Abstract
Soil salinization can lead to environmental and ecological problems worldwide. Abiotic stressors, including salinity, are suspected to regulate microRNA (miRNA) expression. Plants exposed to such abiotic stressors express specific miRNAs, which are genes encoding small non-coding RNAs of 20–24 nucleotides. miRNAs are known to exist widely in plant genomes, and are endogenous. A previous study used miRNA microarray technology and poly(A) polymerase-mediated qRT-PCR technology to analyze the expression profile of miRNAs in two types of plants, Populus cathayana L. (salt-sensitive plants) and Salix matsudana Koidz (highly salinity-tolerant plants), both belonging to the Salicaceae family. miRNA microarray hybridization revealed changes in expression of 161 miRNAs P. cathayana and 32 miRNAs in S. matsudana under salt stress. Differences in expression indicate that the same miRNA has different expression patterns in salt-sensitive plants and salt-tolerant plants under salt stress. These indicate that changes in expression of miRNAs might function as a response to varying salt concentrations. To examine this, we used qRT-PCR to select five miRNA family target genes involved in plant responses to salt stress. Upon saline treatment, the expressions of both ptc-miR474c and ptc-miR398b in P. cathayana were down-regulated, but were up-regulated in S. matsudana. Expression of the miR396 family in both types of plants was suppressed. Furthermore, we have analyzed the different expression patterns between P. cathayana and S. matsudana. Findings of this study can be utilized in future investigations of post-transcriptional gene regulation in P. cathayana and S. matsudana under saline stress.
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References
Ambros V (1989) Hierarchy of regulatory genes controls a larva to adult developmental switch in elegans. Cell 57(1):49–57
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24(5):701–713
Baldwin JC, Dombrowski JE (2006) Evaluation of Lolium temulentum as a model grass species for the study of salinity stress by PCR-based subtractive suppression hybridization analysis. Plant Sci 171(4):459–469
Bartel DP (2004) MicroRNAs genomics biogenesis mechanism and function. Cell 116(2):281–297
Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5):683–692
Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123(7):1279–1291
Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579(26):5923–5931
Choi D, Kim JH, Kende H (2004) Whole genome analysis of the OsGRF gene family encoding plant-specific putative transcription activators in rice (Oryza sativa L). Plant Cell Physiol 45(7):897–904
Chu CY, Rana TM (2006) Translation repression in human cells by microRNA induced gene silencing requires RCK/p54. PLoS Biol 4(7):210–219
Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar cloning and expression in response to wounding and herbivory. Plant Physiol 124(1):285–295
Dai SX, Chen sl, Fritz E, Olbrich A et al (2006) Ion compartmentation in leaf cells of Populus euphratica and P.tomentosa under salt stress. J Beijing For Uni S2:1–5
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Annals Bot 103(1):29–38
Yang F, Xiao X, Zhang S, Korpelainen H, Li C (2009) Salt stress responses in Populus cathayana Rehder. Plant Sci 176(5):669–677
Gomez GA, Verhey SD, Holappa LD, Shen Q, Ho THD, Walker-simmwas MK (1999) An ABA-induced protein kinase, PK2 ABA1, mediates ABA-suppressed gene expression in barley aleurone layers. Proc Natl Acad Sci USA 96(4):1767–1772
Griffiths JS (2004) The microRNA registry. Nucleic Acids 32:109–111
Griffiths JS, Moxon S, Marshall M et al (2005) Annotating non-coding RNAs in complete genomes. Nucleic Acids 33:121–124
Hanley S, Barker JHA, Ooijen JWV et al (2002) A genetic linkage map of willow (Salix viminalis) based on AFLP and microsatellite markers. Theor Appl Genet 105(6):1087–1096
He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factors downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44(6):903–916
Hu HH, Dai MQ, Yao JL, Xiao BZ, Li XH, Zhang QF, Xiong LZ (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103(35):12987–12992
Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229(4):1009–1023
Jia XY, Wang WX, Ren LG et al (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71(1–2):51–59
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNA and their target, including a stress-induced miRNA. Mol Cell 14(6):787–799
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plant. Annu Rev Plant Biol 57:19–53
Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36(1):94–104
Laura Z, Gábor R, András S, Gyöngyi S, Krisztina Ö, Zsuzsanna D et al (2008) Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol 146(4):1721–1737
Liang M, Davis E, Gardner D, Cai X, Wu Y (2006) Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224(5):1185–1196
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14(5):836–843
Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R (2005) MicroRNA dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7(7):719–723
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 −△△CT method. Methods 25(4):402–408
Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus Trichocarpa that are absent from Arabidopsis. Plant Cell 17(8):2186–2203
Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55(1):131–151
Luo YC, Zhou H, Li Y, Chen GY et al (2006) Rice embryogenic calli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant post-embryogenic development. FEBS Lett 580(21):5111–5116
Lurin C, Andres C, Aubour S, Bellaouiet M et al (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16(8):2089–2103
Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459(1–2):39–47
Ma S, Gong Q, Bohnert HJ (2006) Dissecting salt stress pathways. J Exp Bot 57(5):1097–1107
Mizoguchi T, Ichimura K, Irie K (1998) Identification of possible MAPK kinase cascade in Arabjdopsis theliana based on parewise yeast two hybrid analysis and functional complementation test of yeast mutants. FEBS Lett 437(1–2):56–60
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 57(8):473–497
Novorry MJ (1984) Purification and properties of D-manoitol-phosphate dehydrogenase and D-dlucitol-6-phosphate dehydrogenase from Escherichia coli. J Bacteriol 159(3):986–990
Pysh LD et al (1999) The GRAS gene family in A rabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18(1):111–119
Rathinasabapathi B, Burnet M, Russell BL et al (1997) Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plats: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci USA 94(7):3454–3458
Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57(5):1017–1023
Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49(4):592–606
Rhoades JD, Loveday J (1990) Salinity in irrigated agriculture. AGRIS Rec 30:1089–1142
Rhoades M, Reinhart B, Lim L, Burge B et al (2002) Prediction of plant microRNA targets. Cell 110(4):513–520
Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17(3):354–358
Salah E, Abdel G, Marinus P (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283(6):15932–15945
Schauers E, Jacobsen SE, Meinke DW, Ray A (2002) Dicer-like 1 blind men and elephants in Arabidopsis development. Trends Plant Sci 7(11):487–491
Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V et al (2000) Quantitative reverse transcription–polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285(2):194–204
Shen YG, Yan DQ, DU BX, Zhang JS et al (2002) Overexpression of proline transporter gene isolated from halophyte confers salt tolerance in Arabidopsis. J Integr Plant Biol 44(8):956–962
Small ID, Peeters N (2000) The PPR motif: a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25(2):46–47
Stocking SJ, Gilmour MF, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94(3):1035–1040
Seki M, Ishida J, Narusaka M, Fujita M et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019
Sunkar R, Kapoor A, Zhu JK (2006) 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 18(8):2051–2065
Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12(7):301–309
Tang G, Reinhart BJ, Bartel DP et al (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17(1):49–63
Tang G (2005) siRNA and miRNA:an insight into RISCs. Trends Biochem Sci 30(2):106–144
Tang G, Tang X, Mendu V, Jia X, Chen QJ, He L (2008) The art of microRNA: various strategies leading to gene silencing via an ancient pathway. Biochim Biophys Acta 1779(11):655–662
Tran LS, Nakashima K, Sakuma Y, Simpson SD et al (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought responsive Cis-element in the early responsive to dehydrationstress promoter. Plant Cell 16(9):2481–2498
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604
Urao T, Katagiri T (1994) Two genes that encode Ca2 + dependent protein kinase are induced by drought and high salt stress in Arabidopsis theliana. Mol Genet 244:331–340
Vernon DM, Bohnert HJ (1992) A novel metby transferase induced by osmotic stress in the facultative Mesembryanthemum crystallium. EMBO J 11(6):2077–2085
Wei JZ, Tirajoh A, Effendy J, Plant AL (2000) Characterization of salt-induced changes in gene expression in tomato (Lycopersicon esculentum) roots and the role played by abscisic acid. Plant Sci 159(1):135–148
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6(2):251–264
Yang ZX, Wang SZ, Xu G et al (1995) Study on the variation of wood property of juvenile P. cathayana among and within provenances. Scientia Silvae Sinicae 8(4):437–441
Yu SH, Liu J, Fu DR et al (2003) Characteristics of Tacamachaca genes in the Western Sichuan plateau. J Zejiang For Coll 20(1):29–33
Wu Y-Y, Qi-Jun C et al (2005) Salt-tolerant transgenic perennial ryegrass (Lolium perenne L.) obtained by Agrobacterium tumefaciens-mediated transformation of the vacuolar Na+/H+ antiporter gene. Plant Sci 169(1):65–73
Zeng HZ, Luo LJ (2003) A review on plant drought and salt tolerance gene. J Plant Genet Resour 4(3):270–273
Zhang BH, Pan XP, Anderson TA (2006) Indentification of 188 conserved maize microRNAs and the its targets. FEBS Lett 580(5):3752–3762
Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289(1):3–16
Zhang B, Wang Q, Pan X (2007) MicroRNAs and their regulatory roles in animals and plants. Cell Physiol 210(2):279–289
Zhao B, Ge LF, Liang RQ et al (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10(29):1–10
Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold- inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779(11):780–788
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We would like to thank Dr. Han-Jiang Fu of the Academy of Military Medical Science and Dr. Zhangxun Wang of the Tongji University School of Medicine for their technical assistance. This work was supported by the National Natural Science Fundation of China (30972340) and Natural Science Fundation of Zhejiang Province (R3090070).
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Jing Zhou and Mingying Liu contributed equally to this study.
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Zhou, J., Liu, M., Jiang, J. et al. Expression profile of miRNAs in Populus cathayana L. and Salix matsudana Koidz under salt stress. Mol Biol Rep 39, 8645–8654 (2012). https://doi.org/10.1007/s11033-012-1719-4
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DOI: https://doi.org/10.1007/s11033-012-1719-4