Expression of miRNAs involved in phosphate homeostasis and senescence is altered in glyphosate-treated maize

• Autorzy: Zywicki M. , Gracz J. , Karlowski W. , Twardowski T. , Tyczewska A.
• Języki publikacji: EN

Abstrakty

EN

Glyphosate is a systemic, nonselective and most widely used herbicide in the world. The introduction of glyphosate-resistant crops in the mid-1990s resulted in a dramatic increase in the use of glyphosate herbicide making it most widely used herbicide in the world. The average maize yield loss in the field caused by pests is around 20 % but in many regions it is much higher. It is now clear that glyphosate causes broader range of physiological alterations than previously assumed and some plants gain higher level of resistance to glyphosate without the need to use genetic engineering methods. To understand the mechanisms of such heightened resistance we must first know the processes mediating the plants’ death in response to glyphosate treatment. Here, we show that 12 miRNAs, belonging to miR167, miR396, miR159, miR156, miR169, miR444 and miR827 families, are significantly upregulated, and one, miR166, downregulated following glyphosate treatment. These miRNAs have been previously shown to be involved in abiotic stress responses and implicated in senescence. Strikingly, two of the induced miRNAs, miR444 and miR827, have been shown to regulate phosphate transport pathways, which seem to be common for Pi and glyphosate uptake.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 12
• Opis fizyczny: Article: 265 [10 p.], fig.,ref.

Twórcy

autor

Zywicki M.

• Department of Computational Biology, Faculty of Biology, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University in Poznan, Umultowska 89, 61-614, Poznan, Poland

autor

Gracz J.

• Department of RNA Biology, Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznan, Poland

autor

Karlowski W.

• Department of Computational Biology, Faculty of Biology, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University in Poznan, Umultowska 89, 61-614, Poznan, Poland

autor

Twardowski T.

• Department of RNA Biology, Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznan, Poland

autor

Tyczewska A.

• Department of RNA Biology, Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznan, Poland

Bibliografia

• Allu AD, Soja AM, Wu A, Szymanski J, Balazadeh S (2014) Salt stress and senescence: identification of cross-talk regulatory components. J Exp Bot 65:3993–4008. doi:10.1093/jxb/eru173
• Baev V, Naydenov M, Apostolova E et al (2010) Identification of RNA-dependent DNA-methylation regulated promoters in Arabidopsis. Plant Physiol Biochem 48:393–400. doi:10.1016/j. plaphy.2010.03.013
• Brecke BJ, Duke WB (1980) Effect of glyphosate on intact bean plants (Phaseolus vulgaris L.) and isolated cells. Plant Physiol 66:656–659
• Buchanan-Wollaston V, Page T, Harrison E et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585
• Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159. doi:10.1093/nar/gkr319
• Debernardi JM, Mecchia MA, Vercruyssen L et al (2014) Posttranscriptional control of GRF transcription factors by micro-RNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 79:413–426. doi:10.1111/tpj.12567
• Denis M-H, Delrot S (1993) Carrier-mediated uptake of glyphosate in broad bean (Vicia faba) via a phosphate transporter. Physiol Plant 87:569–575. doi:10.1111/j.1399-3054.1993.tb02508.x
• Ding D, Zhang L, Wang H et al (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38. doi:10.1093/aob/mcn205
• Duke SO, Powles SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319–325. doi:10.1002/ps.1518
• Friedländer MR, Mackowiak SD, Li N et al (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40:37–52. doi:10.1093/nar/gkr688
• Fu L, Niu B, Zhu Z et al (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152. doi:10.1093/bioinformatics/bts565
• Gao P, Bai X, Yang L et al (2010) Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 231:991–1001. doi:10.1007/s00425-010-1104-2
• Geiger DR, Kapitan SW, Tucci MA (1986) Glyphosate inhibits photosynthesis and allocation of carbon to starch in sugar beet leaves. Plant Physiol 82:468–472
• Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol (Stuttg) 10(Suppl 1):37–49. doi:10.1111/j.1438-8677.2008.00114.x
• Hackenberg M, Shi B-J, Gustafson P, Langridge P (2013) Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol 13:214. doi:10.1186/1471-2229-13-214
• Heap I (2015) International Survey of Herbicide Resistant Weeds. Online. Internet. Available: http://www.weedscience.com. Accessed 21 May 2015
• Hetherington PR, Marshall G, Kirkwood RC, Warner JM (1998) Absorption and efflux of glyphosate by cell suspensions. J Exp Bot 49:527–533. doi:10.1093/jxb/49.320.527
• Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J Plant Physiol 158:1317–1323. doi:10.1078/0176-1617-00608
• Jian X, Zhang L, Li G et al (2010) Identification of novel stressregulated microRNAs from Oryza sativa L. Genomics 95:47–55. doi:10.1016/j.ygeno.2009.08.017
• Jurka J (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 16:418–420
• Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73. doi:10.1093/nar/gkt1181
• Kulcheski FR, de Oliveira LF, Molina LG et al (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genom 12:307. doi:10.1186/1471-2164-12-307
• Li T, Li H, Zhang Y-X, Liu J-Y (2011) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833. doi:10.1093/nar/gkq1047
• Lin S-I, Santi C, Jobet E et al (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51:2119–2131. doi:10.1093/pcp/pcq170
• Lin W-Y, Huang T-K, Chiou T-J (2013) Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25:4061–4074. doi:10.1105/tpc.113.116012
• Liu Z, Kumari S, Zhang LZ et al (2012) Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS One 7:e39786. doi:10.1371/journal.pone.0039786
• Liu T-Y, Lin W-Y, Huang T-K, Chiou T-J (2014) MicroRNAmediated surveillance of phosphate transporters on the move. Trends Plant Sci 19:647–655. doi:10.1016/j.tplants.2014.06.004
• Lundmark M, Kørner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plant 140:57–68. doi:10.1111/j.1399-3054.2010.01384.x
• Martin M (2011) Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet.journal 17: 10
• Meng Y, Shao C, Ma X et al (2012) Expression-based functional investigation of the organ-specific microRNAs in Arabidopsis. PLoS One 7:e50870. doi:10.1371/journal.pone.0050870
• Menne H, Köcher H (2008) HRAC Classification of Herbicides and Resistance Development. In:Modern Crop Protection Compounds. Hedelberg, Germany pp 5–26 doi:10.1002/9783527619580.ch1
• Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457:413–420. doi:10.1038/nature07756
• Morin F, Vera V, Nurit F et al (1997) Glyphosate Uptake in Catharanthus roseus Cells: role of a Phosphate Transporter. Pestic Biochem Physiol 58:13–22
• Orcaray L, Zulet A, Zabalza A, Royuela M (2012) Impairment of carbon metabolism induced by the herbicide glyphosate. J Plant Physiol 169:27–33. doi:10.1016/j.jplph.2011.08.009
• Pei L, Jin Z, Li K et al (2013) Identification and comparative analysis of low phosphate tolerance-associated microRNAs in two maize genotypes. Plant Physiol Biochem 70:221–234. doi:10.1016/j.plaphy.2013.05.043
• Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392
• Reimand J, Arak T, Vilo J (2011) g:profiler–a web server for functional interpretation of gene lists (2011 update). Nucleic Acids Res 39:W307–W315. doi:10.1093/nar/gkr378
• Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi:10.1093/bioinformatics/btp616
• Romero DM, Ríos de Molina MC, Juárez AB (2011) Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotoxicol Environ Saf 74:741–747. doi:10.1016/j.ecoenv.2010.10.034
• Serra A-A, Nuttens A, Larvor V et al (2013) Low environmentally relevant levels of bioactive xenobiotics and associated degradation products cause cryptic perturbations of metabolism and molecular stress responses in Arabidopsis thaliana. J Exp Bot 64:2753–2766. doi:10.1093/jxb/ert119
• Shaner DL (2009) Role of Translocation as A Mechanism of Resistance to Glyphosate. Weed Sci 57:118–123. doi:10.1614/WS-08-050.1
• Shen J, Xie K, Xiong L (2010) Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Mol Genet Genomics 284:477–488. doi:10.1007/s00438-010-0581-0
• Thatcher SR, Burd S, Wright C et al (2015) Differential expression of miRNAs and their target genes in senescing leaves and siliques: insights from deep sequencing of small RNAs and cleaved target RNAs. Plant, Cell Environ 38:188–200. doi:10.1111/pce.12393
• Van der Graaff E, Schwacke R, Schneider A et al (2006) Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792
• Wu G, Park MY, Conway SR et al (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759. doi:10.1016/j.cell.2009.06.031
• Xu X, Bai H, Liu C et al (2014) Genome-wide analysis of microRNAs and their target genes related to leaf senescence of rice. PloS One 9:e114313. doi:10.1371/journal.pone.0114313
• Yan Y, Wang H, Hamera S, Chen X, Fang R (2014) miR444a has multiple functions in the rice nitrate-signaling pathway. Plant J 78:44–55. doi:10.1111/tpj.12446
• Yao Z-F, Liang C-Y, Zhang Q et al (2014) SPX1 is an important component in the phosphorus signalling network of common bean regulating root growth and phosphorus homeostasis. J Exp Bot 65:3299–3310. doi:10.1093/jxb/eru183
• Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167:1289–1297. doi:10.1016/j.jplph.2010.04.017
• Zhao X, Liu X, Guo C et al (2013) Identification and characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. J Plant Biochem Biotechnol 22:113–123. doi:10.1007/s13562-012-0117-2
• Zhou J, Cheng Y, Yin M et al (2015) Identification of novel miRNAs and miRNA expression profiling in wheat hybrid necrosis. PloS One 10:e0117507. doi:10.1371/journal.pone.0117507
• Zhu YY, Zeng HQ, Dong CX et al (2010) microRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Sci 178:23–29. doi:10.1016/j.jplph. 2010.04.017