SHORT COMMUNICATION
Temporal expression of three conserved putative microRNAs
in response of Citrus × Limon to Xanthomonas citri subsp. citri
and Xanthomonas fuscans subsp. Aurantifolii
More details
Hide details
1
Shahid Beheshti University, Tehran, Iran
2
Oil Seeds Research Department, Seed and Plant Improvement Institute, Karaj, Iran
Submission date: 2016-12-26
Final revision date: 2017-07-03
Acceptance date: 2017-07-05
Publication date: 2018-01-02
BioTechnologia 2017;98(3):257-264
KEYWORDS
TOPICS
ABSTRACT
Citrus canker is a widespread bacterial disease that severely affects Citrus production. Xanthomonas spp. are the causative agents of the disease, which manifests as necrotic pustule-like lesions on the plant organs including leaves, fruits, and stems. MicroRNAs (miRNAs) are well-established post-transcriptional gene expression regulators that modulate plant responses during many stress conditions. Accordingly, some bacteria-responsive miRNAs have been shown to have regulatory functions in the plant-pathogen interactions. In this study, we successfully assessed the expression patterns of three conserved miRNAs: miR159, miR167, and miR398, in Citrus × Limon (lemon) infiltrated with Xanthomonas strains A and C using stem-loop RT-qPCR. Our results showed that the expressions of miR159 and mir167 have nearly similar patterns upon inoculations, while the expression of miR398 remains constantly up-regulated after an early induction.
REFERENCES (50)
1.
Alonso-Peral M.M., Li J., Li Y., et al. (2010) The microRNA159- regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol. 154: 757-771.
2.
Barciszewska-Pacak M., Milanowska K., Knop K., Bielewicz D., Nuc P., Plewka P., Pacak A.M., 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.
3.
Bartel D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
4.
Benes V., Castoldi M. (2010) Expression profiling of micro- RNA using real-time quantitative PCR, how to use it and what is available. Methods 50: 244-249.
5.
Bonnet E., Wuyts J., Rouzé 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: 11511-11516.
6.
Brunings A.M., Gabriel D.W. (2003) Xanthomonas citri: breaking the surface. Mol. Plant Pathol. 4: 141-157.
7.
Carrington J.C., Ambros V. (2003) Role of microRNAs in plant and animal development. Science 301: 336-338.
8.
Cernadas R.A., Camillo L.R., Benedetti C.E. (2008) Transcriptional analysis of the sweet orange interaction with the citrus canker pathogens Xanthomonas axonopodis pv. citri and Xanthomonas axonopodis pv. aurantifolii. Mol. Plant Pathol. 9: 609-631.
9.
Cernadas R.A., Benedetti C.E. (2009) Role of auxin and gibberellin in citrus canker development and in the transcriptional control of cell-wall remodeling genes modulated by Xanthomonas axonopodis pv. citri. Plant Sci. 177: 190-195.
10.
Chen C., Ridzon D.A., Broomer A.J., et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucl. Acids Res. 33: e179.
11.
Chen Z., Agnew J.L., Cohen J.D., et al. (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl Acad. Sci. USA 104: 20131-20136.
12.
Chen M., Cao Z. (2015) Genome-wide expression profiling of microRNAs in poplar upon infection with the foliar rust fungus Melampsora larici-populina. BMC Genom. 16: 1471-2164.
13.
Denancé N., Sánchez-Vallet A., Goffner D., Molina A. (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant. Sci 4: 155.
14.
Draper J. (1997) Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci. 2: 162-165.
15.
Economos C., Clay W.D. (1999) Nutritional and health benefits of citrus fruits. Food Nutr. Agric. 24: 11-18.
16.
Glazińska P., Wojciechowski W., Wilmowicz E., et al. (2014) The involvement of InMIR167 in the regulation of expression of its target gene InARF8, and their participation in the vegetative and generative development of Ipomoea nil plants. J. Plant Physiol. 171: 225-234.
17.
Heidrich K., Blanvillain-Baufumé S., Parker J.E. (2012) Molecular and spatial constraints on NB-LRR receptor signaling. Curr. Opin. Plant Biol. 15: 385-391.
18.
Hu Y., Duan S., Zhang Y., et al. (2016) Temporal transcription profiling of sweet orange in response to PthA4-mediated Xanthomonas citri subsp. citri infection. Phytopathology 106: 442-451.
19.
Hutchison K.W., Singer P.B., McInnis S., et al. (1999) Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin. Plant Physiol. 120: 827-832.
20.
Jagadeeswaran G., Saini A., Sunkar R. (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229: 1009-1014.
21.
Jones J.D., Dangl J.L. (2006) The plant immune system. Nature 444: 323-329.
22.
Khalaf A.A., Gmitter F.G., Conesa A., et al. (2011) Fortunella margarita transcriptional reprogramming triggered by Xanthomonas citri subsp. citri. BMC Plant Biol. 11: 1471-2229.
23.
Khraiwesh B., Zhu J.K., Zhu J. (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta 1819: 137-148.
24.
Kramer M.F. (2011) STEM-LOOP RT-qPCR for miRNAS. Current protocols in molecular biology. Ed. Ausubel F.M. et al. Unit15.10.
25.
Kumar N., Ebel R.C., Roberts P.D. (2011a) H2O2 metabolism during sweet orange (Citrus sinensis L. Osb.) ‘Hamlin’ Xanthomonas axonopodis pv. citri interaction. Sci. Hort. 128: 465-472.
26.
Kumar N., Ebel R.C., Roberts P.D. (2011b) Superoxide dismutase activity in kumquat leaves infected with Xanthomonas axonopodis pv. citri. J. Hortic. Sci. Biotechnol. 86: 62-68.
27.
Li Y., Zhang Q., Zhang J., et al. (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol. 152: 2222-2231.
28.
Lin H.C., Hsu S.T., Tzeng K.C. (2009) Histopathology and bacterial populations of atypical symptoms-inducing Xanthomonas axonopodis pv. citri strains in leaves of grapefruit and mexican lime. J. Plant Path. 18: 125-134.
29.
Livak K.J., Schmittgen T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2!ΔΔCT method. Methods 25: 402-408.
30.
Mafra V., Kubo K.S., Alves-Ferreira M., et al. (2012) Reference genes for accurate transcript normalization in citrus genotypes under different experimental conditions. Plos One 7(2): e31263.
31.
Millar A.A., Gubler F. (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705-721.
32.
Morel J.B., Dangl J.L. (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Diffe 4: 671-683.
33.
Navarro L., Dunoyer P., Jay F., et al. (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436-439.
34.
Nicaise V., Roux M., Zipfel C. (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol. 150: 1638-1647.
35.
Pérez-Quintero A.L., Quintero A., Urrego O., et al. (2012) Bioinformatic identification of cassava miRNAs differentially expressed in response to infection by Xanthomonas axonopodis pv. manihotis. BMC Plant Biol. 12: 29.
36.
Reyes J.L., Chua N.H. (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 49: 592-606.
37.
Rhoades M.W., Reinhart B.J., Lim L.P., et al. (2002) Prediction of plant microRNA targets. Cell 110: 513-520.
38.
Rouseff R.L., Nagy S. (1994) Health and nutritional benefits of citrus fruit components. Food Tech 48: 125-132.
39.
Ruijter J.M., Ramakers C., Hoogaars W.M.H., et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucl. Acids Res. 37: e45.
40.
Schubert T.S., Rizvi S.A., Sun X., et al. (2009) Meeting the challenge of eradicating citrus canker in Florida-Again. Plant Dis. 85: 340-356.
41.
Shi Q., Febres V.J., Jones J.B., Moore G.A. (2015) Responsiveness of different citrus genotypes to the Xanthomonas citri ssp. citri-derived pathogen-associated molecular pattern (PAMP) flg22 correlates with resistance to citrus canker. Mol. Plant Path. 16: 507-520.
42.
Sunkar R., Zhu J.K. (2004) Novel and stress-regulated micro- RNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019.
43.
Sunkar R., Kapoor A., Zhu J.K. (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by down-regulation of miR398 and important for oxidative stress tolerance. Plant Cell 18: 2051-2065.
45.
Varkonyi-Gasic E., Wu R., Wood M., et al. (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Meth. 3: 12.
46.
Viloria Z., Drouillard D.L., Graham J.H., Grosser J.W. (2004) Screening triploid hybrids of 'Lakeland' limequat for resistance to citrus canker. Plant Dis. 88: 1056-1060.
47.
Wang D., Pajerowska-Mukhtar K., Culler A.H., Dong X. (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17: 1784-1790.
48.
Wu G., Poethig R.S. (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539-3547.
49.
Zeier J., Delledonne M., Mishina T., et al. (2004) Genetic elucidation of nitric oxide signaling in incompatible plantpathogen interactions. Plant Physiol. 136: 2875-2886.
50.
Zhang W., Gao S., Zhou X., et al. (2011) Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol. Biol. 75: 93-105.