Whole-transcriptome RNA Sequencing Reveals the Global Molecular Responses and CeRNA Regulatory Network of MRNAs, LncRNAs, MiRNAs and CircRNAs in Response to Copper Toxicity in Ziyang Xiangcheng (Citrus Junos Sieb. Ex Tanaka)

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2019 Nov 23

PMID 31752684

Citations 24

Authors

Xing-Zheng Fu

Xiao-Yong Zhang

Jie-Ya Qiu

Xue Zhou

Meng Yuan

Yi-Zhong He

Chang-Pin Chun

Li Cao

Li-Li Ling

Liang-Zhi Peng

Affiliations

Soon will be listed here.

Abstract

Background: Copper (Cu) toxicity has become a potential threat for citrus production, but little is known about related mechanisms. This study aims to uncover the global landscape of mRNAs, long non-coding RNAs (lncRNAs), circular RNAs (circRNAs) and microRNAs (miRNAs) in response to Cu toxicity so as to construct a regulatory network of competing endogenous RNAs (ceRNAs) and to provide valuable knowledge pertinent to Cu response in citrus.

Results: Tolerance of four commonly used rootstocks to Cu toxicity was evaluated, and 'Ziyang Xiangcheng' (Citrus junos) was found to be the most tolerant genotype. Then the roots and leaves sampled from 'Ziyang Xiangcheng' with or without Cu treatment were used for whole-transcriptome sequencing. In total, 5734 and 222 mRNAs, 164 and 5 lncRNAs, 45 and 17 circRNAs, and 147 and 130 miRNAs were identified to be differentially expressed (DE) in Cu-treated roots and leaves, respectively, in comparison with the control. Gene ontology enrichment analysis showed that most of the DEmRNAs and targets of DElncRNAs and DEmiRNAs were annotated to the categories of 'oxidation-reduction', 'phosphorylation', 'membrane', and 'ion binding'. The ceRNA network was then constructed with the predicted pairs of DEmRNAs-DEmiRNAs and DElncRNAs-DEmiRNAs, which further revealed regulatory roles of these DERNAs in Cu toxicity.

Conclusions: A large number of mRNAs, lncRNAs, circRNAs, and miRNAs in 'Ziyang Xiangcheng' were altered in response to Cu toxicity, which may play crucial roles in mitigation of Cu toxicity through the ceRNA regulatory network in this Cu-tolerant rootstock.

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References

Yeh C, Hsiao L, Huang H . Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol. 2004; 45(9):1306-12. DOI: 10.1093/pcp/pch135. View

Liang W, Fu W, Wong C, Wang Y, Wang W, Hu G . The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer. Oncotarget. 2015; 6(26):22513-25. PMC: 4673179. DOI: 10.18632/oncotarget.4154. View

Pilon M . The copper microRNAs. New Phytol. 2016; 213(3):1030-1035. DOI: 10.1111/nph.14244. View

Quinn J, Chang H . Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2015; 17(1):47-62. DOI: 10.1038/nrg.2015.10. View

Zhu M, Zhang M, Xing L, Li W, Jiang H, Wang L . Transcriptomic Analysis of Long Non-Coding RNAs and Coding Genes Uncovers a Complex Regulatory Network That Is Involved in Maize Seed Development. Genes (Basel). 2017; 8(10). PMC: 5664124. DOI: 10.3390/genes8100274. View

Li Q, Zhang Y, Chen Y, Yu Y . Circular RNAs roll into the regulatory network of plants. Biochem Biophys Res Commun. 2017; 488(2):382-386. DOI: 10.1016/j.bbrc.2017.05.061. View

Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D . Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13(11):2498-504. PMC: 403769. DOI: 10.1101/gr.1239303. View

Clemens S . Molecular mechanisms of plant metal tolerance and homeostasis. Planta. 2001; 212(4):475-86. DOI: 10.1007/s004250000458. View

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S . TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14(4):R36. PMC: 4053844. DOI: 10.1186/gb-2013-14-4-r36. View

10.

Cambrolle J, Garcia J, Figueroa M, Cantos M . Evaluating wild grapevine tolerance to copper toxicity. Chemosphere. 2014; 120:171-8. DOI: 10.1016/j.chemosphere.2014.06.044. View

11.

Wang K, Liu C, Zhou L, Wang J, Wang M, Zhao B . APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun. 2015; 6:6779. DOI: 10.1038/ncomms7779. View

12.

Sunkar R, Kapoor A, Zhu J . Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell. 2006; 18(8):2051-65. PMC: 1533975. DOI: 10.1105/tpc.106.041673. View

13.

Wang X, Xu Y, Zhang S, Cao L, Huang Y, Cheng J . Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat Genet. 2017; 49(5):765-772. DOI: 10.1038/ng.3839. View

14.

Yan J, Chia J, Sheng H, Jung H, Zavodna T, Zhang L . Arabidopsis Pollen Fertility Requires the Transcription Factors CITF1 and SPL7 That Regulate Copper Delivery to Anthers and Jasmonic Acid Synthesis. Plant Cell. 2017; 29(12):3012-3029. PMC: 5757271. DOI: 10.1105/tpc.17.00363. View

15.

Lubkowitz M . The oligopeptide transporters: a small gene family with a diverse group of substrates and functions?. Mol Plant. 2011; 4(3):407-15. DOI: 10.1093/mp/ssr004. View

16.

Burkhead J, Gogolin Reynolds K, Abdel-Ghany S, Cohu C, Pilon M . Copper homeostasis. New Phytol. 2009; 182(4):799-816. DOI: 10.1111/j.1469-8137.2009.02846.x. View

17.

Araki R, Mermod M, Yamasaki H, Kamiya T, Fujiwara T, Shikanai T . SPL7 locally regulates copper-homeostasis-related genes in Arabidopsis. J Plant Physiol. 2018; 224-225:137-143. DOI: 10.1016/j.jplph.2018.03.014. View

18.

Gupta O, Sharma P, Gupta R, Sharma I . MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol Biol. 2013; 84(1-2):1-18. DOI: 10.1007/s11103-013-0120-6. View

19.

Jonak C, Nakagami H, Hirt H . Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 2004; 136(2):3276-83. PMC: 523386. DOI: 10.1104/pp.104.045724. View

20.

Huang X, Deng F, Yamaji N, Pinson S, Fujii-Kashino M, Danku J . A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun. 2016; 7:12138. PMC: 4941113. DOI: 10.1038/ncomms12138. View