Chromosome-level Assembly, Dosage Compensation and Sex-biased Gene Expression in the Small Brown Planthopper,Laodelphax striatellus

Abstract

In insects, sex chromosome differentiation often results in­ unequal gene dosages between sexes. Dosage compensation mechanisms evolve to balance gene expression, but the degree and mechanism of regulation often vary by insect species. In hemipteran species, the small brown planthopper (SBPH), Laodelphax striatellus, is an injurious crop pest, with a sex chromosome type XX in females and XO in males. This species offers the opportunity to study dosage compensation and sex-biased gene expression. In this study, we generated a chromosome-level genome of SBPH using Oxford Nanopore Technologies (ONT) and high-throughput chromatin conformation capture (Hi-C) technology. We also sequenced RNA-seq data from 16 tissue samples to annotate the genome and analyze gene dosage compensation. We finally obtained a 510.2 megabases (Mb) genome with 99.12% of the scaffolds anchored on 15 chromosomes (14 autosomes and 1 X-chromosome) and annotated 16160 protein-coding genes based on full-length cDNA sequencing data. Furthermore, we found complete dosage compensation in all L. striatellus somatic tissues, but lack of dosage compensation in gonad tissue testis. We also found that female-biased genes were significantly enriched on the X-chromosome in all tissues, whereas male-biased genes in gonad tissues were enriched on autosomes. This study not only provides a high-quality genome assembly but also lays a foundation for a better understanding of the sexual regulatory network in hemipteran insects.

Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development

“…More generally, the observation of reduced X-expression in male gonads without investigation of associated mechanism is typically interpreted as lack of dosage compensation in this tissue [11,12,52,74]. However, as we observe in Timema, dosage compensation in males may well be ubiquitous across tissues and developmental stages in many species, and reduced X-expression patterns would solely be driven by MSCI.…”

“…Thus, downregulation of X-linked expression in females underlies dosage compensation in eutherian mammals and the worm Caenorhabditis elegans: In eutherian mammals, females inactivate one of the X chromosomes in each cell [6,7], whereas in C. elegans, the expression of both X chromosome copies in hermaphrodites is reduced to achieve similar total expression levels as for the single X in males [8,9]. Upregulation of the single X in males appears to underlie dosage compensation in a diversity of insect species [10][11][12][13].…”

“…Interestingly, in all studied XO and XY species that feature dosage compensation via X upregulation in males, the single X in males is much less expressed in the testes than in the somatic tissues [11][12][13]21]. This is thought to be due to the presence of dosage compensation in somatic tissues and the absence of dosage compensation in the reproductive tissues, perhaps because the gene expression optima in male versus female gonads are so different that there is no or reduced selection for dosage compensation in this tissue [11].…”

Chromosome‐level genome assembly of the aster leafhopper (Macrosteles quadrilineatus) reveals the role of environment and microbial symbiosis in shaping pest insect genome evolution

“…Strong selection pressures against sex chromosome rearrangements may arise from constraints to maintain dosage compensation mechanisms and avoid X chromosome elimination errors in XO male determination (Pal & Vicoso, 2015; Sharp et al., 2002). In the context of leafhoppers that display this XO sex determination, these selection pressures may lead to a lack of sex chromosome rearrangement (Halkka, 1960; Hu et al., 2022). Despite distinctive genomic conservation in leafhoppers, their chromosomes still exhibit some level of architectural plasticity.…”

Functional analysis of neutral lipases in bug feeding and reproduction

“…The natural lipases from R. pedestris and L. striatellus 20 were used to construct a phylogenetic tree. Briefly, the amino acid sequences were aligned with MAFFT (v7.310) with default parameters (maxiterate1000), and ambiguously aligned regions were trimmed by Gblock50 21 .…”