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柳枝稷干旱胁迫过程中 ncRNAs 和 mRNAs 相互作用的转录组分析。

Transcriptomic analysis of ncRNAs and mRNAs interactions during drought stress in switchgrass.

机构信息

Institute of Leisure Agriculture, Shandong Academy of Agricultural Science, Jinan 250100, China; Key Laboratory of East China Urban Agriculture, Ministry of Agriculture, Jinan 250100, China; Shandong Engineering Research Center of Ecological and Horticultural Plant Breeding, Jinan 250100, China.

Institute of Leisure Agriculture, Shandong Academy of Agricultural Science, Jinan 250100, China; College of Grassland Science and Technology, China Agricultural University, No.2 Yuan Mingyuan West Road, Beijing 100193, China.

出版信息

Plant Sci. 2024 Feb;339:111930. doi: 10.1016/j.plantsci.2023.111930. Epub 2023 Nov 24.

DOI:10.1016/j.plantsci.2023.111930
PMID:38007196
Abstract

Switchgrass (Panicum virgatum L.) plays a pivotal role as a bioenergy feedstock in the production of cellulosic ethanol and contributes significantly to enhancing ecological grasslands and soil quality. The utilization of non-coding RNAs (ncRNAs) has gained momentum in deciphering the intricate genetic responses to abiotic stress in various plant species. Nevertheless, the current research landscape lacks a comprehensive exploration of the responses of diverse ncRNAs, including long non-coding RNAs (lncRNAs), circular RNAs (circRNAs), and microRNAs (miRNAs), to drought stress in switchgrass. In this study, we employed whole transcriptome sequencing to comprehensively characterize the expression profiles of both mRNA and ncRNAs during episodes of drought stress in switchgrass. Our analysis identified a total of 12,511 mRNAs, 59 miRNAs, 38 circRNAs, and 368 lncRNAs that exhibited significant differential expression between normal and drought-treated switchgrass leaves. Notably, the majority of up-regulated mRNAs displayed pronounced enrichment within the starch and sucrose metabolism pathway, as validated through KEGG analysis. Co-expression analysis illuminated that differentially expressed (DE) lncRNAs conceivably regulated 1308 protein-coding genes in trans and 7110 protein-coding genes in cis. Furthermore, both cis- and trans-target mRNAs of DE lncRNAs exhibited enrichment in four common KEGG pathways. The intricate interplay between lncRNAs and circRNAs with miRNAs via miRNA response elements was explored within the competitive endogenous RNA (ceRNA) network framework. As a result, we constructed elaborate regulatory networks, including lncRNA-novel_miRNA480-mRNA, lncRNA-novel_miRNA304-mRNA, lncRNA/circRNA-novel_miRNA122-PvSS4, and lncRNA/circRNA-novel_miRNA14-PvSS4, and subsequently validated the functionality of the target gene, starch synthase 4 (PvSS4). Furthermore, through the overexpression of PvSS4, we ascertained its capacity to enhance drought tolerance in yeast. However, it is noteworthy that PvSS4 did not exhibit any discernible impact under salt stress conditions. These findings, as presented herein, not only contribute substantively to our understanding of ceRNA networks but also offer a basis for further investigations into their potential functions in response to drought stress in switchgrass.

摘要

柳枝稷(Panicum virgatum L.)作为纤维素乙醇生产的生物能源原料,在增强生态草原和土壤质量方面发挥着关键作用。非编码 RNA(ncRNA)的利用在破译各种植物物种对非生物胁迫的复杂遗传反应方面取得了进展。然而,目前的研究领域缺乏对不同 ncRNA(包括长非编码 RNA(lncRNA)、环状 RNA(circRNA)和 microRNA(miRNA))对柳枝稷干旱胁迫响应的全面探索。在这项研究中,我们采用全转录组测序技术,全面描述了柳枝稷叶片在干旱胁迫过程中 mRNA 和 ncRNA 的表达谱。我们的分析共鉴定了 12511 个 mRNAs、59 个 miRNAs、38 个 circRNAs 和 368 个 lncRNAs,它们在正常和干旱处理的柳枝稷叶片之间表现出显著的差异表达。值得注意的是,通过 KEGG 分析验证,大多数上调的 mRNAs 在淀粉和蔗糖代谢途径中表现出明显的富集。共表达分析表明,差异表达(DE)lncRNA 可能在反式调控 1308 个蛋白编码基因和顺式调控 7110 个蛋白编码基因。此外,DE lncRNA 的顺式和反式靶基因在四个常见的 KEGG 途径中都表现出富集。通过 miRNA 反应元件在竞争内源性 RNA(ceRNA)网络框架内探索了 lncRNA、circRNA 与 miRNA 之间的复杂相互作用。结果,我们构建了精细的调控网络,包括 lncRNA-novel_miRNA480-mRNA、lncRNA-novel_miRNA304-mRNA、lncRNA/circRNA-novel_miRNA122-PvSS4 和 lncRNA/circRNA-novel_miRNA14-PvSS4,并随后验证了靶基因淀粉合酶 4(PvSS4)的功能。此外,通过过表达 PvSS4,我们确定了它在酵母中增强耐旱性的能力。然而,值得注意的是,PvSS4 在盐胁迫条件下没有表现出任何明显的影响。本文的这些发现不仅为我们理解 ceRNA 网络做出了实质性的贡献,也为进一步研究它们在柳枝稷响应干旱胁迫中的潜在功能提供了基础。

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