were found in cuticle genes, including those that transcribe cuticular proteins and sclerotization enzymes (SI Appendix, Figs.…”

A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

“…Diversification of transcription factor (TF) families potentially signals greater complexity of gene regulation, including enhanced cell specificity and refined spatiotemporal signaling 62 . Notably, several TF families are substantially expanded in L .…”

Transcriptomics supports local sensory regulation in the antenna of the kissing-bug Rhodnius prolixus

“…The increased male expression of HR3, which is the heterodimer partner of Eip75B, suggests a sex-specific role in antennae. Vidal et al [56] reported 19 nuclear hormone receptor genes in the genome of R. prolixus that belong to the NR1-NR6 subfamilies. These genes were all annotated by the present study that also allowed identifying a duplication of the HNF4A gene.…”