Complexity of miRNA-dependent regulation in root symbiosis

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1595, 2012, Pages 1570-1579

  Bazin, Jérémie ^a,b   Bustos Sanmamed, Pilar ^a   Hartmann, Caroline ^a,b   Lelandais Brière, Christine ^a,b   Crespi, Martin ^a  

^a CEA SACLAY   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Evolution; Legumes; Microrna; Plant defence; Symbiosis; Transcription factor

Indexed keywords

ARBUSCULAR MYCORRHIZA; BIOLOGICAL DEVELOPMENT; CYTOLOGY; ECOMORPHOLOGY; ECOPHYSIOLOGY; EVOLUTIONARY BIOLOGY; FUNCTIONAL ROLE; FUNGUS; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; LEGUME; NITROGEN FIXATION; NODULATION; PATHOGEN; PHYLOGENETICS; PLANT DEFENSE; RHIZOBACTERIUM; RNA; ROOT SYSTEM; SOIL FAUNA; SOIL-VEGETATION INTERACTION; SYMBIOSIS;

EID: 84859947792     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0228     Document Type: Review

References (59)

1. Truchet, G., Barker, D. G., Camut, S., Debilly, F., Vasse, J. & Huguet, T. 1989 Alfalfa nodulation in the absence of Rhizobium. Mol. Gen. Genet. 219, 65-68. (doi:10.1007/ BF00261158)
2. Madsen, E. B. et al. 2011 Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 65, 404-417. (doi:10.1111/j.1365-313X.2010.04431.x)
3. Madsen, E. B. et al. 2003 A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637-640. (doi:10.1038/nature02045)
4. Geurts, R., Fedorova, E. & Bisseling, T. 2005 Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 8, 346-352. (doi:10.1016/j.pbi.2005.05.013)
5. Crespi, M. & Frugier, F. 2008 De novo organ formation from differentiated cells: root nodule organogenesis. Sci. Signal. 1, RE11. (doi:10.1126/scisignal.149re11)
6. Desbrosses, G. J. & Stougaard, J. 2011 Root nodulation: A paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 10, 348-358. (doi:1931-3128/j.chom.2011.09.005)
7. Murray, J. D. 2011 Invasion by invitation: Rhizobial infection in legumes. Mol. Plant-Microbe Interact. 24, 631-639. (doi:10.1094/mpmi-08-10-0181)
8. Maillet, F. et al. 2011 Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-63. (doi:10.1038/nature09622)
9. Seddas, P. M. A. et al. 2009 Symbiosis-related plant genes modulate molecular responses in an arbuscular mycorrhizal fungus during early root interactions. Mol. Plant-Microbe Interact. 22, 341-351. (doi:10.1094/mpmi-22-3-0341)
10. Soto, M. J., Dominguez-Ferreras, A., Perez-Mendoza, D., Sanjuan, J. & Olivares, J. 2009 Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell Microbiol. 11, 381-388. (doi:CMI1282/j.1462-5822.2008.01282.x)
11. Vasse, J., Debilly, F. & Truchet, G. 1993 Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J. 4, 555-566. (doi:10.1046/j.1365-313X.1993. 04030555.x)
12. Bozso, Z., Maunoury, N., Szatmari, A., Mergaert, P., Ott, P. G., Zsiros, L. R., Szabo, E., Kondorosi, E. & Klement, Z. 2009 Transcriptome analysis of a bacterially induced basal and hypersensitive response of Medicago truncatula. Plant Mol. Biol. 70, 627-646. (doi:10.1007/ s11103-009-9496-8)
13. Marino, D., Andrio, E., Danchin, E. G. J., Oger, E., Gucciardo, S., Lambert, A., Puppo, A. & Pauly, N. 2011 A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytol. 189, 580-592. (doi:10.1111/j.1469-8137.2010.03509.x)
14. D'Haeze, W. & Holsters, M. 2004 Surface polysacchar-ides enable bacteria to evade plant immunity. Trends Microbiol. 12, 555-561. (doi:10.1016/j.tim.2004.10.009)
15. Nakagawa, T. et al. 2011 From defense to symbiosis: Limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant J. 65, 169-180. (doi:10.1111/j.1365-313X.2010.04411.x)
16. Khan, G., Declerck, M., Sorin, C., Hartmann, C., Crespi, M. & Lelandais-Brière, C. 2011 MicroRNAs as regulators of root development and architecture. Plant Mol. Biol. 77, 47-58. (doi:10.1007/s11103-011-9793-x)
17. Khan, G. A., Hudik, E., Sorin, C., Hartmann, C., Crespi, M. & Lelandais-Brière, C. 2011 Non coding RNAs in plants; RNA technologies. Berlin, Germany: Springer.
18. Boualem, A., Laporte, P., Jovanovic, M., Laffont, C., Plet, J., Combier, J. P., Niebel, A., Crespi, M. & Frugier, F. 2008 MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J. 54, 876-887. (doi:10.1111/j.1365-313X.2008.03448.x)
19. Combier, J. P. et al. 2006 MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev. 20, 3084-3088. (doi:10.1101/gad.402806)
20. Vazquez, F. 2006 Arabidopsis endogenous small RNAs: Highways and byways. Trends Plant Sci. 11, 460-468. (doi:10.1016/j.tplants.2006.07.006)
21. Xie, Z. X., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., Jacobsen, S. E. & Carrington, J. C. 2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, 642-652. (doi:e10410.1371/journal.pbio.0020104)
22. Voinnet, O. 2009 Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687. (doi:10.1016/j.cell. 2009.01.046)
23. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L. & Voinnet, O. 2008 Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190. (doi:10. 1126/science.1159151)
24. Vaucheret, H. 2006 Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev. 20, 759-771. (doi:10.1101/gad.1410506)
25. Bardou, F., Merchan, F., Ariel, F. & Crespi, M. 2011 Dual RNAs in plants. Biochimie 93, 1950-1954. (doi:10.1016/j.biochi.2011.07.028)
26. Saze, H. & Kakutani, T. 2011 Differentiation of epigenetic modifications between transposons and genes. Curr. Opin. Plant Biol. 14, 81-87. (doi:10.1016/j.pbi. 2010.08.017)
27. Capitao, C., Paiva, J. A. P., Santos, D. M. & Fevereiro, P. 2011 In Medicago truncatula, water deficit modulates the transcript accumulation of components of small RNA pathways. BMC Plant Biol. 11, 79. (doi:10.1186/1471-2229-11-79)
28. Rubio-Somoza, I. & Weigel, D. 2011 MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 16, 258-264. (doi:10.1016/j.tplants.2011.03.001)
29. Rubio-Somoza, I., Cuperus, J. T., Weige, D. & Carrington, J. C. 2009 Regulation and functional specialization of small RNA-target nodes during plant development. Curr. Opin. Plant Biol. 12, 622-627. (doi:10.1016/j.pbi.2009.07.003)
30. Allen, E., Xie, Z. X., Gustafson, A. M., Sung, G. H., Spatafora, J. W. & Carrington, J. C. 2004 Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36, 1282-1290. (doi:10.1038/ng1478)
31. Cuperus, J. T., Fahlgren, N. & Carrington, J. C. 2011 Evolution and functional diversification of MIRNA genes. Plant Cell 23, 431-442. (doi:10.1105/tpc.110.082784)
32. Fahlgren, N. et al. 2007 High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2, e219. (doi:10. 1371/journal.pone.0000219)
33. Zhang, B. H., Pan, X. P., Cannon, C. H., Cobb, G. P. & Anderson, T. A. 2006 Conservation and divergence of plant microRNA genes. Plant J. 46, 243-259. (doi:10. 1111/j.1365-313X.2006.02697.x)
34. Lelandais-Briere, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., Gouzy, J. & Crespi, M. 2009 Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21, 2780-2796. (doi:10.1105/tpc.109.068130)
35. Naya, L., Khan, G. A., Sorin, C., Hartmann, C., Crespi, M. & Lelandais-Briere, C. 2010 Cleavage of a non-conserved target by a specific miR156 isoform in root apexes of Medicago truncatula. Plant Signal Behav. 5, 328-331.
36. Branscheid, A., Devers, E. A., May, P. & Krajinski, F. 2011 Distribution pattern of small RNA and degradome reads provides information on miRNA gene structure and regulation. Plant Signal Behav. 6, 1609-1611.
37. De Luis Margarit, A. 2010 Etude des microRNAs impliqués dans la symbiose de Lotus japonicus. Doctoral thesis, Strasbourg University, Strasbourg, France.
38. Subramanian, S., Fu, Y., Sunkar, R., Barbazuk, W. B., Zhu, J. K. & Yu, O. 2008 Novel and nodulation-regulated microRNAs in soybean roots. BMC Genom. 9, 160. (doi:10.1186/1471-2164-9-160)
39. D'haeseleer, K. et al. 2011 Transcriptional and post-transcriptional regulation of a NAC1 transcription factor in Medicago truncatula roots. New Phytol. 191, 647-661. (doi:10.1111/j.1469-8137.2011.03719.x)
40. 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. (doi:10.1105/tpc.105.033076)
41. Gutierrez, L., Bussell, J. D., Pa ̌curar, D. I., Schwambach, J., Pa ̌curar, M. & Bellini, C. 2009 Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant cell. 21, 3119-3132. (doi:10.1105/tpc.108.064758)
42. Padmanabhan, C., Zhang, X. M. & Jin, H. L. 2009 Host small RNAs are big contributors to plant innate immunity. Curr. Opin. Plant Biol. 12, 465-472. (doi:10.1016/ j.pbi.2009.06.005)
43. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O. & Jones, J. D. G. 2006 A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439. (doi:10.1126/science.1126088)
44. Li, H., Deng, Y., Wu, T. L., Subramanian, S. & Yu, O. 2010 Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiol. 153, 1759-1770. (doi:10.1104/pp.110.156950)
45. Carlsbecker, A. et al. 2010 Cell signalling by micro-RNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316-321. (doi:10.1038/nature08977)
46. Axtell, M. J. & Bartel, D. P. 2005 Antiquity of micro-RNAs and their targets in land plants. Plant Cell 17, 1658-1673. (doi:10.1105/tpc.105.032185)
47. Zhang, B. H., Pan, X. P. & Stellwag, E. J. 2008 Identification of soybean microRNAs and their targets. Planta 229, 161-182. (doi:10.1007/s00425-008-0818-x)
48. Devers, E. A., Branscheid, A., May, P. & Krajinski, F. 2011 Stars and symbiosis: MicroRNA-and MicroRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 156, 1990-2010. (doi:10. 1104/pp.111.172627)
49. Nag, A. & Jack, T. 2010 Sculpting the flower; the role of microRNAs in flower development. Curr. Top. Dev. Biol. 91, 349-378. (doi:10.1016/S0070-2153(10) 91012-0)
50. Zhang, X., Zou, Z., Gong, P., Zhang, J., Ziaf, K., Li, H., Xiao, F. & Ye, Z. 2011 Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol. Lett. 33, 403-409. (doi:10.1007/s10529-010-0436-0)
51. Zhao, M., Ding, H., Zhu, J.-K., Zhang, F. & Li, W.-X. 2011 Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol. 190, 906-915. (doi:10.1111/j.1469-8137.2011.03647.x)
52. Li, Y. J., Fu, Y. R., Ji, L. S., Wu, C. A. & Zheng, C. C. 2010 Characterization and expression analysis of the Arabidopsis mir169 family. Plant Sci. 178, 271-280. (doi:10.1016/j.plantsci.2010.01.007)
53. Kalo, P. et al. 2005 Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786-1789. (doi:10. 1126/science.1110951)
54. Kulcheski, F. R. et al. 2011 Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genom. 12, 307. (doi:10.1186/1471-2164-12-307)
55. Qi, Y., Tsuda, K., Nguyen, L. V., Wang, X., Lin, J., Murphy, A. S., Glazebrook, J., Thordal-Christensen, H. & Katagiri, F. 2011 Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J. Biol. Chem. 286, 31297-31307. (doi:10.1074/jbc.M110.211615)
56. Jagadeeswaran, G. et al. 2009 Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families. New Phytol. 184, 85-98. (doi:10.1111/j.1469-8137. 2009.02915.x)
57. Li, Y., Li, C. Q., Ding, G. H. & Jin, Y. X. 2011 Evolution of MIR159/319 microRNA genes and their post-transcriptional regulatory link to siRNA pathways. BMC Evol. Biol. 11, 122. (doi:10.1186/1471-2148-11-122)
58. Klevebring, D., Street, N. R., Fahlgren, N., Kasschau, K. D., Carrington, J. C., Lundeberg, J. & Jansson, S. 2009 Genome-wide profiling of populus small RNAs. BMC Genom. 10, 620. (doi:10.1186/1471-2164-10-620)
59. He, X.-F., Fang, Y.-Y., Feng, L. & Guo, H.-S. 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 Letters 582, 2445-2452. (doi:10.1016/j.febslet.2008.06.011)