MicroRNA166 controls root and nodule development in Medicago truncatula

Plant Journal

Volumn 54, Issue 5, 2008, Pages 876-887

  Boualem, Adnane ^a   Laporte, Philippe ^a   Jovanovic, Mariana ^a   Laffont, Carole ^a   Plet, Julie ^a   Combier, Jean Philippe ^b   Niebel, Andreas ^b   Crespi, Martin ^a   Frugier, Florian ^a  

^a CNRS   (France)

^b LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

Clustered miRNA; HD ZIP III transcription factors; Lateral root; Polycistronic miRNA; Rhizobium; Symbiotic nodulation

Indexed keywords

MICRORNA; PRIMER DNA;

ARTICLE; BARREL MEDIC; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BASE SEQUENCE; BLOTTING, NORTHERN; DNA PRIMERS; GENE EXPRESSION REGULATION, PLANT; IN SITU HYBRIDIZATION; MEDICAGO TRUNCATULA; MICRORNAS; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANIMALIA; MEDICAGO TRUNCATULA; RHIZOBIUM;

EID: 44349155320     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03448.x     Document Type: Article

References (58)

1. Alvarez, J.P., Pekker, I., Goldshmidt, A., Blum, E., Amsellem, Z. Eshed, Y. (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell, 18, 1134 1151.
2. Aravin, A.A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J. Tuschl, T. (2003) The small RNA profile during Drosophila melanogaster development. Dev. Cell, 5, 337 350.
3. Ardourel, M., Demont, N., Debelle, F., Maillet, F., de Billy, F., Prome, J.C., Denarie, J. Truchet, G. (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell, 6, 1357 1374.
4. Auriac, M.C. Timmers, A.C. (2007) Nodulation studies in the model legume Medicago truncatula: advantages of using the constitutive EF1α promoter and limitations in detecting fluorescent reporter proteins in nodule tissues. Mol. Plant Microbe Interact. 20, 1040 1047.
5. Beveridge, C.A., Mathesius, U., Rose, R.J. Gresshoff, P.M. (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr. Opin. Plant Biol. 10, 44 51.
6. Boisson-Dernier, A., Chabaud, M., Garcia, F., Becard, G., Rosenberg, C. Barker, D.G. (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol. Plant Microbe Interact. 14, 695 700.
7. Bright, L.J., Liang, Y., Mitchell, D.M. Harris, J.M. (2005) The LATD gene of Medicago truncatula is required for both nodule and root development. Mol. Plant Microbe Interact. 18, 521 532.
8. Casimiro, I., Beeckman, T., Graham, N., Bhalerao, R., Zhang, H., Casero, P., Sandberg, G. Bennett, M.J. (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci. 8, 165 171.
9. Chuck, G., Cigan, A.M., Saeteurn, K. Hake, S. (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39, 544 549.
10. Coba de la Pena, T., Frugier, F., McKhann, H.I., Bauer, P., Brown, S., Kondorosi, A. Crespi, M. (1997) A carbonic anhydrase gene is induced in the nodule primordium and its cell-specific expression is controlled by the presence of Rhizobium during development. Plant J. 11, 407 420.
11. Combier, J.P., Frugier, F., de Billy, F. 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.
12. Complainville, A., Brocard, L., Roberts, I., Dax, E., Sever, N., Sauer, N., Kondorosi, A., Wolf, S., Oparka, K. Crespi, M. (2003) Nodule initiation involves the creation of a new symplasmic field in specific root cells of medicago species. Plant Cell, 15, 2778 2791.
13. Emery, J.F., Floyd, S.K., Alvarez, J., Eshed, Y., Hawker, N.P., Izhaki, A., Baum, S.F. Bowman, J.L. (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13, 1768 1774.
14. 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.
15. Floyd, S.K. Bowman, J.L. (2004) Gene regulation: ancient microRNA target sequences in plants. Nature, 428, 485 486.
16. 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.
17. Gonzalez-Rizzo, S., Crespi, M. Frugier, F. (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell, 18, 2680 2693.
18. Guddeti, S., Zhang, D.C., Li, A.L., Leseberg, C.H., Kang, H., Li, X.G., Zhai, W.X., Johns, M.A. Mao, L. (2005) Molecular evolution of the rice miR395 gene family. Cell Res. 15, 631 638.
19. Hawker, N.P. Bowman, J.L. (2004) Roles for Class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol. 135, 2261 2270.
20. Hirsch, J., Lefort, V., Vankersschaver, M., Boualem, A., Lucas, A., Thermes, C., d'Aubenton-Carafa, Y. Crespi, M. (2006) Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts. Plant Physiol. 140, 1192 1204.
21. Jones-Rhoades, M.W. Bartel, D.P. (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell, 14, 787 799.
22. Jones-Rhoades, M.W., Bartel, D.P. Bartel, B. (2006) MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19 53.
23. Juarez, M.T., Kui, J.S., Thomas, J., Heller, B.A. Timmermans, M.C. (2004) MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature, 428, 84 88.
24. Kidner, C.A. Martienssen, R.A. (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature, 428, 81 84.
25. Kim, J., Jung, J.H., Reyes, J.L. et al. (2005) MicroRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J. 42, 84 94.
26. Lai, E.C., Tomancak, P., Williams, R.W. Rubin, G.M. (2003) Computational identification of Drosophila microRNA genes. Genome Biol. 4, R42.
27. Laufs, P., Peaucelle, A., Morin, H. Traas, J. (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development, 131, 4311 4322.
28. Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H. Kim, V.N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051 4060.
29. Li, A. Mao, L. (2007) Evolution of plant microRNA gene families. Cell Res. 17, 212 218.
30. Li, X. Zhang, Y.Z. (2005) Computational detection of microRNAs targeting transcription factor genes in Arabidopsis thaliana. Comput. Biol. Chem. 29, 360 367.
31. Lu, C., Kulkarni, K., Souret, F.F. et al. (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res. 16, 1276 1288.
32. Malamy, J.E. (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28, 67 77.
33. Mallory, A.C., Reinhart, B.J., Jones-Rhoades, M.W., Tang, G., Zamore, P.D., Barton, M.K. Bartel, D.P. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J. 23, 3356 3364.
34. McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J. Barton, M.K. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature, 411, 709 713.
35. McHale, N.A. Koning, R.E. (2004) MicroRNA-directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell, 16, 1730 1740.
36. Nikovics, K., Blein, T., Peaucelle, A., Ishida, T., Morin, H., Aida, M. Laufs, P. (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell, 18, 2929 2945.
37. Nogueira, F.T., Madi, S., Chitwood, D.H., Juarez, M.T. Timmermans, M.C. (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev. 21, 750 755.
38. Ochando, I., Jover-Gil, S., Ripoll, J.J., Candela, H., Vera, A., Ponce, M.R., Martinez-Laborda, A. Micol, J.L. (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in arabidopsis. Plant Physiol. 141, 607 619.
39. Prigge, M.J. Clark, S.E. (2006) Evolution of the class III HD-Zip gene family in land plants. Evol. Dev. 8, 350 361.
40. Prigge, M.J., Otsuga, D., Alonso, J.M., Ecker, J.R., Drews, G.N. Clark, S.E. (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell, 17, 61 76.
41. Quandt, H.J., Pühler, A. Broer, I. (1993) Transgenic root nodules of Vicia hirsuta: a fast and efficient system for the study of gene expression in indeterminate type nodules. Mol. Plant-Microbe Interact. 6, 699 706.
42. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B. Bartel, D.P. (2002) Prediction of plant microRNA targets. Cell, 110, 513 520.
43. Schwab, R., Palatnik, J.F., Riester, M., Schommer, C., Schmid, M. Weigel, D. (2005) Specific effects of microRNAs on the plant transcriptome. Dev. Cell, 8, 517 527.
44. Sessa, G., Steindler, C., Morelli, G. Ruberti, I. (1998) The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol. Biol. 38, 609 622.
45. Sunkar, R. Zhu, J.K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001 2019.
46. Talmor-Neiman, M., Stav, R., Frank, W., Voss, B. Arazi, T. (2006) Novel micro-RNAs and intermediates of micro-RNA biogenesis from moss. Plant J. 47, 25 37.
47. Truchet, G., Debelle, F., Vasse, J., Terzaghi, B., Garnerone, A.M., Rosenberg, C., Batut, J., Maillet, F. Denarie, J. (1985) Identification of a Rhizobium meliloti pSym2011 region controlling the host specificity of root hair curling and nodulation. J. Bacteriol. 164, 1200 1210.
48. Valoczi, A., Varallyay, E., Kauppinen, S., Burgyan, J. Havelda, Z. (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J. 47, 140 151.
49. Vasse, J., de Billy, F., Camut, S. Truchet, G. (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J. Bacteriol. 172, 4295 4306.
50. Vaucheret, H., Mallory, A.C. Bartel, D.P. (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol. Cell, 22, 129 136.
51. Wang, S., Zhu, Q.H., Guo, X., Gui, Y., Bao, J., Helliwell, C. Fan, L. (2007) Molecular evolution and selection of a gene encoding two tandem microRNAs in rice. FEBS Lett. 581, 4789 4793.
52. Williams, L., Grigg, S.P., Xie, M., Christensen, S. Fletcher, J.C. (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development, 132, 3657 3668.
53. Willmann, M.R. Poethig, R.S. (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr. Opin. Plant Biol. 10, 503 511.
54. Wopereis, J., Pajuelo, E., Dazzo, F.B., Jiang, Q., Gresshoff, P.M., De Bruijn, F.J., Stougaard, J. Szczyglowski, K. (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J. 23, 97 114.
55. Zhong, R. Ye, Z.H. (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell, 11, 2139 2152.
56. Zhong, R. Ye, Z.H. (2004) Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol. 45, 369 385.
57. Zhou, G.K., Kubo, M., Zhong, R., Demura, T. Ye, Z.H. (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol. 48, 391 404.
58. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406 3415.