Roles of small RNAs in soybean defense against Phytophthora sojae infection

Plant Journal

Volumn 79, Issue 6, 2014, Pages 928-940

  Wong, James ^a   Gao, Lei ^a   Yang, Yang ^b   Zhai, Jixian ^c   Arikit, Siwaret ^c   Yu, Yu ^a   Duan, Shuyi ^a,d   Chan, Vicky ^a   Xiong, Qin ^a,d   Yan, Jun ^e,g   Li, Shengben ^a   Liu, Renyi ^a   Wang, Yuanchao ^d   Tang, Guiliang ^e   Meyers, Blake C ^b   Chen, Xuemei ^a,f   Ma, Wenbo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHANGHAI MARITIME UNIVERSITY   (China)

^c UNIVERSITY OF DELAWARE   (United States)

^d NANJING AGRICULTURAL UNIVERSITY   (China)

^e MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g PURDUE UNIVERSITY   (United States)

Author keywords

defense gene regulation; Glycine max; microRNAs; oomycetes; phasiRNAs; Phytophthora sojae

Indexed keywords

AMINO ACIDS; ENCODING (SYMBOLS); FLAVONOIDS; GENE EXPRESSION; PATHOGENS; PROTEINS; RNA;

GLYCINE MAX; MICRORNAS; OOMYCETES; PHASIRNAS; PHYTOPHTHORA;

PLANTS (BOTANY);

ISOFLAVONE DERIVATIVE; MICRORNA; PLANT RNA; SMALL INTERFERING RNA;

DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; PARASITOLOGY; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; PLANT ROOT; REPORTER GENE; SOYBEAN;

DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HOST-PARASITE INTERACTIONS; ISOFLAVONES; MICRORNAS; PHYTOPHTHORA; PLANT DISEASES; PLANT ROOTS; RNA, PLANT; RNA, SMALL INTERFERING; SOYBEANS;

EID: 84907018112     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12590     Document Type: Article

References (70)

1. Addo-Quaye, C., Miller, W., and, Axtell, M.J., (2009) CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics, 25, 130-131.
2. Ambros, V., (2004) The functions of animal microRNAs. Nature, 431, 350-355.
3. Barrera-Figueroa, B.E., Gao, L., Diop, N.N., Wu, Z., Ehlers, J.D., Roberts, P.A., Close, T.J., Zhu, J.K., and, Liu, R., (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol. 11, 127.
4. Baulcombe, D., (2004) RNA silencing in plants. Nature, 431, 356-363.
5. Bednarek, P., and, Osbourn, A., (2009) Plant-microbe interactions: chemical diversity in plant defense. Science, 324, 746-748.
6. Boller, T., and, He, S.Y., (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 324, 742-744.
7. Bourke, P.M.A., (1964) Emergence of potato blight, 1843-46. Nature, 203, 805-808.
8. Brunner, F., Rosahl, S., Lee, J., Rudd, J.J., Geiler, C., Kauppinen, S., Rasmussen, G., Scheel, D., and, Nurnberger, T., (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J. 21, 6681-6688.
9. Campo, S., Peris-Peris, C., Siré, C., Moreno, A.B., Donaire, L., Zytnicki, M., Notredame, C., Llave, C., and, 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.
10. Chen, X., (2009) Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25, 21-44.
11. Chen, X., (2010) Small RNAs-secrets and surprises of the genome. Plant J. 61, 941-958.
12. Chen, X., (2012) Small RNAs in development-insights from plants. Curr. Opin. Genet. Dev. 22, 361-367.
13. Day, B., and, Graham, T., (2007) The plant host-pathogen interface: cell wall and membrane dynamics of pathogen-induced responses. Ann. N. Y. Acad. Sci. 1113, 123-134.
14. De Paoli, E., Dorantes-Acosta, A., Zhai, J., Accerbi, M., Jeong, D.H., Park, S., Meyers, B.C., Jorgensen, R.A., and, Green, P.J., (2009) Distinct extremely abundant siRNAs associated with cosuppression in petunia. RNA, 15, 1965-1970.
15. Diaz-Pendon, J.A., Li, F., Li, W.X., and, Ding, S.W., (2007) Suppression of antiviral silencing by Cucumber Mosaic Virus 2b Protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell, 19, 2053-2063.
16. Dodds, P.N., and, Rathjen, J.P., (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548.
17. Dorrance, A., Jia, H., and, Abney, T., (2004) Evaluation of soybean differentials for their interaction with Phytophthora sojae. Plant Health Prog. doi: 10.1094/PHP-2004-0309-01-RS.
18. Dou, D., Kale, S.D., Wang, X., et al. (2008) Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell, 20, 1118-1133.
19. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and, Pikaard, C.S., (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
20. Eitas, T.K., and, Dangl, J.L., (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 13, 472-477.
21. Erwin, D.C., and, Ribeiro, O.K., (1996) Phytophthora Diseases Worldwide. St. Paul, MN: American Phytopathological Society.
22. Fahlgren, N., Howell, M.D., Kasschau, K.D., et al. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE, 2, e219.
23. Fellbrich, G., Romanski, A., Varet, A., Blume, B., Brunner, F., Engelhardt, S., Felix, G., Kemmerling, B., Krzymowska, M., and, Nurnberger, T., (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J. 32, 375-390.
24. Griffiths-Jones, S., Saini, H.K., van Dongen, S., and, Enright, A.J., (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, D154-D158.
25. Grünwald, N.J., Martin, F.N., Larsen, M.M., Sullivan, C.M., Press, C.M., Coffey, M.D., Hansen, E.M., and, Parke, J.L., (2011) Phytophthora-ID.org: a sequence-based Phytophthora identification tool. Plant Dis. 95, 337-342.
26. Guo, N., Ye, W.W., Wu, X.L., Shen, D.Y., Wang, Y.C., Xing, H., and, Dou, D.L., (2011) Microarray profiling reveals microRNAs involving soybean resistance to Phytophthora sojae. Genome 54, 954-958.
27. Hawker, N.P., and, Bowman, J.L., (2004) Roles for class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol. 135, 2261-2270.
28. Howell, M.D., Fahlgren, N., Chapman, E.J., Cumbie, J.S., Sullivan, C.M., Givan, S.A., Kasschau, K.D., and, Carrington, J.C., (2007) Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. Plant Cell, 19, 926-942.
29. Hu, Z., Jiang, Q., Ni, Z., Chen, R., Xu, S., and, Zhang, H., (2013) Analyses of a Glycine max degradome library identify microRNA targets and microRNAs that trigger secondary siRNA biogenesis. J. Integr. Plant Biol. 55, 160-176.
30. Jones, J.D., and, Dangl, J.L., (2006) The plant immune system. Nature, 444, 323-329.
31. Katiyar-Agarwal, S., and, Jin, H., (2010) Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 48, 225-246.
32. Kereszt, A., Li, D., Indrasumunar, A., Nguyen, C.D., Nontachaiyapoom, S., Kinkema, M., and, Gresshoff, P.M., (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat. Protoc. 2, 948-952.
33. Kotera, E., Tasaka, M., and, Shikanai, T., (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature, 433, 326-330.
34. Li, R., Yu, C., Li, Y., Lam, T.W., Yiu, S.M., Kristiansen, K., and, Wang, J., (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics, 25, 1966-1967.
35. Li, Y., Zhang, Q., Zhang, J., Wu, L., Qi, Y., and, Zhou, J.M., (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol. 152, 2222-2231.
36. Li, F., Pignatta, D., Bendix, C., Brunkard, J.O., Cohn, M.M., Tung, J., Sun, H., Kumar, P., and, Baker, B., (2012) MicroRNA regulation of plant innate immune receptors. Proc. Natl Acad. Sci. USA, 109, 1790-1795.
37. Lu, S., Sun, Y.H., Amerson, H., and, Chiang, V.L., (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J. 51, 1077-1098.
38. Lygin, A.V., Hill, C.B., Zernova, O.V., Crull, L., Widholm, J.M., Hartman, G.L., and, Lozovaya, V.V., (2010) Response of soybean pathogens to glyceollin. Phytopathology, 100, 897-903.
39. Markham, N.R., and, Zuker, M., (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol. 453, 3-31.
40. McHale, L., Tan, X., Koehl, P., and, Michelmore, R.W., (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol. 7, 212.
41. Meyers, B.C., Morgante, M., and, Michelmore, R.W., (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J. 32, 77-92.
42. Meyers, B.C., Axtell, M.J., Bartel, B., et al. (2008) Criteria for annotation of plant microRNAs. Plant Cell, 20, 3186-3190.
43. Monaghan, J., and, Zipfel, C., (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349-357.
44. Morgan, R.L., Zhou, H., Lehto, E., Nguyen, N., Bains, A., Wang, X., and, Ma, W., (2010) Catalytic domain of the diversified Pseudomonas syringae type III effector HopZ1 determines the allelic specificity in plant hosts. Mol. Microbiol. 76, 437-455.
45. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O., and, Jones, J.D., (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312, 436-439.
46. Navarro, L., Jay, F., Nomura, K., He, S.Y., and, Voinnet, O., (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science, 321, 964-967.
47. Pearson, W.R., (2000) Flexible sequence similarity searching with the FASTA3 program package. Methods Mol. Biol. 132, 185-219.
48. Prikryl, J., Rojas, M., Schuster, G., and, Barkan, A., (2010) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl Acad. Sci. USA, 108, 415-420.
49. Qiao, Y., Liu, L., Xiong, Q., et al,. (2013) Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45, 330-333.
50. Robert-Seilaniantz, A., MacLean, D., Jikumaru, Y., Hill, L., Yamaguchi, S., Kamiya, Y., and, Jones, J.D., (2011) The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J. 67, 218-231.
51. Shultz, R.W., Tatineni, V.M., Hanley-Bowdoin, L., and, Thompson, W.F., (2007) Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol. 144, 1697-1714.
52. Si-Ammour, A., Windels, D., Arn-Bouldoires, E., Kutter, C., Ailhas, J., Meins, F. Jr, and, 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.
53. Subramanian, S., Graham, M.Y., Yu, O., and, Graham, T.L., (2005) RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae. Plant Physiol. 137, 1345-1353.
54. Sunkar, R., Chinnusamy, V., Zhu, J., and, Zhu, J.K., (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12, 301-309.
55. Tang, G., Yan, J., Gu, Y., Qiao, M., Fan, R., Mao, Y., and, Tang, X., (2012) Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods, 58, 118-125.
56. Thakur, V., Wanchana, S., Xu, M., Bruskiewich, R., Quick, W.P., Mosig, A., and, Zhu, X.G., (2011) Characterization of statistical features for plant microRNA prediction. BMC Genomics, 12, 108.
57. Torres, M.A., Jones, J.D., and, Dangl, J.L., (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378.
58. Turner, M., Yu, O., and, Subramanian, S., (2012) Genome organization and characteristics of soybean microRNAs. BMC Genomics, 13, 169.
59. Tyler, B.M., (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 8, 1-8.
60. Vidal, E.A., Araus, V., Lu, C., Parry, G., Green, P.J., Coruzzi, G.M., and, Gutierrez, R.A., (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 107, 4477-4482.
61. Voinnet, O., (2009) Origin, biogenesis, and activity of plant microRNAs. Cell, 136, 669-687.
62. West, C.A., (1981) Fungal elicitors of the phytoalexin response in higher plants. Naturwissenschaften, 68, 447-457.
63. Whisson, S.C., Boevink, P.C., Moleleki, L., et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450, 115-118.
64. Xia, R., Meyers, B.C., Liu, Z., Beers, E.P., Ye, S., and, Liu, Z., (2013) MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA biogenesis in eudicots. Plant Cell, 25, 1555-1572.
65. Yan, J., Gu, Y., Jia, X., Kang, W., Pan, S., Tang, X., Chen, X., and, Tang, G., (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell, 24, 415-427.
66. Ye, W., Wang, X., Tao, K., Lu, Y., Dai, T., Dong, S., Dou, D., Gijzen, M., and, Wang, Y., (2011) Digital gene expression profiling of the Phytophthora sojae transcriptome. Mol. Plant Microbe Interact. 24, 1530-1539.
67. Yoshida, K., Schuenemann, V.J., Cano, L.M., et al. (2013) The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife, 2, e00731.
68. Zhai, J., Jeong, D.H., De Paoli, E., et al. (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 25, 2540-2553.
69. 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.
70. Zhou, L., Mideros, S.X., Bao, L., et al. (2009) Infection and genotype remodel the entire soybean transcriptome. BMC Genomics, 10, 49.