Developmental changes in barley microRNA expression profiles coupled with miRNA targets analysis.

Andrzej Miroslaw Pacak; Katarzyna Kruszka; Aleksandra Świda-Barteczka; Przemysław Nuc; Wojciech Karlowski; Artur Jarmołowski; Zofia Szweykowska-Kulińska

doi:10.18388/abp.2016_1347

Andrzej Miroslaw Pacak Adam Mickiewicz University in Poznan
Katarzyna Kruszka Adam Mickiewicz University in Poznan
Aleksandra Świda-Barteczka Adam Mickiewicz University in Poznan
Przemysław Nuc Adam Mickiewicz University in Poznan
Wojciech Karlowski Adam Mickiewicz University in Poznan
Artur Jarmołowski Adam Mickiewicz University in Poznan
Zofia Szweykowska-Kulińska Adam Mickiewicz University in Poznan

DOI: https://doi.org/10.18388/abp.2016_1347

Keywords: microRNA, barley, NGS, degradome

Abstract

MicroRNAs are 18-24 nt long single stranded RNAs that are crucial regulators of gene expression and control plant development and response to environmental cues. We have analyzed microtranscriptomes of five barley developmental stages. Generally during barley development miR168-3p, miR1432-5p levels increase and miR156-5p, miR169-3p decrease. We have identified two miR156-5p izomiRs (called 5’U miR156-5p - 20 nt and 5’UU miR156-5p - 21 nt), which were differently expressed during barley development. 5’ U miR156-5p level decreased in 3-week, 6-week and 68-day old barley, when compared to 1-week-old plants. Meanwhile, 5’ UU miR156-5p level increased significantly in 68-day old barley plants. Moreover, only 5’ U miR156 isomiR recognizes and guides unique transcription factor mRNAs from Squamosa Promoter Like Binding Protein (SPL) family. We identified many non-canonical microRNAs with the expression levels changed during barley development. Here we present the profiles of microRNAs expression characteristic for particular barley developmental stages. These analyses are accompanied by the experimental degradome analysis of miRNA targets.

References

Alaba S, Piszczalka P, Pietrykowska H, Pacak AM, Sierocka I, Nuc PW, Singh K, Plewka P, Sulkowska A, Jarmolowski A (2015) The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants. New Phytologist 206: 352-367.

Allen RS, Li J, Alonso-Peral MM, White RG, Gubler F, Millar AA (2010) MicroR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 1: 18-18.

Barciszewska-Pacak M, Milanowska K, Knop, K, Bielewicz D, Nuc P, Plewka P, Pacak AM, Vazquez F, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2015) Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Front Plant Sci 6: 410. doi: 10.3389/fpls.2015.00410.

Baumberger N, Baulcombe D (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proceedings of the National Academy of Sciences of the United States of America 102: 11928-11933.

Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA, Nguyen T, Cuperus JT, Carrington JC (2012) Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. The Plant Cell 24: 3613-3629.

Dai X, Zhao PX (2011). psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39: W155-159. doi: 10.1093/nar/gkr319.

Devaux P, Adamski P, Surma M (1992). Inheritance of seed set in crosses of spring barley and Hordeum bulbosum L. Crop science 32: 269-271.

Endo Y, Iwakawa Ho, Tomari Y (2013) Arabidopsis ARGONAUTE7 selects miR390 through multiple checkpoints during RISC assembly. EMBO reports 14: 652-658.

Fahlgren N, Howell M.D, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2: e219. doi: 10.1371/journal.pone.0000219.

Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16: 939-944. doi: 10.1016/j.cub.2006.03.065.

Fan T, Li X, Yang W, Xia K, Ouyang J, Zhang M (2015) Rice osa-miR171c Mediates Phase Change from Vegetative to Reproductive Development and Shoot Apical Meristem Maintenance by Repressing Four OsHAM Transcription Factors. PLoS One 10: e0125833. doi: 10.1371/journal.pone.0125833.

Garcia-Ruiz H, Carbonell A, Hoyer JS, Fahlgren N, Gilbert KB, Takeda A, Giampetruzzi A, Garcia Ruiz MT, McGinn MG, Lowery N, Martinez Baladejo MT, Carrington JC (2015) Roles and programming of Arabidopsis ARGONAUTE proteins during Turnip mosaic virus infection. PLoS Pathog 11: e1004755. doi: 10.1371/journal.ppat.1004755.

German MA, Luo S, Schroth G, Meyers BC, Green PJ (2009) Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nature protocols 4: 356-362.

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 biology 13: 214.

Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39: 282-291. doi: 10.1016/j.molcel.2010.05.014.

Kruszka K, Pacak A, Swida-Barteczka A, Stefaniak .K, Kaja E, Sierocka I, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2013) Developmentally regulated expression and complex processing of barley pri-microRNAs. BMC Genomics 14: 34. doi: 10.1186/1471-2164-14-34.

Lin SI, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil JL, Breitler JC, Perin C, Ko SS, Guiderdoni E, Chiou TJ, Echeverria M (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.

Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei Z, Clarke TH, Reed JW, van der Knaap E (2014) Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J Exp Bot 65: 2507-2520. doi: 10.1093/jxb/eru141.

Lukasik A, Pietrykowska H, Paczek L, Szweykowska-Kulinska Z, Zielenkiewicz P (2013) High-throughput sequencing identification of novel and conserved miRNAs in the Brassica oleracea leaves. BMC Genomics 14: 801. doi: 10.1186/1471-2164-14-801.

Mallory A, Vaucheret H (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22: 3879-3889. doi: 10.1105/tpc.110.080671.

Marin E, Jouannet V, Herz A, Lokers, AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. The Plant Cell 22: 1104-1117.

Pandey R, Joshi G, Bhardwaj AR, Agarwal M, Katiyar-Agarwal S (2014) A comprehensive genome-wide study on tissue-specific and abiotic stress-specific miRNAs in Triticum aestivum. PLoS One 9: e95800. doi: 10.1371/journal.pone.0095800.

Schirle NT, MacRae IJ (2012) The crystal structure of human Argonaute2. Science 336: 1037-1040. doi: 10.1126/science.1221551.

Schreiber AW, Shi B-J, Huang C-Y, Langridge P, Baumann U (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC genomics 12: 1.

Si-Ammour A, Windels D, Arn-Bouldoires E, Kutter C, Ailhas J, Meins F, Jr, Vazquez F (2011) miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiol 157: 683-691. doi: 10.1104/pp.111.180083.

Sobkowiak L, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2012) Non-Canonical Processing of Arabidopsis pri-miR319a/b/c Generates Additional microRNAs to Target One RAP2.12 mRNA Isoform. Front Plant Sci 3: 46. doi: 10.3389/fpls.2012.00046.

Spanudakis E, Jackson S (2014) The role of microRNAs in the control of flowering time. J Exp Bot 65: 365-380. doi: 10.1093/jxb/ert453.

Van Damme M, Huibers RP, Elberse J, Van den Ackerveken G (2008) Arabidopsis DMR6 encodes a putative 2OG‐Fe (II) oxygenase that is defense‐associated but required for susceptibility to downy mildew. The Plant Journal 54: 785-793.

Wang L, Gu X, Xu D, Wang W, Wang H, Zeng M, Chang Z, Huang H, Cui X (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 62: 761-773. doi: 10.1093/jxb/erq307.

Xie K, Shen J, Hou X, Yao J, Li X, Xiao J, Xiong L (2012) Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol 158: 1382-1394. doi: 10.1104/pp.111.190488.

Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142: 280-293. doi: 10.1104/pp.106.084475.

Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed research 14: 415-421.

Zhang X, Niu D, Carbonell A, Wang A, Lee A, Tun V, Wang Z, Carrington JC, Chang CE, Jin H (2014) ARGONAUTE PIWI domain and microRNA duplex structure regulate small RNA sorting in Arabidopsis. Nat Commun 5: 5468. doi: 10.1038/ncomms6468.

Zielezinski A, Dolata J, Alaba S, Kruszka K, Pacak A, Swida-Barteczka A, Knop K, Stepien A, Bielewicz D, Pietrykowska H (2015) mirEX 2.0-an integrated environment for expression profiling of plant microRNAs. BMC plant biology 15: 144.