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Effects of oxidative stress on sex-specific gene expression in the copepod Tigriopus californicus revealed by single individual RNA-seq.

ABSTRACT: Oxidative stress reflects the imbalance of pro-oxidants and antioxidants. Prolonged oxidative stress can induce cellular damage, diseases and aging, and the effects may be sex-specific. Tigriopus californicus has recently been proposed as an alternative model system for sex-specific studies due to the absence of sex chromosomes. In this study, we used comparative transcriptomic analyses to assess sex-specific transcriptional responses to oxidative stress. Male and female individuals were maintained separately in one of three treatments: 1) control conditions with an algae diet, 2) pro-oxidant (H2O2) conditions with an algae diet or 3) decreased antioxidant conditions (reduced carotenoids due to a yeast diet). Single individual RNA-seq was then conducted for twenty-four libraries using Ligation Mediated RNA sequencing (LM-Seq). Variance in gene expression was partitioned into 62.3% between sexes, 26.85% among individuals and 10.85% among treatments. Within each of the three treatments, expression was biased toward females. However, compared to the control treatment, males in both pro-oxidant and decreased antioxidant treatments differentially expressed more genes while females differentially expressed fewer genes but with a greater magnitude of fold change. As the first study of copepods to apply single individual RNA-seq, the findings will contribute to a better understanding of transcriptomic variation among individuals as well as sex-specific response mechanisms to oxidative stress in the absence of sex chromosomes.

SUBMITTER: Li N

PROVIDER: S-EPMC6697563 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Effects of oxidative stress on sex-specific gene expression in the copepod Tigriopus californicus revealed by single individual RNA-seq.

Li Ning N Arief Natasha N Edmands Suzanne S

Comparative biochemistry and physiology. Part D, Genomics & proteomics 20190711

Oxidative stress reflects the imbalance of pro-oxidants and antioxidants. Prolonged oxidative stress can induce cellular damage, diseases and aging, and the effects may be sex-specific. Tigriopus californicus has recently been proposed as an alternative model system for sex-specific studies due to the absence of sex chromosomes. In this study, we used comparative transcriptomic analyses to assess sex-specific transcriptional responses to oxidative stress. Male and female individuals were maintai ...[more]

PMID: 31325755

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Project description:BackgroundAs yet, few genomic resources have been developed in crustaceans. This lack is particularly evident in Copepoda, given the extraordinary numerical abundance, and taxonomic and ecological diversity of this group. Tigriopus californicus is ideally suited to serve as a genetic model copepod and has been the subject of extensive work in environmental stress and reproductive isolation. Accordingly, we set out to develop a broadly-useful panel of genetic markers and to construct a linkage map dense enough for quantitative trait locus detection in an interval mapping framework for T. californicus--a first for copepods.ResultsOne hundred and ninety Single Nucleotide Polymorphisms (SNPs) were used to genotype our mapping population of 250 F2 larvae. We were able to construct a linkage map with an average intermarker distance of 1.8 cM, and a maximum intermarker distance of 10.3 cM. All markers were assembled into linkage groups, and the 12 linkage groups corresponded to the 12 known chromosomes of T. californicus. We estimate a total genome size of 401.0 cM, and a total coverage of 73.7%. Seventy five percent of the mapped markers were detected in 9 additional populations of T. californicus. Of available model arthropod genomes, we were able to show more colocalized pairs of homologues between T. californicus and the honeybee Apis mellifera, than expected by chance, suggesting preserved macrosynteny between Hymenoptera and Copepoda.ConclusionsOur study provides an abundance of linked markers spanning all chromosomes. Many of these markers are also found in multiple populations of T. californicus, and in two other species in the genus. The genomic resource we have developed will enable mapping throughout the geographical range of this species and in closely related species. This linkage map will facilitate genome sequencing, mapping and assembly in an ecologically and taxonomically interesting group for which genomic resources are currently under development.

Project description:BackgroundGene conversion of duplicated genes can slow the divergence of paralogous copies over time but can also result in other interesting evolutionary patterns. Islands of genetic divergence that persist in the face of gene conversion can point to gene regions undergoing selection for new functions. Novel combinations of genetic variation that differ greatly from the original sequence can result from the transfer of genetic variation between paralogous genes by rare gene conversion events. Genetically divergent populations of the copepod Tigriopus californicus provide an excellent model to look at the patterns of divergence among paralogs across multiple independent evolutionary lineages.ResultsIn this study the evolution of a set of paralogous genes encoding putative aspartate transaminase proteins (called GOT1 here) are examined in populations of the copepod T. californicus. One pair of duplicated genes, GOT1p1 and GOT1p2, has regions of high divergence between the copies in the face of apparent on-going gene conversion. The GOT1p2 gene also has unique haplotypes in two populations that appear to have resulted from a transfer of genetic variation via inter-paralog gene conversion. A second pair of duplicated genes GOT1Sr and GOT1Sd also shows evidence of gene conversion, but this gene conversion does not appear to have maintained each as a functional copy in all populations.ConclusionsThe patterns of conservation and sequence divergence across this set of paralogous genes among populations of T. californicus suggest that some interesting evolutionary patterns are occurring at these loci. The results for the GOT1p1/GOT1p2 paralogs illustrate how gene conversion can factor in the creation of a mosaic pattern of regions of high divergence and low divergence. When coupled with rare gene conversion events of divergent regions, this pattern can result in the formation of novel proteins differing substantially from either original protein. The evolutionary patterns across these paralogs show how gene conversion can both constrain and facilitate diversification of genetic sequences.

Project description:BackgroundGeographic variation in the thermal environment impacts a broad range of biochemical and physiological processes and can be a major selective force leading to local population adaptation. In the intertidal copepod Tigriopus californicus, populations along the coast of California show differences in thermal tolerance that are consistent with adaptation, i.e., southern populations withstand thermal stresses that are lethal to northern populations. To understand the genetic basis of these physiological differences, we use an RNA-seq approach to compare genome-wide patterns of gene expression in two populations known to differ in thermal tolerance.ResultsObserved differences in gene expression between the southern (San Diego) and the northern (Santa Cruz) populations included both the number of affected loci as well as the identity of these loci. However, the most pronounced differences concerned the amplitude of up-regulation of genes producing heat shock proteins (Hsps) and genes involved in ubiquitination and proteolysis. Among the hsp genes, orthologous pairs show markedly different thermal responses as the amplitude of hsp response was greatly elevated in the San Diego population, most notably in members of the hsp70 gene family. There was no evidence of accelerated evolution at the sequence level for hsp genes. Among other sets of genes, cuticle genes were up-regulated in SD but down-regulated in SC, and mitochondrial genes were down-regulated in both populations.ConclusionsMarked changes in gene expression were observed in response to acute sub-lethal thermal stress in the copepod T. californicus. Although some qualitative differences were observed between populations, the most pronounced differences involved the magnitude of induction of numerous hsp and ubiquitin genes. These differences in gene expression suggest that evolutionary divergence in the regulatory pathway(s) involved in acute temperature stress may offer at least a partial explanation of population differences in thermal tolerance observed in Tigriopus.

Dataset Information

Effects of oxidative stress on sex-specific gene expression in the copepod Tigriopus californicus revealed by single individual RNA-seq.

Publications

Effects of oxidative stress on sex-specific gene expression in the copepod Tigriopus californicus revealed by single individual RNA-seq.

Similar Datasets

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