5.9
CiteScore
5.9
Impact Factor
Volume 42 Issue 11
Nov.  2015
Turn off MathJax
Article Contents

Dynamic and Coordinated Expression Changes of Rice Small RNAs in Response to Xanthomonas oryzae pv. oryzae

doi: 10.1016/j.jgg.2015.08.001
More Information
  • Corresponding author: E-mail address: xjwang@genetics.ac.cn (Xiu-Jie Wang); E-mail address: jiayt@im.ac.cn (Yan-Tao Jia)
  • Received Date: 2015-06-08
  • Accepted Date: 2015-08-07
  • Rev Recd Date: 2015-08-04
  • Available Online: 2015-08-17
  • Publish Date: 2015-11-20
  • Endogenous small RNAs are newly identified players in plant immune responses, yet their roles in rice (Oryza sativa) responding to pathogens are still less understood, especially for pathogens that can cause severe yield losses. We examined the small RNA expression profiles of rice leaves at 2, 6, 12, and 24 hours post infection of Xanthomonas oryzae pv. oryzae (Xoo) virulent strain PXO99, the causal agent of rice bacterial blight disease. Dynamic expression changes of some miRNAs and trans-acting siRNAs were identified, together with a few novel miRNA targets, including an RLK gene targeted by osa-miR159a.1. Coordinated expression changes were observed among some small RNAs in response to Xoo infection, with small RNAs exhibiting the same expression pattern tended to regulate genes in the same or related signaling pathways, including auxin and GA signaling pathways, nutrition and defense-related pathways. These findings reveal the dynamic and complex roles of small RNAs in rice-Xoo interactions, and identify new targets for regulating plant responses to Xoo.
  • These authors contributed equally to this work.
  • loading
  • [1]
    Adhikari, T.B., Mew, T.W., Teng, P.S. Plant Disease, 78 (1994),pp. 73-77
    [2]
    Albrecht, C., Boutrot, F., Segonzac, C. et al. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1 Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 303-308
    [3]
    Allen, E., Xie, Z., Gustafson, A.M. et al. microRNA-directed phasing during trans-acting siRNA biogenesis in plants Cell, 121 (2005),pp. 207-221
    [4]
    Altschul, S.F., Gish, W., Miller, W. et al. Basic local alignment search tool J. Mol. Biol., 215 (1990),pp. 403-410
    [5]
    Axtell, M.J. Classification and comparison of small RNAs from plants Annu. Rev. Plant Biol., 64 (2013),pp. 137-159
    [6]
    Bari, R., Jones, J.D. Role of plant hormones in plant defence responses Plant Mol. Biol., 69 (2009),pp. 473-488
    [7]
    Bart, R.S., Chern, M., Vega-Sanchez, M.E. et al. PLoS Genet., 6 (2010),p. e1001123
    [8]
    Beauclair, L., Yu, A., Bouche, N. Plant J., 62 (2010),pp. 454-462
    [9]
    Belkhadir, Y., Jaillais, Y., Epple, P. et al. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 297-302
    [10]
    Boccara, M., Sarazin, A., Thiebeauld, O. et al. PLoS Pathog., 10 (2014),p. e1003883
    [11]
    Chen, L.Q., Hou, B.H., Lalonde, S. et al. Sugar transporters for intercellular exchange and nutrition of pathogens Nature, 468 (2010),pp. 527-532
    [12]
    Dangl, J.L., Jones, J.D. Plant pathogens and integrated defence responses to infection Nature, 411 (2001),pp. 826-833
    [13]
    Deng, H., Liu, H., Li, X. et al. A CCCH-type zinc finger nucleic acid-binding protein quantitatively confers resistance against rice bacterial blight disease Plant Physiol., 158 (2012),pp. 876-889
    [14]
    Ding, B., Bellizzi Mdel, R., Ning, Y. et al. HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice Plant Cell, 24 (2012),pp. 3783-3794
    [15]
    Ding, X., Cao, Y., Huang, L. et al. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansion expression and promotes salicylate- and jasmonate-independent basal immunity in rice Plant Cell, 20 (2008),pp. 228-240
    [16]
    Dobrenel, T., Marchive, C., Azzopardi, M. et al. Sugar metabolism and the plant target of rapamycin kinase: a sweet operaTOR? Front Plant Sci., 4 (2013),p. 93
    [17]
    Dobrenel, T., Marchive, C., Sormani, R. et al. Regulation of plant growth and metabolism by the TOR kinase Biochem. Soc. Trans., 39 (2011),pp. 477-481
    [18]
    Dodds, P.N., Rathjen, J.P. Plant immunity: towards an integrated view of plant-pathogen interactions Nat. Rev. Genet., 11 (2010),pp. 539-548
    [19]
    Domingo, C., Andres, F., Tharreau, D. et al. Mol. Plant Microbe Interact., 22 (2009),pp. 201-210
    [20]
    Du, P., Wu, J., Zhang, J. et al. Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors PLoS Pathog., 7 (2011),p. e1002176
    [21]
    Dugas, D.V., Bartel, B. Plant Mol. Biol., 67 (2008),pp. 403-417
    [22]
    Fahlgren, N., Howell, M.D., Kasschau, K.D. et al. PLoS One, 2 (2007),p. e219
    [23]
    Fei, Q., Xia, R., Meyers, B.C. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks Plant Cell, 25 (2013),pp. 2400-2415
    [24]
    Fitzgerald, H.A., Canlas, P.E., Chern, M.S. et al. Plant J., 43 (2005),pp. 335-347
    [25]
    Gielen, H., Remans, T., Vangronsveld, J. et al. MicroRNAs in metal stress: specific roles or secondary responses? Int. J. Mol. Sci., 13 (2012),pp. 15826-15847
    [26]
    Gnanamanickam, S.S., Priyadarisini, V.B., Narayanan, N.N. et al. An overview of bacterial blight disease of rice and strategies for its management Current Sci., 77 (1999),pp. 1435-1444
    [27]
    Gomi, K., Satoh, M., Ozawa, R. et al. Plant J., 61 (2010),pp. 46-57
    [28]
    Guilfoyle, T.J., Hagen, G. Auxin response factors Curr. Opin. Plant Biol., 10 (2007),pp. 453-460
    [29]
    Guleria, P., Mahajan, M., Bhardwaj, J. et al. Plant small RNAs: biogenesis, mode of action and their roles in abiotic stresses Genomics Proteomics Bioinformatics, 9 (2011),pp. 183-199
    [30]
    Heller, J., Tudzynski, P. Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease Annu. Rev. Phytopathol., 49 (2011),pp. 369-390
    [31]
    Jagadeeswaran, G., Saini, A., Sunkar, R. Planta, 229 (2009),pp. 1009-1014
    [32]
    Jaillais, Y., Belkhadir, Y., Balsemao-Pires, E. et al. Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 8503-8507
    [33]
    Jeong, D.H., Park, S., Zhai, J. et al. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage Plant Cell, 23 (2011),pp. 4185-4207
    [34]
    Jiang, Y., Chen, X., Ding, X. et al. The XA21 binding protein XB25 is required for maintaining XA21-mediated disease resistance Plant J., 73 (2013),pp. 814-823
    [35]
    Jones, D.A., Takemoto, D. Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules Curr. Opin. Immunol., 16 (2004),pp. 48-62
    [36]
    Kallman, T., Chen, J., Gyllenstrand, N. et al. A significant fraction of 21-nucleotide small RNA originates from phased degradation of resistance genes in several perennial species Plant Physiol., 162 (2013),pp. 741-754
    [37]
    Katiyar-Agarwal, S., Gao, S., Vivian-Smith, A. et al. Genes Dev., 21 (2007),pp. 3123-3134
    [38]
    Katiyar-Agarwal, S., Jin, H. Role of small RNAs in host-microbe interactions Annu. Rev. Phytopathol., 48 (2010),pp. 225-246
    [39]
    Katiyar-Agarwal, S., Morgan, R., Dahlbeck, D. et al. A pathogen-inducible endogenous siRNA in plant immunity Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 18002-18007
    [40]
    Kazan, K., Manners, J.M. Linking development to defense: auxin in plant-pathogen interactions Trends Plant Sci., 14 (2009),pp. 373-382
    [41]
    Khraiwesh, B., Zhu, J.K., Zhu, J. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants Biochim. Biophys. Acta, 1819 (2012),pp. 137-148
    [42]
    Kobe, B., Kajava, A.V. The leucine-rich repeat as a protein recognition motif Curr. Opin. Struct. Biol., 11 (2001),pp. 725-732
    [43]
    Kozomara, A., Griffiths-Jones, S. miRBase: integrating microRNA annotation and deep-sequencing data Nucleic Acids Res., 39 (2011),pp. D152-D157
    [44]
    Lee, S.W., Han, S.W., Sririyanum, M. et al. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity Science, 326 (2009),pp. 850-853
    [45]
    Li, F., Pignatta, D., Bendix, C. et al. MicroRNA regulation of plant innate immune receptors Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 1790-1795
    [46]
    Li, J., Wu, Y., Qi, Y. Sci. China Life Sci., 57 (2014),pp. 36-45
    [47]
    Li, Y., Lu, Y.G., Shi, Y. et al. Plant Physiol., 164 (2014),pp. 1077-1092
    [48]
    Li, Y., Zhang, Q., Zhang, J. et al. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity Plant Physiol., 152 (2010),pp. 2222-2231
    [49]
    Li, Y.F., Zheng, Y., Addo-Quaye, C. et al. Transcriptome-wide identification of microRNA targets in rice Plant J., 62 (2010),pp. 742-759
    [50]
    Li, Z., Zhou, X. Small RNA biology: from fundamental studies to applications Sci. China Life Sci., 56 (2013),pp. 1059-1062
    [51]
    Li, Z.K., Arif, M., Zhong, D.B. et al. Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 7994-7999
    [52]
    Lin, S.I., Santi, C., Jobet, E. et al. Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation Plant Cell Physiol., 51 (2010),pp. 2119-2131
    [53]
    Liu, J., Cheng, X., Liu, D. et al. The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling PLoS Genet., 10 (2014),p. e1004755
    [54]
    Livak, K.J., Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods, 25 (2001),pp. 402-408
    [55]
    Marchler-Bauer, A., Zheng, C., Chitsaz, F. et al. CDD: conserved domains and protein three-dimensional structure Nucleic Acids Res., 41 (2013),pp. D348-D352
    [56]
    Marger, M.D., A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport Trends Biochem. Sci., 18 (1993),pp. 13-20
    [57]
    Mittler, R., Vanderauwera, S., Gollery, M. et al. Reactive oxygen gene network of plants Trends Plant Sci., 9 (2004),pp. 490-498
    [58]
    Nakashita, H., Yasuda, M., Nitta, T. et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice Plant J., 33 (2003),pp. 887-898
    [59]
    Navarro, L., Dunoyer, P., Jay, F. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling Science, 312 (2006),pp. 436-439
    [60]
    Navarro, L., Jay, F., Nomura, K. et al. Suppression of the microRNA pathway by bacterial effector proteins Science, 321 (2008),pp. 964-967
    [61]
    Pao, S.S., Paulsen, I.T., Major facilitator superfamily Microbiol. Mol. Biol. Rev., 62 (1998),pp. 1-34
    [62]
    Pumplin, N., Voinnet, O. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence Nat. Rev. Microbiol., 11 (2013),pp. 745-760
    [63]
    Qiao, Y., Liu, L., Xiong, Q. et al. Oomycete pathogens encode RNA silencing suppressors Nat. Genet., 45 (2013),pp. 330-333
    [64]
    Remy, E., Cabrito, T.R., Baster, P. et al. Plant Cell, 25 (2013),pp. 901-926
    [65]
    Robert-Seilaniantz, A., MacLean, D., Jikumaru, Y. et al. The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates Plant J., 67 (2011),pp. 218-231
    [66]
    Rodrigues, J.A., Ruan, R., Nishimura, T. et al. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm Proc. Natl. Acad. Sci. USA, 110 (2013),pp. 7934-7939
    [67]
    Ruiz-Ferrer, V., Voinnet, O. Roles of plant small RNAs in biotic stress responses Annu. Rev. Plant Biol., 60 (2009),pp. 485-510
    [68]
    Sa-Correia, I., Tenreiro, S. J. Biotechnol., 98 (2002),pp. 215-226
    [69]
    , Beatty, J.T., Goffeau, A., Harley, K.T. et al. The major facilitator superfamily J. Mol. Microbiol. Biotechnol., 1 (1999),pp. 257-279
    [70]
    Seo, J.K., Wu, J., Lii, Y. et al. Contribution of small RNA pathway components in plant immunity Mol. Plant Microbe Interact., 26 (2013),pp. 617-625
    [71]
    Shen, X., Yuan, B., Liu, H. et al. Plant J., 64 (2010),pp. 86-99
    [72]
    Shivaprasad, P.V., Chen, H.M., Patel, K. et al. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs Plant Cell, 24 (2012),pp. 859-874
    [73]
    Simmons, C.R., Fridlender, M., Navarro, P.A. et al. A maize defense-inducible gene is a major facilitator superfamily member related to bacterial multidrug resistance efflux antiporters Plant Mol. Biol., 52 (2003),pp. 433-446
    [74]
    Song, X., Li, P., Zhai, J. et al. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis Plant J., 69 (2012),pp. 462-474
    [75]
    Song, X., Wang, D., Ma, L. et al. Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development Plant J., 71 (2012),pp. 378-389
    [76]
    Sun, X., Cao, Y., Yang, Z. et al. Plant J., 37 (2004),pp. 517-527
    [77]
    Sunkar, R., Kapoor, A., Zhu, J.K. Plant Cell, 18 (2006),pp. 2051-2065
    [78]
    Tao, Z., Liu, H., Qiu, D. et al. A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions Plant Physiol., 151 (2009),pp. 936-948
    [79]
    Truman, W.M., Bennett, M.H., Turnbull, C.G. et al. Plant Physiol., 152 (2010),pp. 1562-1573
    [80]
    Tsuji, H., Aya, K., Ueguchi-Tanaka, M. et al. GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers Plant J., 47 (2006),pp. 427-444
    [81]
    Wang, D., Pajerowska-Mukhtar, K., Culler, A.H. et al. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway Curr. Biol., 17 (2007),pp. 1784-1790
    [82]
    Wang, Z.Y. Brassinosteroids modulate plant immunity at multiple levels Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 7-8
    [83]
    Wei, L.Q., Yan, L.F., Wang, T. Genome Biol., 12 (2011),p. R53
    [84]
    Weiberg, A., Wang, M., Lin, F.M. et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways Science, 342 (2013),pp. 118-123
    [85]
    Wu, G. Plant microRNAs and development J. Genet. Genomics, 40 (2013),pp. 217-230
    [86]
    Wu, L., Zhang, Q., Zhou, H. et al. Rice microRNA effector complexes and targets Plant Cell, 21 (2009),pp. 3421-3435
    [87]
    Xia, K., Wang, R., Ou, X. et al. PLoS One, 7 (2012),p. e30039
    [88]
    Yamasaki, H., Abdel-Ghany, S.E., Cohu, C.M. et al. J. Biol. Chem., 282 (2007),pp. 16369-16378
    [89]
    Yang, D.L., Yang, Y., He, Z. Roles of plant hormones and their interplay in rice immunity Mol. Plant., 6 (2013),pp. 675-685
    [90]
    Yuan, M., Chu, Z., Li, X. et al. Plant Cell, 22 (2010),pp. 3164-3176
    [91]
    Zhai, J., Jeong, D.H., De Paoli, E. et al. Genes Dev., 25 (2011),pp. 2540-2553
    [92]
    Zhai, J., Zhao, Y., Simon, S.A. et al. Plant microRNAS display differential 3' truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species Plant Cell, 25 (2013),pp. 2417-2428
    [93]
    Zhang, X., Zhao, H., Gao, S. et al. Mol. Cell, 42 (2011),pp. 356-366
    [94]
    Zhang, Y.C., Yu, Y., Wang, C.Y. et al. Nat. Biotechnol., 31 (2013),pp. 848-852
    [95]
    Zhao, Y.T., Wang, M., Fu, S.X. et al. Plant Physiol., 158 (2012),pp. 813-823
    [96]
    Zheng, Q., Wang, X.J. GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis Nucleic Acids Res., 36 (2008),pp. W358-W363
    [97]
    Zhou, C.M., Wang, J.W. Regulation of flowering time by microRNAs J. Genet. Genomics, 40 (2013),pp. 211-215
    [98]
    Zhou, M., Gu, L., Li, P. et al. Degradome sequencing reveals endogenous small RNA targets in rice Front. Biol., 5 (2010),pp. 67-90
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (90) PDF downloads (2) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return