Abstract
Cross-kingdom RNAi is a well-documented phenomenon where sRNAs generated by host and pathogens may govern resistance or susceptible phenotypes during host-pathogen interaction. With the first example of the direct involvement of fungal generated sRNAs in virulence of plant pathogenic fungi Botrytis cinerea and recently from Puccinia striiformis f. sp. tritici, we attempted to identify sRNAs in Puccinia triticina (P. triticina). Four sRNA libraries were prepared and sequenced using Illumina sequencing technology and a total of ~ 1–1.28 million potential sRNAs and two microRNA-like small RNA (mil-RNAs) candidates were identified. Computational prediction of targets using a common set of sRNAs and P. triticina mil-RNAs (pt-mil-RNAs) within P. triticina and wheat revealed the majority of the targets as repetitive elements in P. triticina whereas in wheat, the target genes were identified to be involved in many biological processes including defense-related pathways. We found 9 receptor-like kinases (RLKs) and 14 target genes of each related to reactive oxygen species (ROS) pathway and transcription factors respectively, including significant numbers of target genes from various other categories. Expression analysis of twenty selected sRNAs, targeting host genes pertaining to ROS related, disease resistance, metabolic processes, transporter, apoptotic inhibitor, and transcription factors along with two pt-mil-RNAs by qRT-PCR showed distinct patterns of expression of the sRNAs in urediniospore-specific libraries. In this study, for the first time, we report identification of novel sRNAs identified in P. triticina including two pt-mil-RNAs that may play an important role in biotrophic growth and pathogenicity.
Similar content being viewed by others
Data availability
Small RNA data generated in this study is deposited in NCBI-SRA database under BioProject ID- PRJNA416416, BioSample accessions SAMN07962156, SAMN07962160, SAMN07962164, and SAMN07962167.
References
Acharya BR, Raina S, Maqbool SB, Jagadeeswaran G, Mosher SL, Appel HM, Schultz JC, Klessig DF, Raina R (2007) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J 50:488–499. https://doi.org/10.1111/j.1365-313X.2007.03064.x
Akpinar BA, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genomics 15:587–598
Alam MM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, Yamaoka N, Shimomoto K, Takayama K, Nishina H, Nishiguchi M (2015) Overexpression of a rice heme activator protein gene (OsHAP2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnol J 13:85–96. https://doi.org/10.1111/pbi.12239
Alptekin B, Budak H (2017) Wheat miRNA ancestors: evident by transcriptome analysis of A, B, and D genome donors. Funct Integr Genomics 17:171–187
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available at http://www.bioinformatics.babraham.ac.uk/projects/download.html
Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, Pozniak CJ, Choulet F, Distelfeld A, Poland J (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403). https://doi.org/10.1126/science.aar7191
Aravin AA, Naumova NM, Tulin AV, Vagin VV, Rozovsky YM, Gvozdev VA (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 11:1017–1027
Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159. https://doi.org/10.1146/annurev-arplant-050312-120,043
Bai Y, Lan F, Yang W, Zhang F, Yang K, Li Z, Gao P, Wang S (2015) sRNA profiling in Aspergillus flavus reveals differentially expressed miRNA-like RNAs response to water activity and temperature. Fungal Genet Biol 81:113–119. https://doi.org/10.1016/j.fgb.2015.03.004
Baldrich P, Campo S, Wu MT, Liu TT, Hsing YI, San Segundo B (2015) MicroRNA-mediated regulation of gene expression in the response of rice plants to fungal elicitors. RNA Biol 12:847–863. https://doi.org/10.1080/15476286.2015.1050577
Bao W, Kojima KK, Kohany O (2015) Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA 6:11. https://doi.org/10.1186/s13100-015-0041-9
Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326
Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12:846–860
Bolton MD, Kolmer JA, Garvin DF (2008) Wheat leaf rust caused by Puccinia triticina. Mol Plant Pathol 9:563–575. https://doi.org/10.1111/j.1364-3703.2008.00487.x
Bonnet E, Wuyts J, Rouze P, Van de Peer Y (2004) Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics 20:2911–2917. https://doi.org/10.1093/bioinformatics/bth374
Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, Le Bihan T, Kumar S, Abreu-Goodger C, Lear M, Harcus Y, Ceroni A, Babayan SA, Blaxter M, Ivens A, Maizels RM (2014) Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun 5:5488. https://doi.org/10.1038/ncomms6488
Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15:523–531
Cagirici HB, Biyiklioglu S, Budak H (2017) Assembly and annotation of transcriptome provided evidence of miRNA mobility between wheat and wheat stem sawfly. Front Plant Sci 8:1653
Cantu D, Vanzetti LS, Sumner A, Dubcovsky M, Matvienko M, Distelfeld A, Michelmore RW, Dubcovsky J (2010) Small RNAs, DNA methylation and transposable elements in wheat. BMC Genomics 11:408. https://doi.org/10.1186/1471-2164-11-408
Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X, Kojima KK, Jurka J, Michelmore RW, Dubcovsky J (2011) Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One 6:e24230. https://doi.org/10.1371/journal.pone.0024230
Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29. https://doi.org/10.1104/pp.108.117887
Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896. https://doi.org/10.1038/nrg2179
Chen R, Jiang N, Jiang Q, Sun X, Wang Y, Zhang H, Hu Z (2014) Exploring microRNA-like small RNAs in the filamentous fungus Fusarium oxysporum. PLoS One 9:e104956. https://doi.org/10.1371/journal.pone.0104956
Chen Y, Gao Q, Huang M, Liu Y, Liu Z, Liu X, Ma Z (2015) Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci Rep 5:12500. https://doi.org/10.1038/srep12500
Choi J, Kim KT, Jeon J, Wu J, Song H, Asiegbu FO, Lee YH (2014) funRNA: a fungi-centered genomics platform for genes encoding key components of RNAi. BMC Genomics 15:S14. https://doi.org/10.1186/1471-2164-15-S9-S14
Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Cuomo CA, Bakkeren G, Khalil HB, Panwar V, Joly D, Linning R, Sakthikumar S, Song X, Adiconis X, Fan L, Goldberg JM, Levin JZ, Young S, Zeng Q, Anikster Y, Bruce M, Wang M, Yin C, McCallum B, Szabo LJ, Hulbert S, Chen X, Fellers JP (2017) Comparative analysis highlights variable genome content of wheat rusts and divergence of the mating loci. G3 (Bethesda) 7:361–376. https://doi.org/10.1534/g3.116.032797
Dahlmann TA, Kuck U (2015) Dicer-dependent biogenesis of small RNAs and evidence for microRNA-like RNAs in the penicillin producing fungus Penicillium chrysogenum. PLoS One 10:e0125989. https://doi.org/10.1371/journal.pone.0125989
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159. https://doi.org/10.1093/nar/gkr319
Dean JD, Goodwin PH, Hsiang T (2005) Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56:1525–1533. https://doi.org/10.1093/jxb/eri145
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350. https://doi.org/10.1016/j.phytochem.2009.12.012
Dobon A, Bunting DC, Cabrera-Quio LE, Uauy C, Saunders DG (2016) The host-pathogen interaction between wheat and yellow rust induces temporally coordinated waves of gene expression. BMC Genomics 17:380. https://doi.org/10.1186/s12864-016-2684-4
Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kues U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M, Quesneville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan GA, Henrissat B, Van de Peer Y, Rouze P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A 108:9166–9171. https://doi.org/10.1073/pnas.1019315108
Franceschetti M, Maqbool A, Jiménez-Dalmaroni MJ, Pennington HG, Kamoun S, Banfield MJ (2017) Effectors of filamentous plant pathogens: commonalities amid diversity. Microbiol Mol Biol Rev 81(2):e00066–e00016
Fulci V, Macino G (2007) Quelling: post-transcriptional gene silencing guided by small RNAs in Neurospora crassa. Curr Opin Microbiol 10:199–203. https://doi.org/10.1016/j.mib.2007.03.016
Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108. https://doi.org/10.1038/nrg2504
Gou M, Shi Z, Zhu Y, Bao Z, Wang G, Hua J (2012) The F-box protein CPR1/CPR30 negatively regulates R protein SNC1 accumulation. Plant J 69:411–420
He XF, Fang YY, Feng L, Guo HS (2008) Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Lett 582:2445–2452. https://doi.org/10.1016/j.febslet.2008.06.011
Hoff KJ, Stanke M (2013) WebAUGUSTUS--a web service for training AUGUSTUS and predicting genes in eukaryotes. Nucleic Acids Res 41:W123–W128. https://doi.org/10.1093/nar/gkt418
Huerta-Espino J, Singh RP, Germán S, McCallum BD, Park RF, Chen WQ, Bhardwaj SC, Goyeau H (2011) Global status of wheat leaf rust caused by Puccinia triticina. Euphytica 179:143–160. https://doi.org/10.1007/s10681-011-0361-x
Jahan SN, Åsman AK, Corcoran P, Fogelqvist J, Vetukuri RR, Dixelius C (2015) Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. J Exp Bot 66:2785–2794
Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim H, Yu Y, Dean RA, Wing RA, Soderlund C, Wang GL (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiol 138:105–115. https://doi.org/10.1104/pp.104.055624
Jiang N, Yang Y, Janbon G, Pan J, Zhu X (2012) Identification and functional demonstration of miRNAs in the fungus Cryptococcus neoformans. PLoS One 7:e52734. https://doi.org/10.1371/journal.pone.0052734
Jones-Rhoades MW (2012) Conservation and divergence in plant microRNAs. Plant Mol Biol 80:3–16
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. https://doi.org/10.1146/annurev.arplant.57.032905.105218
Kang K, Zhong J, Jiang L, Liu G, Gou CY, Wu Q, Wang Y, Luo J, Gou D (2013) Identification of microRNA-Like RNAs in the filamentous fungus Trichoderma reesei by solexa sequencing. PLoS One 8:e76288. https://doi.org/10.1371/journal.pone.0076288
Kantar M, Akpınar BA, Valárik M, Lucas SJ, Doležel J, Hernández P, Budak H, Consortium IWGS (2012) Subgenomic analysis of microRNAs in polyploid wheat. Funct Integr Genomics 12:465–479
Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246. https://doi.org/10.1146/annurev-phyto-073009-114,457
Khatkar BS, Chaudhary N, Dangi P (2016) Production and consumption of grains in India. In: Reference Module in Food Science. Elsevier
Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148. https://doi.org/10.1016/j.bbagrm.2011.05.001
Kiran K, Rawal HC, Dubey H, Jaswal R, Devanna BN, Gupta DK, Bhardwaj SC, Prasad P, Pal D, Chhuneja P, Balasubramanian P, Kumar J, Swami M, Solanke AU, Gaikwad K, Singh NK, Sharma TR (2016) Draft genome of the wheat rust pathogen (Puccinia triticina) unravels genome-wide structural variations during evolution. Genome Biol Evol 8:2702–2721. https://doi.org/10.1093/gbe/evw197
Kiran K, Rawal HC, Dubey H, Jaswal R, Bhardwaj SC, Prasad P, Pal D, Devanna BN, Sharma TR (2017) Dissection of genomic features and variations of three pathotypes of Puccinia striiformis through whole genome sequencing. Sci Rep 7:42419. https://doi.org/10.1038/srep42419
Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450. https://doi.org/10.1016/j.devcel.2006.09.009
Kohorn BD, Kohorn SL (2012) The cell wall-associated kinases, WAKs, as pectin receptors. Front Plant Sci 3:88. https://doi.org/10.3389/fpls.2012.00088
Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73. https://doi.org/10.1093/nar/gkt1181
Kurtoglu KY, Kantar M, Lucas SJ, Budak H (2013) Unique and conserved microRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 8:e69801
Kurtoglu KY, Kantar M, Budak H (2014) New wheat microRNA using whole-genome sequence. Funct Integr Genomics 14:363–379
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Lau SK, Chow WN, Wong AY, Yeung JM, Bao J, Zhang N, Lok S, Woo PC, Yuen KY (2013) Identification of microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus Penicillium marneffei. PLoS Negl Trop Dis 7:e2398. https://doi.org/10.1371/journal.pntd.0002398
Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK, Pertsemlidis A, Lewis ZA, Freitag M, Selker EU, Mello CC, Liu Y (2010) Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol Cell 38:803–814. https://doi.org/10.1016/j.molcel.2010.04.005
Li J, Todd TC, Oakley TR, Lee J, Trick HN (2010) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232:775–785
Li S, Castillo-Gonzalez C, Yu B, Zhang X (2017) The functions of plant small RNAs in development and in stress responses. Plant J 90:654–670. https://doi.org/10.1111/tpj.13444
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656
Lin R, Zhao W, Meng X, Peng Y-L (2007) Molecular cloning and characterization of a rice gene encoding AP2/EREBP-type transcription factor and its expression in response to infection with blast fungus and abiotic stresses. Physiol Mol Plant Pathol 70:60–68. https://doi.org/10.1016/j.pmpp.2007.06.002
Liu C, Pedersen C, Schultz-Larsen T, Aguilar GB, Madriz-Ordenana K, Hovmoller MS, Thordal-Christensen H (2016) The stripe rust fungal effector PEC6 suppresses pattern-triggered immunity in a host species-independent manner and interacts with adenosine kinases. New Phytol. https://doi.org/10.1111/nph.14034
Lorenz R, Bernhart SH, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL (2011) ViennaRNA Package 2.0. Algorithms Mol Biol 6:26. https://doi.org/10.1186/1748-7188-6-26
Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–1442. https://doi.org/10.1126/science.1204903
Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35. https://doi.org/10.1038/nrg1500
McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212. https://doi.org/10.1186/gb-2006-7-4-212
Mueth NA, Ramachandran SR, Hulbert SH (2015) Small RNAs from the wheat stripe rust fungus (Puccinia striiformis f.sp. tritici). BMC Genomics 16:718. https://doi.org/10.1186/s12864-015-1895-4
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 312:436–439. https://doi.org/10.1126/science.1126088
Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935. https://doi.org/10.1093/bioinformatics/btt509
Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, Finn RD (2015) Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43:D130–D137. https://doi.org/10.1093/nar/gku1063
Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–3141
Nunes CC, Gowda M, Sailsbery J, Xue M, Chen F, Brown DE, Oh Y, Mitchell TK, Dean RA (2011) Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC genomics 12:288
Ordonez ME, Kolmer JA (2007) Simple sequence repeat diversity of a worldwide collection of Puccinia triticina from durum wheat. Phytopathology 97:574–583. https://doi.org/10.1094/PHYTO-97-5-0574
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655. https://doi.org/10.1104/pp.109.138990
Panwar V, McCallum B, Bakkeren G (2013) Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol Biol 81(6):595–608
Panwar V, Jordan M, McCallum B, Bakkeren G (2018) Host-induced silencing of essential genes in Puccinia triticina through transgenic expression of RNA i sequences reduces severity of leaf rust infection in wheat. Plant Biotechnol J 16(5):1013–1023
Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF 3rd, Mantovani R (2012) The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell 24:4777–4792. https://doi.org/10.1105/tpc.112.105734
Pré M, Atallah M, Champion A, De Vos M, Pieterse CM, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357
Qi T, Zhu X, Tan C, Liu P, Guo J, Kang Z, Guo J (2018) Host-induced gene silencing of an important pathogenicity factor P s CPK 1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust. Plant Biotechnol J 16(3):797–807
Quinlan AR (2014) BEDTools: the Swiss-army tool for genome feature analysis. Curr Protoc Bioinformatics 47:11.12.1–11.12.34. https://doi.org/10.1002/0471250953.bi1112s47
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol 7:33. https://doi.org/10.1186/1471-2199-7-33
Smit A, Hubley R, Green P (2017) Repeatmasker open–4.0. 2013–2015. http://repeatmasker.org
Sperschneider J, Dodds PN, Gardiner DM, Manners JM, Singh KB, Taylor JM (2015) Advances and challenges in computational prediction of effectors from plant pathogenic fungi. PLoS Pathog 11:e1004806
Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263
Stocks MB, Moxon S, Mapleson D, Woolfenden HC, Mohorianu I, Folkes L, Schwach F, Dalmay T, Moulton V (2012) The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets. Bioinformatics 28:2059–2061. https://doi.org/10.1093/bioinformatics/bts311
Supek F, Bosnjak M, Skunca N, Smuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6:e21800. https://doi.org/10.1371/journal.pone.0021800
Tsuda K, Somssich IE (2015) Transcriptional networks in plant immunity. New Phytol 206:932–947. https://doi.org/10.1111/nph.13286
Turra D, Segorbe D, Di Pietro A (2014) Protein kinases in plant-pathogenic fungi: conserved regulators of infection. Annu Rev Phytopathol 52:267–288. https://doi.org/10.1146/annurev-phyto-102313-050143
Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylides C, Roby D (2002) A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci U S A 99:10179–10184. https://doi.org/10.1073/pnas.152047199
Vetukuri RR, Åsman AK, Tellgren-Roth C, Jahan SN, Reimegård J, Fogelqvist J, Savenkov E, Söderbom F, Avrova AO, Whisson SC (2012) Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLoS One 7:e51399
Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu GZ, Li L, Benny U, Oard J, Ronald PC, Song WY (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635–3646. https://doi.org/10.1105/tpc.106.046730
Wang S, Li P, Zhang J, Qiu D, Guo L (2016) Generation of a high resolution map of sRNAs from Fusarium graminearum and analysis of responses to viral infection. Sci Rep 6:26151
Wang B, Sun Y, Song N, Zhao M, Liu R, Feng H, Wang X, Kang Z (2017) Puccinia striiformis f. sp. tritici microRNA-like RNA 1 (Pst-milR1), an important pathogenicity factor of Pst, impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene. New Phytol 215:338–350. https://doi.org/10.1111/nph.14577
Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123. https://doi.org/10.1126/science.1239705
Wellings CR (2011) Global status of stripe rust: a review of historical and current threats. Euphytica 179:129–141. https://doi.org/10.1007/s10681-011-0360-y
Wu JQ, Sakthikumar S, Dong C, Zhang P, Cuomo CA, Park RF (2017) Comparative genomics integrated with association analysis identifies candidate effector genes corresponding to Lr20 in phenotype-paired Puccinia triticina isolates from Australia. Front Plant Sci 8:148. https://doi.org/10.3389/fpls.2017.00148
Yadav IS, Sharma A, Kaur S, Nahar N, Bhardwaj SC, Sharma TR, Chhuneja P (2016) Comparative temporal transcriptome profiling of wheat near isogenic line carrying Lr57 under compatible and incompatible interactions. Front Plant Sci 7:1943. https://doi.org/10.3389/fpls.2016.01943
Yang F (2015) Genome-wide analysis of small RNAs in the wheat pathogenic fungus Zymoseptoria tritici. Fungal Biol 119:631–640. https://doi.org/10.1016/j.funbio.2015.03.008
Yang Q, Ye QA, Liu Y (2015) Mechanism of siRNA production from repetitive DNA. Genes Dev 29:526–537. https://doi.org/10.1101/gad.255828.114
Zhou J, Fu Y, Xie J, Li B, Jiang D, Li G, Cheng J (2012a) Identification of microRNA-like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol Gen Genomics 287:275–282. https://doi.org/10.1007/s00438-012-0678-8
Zhou Q, Wang Z, Zhang J, Meng H, Huang B (2012b) Genome-wide identification and profiling of microRNA-like RNAs from Metarhizium anisopliae during development. Fungal Biol 116:1156–1162. https://doi.org/10.1016/j.funbio.2012.09.001
Zhu X, Qi T, Yang Q, He F, Tan C, Ma W, Voegele RT, Kang Z, Guo J (2017) Host-induced gene silencing of the MAPKK gene PsFUZ7 confers stable resistance to wheat stripe rust. Plant Physiol 175:1853–1863. https://doi.org/10.1104/pp.17.01223
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Acknowledgments
TRS is thankful to the Department of Science and Technology, Govt. of India, for JC Bose National Fellowship. HD is thankful to the University Grants Commission (UGC), New Delhi, for providing Junior Research Fellowship (JRF).
Author information
Authors and Affiliations
Contributions
TRS conceived and designed the experiments, HD generated data, and HD and PJ performed computational analysis. HD, KK, and RJ performed biological experiments, SCB contributed in providing biological material, and AMK and TKM provided input during manuscript writing. HD, KK, and TRS wrote the manuscript.
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Dubey, H., Kiran, K., Jaswal, R. et al. Discovery and profiling of small RNAs from Puccinia triticina by deep sequencing and identification of their potential targets in wheat. Funct Integr Genomics 19, 391–407 (2019). https://doi.org/10.1007/s10142-018-00652-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-018-00652-1