Transcriptomic and proteomic elucidation of Z chromosome dosage compensation in Helicoverpa armigera

IF 2.3 2区农林科学 Q3 BIOCHEMISTRY & MOLECULAR BIOLOGY

Insect Molecular Biology Pub Date : 2024-07-01 DOI:10.1111/imb.12939

Zhongyuan Deng, Yakun Zhang, Xingcheng Xie, Huihui Li, Han Guo, Xinzhi Ni, Xianchun Li

{"title":"Transcriptomic and proteomic elucidation of Z chromosome dosage compensation in Helicoverpa armigera","authors":"Zhongyuan Deng, Yakun Zhang, Xingcheng Xie, Huihui Li, Han Guo, Xinzhi Ni, Xianchun Li","doi":"10.1111/imb.12939","DOIUrl":null,"url":null,"abstract":"Transcriptomic data have been used to study sex chromosome dosage compensation (SCDC) in approximately 10 Lepidoptera ZW species, yielding a consensus compensation pattern of Z <math>\n <mrow>\n <mo>≈</mo>\n <mi>ZZ</mi>\n <mo><</mo>\n <mi>AA</mi>\n <mo>.</mo>\n </mrow></math> It remains unclear whether this compensation pattern holds when examining more Lepidoptera ZW species and/or using proteomic data to analyse SCDC. Here we combined transcriptomic and proteomic data as well as transcriptional level of six individual Z genes to reveal the SCDC pattern in Helicoverpa armigera, a polyphagous lepidopteran pest of economic importance. Transcriptomic analysis showed that the Z chromosome expression of H. armigera was balanced between male and female but substantially reduced relative to autosome expression, exhibiting an SCDC pattern of Z <math>\n <mrow>\n <mo>≈</mo>\n <mi>ZZ</mi>\n <mo><</mo>\n <mi>AA</mi>\n </mrow></math>. When using H. amigera midgut proteomic data, the SCDC pattern of this species changed from Z <math>\n <mrow>\n <mo>≈</mo>\n <mi>ZZ</mi>\n <mo><</mo>\n <mi>AA</mi>\n </mrow></math> at transcriptomic level to Z = ZZ = AA at the proteomic level. RT-qPCR analysis of transcript abundance of six Z genes found that compensation for each Z gene could vary from no compensation to overcompensation, depending on the individual genes and tissues tested. These results demonstrate for the first time the existence of a translational compensation mechanism, which is operating in addition to a translational mechanism, such as has been reported in other lepidopteran species. And the transcriptional compensation mechanism functions to accomplish Z chromosome dosage balance between the sexes (M = F on the Z chromosome), whereas the translation compensation mechanism operates to achieve dosage compensation between Z chromosome and autosome (Z = AA).","PeriodicalId":13526,"journal":{"name":"Insect Molecular Biology","volume":"33 6","pages":"744-755"},"PeriodicalIF":2.3000,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Insect Molecular Biology","FirstCategoryId":"97","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/imb.12939","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

Transcriptomic data have been used to study sex chromosome dosage compensation (SCDC) in approximately 10 Lepidoptera ZW species, yielding a consensus compensation pattern of Z $\approx ZZ < AA .$ It remains unclear whether this compensation pattern holds when examining more Lepidoptera ZW species and/or using proteomic data to analyse SCDC. Here we combined transcriptomic and proteomic data as well as transcriptional level of six individual Z genes to reveal the SCDC pattern in Helicoverpa armigera, a polyphagous lepidopteran pest of economic importance. Transcriptomic analysis showed that the Z chromosome expression of H. armigera was balanced between male and female but substantially reduced relative to autosome expression, exhibiting an SCDC pattern of Z $\approx ZZ < AA$ . When using H. amigera midgut proteomic data, the SCDC pattern of this species changed from Z $\approx ZZ < AA$ at transcriptomic level to Z = ZZ = AA at the proteomic level. RT-qPCR analysis of transcript abundance of six Z genes found that compensation for each Z gene could vary from no compensation to overcompensation, depending on the individual genes and tissues tested. These results demonstrate for the first time the existence of a translational compensation mechanism, which is operating in addition to a translational mechanism, such as has been reported in other lepidopteran species. And the transcriptional compensation mechanism functions to accomplish Z chromosome dosage balance between the sexes (M = F on the Z chromosome), whereas the translation compensation mechanism operates to achieve dosage compensation between Z chromosome and autosome (Z = AA).

Abstract Image

查看原文本刊更多论文

Helicoverpa armigera Z 染色体剂量补偿的转录组和蛋白质组阐释。

转录组数据已被用于研究约 10 个鳞翅目 ZW 种类的性染色体剂量补偿（SCDC），得出的共识补偿模式为 Z ≈ ZZ AA . $$ \approx \mathrm{ZZ} 。在研究更多鳞翅目 ZW 种类和/或使用蛋白质组数据分析 SCDC 时，这种补偿模式是否成立仍不清楚。在此，我们结合转录组和蛋白质组数据以及六个 Z 基因的转录水平，揭示了 Helicoverpa armigera（一种具有重要经济价值的多食性鳞翅目害虫）的 SCDC 模式。转录组分析表明，H. armigera 的 Z 染色体表达在雌雄之间是平衡的，但相对于自体的表达大幅降低，表现出 Z ≈ ZZ AA $$ \approx \mathrm{ZZ} 的 SCDC 模式。当使用 H. amigera 中肠蛋白组数据时，该物种的 SCDC 模式从转录组水平的 Z ≈ ZZ AA $$ \approx \mathrm{ZZ} 变为蛋白组水平的 Z = ZZ = AA。对 6 个 Z 基因转录本丰度的 RT-qPCR 分析发现，每个 Z 基因的补偿可从无补偿到过度补偿不等，具体取决于测试的各个基因和组织。这些结果首次证明了翻译补偿机制的存在，这种机制是在翻译机制之外运行的，如在其他鳞翅目物种中所报道的那样。转录补偿机制的作用是实现 Z 染色体在两性之间的剂量平衡（Z 染色体上的 M = F），而翻译补偿机制的作用是实现 Z 染色体和自体之间的剂量补偿（Z = AA）。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Insect Molecular Biology 生物-昆虫学

CiteScore

4.80

自引率

3.80%

发文量

审稿时长

6-12 weeks

期刊介绍： Insect Molecular Biology has been dedicated to providing researchers with the opportunity to publish high quality original research on topics broadly related to insect molecular biology since 1992. IMB is particularly interested in publishing research in insect genomics/genes and proteomics/proteins. This includes research related to: • insect gene structure • control of gene expression • localisation and function/activity of proteins • interactions of proteins and ligands/substrates • effect of mutations on gene/protein function • evolution of insect genes/genomes, especially where principles relevant to insects in general are established • molecular population genetics where data are used to identify genes (or regions of genomes) involved in specific adaptations • gene mapping using molecular tools • molecular interactions of insects with microorganisms including Wolbachia, symbionts and viruses or other pathogens transmitted by insects Papers can include large data sets e.g.from micro-array or proteomic experiments or analyses of genome sequences done in silico (subject to the data being placed in the context of hypothesis testing).