Skip to main content

Advertisement

SpringerLink
Log in

Stem and leaf rust–induced miRNAome in bread wheat near-isogenic lines and their comparative analysis

  • Genomics, Transcriptomics, Proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Wheat rusts remain a major threat to global wheat production and food security. The R-gene-mediated resistance has been employed as an efficient approach to develop rust-resistant varieties. However, evolution of new fungal races and infection strategies put forward the urgency of unravelling novel molecular players, including non-coding RNAs for plant response. This study identified microRNAs associated with Sr36 and Lr45 disease resistance genes in response to stem and leaf rust, respectively. Here, small RNA sequencing was performed on susceptible and resistant wheat near-isogenic lines inoculated with stem and leaf rust pathotypes. microRNA mining in stem rust–inoculated cultivars revealed a total of distinct 26 known and 7 novel miRNAs, and leaf rust libraries culminated with 22 known and 4 novel miRNAs. The comparative analysis between two disease sets provides a better understanding of altered miRNA profiles associated with respective R-genes and infections. Temporal differential expression pattern of miRNAs pinpoints their role during the progress of infection. Differential expression pattern of miRNAs among various treatments as well as time-course expression of miRNAs revealed stem and leaf rust–responsive miRNAs and their possible role in balancing disease resistance/susceptibility. Disclosure of guide strand, passenger strand and a variant of novel-Tae-miR02 from different subgenome origins might serve as a potential link between stem and leaf rust defence mechanisms downstream to respective R-genes. The outcome from the analysis of microRNA dynamics among two rust diseases and further characterization of identified microRNAs can contribute to significant novel insights on wheat-rust interactions and rust management.

Key points

• Identification and comparative analysis of stem and leaf rust–responsive miRNAs.

• Chromosomal location and functional prediction of miRNAs.

• Time-course expression analysis of pathogen-responsive miRNAs.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets generated during and/or analysed during the current study are available in the DDBJ repository, under the BioProject Accession number: PRJDB11752 (www.ddbj.nig.ac.jp).

References

  • Abuqamar S, Ajeb S, Sham A, Enan MR, Iratni R (2013) A mutation in the expansin-like A2 gene enhances resistance to necrotrophic fungi and hypersensitivity to abiotic stress in Arabidopsis thaliana. Mol Plant Pathol 14:813–827. https://doi.org/10.1111/mpp.12049

    Article  CAS  Google Scholar 

  • Ahmed F, Senthil-Kumar M, Lee S, Dai X, Mysore KS, Zhao PX (2014) Comprehensive analysis of small RNA-seq data reveals that combination of miRNA with its isomiRs increase the accuracy of target prediction in Arabidopsis thaliana. RNA Biol 11:1414–1429. https://doi.org/10.1080/15476286.2014.996474

    Article  Google Scholar 

  • Alaux M, Rogers J, Letellier T, Flores R, Alfama F, Pommier C, Mohellibi N, Durand S, Kimmel E, Michotey C, Guerche C, Loaec M, Lainé M, Steinbach D, Choulet F, Rimbert H, Leroy P, Guilhot N, Salse J, Feuillet C, Paux E, Eversole K, Adam-Blondon A-F, Quesneville H, Consortium IWGS (2018) Linking the international wheat genome sequencing consortium bread wheat reference genome sequence to wheat genetic and phenomic data. Genome Biol 19:111. https://doi.org/10.1186/s13059-018-1491-4

    Article  CAS  Google Scholar 

  • Axtell MJ, Meyers BC (2018) Revisiting criteria for plant microRNA annotation in the era of big data. Plant Cell 30:272–284

    Article  CAS  Google Scholar 

  • Baranova OA, Lapochkina IF, Anisimova AV, Gajnullin NR, Iordanskaya IV, Makarova IY (2016) Identification of Sr genes in new common wheat sources of resistance to stem rust race Ug99 using molecular markers. Russ J Genet Appl Res 6:344–350

    Article  CAS  Google Scholar 

  • Bhardwaj SC, Singh GP, Gangwar OP, Prasad P, Kumar S (2019) Status of wheat rust research and progress in rust management-Indian context. Agronomy 9:892

    Article  CAS  Google Scholar 

  • Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15:523–531

    Article  CAS  Google Scholar 

  • Burkhardt A, Day B (2016) Transcriptome and small RNAome dynamics during a resistant and susceptible interaction between cucumber and downy mildew. Plant Genome 9:plantgenome2015.08.0069. https://doi.org/10.3835/plantgenome2015.08.0069

  • Campo S, Peris-Peris C, Siré C, Moreno AB, Donaire L, Zytnicki M, Notredame C, Llave C, San Segundo B (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol 199:212–227. https://doi.org/10.1111/nph.12292

    Article  CAS  Google Scholar 

  • Chen Z (2001) A superfamily of proteins with novel cysteine-rich repeats. Plant Physiol 126:473–476. https://doi.org/10.1104/pp.126.2.473

    Article  CAS  Google Scholar 

  • Chen L, Zhang Y-H, Zheng M, Huang T, Cai Y-D (2016) Identification of compound-protein interactions through the analysis of gene ontology, KEGG enrichment for proteins and molecular fragments of compounds. Mol Genet Genomics 291:2065–2079

    Article  CAS  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  Google Scholar 

  • Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832

  • Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172. https://doi.org/10.1016/j.pbi.2015.05.014

    Article  CAS  Google Scholar 

  • Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res 46:W49–W54

    Article  CAS  Google Scholar 

  • Djami-Tchatchou AT, Sanan-Mishra N, Ntushelo K, Dubery IA (2017) Functional roles of microRNAs in agronomically important plants-potential as targets for crop improvement and protection. Front Plant Sci 8:378. https://doi.org/10.3389/fpls.2017.00378

    Article  Google Scholar 

  • Dutta S, Jha SK, Prabhu KV, Kumar M, Mukhopadhyay K (2019a) Leaf rust (Puccinia triticina) mediated RNAi in wheat (Triticum aestivum L.) prompting host susceptibility. Funct Integr Genomics 19:437–452. https://doi.org/10.1007/s10142-019-00655-6

    Article  CAS  Google Scholar 

  • Dutta S, Kumar M, Mukhopadhyay K (2019b) Identification and validation of leaf rust responsive wheat isomiRs and their target genes in both wheat and Puccinia triticina. Trop Plant Biol 12:318–335. https://doi.org/10.1007/s12042-019-09235-1

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  Google Scholar 

  • Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014) The past, present and future of breeding rust resistant wheat. Front Plant Sci 5:641

    Article  Google Scholar 

  • Fang X, Qi Y (2016) RNAi in plants: an argonaute-centered view. Plant Cell 28:272–285. https://doi.org/10.1105/tpc.15.00920

    Article  CAS  Google Scholar 

  • Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40:37–52

    Article  Google Scholar 

  • Fujimoto S, Matsunaga S, Yonemura M, Uchiyama S, Azuma T, Fukui K (2004) Identification of a novel plant MAR DNA binding protein localized on chromosomal surfaces. Plant Mol Biol 56:225–239. https://doi.org/10.1007/s11103-004-3249-5

    Article  CAS  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525. https://doi.org/10.1007/s10265-011-0412-3

    Article  CAS  Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445. https://doi.org/10.1104/pp.106.078717

    Article  CAS  Google Scholar 

  • Gao F, Wang K, Liu Y, Chen Y, Chen P, Shi Z, Luo J, Jiang D, Fan F, Zhu Y, Li S (2015) Blocking miR396 increases rice yield by shaping inflorescence architecture. Nat Plants 2:15196

    Article  CAS  Google Scholar 

  • Garland SH, Lewin L, Abedinia M, Henry R, Blakeney A (1999) The use of microsatellite polymorphisms for the identification of Australian breeding lines of rice (Oryza sativa L.). Euphytica 108:53–63

  • Garretón V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516–1526. https://doi.org/10.1104/pp.009886

    Article  CAS  Google Scholar 

  • Gidhi A, Kumar M, Mukhopadhyay K (2021) The auxin response factor gene family in wheat (Triticum aestivum L.): Genome-wide identification, characterization and expression analyses in response to leaf rust. South African J Bot 140:312–325. https://doi.org/10.1016/j.sajb.2020.06.017

    Article  CAS  Google Scholar 

  • Goedhart J, Luijsterburg MS (2020) VolcaNoseR is a web app for creating, exploring, labeling and sharing volcano plots. Sci Rep 10:20560. https://doi.org/10.1038/s41598-020-76603-3

    Article  CAS  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140–D144. https://doi.org/10.1093/nar/gkj112

    Article  CAS  Google Scholar 

  • Gu J, Sun J, Liu N, Sun X, Liu C, Wu L, Liu G, Zeng F, Hou C, Han S, Zhen W, Wang D (2020) A novel cysteine-rich receptor-like kinase gene, TaCRK2, contributes to leaf rust resistance in wheat. Mol Plant Pathol 21:732–746. https://doi.org/10.1111/mpp.12929

    Article  Google Scholar 

  • Gupta OP, Permar V, Koundal V, Singh UD, Praveen S (2012) MicroRNA regulated defense responses in Triticum aestivum L. during Puccinia graminis f. sp. tritici infection. Mol Biol Rep 39:817–824

    Article  CAS  Google Scholar 

  • Gupta PK (2015) MicroRNAs and target mimics for crop improvement. Curr Sci 1624–1633

  • Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773

    CAS  Google Scholar 

  • Hayden MJ, Sharp PJ (2001) Sequence-tagged microsatellite profiling (STMP): a rapid technique for developing SSR markers. Nucleic Acids Res 29:e43–e43. https://doi.org/10.1093/nar/29.8.e43

    Article  CAS  Google Scholar 

  • Hazen SP, Naef F, Quisel T, Gendron JM, Chen H, Ecker JR, Borevitz JO, Kay SA (2009) Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol 10:R17. https://doi.org/10.1186/gb-2009-10-2-r17

    Article  CAS  Google Scholar 

  • Hiebert C, Spielmeyer W, McCartney C, Kassa M, Fetch T, You F, Menzies J, Humphreys G, McCallum B (2015) Stem rust resistance: two approaches. Advances in wheat genetics: from genome to field. Springer, Tokyo, pp 183–191

    Chapter  Google Scholar 

  • Hsieh L-C, Lin S-I, Shih AC-C, Chen J-W, Lin W-Y, Tseng C-Y, Li W-H, Chiou T-J (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132. https://doi.org/10.1104/pp.109.147280

    Article  Google Scholar 

  • Hu G, Rijkenberg FHJ (1998) Scanning electron microscopy of early infection structure formation by Puccinia recondita f. sp. tritici on and in susceptible and resistant wheat lines. Mycol Res 102:391–399. https://doi.org/10.1017/S0953756297005054

    Article  Google Scholar 

  • Jain N, Sinha N, Krishna H, Singh PK, Gautam T, Prasad P, Balyan HS, Gupta PK (2020) A study of miRNAs and lncRNAs during Lr28-mediated resistance against leaf rust in wheat (Triticum aestivum L.). Physiol Mol Plant Pathol 112:101552. https://doi.org/10.1016/j.pmpp.2020.101552

    Article  CAS  Google Scholar 

  • Karlova R, van Haarst JC, Maliepaard C, van de Geest H, Bovy AG, Lammers M, Angenent GC, de Maagd RA (2013) Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J Exp Bot 64:1863–1878. https://doi.org/10.1093/jxb/ert049

    Article  CAS  Google Scholar 

  • Kaur A, Pati PK, Pati AM, Nagpal AK (2017) In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS ONE 12:e0184523

    Article  Google Scholar 

  • Kolmer JA, Chen X, Jin Y (2009) Diseases which challenge global wheat production-the cereal rusts. Carver BF(ed) Wheat: Science and trade. Wiley Press Hoboken, NJ, USA, pp 89–124

    Chapter  Google Scholar 

  • Kumar D, Dutta S, Singh D, Prabhu KV, Kumar M, Mukhopadhyay K (2017a) Uncovering leaf rust responsive miRNAs in wheat (Triticum aestivum L.) using high-throughput sequencing and prediction of their targets through degradome analysis. Planta 245:161–182

    Article  CAS  Google Scholar 

  • Kumar G, Singh A, Vinutha T, Kumar S, Kumar RR, Praveen S (2017b) Possible role of miRNAs and their targets, in modulating leaf morphology and plant growth during leaf curl virus infection in tomato. Indian J Plant Physiol 22:608–615. https://doi.org/10.1007/s40502-017-0345-5

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  Google Scholar 

  • Langmead B (2010) Aligning short sequencing reads with Bowtie. Curr Protoc Bioinforma 32:11–17

    Article  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  Google Scholar 

  • Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou J-M (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 152:2222–2231. https://doi.org/10.1104/pp.109.151803

    Article  CAS  Google Scholar 

  • Li W, Wang F, Wang J, Fan F, Zhu J, Yang J, Liu F, Zhong W (2015) Overexpressing CYP71Z2 enhances resistance to bacterial blight by suppressing auxin biosynthesis in rice. PLoS ONE 10:e0119867–e0119867. https://doi.org/10.1371/journal.pone.0119867

    Article  CAS  Google Scholar 

  • Li Y-F, Wei K, Wang M, Wang L, Cui J, Zhang D, Guo J, Zhao M, Zheng Y (2019) Identification and temporal expression analysis of conserved and novel microRNAs in the leaves of winter wheat grown in the field. Front Genet 10:779. https://doi.org/10.3389/fgene.2019.00779

    Article  CAS  Google Scholar 

  • Liu B, Sun G (2017) microRNAs contribute to enhanced salt adaptation of the autopolyploid Hordeum bulbosum compared with its diploid ancestor. Plant J 91:57–69. https://doi.org/10.1111/tpj.13546

    Article  CAS  Google Scholar 

  • Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305. https://doi.org/10.1104/pp.105.063420

    Article  CAS  Google Scholar 

  • Liu P-P, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146. https://doi.org/10.1111/j.1365-313X.2007.03218.x

    Article  CAS  Google Scholar 

  • Liu P-P, Bhattacharjee S, Klessig DF, Moffett P (2010) Systemic acquired resistance is induced by R gene-mediated responses independent of cell death. Mol Plant Pathol 11:155–160

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:1–21

    Article  Google Scholar 

  • Lu H, Zou Y, Feng N (2010) Overexpression of AHL20 negatively regulates defenses in Arabidopsis. J Integr Plant Biol 52:801–808. https://doi.org/10.1111/j.1744-7909.2010.00969.x

    Article  CAS  Google Scholar 

  • Marsalis MA, Goldberg NP (2011) Leaf, stem and stripe rust diseases of wheat. Guide A-415

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J 17:10–12

    Article  Google Scholar 

  • McCouch SR, Chen X, Panaud O, Temnykh S, Xu Y, Cho YG, Huang N, Ishii T, Blair M (1997) Microsatellite marker development, mapping and applications in rice genetics and breeding- Oryza: From Molecule to Plant. In: Sasaki T, Moore G (eds). Springer Netherlands, Dordrecht, pp 89–99

  • Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12:1612–1619. https://doi.org/10.1261/rna.130506

    Article  CAS  Google Scholar 

  • Naik BK, Sharma JB, Sivasamy M, Prabhu KV, Tomar RS, Tomar SMS (2015) Molecular mapping and validation of the microsatellite markers linked to the Secale cereale-derived leaf rust resistance gene Lr45 in wheat. Mol Breed 35:1–10

    Article  CAS  Google Scholar 

  • Nair MM, Manickavelu A (2020) MicroRNAs as fine-tuners of gene regulation in plant-microbe interactions. Curr Sci 119:1282–1290

    Article  CAS  Google Scholar 

  • Narang D, Kaur S, Steuernagel B, Ghosh S, Bansal U, Li J, Zhang P, Bhardwaj S, Uauy C, Wulff BBH, Chhuneja P (2020) Discovery and characterisation of a new leaf rust resistance gene introgressed in wheat from wild wheat Aegilops peregrina. Sci Rep 10:1–9

    Article  Google Scholar 

  • Natarajan B, Kalsi HS, Godbole P, Malankar N, Thiagarayaselvam A, Siddappa S, Thulasiram HV, Chakrabarti SK, Banerjee AK (2018) MiRNA160 is associated with local defense and systemic acquired resistance against Phytophthora infestans infection in potato. J Exp Bot 69:2023–2036. https://doi.org/10.1093/jxb/ery025

    Article  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science (80-) 312:436–439. https://doi.org/10.1126/science.1126088

    Article  CAS  Google Scholar 

  • Pérez-Quintero ÁL, Quintero A, Urrego O, Vanegas P, López C (2012) Bioinformatic identification of cassava miRNAs differentially expressed in response to infection by Xanthomonas axonopodis pv. manihotis. BMC Plant Biol 12:1–11

    Article  Google Scholar 

  • Periyannan S, Milne RJ, Figueroa M, Lagudah ES, Dodds PN (2017) An overview of genetic rust resistance: from broad to specific mechanisms. PLoS Pathog 13:e1006380

    Article  Google Scholar 

  • Petrov V, Vermeirssen V, De Clercq I, Van Breusegem F, Minkov I, Vandepoele K, Gechev TS (2012) Identification of cis-regulatory elements specific for different types of reactive oxygen species in Arabidopsis thaliana. Gene 499:52–60. https://doi.org/10.1016/j.gene.2012.02.035

    Article  CAS  Google Scholar 

  • Quesada V (2016) The roles of mitochondrial transcription termination factors (MTERFs) in plants. Physiol Plant 157:389–399. https://doi.org/10.1111/ppl.12416

    Article  CAS  Google Scholar 

  • Roberti M, Polosa PL, Bruni F, Manzari C, Deceglie S, Gadaleta MN, Cantatore P (2009) The MTERF family proteins: Mitochondrial transcription regulators and beyond. Biochim Biophys Acta - Bioenerg 1787:303–311. https://doi.org/10.1016/j.bbabio.2009.01.013

    Article  CAS  Google Scholar 

  • Sablok G, Srivastva AK, Suprasanna P, Baev V, Ralph PJ (2015) isomiRs: increasing evidences of isomiRs complexity in plant stress functional biology. Front Plant Sci 6:949. https://doi.org/10.3389/fpls.2015.00949

  • Sánchez-Retuerta C, Suaréz-López P, Henriques R (2018) Under a new light: regulation of light-dependent pathways by non-coding RNAs. Front Plant Sci 9:962. https://doi.org/10.3389/fpls.2018.00962

  • Shahmuradov IA, Umarov RK, Solovyev VV (2017) TSSPlant: a new tool for prediction of plant Pol II promoters. Nucleic Acids Res 45:e65–e65

    CAS  Google Scholar 

  • Singh D, Bhaganagare G, Bandopadhyay R, Prabhu KV, Gupta PK, Mukhopadhyay K (2012) Targeted spatio-temporal expression based characterization of state of infection and time-point of maximum defense in wheat NILs during leaf rust infection. Mol Biol Rep 39:9373–9382

    Article  CAS  Google Scholar 

  • Soto-Suárez M, Baldrich P, Weigel D, Rubio-Somoza I, San Segundo B (2017) The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens. Sci Rep 7:44898

    Article  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP et al (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452

    Article  CAS  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    Article  CAS  Google Scholar 

  • Tyagi S, Kumar A, Gautam T, Pandey R, Rustgi S, Mir RR (2021) Development and use of miRNA-derived SSR markers for the study of genetic diversity, population structure, and characterization of genotypes for breeding heat tolerant wheat varieties. PLoS ONE 16:1–17. https://doi.org/10.1371/journal.pone.0231063

    Article  CAS  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40:e115–e115. https://doi.org/10.1093/nar/gks596

    Article  CAS  Google Scholar 

  • Varkonyi-Gasic E (2017) Stem-Loop qRT-PCR for the Detection of Plant microRNAs. Methods Mol Biol 1456:163–175

  • Wang J-W, Wang L-J, Mao Y-B, Cai W-J, Xue H-W, Chen X-Y (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216. https://doi.org/10.1105/tpc.105.033076

    Article  CAS  Google Scholar 

  • Wang X, McCallum BD, Fetch T, Bakkeren G, Saville BJ (2015) Sr36- and Sr5-mediated resistance response to Puccinia graminis f. sp. tritici is associated with callose deposition in wheat guard cells. Phytopathology® 105:728–737. https://doi.org/10.1094/PHYTO-08-14-0213-R

    Article  CAS  Google Scholar 

  • Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpiński S, Karpińska B, Kangasjärvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:95. https://doi.org/10.1186/1471-2229-10-95

    Article  CAS  Google Scholar 

  • Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA Genes. Plant Physiol 138:2145–2154. https://doi.org/10.1104/pp.105.062943

    Article  CAS  Google Scholar 

  • Yang K, Sablok G, Qiao G, Nie Q, Wen X (2017) isomiR2Function: an integrated workflow for identifying microRNA variants in plants. Front Plant Sci 8:322

    Google Scholar 

  • Yeh Y-H, Chang Y-H, Huang P-Y, Huang J-B, Zimmerli L (2015) Enhanced Arabidopsis pattern-triggered immunity by overexpression of cysteine-rich receptor-like kinases. Front Plant Sci 6:322. https://doi.org/10.3389/fpls.2015.00322

    Article  Google Scholar 

  • Zhang X, Zhao H, Gao S, Wang W-C, Katiyar-Agarwal S, Huang H-D, Raikhel N, Jin H (2011) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393∗-mediated silencing of a golgi-localized SNARE gene, MEMB12. Mol Cell 42:356–366. https://doi.org/10.1016/j.molcel.2011.04.010

    Article  CAS  Google Scholar 

  • Zhang K, Shi X, Zhao X, Ding D, Tang J, Niu J (2015) Investigation of miR396 and growth-regulating factor regulatory network in maize grain filling. Acta Physiol Plant 37:28. https://doi.org/10.1007/s11738-014-1767-6

    Article  CAS  Google Scholar 

  • Zhang Y, Xia R, Kuang H, Meyers BC (2016) The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Mol Biol Evol 33:2692–2705. https://doi.org/10.1093/molbev/msw154

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge Dr. Rebekah Nisha, Dr. Shajitha P and other staffs of the ICAR-Indian Agricultural Research Institute, Wellington, for their help in pathogen inoculation and plant material collection. The authors would like to thank the Central University of Kerala for research facilities. The authors also thank the Department of Science and Technology-Innovation in Science Pursuit for Inspired Research (DST-INSPIRE) and Council of Scientific and Industrial Research-University Grants Commission (CSIR-UGC) for providing financial support.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. MMN and SJ are supported by DST-INSPIRE fellowship and CSIR-UGC fellowship respectively.

Author information

Authors and Affiliations

  1. Department of Genomic Science, Central University of Kerala, Kasaragod, 671316, Kerala, India

    Minu M. Nair, S. Hari Krishna Kumar, S. Jyothsna & Manickavelu Alagu

  2. International Rice Research Institute (IRRI), South Asia Hub, Patancheru, 502324, Telangana, India

    Krishna T. Sundaram

  3. ICAR-National Bureau of Agricultural Insect Resources, Bengaluru, 560024, Karnataka, India

    C. Manjunatha

  4. ICAR-Indian Agricultural, Research Institute, Regional Station, Wellington, 643231, Tamil Nadu, India

    M. Sivasamy

Authors
  1. Minu M. Nair
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Hari Krishna Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Jyothsna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Krishna T. Sundaram
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Manjunatha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Sivasamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manickavelu Alagu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MMN: conceptualization, methodology, investigation, software, validation, data curation, formal analysis, visualization, writing—original draft preparation. HKS: software, data curation, formal analysis, visualization. SJ: data curation, validation, visualization, writing—reviewing and editing. KTS: software. CM: resources, methodology, writing—reviewing and editing. MS: resources, writing—reviewing and editing. MA: conceptualization, funding, supervision, writing—reviewing and editing.

Corresponding author

Correspondence to Manickavelu Alagu.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1681 kb)

Supplementary file2 (XLSX 40 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nair, M.M., Kumar, S.H.K., Jyothsna, S. et al. Stem and leaf rust–induced miRNAome in bread wheat near-isogenic lines and their comparative analysis. Appl Microbiol Biotechnol 106, 8211–8232 (2022). https://doi.org/10.1007/s00253-022-12268-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-022-12268-4

Keywords

Search

Navigation