Abstract
MicroRNAs (miRNAs) are a set of small, non-coding RNAs that negatively and post-transcriptionally mediate their respective target mRNAs by directing the target mRNA cleavage or translational repression. Plant miRNAs have been involved in developmental processes and adaption to biotic and abiotic stresses in their environment. The banded leaf and sheath blight (BLSB) caused by Rhizoctonia solani is extremely harmful to maize. To investigate the functions of miRNAs under R. solani inoculation, miRNA expression in R. solani infected maize (Zea mays L.) was profiled using deep sequencing. In total, 41 significantly differentially expressed known miRNAs and 39 novel R. solani-responsive miRNAs were identified, of which 9 identified miRNAs were further validated by qRT-PCR, and 2 important miRNAs were analyzed by in situ hybridization. Target genes were also predicted for these R. solani-responsive miRNAs; most of these putative target genes encoded transcription factors and proteins associated with metabolic processes or stress responses. In addition, the mRNA expression levels of several target genes that negatively correlated with the levels of corresponding miRNAs under R. solani inoculation were validated by qRT-PCR. These findings hypothesized that these miRNAs play an important role in R. solani resistance in maize, highlighting novel molecular mechanisms of R. solani resistance in plants.
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References
Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283(23):15932–15945
Aiguo Y, Guangtang P, Huazhi Y (2003) Evaluating resistance of inbred lines of corn to maize sheath blight and screening of resistance resources. Plant Prot 29(1):25–28
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402
Ameres SL, Martinez J, Schroeder R (2007) Molecular basis for target RNA recognition and cleavage by human RISC. Cell 130(1):101–112
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell Online 15(11):2730–2741
Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5):683–692
Bonnet E, Wuyts J, Rouze P, Van de Peer Y (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci USA 101(31):11511–11516
Bonnet E, He Y, Billiau K, Van de Peer Y (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26(12):1566–1568
Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54(5):876–887
Carling D, Kuninaga S, Brainard K (2002) Hyphal anastomosis reactions, rDNA-internal transcribed spacer sequences, and virulence levels among subsets of Rhizoctonia solani anastomosis group-2 (AG-2) and AG-BI. Phytopathology 92(1):43–50
Chen J, Tang C, Xue C, Niu X, Song Z (2000) On penetration process of sheath blight pathogen in maize. J Shenyang Agri Univ 31(5):503–506
Chen L, Ren Y, Zhang Y, Xu J, Zhang Z, Wang Y (2012) Genome-wide profiling of novel and conserved Populus microRNAs involved in pathogen stress response by deep sequencing. Planta 235(5):873–883
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18(2):412–421
Chung W, Huang J, Huang H (2005) Formulation of a soil biofungicide for control of damping-off of Chinese cabbage (Brassica chinensis) caused by Rhizoctonia solani. Biol Control 32(2):287–294
Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20(22):3084–3088
Debigaré R, Price SR (2003) Proteolysis, the ubiquitin-proteasome system, and renal diseases. Am J Physiol Renal Physiol 285(1):F1–F8
Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64(11):3077–3086
Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138(2):778–789
Dsouza M, Larsen N, Overbeek R (1997) Searching for patterns in genomic data. Trends Genet 13(12):497–498
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38 (Web Server issue):W64-70
Gao J, Chen Z, Luo M, Peng H, Lin H, Qin C, Yuan G, Shen Y, Ding H, Zhao M, Pan G, Zhang Z (2014) Genome expression profile analysis of the maize sheath in response to inoculation to R. solani. Mol Biol Rep 41(4):2471–2483
Gonzalez-Vera AD, Bernardes-de-Assis J, Zala M, McDonald BA, Correa-Victoria F, Graterol-Matute EJ, Ceresini PC (2010) Divergence between sympatric rice- and maize-infecting populations of Rhizoctonia solani AG-1 IA from Latin America. Phytopathology 100(2):172–182
Guerrero-González M, Rodríguez-Kessler M, Rodríguez-Guerra R, González-Chavira M, Simpson J, Sanchez F, Jiménez-Bremont J (2011) Differential expression of Phaseolus vulgaris genes induced during the interaction with Rhizoctonia solani. Plant Cell Rep 30(8):1465–1473
Huang M, Tan J, Yang J, Yang K (2007) Research advance on Banded Leaf and Sheath Blight of maize. Southwest China J Agri Sci 20(2):209–213
Javelle M, Timmermans MC (2012) In situ localization of small RNAs in plants by using LNA probes. Nat Protoc 7(3):533–541
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, 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 plants. Annu Rev Plant Biol 57:19–53
Jung WJ, Mabood F, Smith DL (2011) Effects of Pseudomonas aureofaciens 63-28 on defense responses in soybean plants infected by Rhizoctonia solani. J Microbiol Biotechnol 21(4):379–386
Khraiwesh B, Pugalenthi G, Fedoroff NV (2013) Identification and Analysis of Red Sea Mangrove (Avicennia marina) microRNAs by High-Throughput Sequencing and Their Association with Stress Responses. PLoS One 8(4):e60774
Kidner CA, Martienssen RA (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8(1):38–44
Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research 39 (Database issue):D152-157
Law CJ, Maloney PC, Wang DN (2008) Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 62:289–305
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24(5):713–714
Li L, YongYi M, ZhiMing Z, PengFei L, GuangTang P, MaoJun Z (2009) Functional effects of different defense enzymes on banded leaf and sheath blight of maize. Journal of Maize Sciences 17 (3):99–102&106
Li Y, Fu Y, Ji L, Wu C, Zheng C (2010a) Characterization and expression analysis of the Arabidopsis mir169 family. Plant Sci 178(3):271–280
Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou J-M (2010b) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 152(4):2222–2231
Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B (2012) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 109(5):1790–1795
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 L, Zhang Z, Zhao M, Wang J, Lin H, Shen Y, Pan G (2011) Molecular cloning and characterization of pathogenesis-related protein 5 in Zea mays and its antifungal activity against Rhizoctonia solani. Afr J Biotechnol 10(83):19286–19293
Liu Z, Kumari S, Zhang L, Zheng Y, Ware D (2012) Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS One 7(6):e39786
Liu H, Qin C, Chen Z, Zuo T, Yang X, Zhou H, Xu M, Cao S, Shen Y, Lin H, He X, Zhang Y, Li L, Ding H, Lubberstedt T, Zhang Z, Pan G (2014) Identification of miRNAs and their target genes in developing maize ears by combined small RNA and degradome sequencing. BMC Genom 15:25
Lu S, Sun YH, Amerson H, Chiang VL (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J 51(6):1077–1098
Luo M, Gao J, Peng H, Pan GT, Zhang ZM (2014) MiR393-targeted TIR1-like (F-box) gene in response to inoculation to R. solani in Zea mays. Acta Physiologiae Plantarum 36(6):1283–1291
Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61(14):4011–4019
Mendoza-Soto AB, Sanchez F, Hernandez G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:105
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312(5772):436–439
Okubara PA, Steber CM, DeMacon VL, Walter NL, Paulitz TC, Kidwell KK (2009) Scarlet-Rz1, an EMS-generated hexaploid wheat with tolerance to the soilborne necrotrophic pathogens Rhizoctonia solani AG-8 and R. oryzae. Theor Appl Genet 119(2):293–303
Qiu F, Zheng Y, Zhang Z, Xu S (2007) Mapping of QTL associated with waterlogging tolerance during the seedling stage in maize. Ann Bot 99(6):1067–1081
Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H (2006) Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression’s C T difference” formula. J Mol Med 84(11):901–910
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527
Shen Y, Jiang Z, Lu S, Lin H, Gao S, Peng H, Yuan G, Liu L, Zhang Z, Zhao M, Rong T, Pan G (2013) Combined small RNA and degradome sequencing reveals microRNA regulation during immature maize embryo dedifferentiation. Biochem Biophys Res Commun 441(2):425–430
Shuai P, Liang D, Zhang Z, Yin W, Xia X (2013) Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genom 14(1):233
Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu J-K, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genom 9(1):160
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019
Sunkar R, Girke T, Zhu J-K (2005) Identification and characterization of endogenous small interfering RNAs from rice. Nucleic Acids Res 33(14):4443–4454
Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell Online 18(8):2051–2065
Thiebaut F, Rojas CA, Grativol C, Motta MR, Vieira T, Regulski M, Martienssen RA, Farinelli L, Hemerly AS, Ferreira PC (2014) Genome-wide identification of microRNA and siRNA responsive to endophytic beneficial diazotrophic bacteria in maize. BMC Genom 15:766
Wang CY, Chen YQ, Liu Q (2011) Sculpting the meristem: the roles of miRNAs in plant stem cells. Biochem Biophys Res Commun 409(3):363–366
Yan J, Zheng J, Ye H (2008) Damage and yield loss in corn caused by corn sheath blight. Journal of Maize Sciences 16
Yang ZM, Chen J (2013) A potential role of microRNAs in plant response to metal toxicity. Metallomics Integrated Biometal Sci 5(9):1184–1190
Yang AG, Pan GT, Ye HZ, Tang L, Rong TZ (2003) Evaluating resistance of inbred lines of corn to maize sheath blight and screening of resistance resources. Plant Prot 29(1):25–28
Zeng X, Yi Y, Liu HL, Zhang ZM, Zhao MJ, pAN GT (2011) Analysis of differential protein induced by Rhizoctonia solani Kühn in different resistant maize inbred lines. J Agric Biotechnol 19(2):250–257
Zhang Z, Zhao M, Ma Y (2006) Advances in the Research of SSH on Disease-resistance Gene Expression of Maize. J Maize Sci 14(3):42–45
Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5(11):e1000716
Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Qi L (2010) Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem Biophys Res Commun 398(3):355–360
Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33(2):403–409
Zhang Z, Liu L, Lin H, Yuan G, Zeng X, Shen Y, Zhao M, Zhao Q, Pan G (2012) Identification of genes differentially expressed in maize (Zea mays L.) during Rhizoctonia Solani Kühn infection by suppression subtractive hybridization. Afr J Biotechnol 11(12):2827–2838
Zhao M, Ding H, Zhu JK, Zhang F, Li WX (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190(4):906–915
Zhao JP, Jiang XL, Zhang BY, Su XH (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7(9):e44968
Zheng A, Lin R, Zhang D, Qin P, Xu L, Ai P, Ding L, Wang Y, Chen Y, Liu Y, Sun Z, Feng H, Liang X, Fu R, Tang C, Li Q, Zhang J, Xie Z, Deng Q, Li S, Wang S, Zhu J, Wang L, Liu H, Li P (2013) The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nature Commun 4:1424
Zhou M, Gu L, Li P, Song X, Wei L, Chen Z, Cao X (2010) Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica). Frontiers in Biology 5 (1):67–90
Zhou ZS, Song JB, Yang ZM (2012) Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot 63(12):4597–4613
Zuo S, Yin Y, Pan C, Chen Z, Zhang Y, Gu S, Zhu L, Pan X (2013) Fine mapping of qSB-11(LE), the QTL that confers partial resistance to rice sheath blight. TAG 126(5):1257–1272
Acknowledgments
This work was supported by National Natural Science Foundation of China (30900901), the Scientific Reserch Fund of SiChuan Provincial Education Department (Grant No. 11ZB123) and SiChuan Provincial Health Department (Grant No. 120371), and the Foundation of Luzhou Municipal Science and Technology Bureau of Sichuan Province (2013-S-47, 2013LZLY-K64).
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Communicated by E. K.-Gebarowska.
M. Luo, H. J. Lin and J. Gao contributed equally to this work.
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The secondary structure of novel miRNA precursors. Predicted secondary structures of novel identified miRNAs, Mature miRNA sequences were shown in green. (PDF 403 kb)
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Functions and percentages of target genes of conserved zma-miRNAs. All predicted targets were included in these calculations. (JPEG 29 kb)
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Functions and percentages of target genes of novel zma-miRNAs. All predicted targets were included in these calculations. (JPEG 25 kb)
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Luo, M., Lin, H., Gao, J. et al. Identification and characterization of differentially expressed microRNAs in response to Rhizoctonia solani in maize. Acta Physiol Plant 37, 250 (2015). https://doi.org/10.1007/s11738-015-2001-x
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DOI: https://doi.org/10.1007/s11738-015-2001-x