Mechanisms of programmed cell death in the midgut and salivary glands fromBradysia hygida(Diptera: Sciaridae) during pupal–adult metamorphosis

Abstract

Programmed cell death is involved with the degeneration/remodeling of larval tissues and organs during holometabolous development. The midgut is a model to study the types of programmed cell death associated with metamorphosis because its structure while degenerating is a substrate for the formation of the adult organ. Another model is the salivary glands from dipteran because their elimination involves different cell death modes. This study aimed to investigate the models of programmed cell death operating during midgut replacement and salivary gland histolysis in Bradysia hygida. We carried out experiments of real‐time observations, morphological analysis, glycogen detection, filamentous‐actin localization, and nuclear acridine orange staining. Our findings allow us to establish that an intact actin cytoskeleton is required for midgut replacement in B. hygida and nuclear condensation and acridine orange staining precede the death of the larval cells. Salivary glands in histolysis present cytoplasmic blebbing, nuclear retraction, and acridine orange staining. This process can be partially reproduced in vitro. We propose that the larval midgut death involves autophagic and apoptotic features and apoptosis is a mechanism involved with salivary gland histolysis.

Anatomical changes of the beetle digestive tract during metamorphosis correspond to dietary changes

“…The midgut contents change from black solid in the larval stage, to nothing in the prepupal stage, and finally a brown liquid called yellow body in the pupal stage, which is absorbed by the midgut before eclosion (Cassia Santos Przepiura et al, 2020). In the pupal hindgut, the black meconium at the early stage is transformed into white-striped content at stage III.…”

“…This finding challenges the view that hindgut symbionts are inevitably lost during molting along with the hindgut cuticle. As the meconium containing remodeled gut tissue and hindgut wall is removed after eclosion (Cassia Santos Przepiura et al, 2020), digestive symbionts may stay in the meconium until the gut transformation is complete and then move to inhabit the new tissue. This process could be one pathway for essential gut symbionts with digestive functions to be maintained from larva to adult.…”

Evolved and plastic gene expression in adaptation to a novel niche

“…This module was enriched for cell cycle processes, such centriole assembly (GO:0098534, rank = 1, p = 5.2×10 −4 ) and replication (GO:0007099, rank = 2, p = 6.2×10 −4 ), chromatin (GO:0006325, rank = 3, p = 1.4×10 −3 ) and microtubule organizing center (GO:0031023; rank = 6, p = 2.7×10 −3 ) organization (Figure S8A, Figure S9A). Further, this module was enriched for salivary gland histolysis (GO:0035070, rank = 8, p = 5.0×10 −3 ), a specific process of salivary gland breakdown during dipteran metamorphosis (de Cassia Santos Przepiura et al, 2020). Together with module 17, this supports a faster life history in CH flies that is significantly slowed by cross-fostering in C. oleraceum buds.…”

Pseudolycoriella hygida (Sauaia and Alves)—An Overview of a Model Organism in Genetics, with New Aspects in Morphology and Systematics

“…These studies included the characterization of the mitotic chromosomes and nucleolar organizing regions [35,36], the molecular characterization of DNA puff-forming regions (reviewed in [18,20]), the direct demonstration that DNA puff proteins are employed to build the cocoon [37,38], studies in transgenic Drosophila, as well as those that determined the levels of ecdysone titers and the role of the hormone on DNA puff gene expression at the end of the fourth larval instar (reviewed in [20]). Further studies established the mechanisms of programmed cell death in larval organs [18,22]. Together, these studies represent a consolidated contribution in the area of insect molecular biology and further emphasize the relevance of studying unconventional model organisms, such as sciarids.…”

“…Together, these studies contributed to the understanding of the role of ecdysone in DNA puff formation, transcription, and DNA replication in DNA puff-forming regions (reviewed in [20]). Besides the characterization of processes typical of sciarids-namely, the unusual mechanism of sex determination and DNA puff formation-the study of sciarids also contributed to the understanding of telomere organization, nucleolar structure [21], antimicrobial peptides, and cell death [22] (reviewed in [18]). More recently, the research focus has shifted to insecticide resistance [23] and to the characterization of germ line restricted chromosomes that occur in a few groups across the tree of life, including sciarids, cecidomyiids, and chironomids (reviewed in [24]).…”