Transcriptome-wide identification and characterization of the copper and cadmium stress-responsive small RNAs and their targets in Arabidopsis thaliana

Springer Science and Business Media LLC - Tập 429 Số 1 - Trang 391-405 - 2018
Ma, Xiaoxia1, Yu, Dongliang1, Shao, Weishan1, Xu, Min1, Zuo, Ziwei1, Wang, Huizhong1, Meng, Yijun1
1College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, People’s Republic of China

Tóm tắt

Copper (Cu) and cadmium (Cd) are toxic to plants at high levels. The current situation that many crops are growing on the farmlands with Cu or Cd contamination leads to a big threat to food safety. Based on the small RNA (sRNA) sequencing data, hundreds of the sRNAs responsive to excessive Cu or Cd treatment were extracted. Degradome sequencing data enabled us to identify the targets of the metal stress-responsive sRNAs. According to our results, many sRNAs are responsive to both treatments, indicating the interactions between the Cu and Cd signals. A total of 151 sRNAs are DCL (Dicer-like) 1-dependent, and 156 sRNAs are DCL2/3/4-dependent. Some sRNAs found their loci on rRNAs or tRNAs, and a total of 12 sRNAs were potentially originated from the TAS transcripts. Functional analysis of the regulatory network showed that some of the sRNA--target pairs played a potential role in plant reproduction, and some pairs were possibly implicated in hormone--stress signal interactions. Our study could inspire the development of an efficient approach, possibly through the manipulation of the sRNA-guided regulatory pathways, to improve the stress tolerance or reduce the toxic metal accumulation levels of plants.

Tài liệu tham khảo

citation_journal_title=Environ Sci Pollut Res Int; citation_title=The effect of excess copper on growth and physiology of important food crops: a review; citation_author=M Adrees, S Ali, M Rizwan, M Ibrahim, F Abbas, M Farid, M Zia-Ur-Rehman, MK Irshad, SA Bharwana; citation_volume=22; citation_publication_date=2015; citation_pages=8148-8162; citation_doi=10.1007/s11356-015-4496-5; citation_id=CR1 citation_journal_title=Plant Mol Biol; citation_title=Genome-wide identification and characterization of tRNA-derived RNA fragments in land plants; citation_author=CS Alves, R Vicentini, GT Duarte, VF Pinoti, M Vincentz, FT Nogueira; citation_volume=93; citation_publication_date=2017; citation_pages=35-48; citation_doi=10.1007/s11103-016-0545-9; citation_id=CR2 citation_journal_title=Trends Plant Sci; citation_title=Evolution of plant microRNAs and their targets; citation_author=MJ Axtell, JL Bowman; citation_volume=13; citation_publication_date=2008; citation_pages=343-349; citation_doi=10.1016/j.tplants.2008.03.009; citation_id=CR3 citation_journal_title=Front Plant Sci; citation_title=Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses; citation_author=M Barciszewska-Pacak, K Milanowska, K Knop, D Bielewicz, P Nuc, P Plewka, AM Pacak, F Vazquez, W Karlowski, A Jarmolowski, Z Szweykowska-Kulinska; citation_volume=6; citation_publication_date=2015; citation_pages=410; citation_doi=10.3389/fpls.2015.00410; citation_id=CR4 Brand LE, W.G. S, R.R.L G (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. J Exp Mar Biol Ecol 96: 225–250 citation_journal_title=Environ Pollut; citation_title=Effects of elevated soil copper on phenology, growth and reproduction of five ruderal plant species; citation_author=LA Brun, J Corff, J Maillet; citation_volume=122; citation_publication_date=2003; citation_pages=361-368; citation_doi=10.1016/S0269-7491(02)00312-3; citation_id=CR6 citation_journal_title=New Phytol; citation_title=Copper homeostasis; citation_author=JL Burkhead, KA Reynolds, SE Abdel-Ghany, CM Cohu, M Pilon; citation_volume=182; citation_publication_date=2009; citation_pages=799-816; citation_doi=10.1111/j.1469-8137.2009.02846.x; citation_id=CR7 citation_journal_title=Nucleic Acids Res; citation_title=GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes; citation_author=PP Chan, TM Lowe; citation_volume=44; citation_publication_date=2016; citation_pages=D184-D189; citation_doi=10.1093/nar/gkv1309; citation_id=CR8 citation_journal_title=Annu Rev Cell Dev Biol; citation_title=Small RNAs and their roles in plant development; citation_author=X Chen; citation_volume=25; citation_publication_date=2009; citation_pages=21-44; citation_doi=10.1146/annurev.cellbio.042308.113417; citation_id=CR9 citation_journal_title=Mol Gen Genomics: MGG; citation_title=Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency; citation_author=M Chen, C Wang, H Bao, H Chen, Y Wang; citation_volume=291; citation_publication_date=2016; citation_pages=1663-1680; citation_doi=10.1007/s00438-016-1210-3; citation_id=CR10 citation_journal_title=Front Plant Sci; citation_title=The new insights into cadmium sensing; citation_author=J Chmielowska-Bak, J Gzyl, R Rucinska-Sobkowiak, M Arasimowicz-Jelonek, J Deckert; citation_volume=5; citation_publication_date=2014; citation_pages=245; citation_id=CR11 citation_journal_title=Annu Rev Plant Biol; citation_title=Toxic heavy metal and metalloid accumulation in crop plants and foods; citation_author=S Clemens, JF Ma; citation_volume=67; citation_publication_date=2016; citation_pages=489-512; citation_doi=10.1146/annurev-arplant-043015-112301; citation_id=CR12 citation_journal_title=Nucleic Acids Res; citation_title=psRNATarget: a plant small RNA target analysis server; citation_author=X Dai, PX Zhao; citation_volume=39; citation_publication_date=2011; citation_pages=W155-W159; citation_doi=10.1093/nar/gkr319; citation_id=CR13 citation_journal_title=Int J Mol Sci; citation_title=Gene networks involved in hormonal control of root development in Arabidopsis thaliana: a framework for studying its disturbance by metal stress; citation_author=S Smet, A Cuypers, J Vangronsveld, T Remans; citation_volume=16; citation_publication_date=2015; citation_pages=19195-19224; citation_doi=10.3390/ijms160819195; citation_id=CR14 citation_journal_title=The Plant journal : for cell and molecular biology; citation_title=Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features; citation_author=C Di, J Yuan, Y Wu, J Li, H Lin, L Hu, T Zhang, Y Qi, MB Gerstein, Y Guo, ZJ Lu; citation_volume=80; citation_publication_date=2014; citation_pages=848-861; citation_doi=10.1111/tpj.12679; citation_id=CR15 citation_journal_title=Biochem Biophys Res Commun; citation_title=The role of microRNAs in copper and cadmium homeostasis; citation_author=YF Ding, C Zhu; citation_volume=386; citation_publication_date=2009; citation_pages=6-10; citation_doi=10.1016/j.bbrc.2009.05.137; citation_id=CR16 citation_journal_title=Nucleic Acids Res; citation_title=agriGO: a GO analysis toolkit for the agricultural community; citation_author=Z Du, X Zhou, Y Ling, Z Zhang, Z Su; citation_volume=38; citation_publication_date=2010; citation_pages=W64-W70; citation_doi=10.1093/nar/gkq310; citation_id=CR17 citation_journal_title=Nucleic Acids Res; citation_title=The Arabidopsis information resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant; citation_author=E Huala, AW Dickerman, M Garcia-Hernandez, D Weems, L Reiser, F LaFond, D Hanley, D Kiphart, M Zhuang, W Huang, LA Mueller, D Bhattacharyya, D Bhaya, BW Sobral, W Beavis, DW Meinke, CD Town, C Somerville, SY Rhee; citation_volume=29; citation_publication_date=2001; citation_pages=102-105; citation_doi=10.1093/nar/29.1.102; citation_id=CR18 citation_journal_title=Nucleic Acids Res; citation_title=miRBase: integrating microRNA annotation and deep-sequencing data; citation_author=A Kozomara, S Griffiths-Jones; citation_volume=39; citation_publication_date=2011; citation_pages=D152-D157; citation_doi=10.1093/nar/gkq1027; citation_id=CR19 citation_journal_title=Genome Biol; citation_title=Ultrafast and memory-efficient alignment of short DNA sequences to the human genome; citation_author=B Langmead, C Trapnell, M Pop, SL Salzberg; citation_volume=10; citation_publication_date=2009; citation_pages=R25; citation_doi=10.1186/gb-2009-10-3-r25; citation_id=CR20 citation_journal_title=Nucleic Acids Res; citation_title=PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences; citation_author=M Lescot, P Dehais, G Thijs, K Marchal, Y Moreau, Y Peer, P Rouze, S Rombauts; citation_volume=30; citation_publication_date=2002; citation_pages=325-327; citation_doi=10.1093/nar/30.1.325; citation_id=CR21 citation_journal_title=Cell Mol Life Sci; citation_title=The molecular mechanism of zinc and cadmium stress response in plants; citation_author=YF Lin, MG Aarts; citation_volume=69; citation_publication_date=2012; citation_pages=3187-3206; citation_doi=10.1007/s00018-012-1089-z; citation_id=CR22 citation_journal_title=Plant Cell Rep; citation_title=Role of salicylic acid in resistance to cadmium stress in plants; citation_author=Z Liu, Y Ding, F Wang, Y Ye, C Zhu; citation_volume=35; citation_publication_date=2016; citation_pages=719-731; citation_doi=10.1007/s00299-015-1925-3; citation_id=CR23 citation_journal_title=Front Plant Sci; citation_title=Reciprocal interactions between cadmium-induced Cell Wall responses and oxidative stress in plants; citation_author=C Loix, M Huybrechts, J Vangronsveld, M Gielen, E Keunen, A Cuypers; citation_volume=8; citation_publication_date=2017; citation_pages=1867; citation_doi=10.3389/fpls.2017.01867; citation_id=CR24 citation_journal_title=Nucleic Acids Res; citation_title=Adenylation of plant miRNAs; citation_author=S Lu, YH Sun, VL Chiang; citation_volume=37; citation_publication_date=2009; citation_pages=1878-1885; citation_doi=10.1093/nar/gkp031; citation_id=CR25 citation_journal_title=Nucleic Acids Res; citation_title=tRNA-derived small RNAs target transposable element transcripts; citation_author=G Martinez, SG Choudury, RK Slotkin; citation_volume=45; citation_publication_date=2017; citation_pages=5142-5152; citation_doi=10.1093/nar/gkx103; citation_id=CR26 citation_journal_title=Curr Opin Plant Biol; citation_title=Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic; citation_author=DG Mendoza-Cozatl, F Hauser, JI Schroeder; citation_volume=14; citation_publication_date=2011; citation_pages=554-562; citation_doi=10.1016/j.pbi.2011.07.004; citation_id=CR27 citation_journal_title=Brief Bioinform; citation_title=Toward microRNA-mediated gene regulatory networks in plants; citation_author=Y Meng, C Shao, M Chen; citation_volume=12; citation_publication_date=2011; citation_pages=645-659; citation_doi=10.1093/bib/bbq091; citation_id=CR28 citation_journal_title=Plant Physiol; citation_title=The regulatory activities of plant microRNAs: a more dynamic perspective; citation_author=Y Meng, C Shao, H Wang, M Chen; citation_volume=157; citation_publication_date=2011; citation_pages=1583-1595; citation_doi=10.1104/pp.111.187088; citation_id=CR29 citation_journal_title=Cell; citation_title=Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide; citation_author=S Mi, T Cai, Y Hu, Y Chen, E Hodges, F Ni, L Wu, S Li, H Zhou, C Long, S Chen, GJ Hannon, Y Qi; citation_volume=133; citation_publication_date=2008; citation_pages=116-127; citation_doi=10.1016/j.cell.2008.02.034; citation_id=CR30 citation_journal_title=Nat Chem Biol; citation_title=Facing the challenges of cu, Fe and Zn homeostasis in plants; citation_author=CM Palmer, ML Guerinot; citation_volume=5; citation_publication_date=2009; citation_pages=333-340; citation_doi=10.1038/nchembio.166; citation_id=CR31 Paytuvi Gallart A, Hermoso Pulido A, Anzar Martinez de Lagran I, Sanseverino W, Aiese Cigliano R (2016) GREENC: a Wiki-based database of plant lncRNAs Nucleic acids research 44: D1161–1166 citation_journal_title=New Phytol; citation_title=The copper microRNAs; citation_author=M Pilon; citation_volume=213; citation_publication_date=2017; citation_pages=1030-1035; citation_doi=10.1111/nph.14244; citation_id=CR33 citation_journal_title=Plant Physiol; citation_title=A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance; citation_author=T Qin, H Zhao, P Cui, N Albesher, L Xiong; citation_volume=175; citation_publication_date=2017; citation_pages=1321-1336; citation_doi=10.1104/pp.17.00574; citation_id=CR34 citation_journal_title=Brief Bioinform; citation_title=A reversed framework for the identification of microRNA-target pairs in plants; citation_author=C Shao, M Chen, Y Meng; citation_volume=14; citation_publication_date=2013; citation_pages=293-301; citation_doi=10.1093/bib/bbs040; citation_id=CR35 citation_journal_title=Plant Cell Physiol; citation_title=CANTATAdb: a collection of plant long non-coding RNAs; citation_author=MW Szczesniak, W Rosikiewicz, I Makalowska; citation_volume=57; citation_publication_date=2016; citation_doi=10.1093/pcp/pcv201; citation_id=CR36 citation_journal_title=Curr Opin Plant Biol; citation_title=Mechanisms to cope with arsenic or cadmium excess in plants; citation_author=N Verbruggen, C Hermans, H Schat; citation_volume=12; citation_publication_date=2009; citation_pages=364-372; citation_doi=10.1016/j.pbi.2009.05.001; citation_id=CR37 citation_journal_title=Curr Med Chem; citation_title=Cadmium and its epigenetic effects; citation_author=B Wang, Y Li, C Shao, Y Tan, L Cai; citation_volume=19; citation_publication_date=2012; citation_pages=2611-2620; citation_doi=10.2174/092986712800492913; citation_id=CR38 citation_journal_title=PLoS One; citation_title=Characterization of small RNAs derived from tRNAs, rRNAs and snoRNAs and their response to heat stress in wheat seedlings; citation_author=Y Wang, H Li, Q Sun, Y Yao; citation_volume=11; citation_publication_date=2016; citation_doi=10.1371/journal.pone.0150933; citation_id=CR39 citation_journal_title=Plant science : an international journal of experimental plant biology; citation_title=Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective; citation_author=BM Waters, RP Sankaran; citation_volume=180; citation_publication_date=2011; citation_pages=562-574; citation_doi=10.1016/j.plantsci.2010.12.003; citation_id=CR40 citation_journal_title=Chemosphere; citation_title=Toxicity of copper on rice growth and accumulation of copper in rice grain in copper contaminated soil; citation_author=J Xu, L Yang, Z Wang, G Dong, J Huang, Y Wang; citation_volume=62; citation_publication_date=2006; citation_pages=602-607; citation_doi=10.1016/j.chemosphere.2005.05.050; citation_id=CR41 citation_journal_title=Chemosphere; citation_title=Accumulation of copper in brown rice and effect of copper on rice growth and grain yield in different rice cultivars; citation_author=YP Yan, JY He, C Zhu, C Cheng, XB Pan, ZY Sun; citation_volume=65; citation_publication_date=2006; citation_pages=1690-1696; citation_doi=10.1016/j.chemosphere.2006.05.022; citation_id=CR42 citation_journal_title=Nucleic Acids Res; citation_title=PNRD: a plant non-coding RNA database; citation_author=X Yi, Z Zhang, Y Ling, W Xu, Z Su; citation_volume=43; citation_publication_date=2015; citation_pages=D982-D989; citation_doi=10.1093/nar/gku1162; citation_id=CR43 citation_journal_title=Rice; citation_title=Bioinformatics resources for deciphering the biogenesis and action pathways of plant small RNAs; citation_author=D Yu, X Ma, Z Zuo, W Shao, H Wang, Y Meng; citation_volume=10; citation_publication_date=2017; citation_pages=38; citation_doi=10.1186/s12284-017-0177-y; citation_id=CR44 citation_journal_title=Plant Signal Behav; citation_title=Role of ROS and auxin in plant response to metal-mediated stress; citation_author=HM Yuan, WC Liu, Y Jin, YT Lu; citation_volume=8; citation_publication_date=2013; citation_doi=10.4161/psb.24671; citation_id=CR45 citation_journal_title=Nucleic Acids Res; citation_title=miRU: an automated plant miRNA target prediction server; citation_author=Y Zhang; citation_volume=33; citation_publication_date=2005; citation_pages=W701-W704; citation_doi=10.1093/nar/gki383; citation_id=CR46 citation_journal_title=Planta; citation_title=A genome-wide survey of microRNA truncation and 3′ nucleotide addition events in larch (Larix leptolepis); citation_author=J Zhang, S Zhang, S Li, S Han, T Wu, X Li, L Qi; citation_volume=237; citation_publication_date=2013; citation_pages=1047-1056; citation_doi=10.1007/s00425-012-1823-7; citation_id=CR47 citation_journal_title=Physiol Plant; citation_title=MiR398 and plant stress responses; citation_author=C Zhu, Y Ding, H Liu; citation_volume=143; citation_publication_date=2011; citation_pages=1-9; citation_doi=10.1111/j.1399-3054.2011.01477.x; citation_id=CR48