Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis

Plant Journal

Volumn 79, Issue 5, 2014, Pages 757-768

  Laloum, Tom ^a,d   Baudin, Maël ^a   Frances, Lisa ^a   Lepage, Agnes ^a   Billault Penneteau, Benjamin ^a   Cerri, Marion R ^a,e   Ariel, Federico ^b   Jardinaud, Marie Françoise ^a,c   Gamas, Pascal ^a   De Carvalho Niebel, Fernanda ^a   Niebel, Andreas ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

CCAAT box binding factor; Legume rhizobium symbiosis; Medicago truncatula; Nod factor signaling; Nuclear factor Y; Transcription factor

Indexed keywords

CHEMICAL ACTIVATION; GENES; NITROGEN FIXATION; SIGNAL TRANSDUCTION;

CCAAT BOX-BINDING FACTOR; LEGUME-RHIZOBIUM SYMBIOSIS; MEDICAGO TRUNCATULA; NOD FACTOR; NUCLEAR FACTORS;

TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); MEDICAGO TRUNCATULA; RHIZOBIACEAE; RHIZOBIUM;

CCAAT BINDING FACTOR; PLANT RNA; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

BARREL MEDIC; CHEMISTRY; CYTOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MICRODISSECTION; NODULATION; PHYSIOLOGY; PLANT ROOT; REPORTER GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; SYMBIOSIS; TOBACCO;

CCAAT-BINDING FACTOR; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; MEDICAGO TRUNCATULA; MICRODISSECTION; PLANT PROTEINS; PLANT ROOTS; RNA, PLANT; ROOT NODULES, PLANT; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; SYMBIOSIS; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84906779032     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12587     Document Type: Article

References (49)

1. Anders, S., and, Huber, W., (2010) Differential expression analysis for sequence count data. Genome Biol. 11, R106.
2. Andriankaja, A., Boisson-Demier, A., Frances, L., Sauviac, L., Jauneau, A., Barker, D., and, de Carvalho-Niebel, F., (2007) AP2-ERF transcription factors mediate Nod factor-dependent mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell, 19, 2866-2885. (Pubitemid 350046234)
3. Ardourel, M., Demont, N., Debelle, F.D., Maillet, F., Debilly, F., Prome, J.C., Denarie, J., and, 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. (Pubitemid 24976493)
4. Boisson-Dernier, A., Andriankaja, A., Chabaud, M., Niebel, A., Journet, E.P., Barker, D.G., and, de Carvalho-Niebel, F., (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol. Plant Microbe Interact. 18, 1269-1276. (Pubitemid 41682598)
5. Capoen, W., Sun, J., Wysham, D., et al. (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl Acad. Sci. USA, 108, 14348-14353.
6. Catoira, R., Galera, C., de Billy, F., Penmetsa, R.V., Journet, E.P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., and, Denarie, J., (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell, 12, 1647-1666.
7. Cerri, M.R., Frances, L., Laloum, T., Auriac, M.C., Niebel, A., Oldroyd, G.E.D., Barker, D.G., Fournier, J., and, de Carvalho-Niebel, F., (2012) Medicago truncatula ERN transcription factors: regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection. Plant Physiol. 160, 2155-2172.
8. 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. (Pubitemid 44790624)
9. Combier, J.P., de Billy, F., Gamas, P., Niebel, A., and, Rivas, S., (2008) Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev. 22, 1549-1559. (Pubitemid 351793088)
10. El-Yahyaoui, F., Kuster, H., Ben Amor, B., et al. (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program(1 w). Plant Physiol. 136, 3159-3176. (Pubitemid 41096314)
11. Gendrel, A.V., Lippman, Z., Martienssen, R., and, Colot, V., (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat. Methods, 2, 213-218. (Pubitemid 41122129)
12. Gnesutta, N., Nardini, M., and, Mantovani, R., (2013) The H2A/H2B-like histone-fold domain proteins at the crossroad between chromatin and different DNA metabolisms. Transcription, 4, 114-119.
13. Grimsrud, P.A., den Os, D., Wenger, C.D., Swaney, D.L., Schwartz, D., Sussman, M.R., Ané, J.M., and, Coon, J.J., (2010) Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol. 152, 19-28.
14. Hirsch, S., Kim, J., Munoz, A., Heckmann, A.B., Downie, J.A., and, Oldroyd, G.E.D., (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell, 21, 545-557.
15. Hogekamp, C., Arndt, D., Pereira, P.A., Becker, J.D., Hohnjec, N., and, Küster, H., (2011) Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol. 157, 2023-2043.
16. Journet, E.P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., Arnould, C., Morandi, D., Barker, D.G., and, Gianinazzi-Pearson, V., (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol. Plant Microbe Interact. 14, 737-748. (Pubitemid 32464113)
17. Kalo, P., Gleason, C., Edwards, A., et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science, 308, 1786-1789. (Pubitemid 40848006)
18. Kang, H., Chu, X., Wang, C., et al. (2014) A MYB coiled coil transcription factor interacts with NSP2 and is involved in nodulation in Lotus japonicus. New Phytol. 201, 837-849.
19. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY((TM)) vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
20. Laloum, T., De Mita, S., Gamas, P., Baudin, M., and, Niebel, A., (2013) CCAAT-box binding transcription factors in plants: Y so many? Trends Plant Sci. 18, 157-166.
21. Laporte, P., Lepage, A., Fournier, J., et al. (2014) The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection. J. Exp. Bot. 65, 481-494.
22. Liu, J.-X., and, Howell, S.H., (2010) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell, 22, 782-796.
23. Mantovani, R., (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene, 239, 15-27. (Pubitemid 29462565)
24. Mantovani, R., Lio, X., Pessara, U., Vanhuisjduijnen, R., Benoist, C., and, Mathis, D., (1994) Dominant-negative analogs of NF-YA. J. Biol. Chem. 269, 20340-20346.
25. Marsh, J., Rakocevic, A., Mitra, R., Brocard, L., Sun, J., Eschstruth, A., Long, S., Schultze, M., Ratet, P., and, Oldroyd, G., (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol. 144, 324-335. (Pubitemid 46941636)
26. Middleton, P., Jakab, J., Penmetsa, R., et al. (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell, 19, 1221-1234. (Pubitemid 46941650)
27. Moreau, S., Verdenaud, M., Ott, T., Letort, S., de Billy, F., Niebel, A., Gouzy, J., de Carvalho-Niebel, F., and, Gamas, P., (2011) Transcription reprogramming during root nodule development in Medicago truncatula. PLoS One, 6, e16463.
28. Murray, J.D., (2011) Invasion by invitation: rhizobial infection in legumes. Mol. Plant Microbe Interact. 24, 631-639.
29. Nardini, M., Gnesutta, N., Donati, G., et al. (2013) Sequence-specific transcription factor NF-Y displays histone-like DNA binding and H2B-like ubiquitination. Cell, 152, 132-143.
30. Oldroyd, G.E.D., (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252-263.
31. Oldroyd, G.E.D., and, Downie, J.A., (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546. (Pubitemid 351813041)
32. Quandt, H.J., Puhler, A., and, 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. (Pubitemid 2041077)
33. Rose, C.M., Venkateshwaran, M., Grimsrud, P.A., Westphall, M.S., Sussman, M.R., Coon, J.J., and, Ane, J.-M., (2012) Medicago PhosphoProtein Database: a repository for Medicago truncatula phosphoprotein data. Front. Plant Sci. 3, 122.
34. Roux, B., Rodde, N., Jardinaud, M.F., et al. (2014) An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J. 77, 817-837.
35. Schaarschmidt, S., Gresshoff, P.M., and, Hause, B., (2013) Analyzing the soybean transcriptome during autoregulation of mycorrhization identifies the transcription factors GmNF-YA1a/b as positive regulators of arbuscular mycorrhization. Genome Biol. 14, R62.
36. Schauser, L., Roussis, A., Stiller, J., and, Stougaard, J., (1999) A plant regulator controlling development of symbiotic root nodules. Nature, 402, 191-195.
37. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol. 151, 1197-1206.
38. Singh, L.N., and, Hannenhalli, S., (2008) Functional diversification of paralogous transcription factors via divergence in DNA binding site motif and in expression. PLoS One, 3, e2345.
39. Singh, S., Katzer, K., Lambert, J., Cerri, M., and, Parniske, M., (2014) CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe, 15, 139-152.
40. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T., and, Geurts, R., (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science, 308, 1789-1791. (Pubitemid 40848007)
41. Soyano, T., Kouchi, H., Hirota, A., and, Hayashi, M., (2013) NODULE INCEPTION directly targets nf-y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet. 9, e1003352.
42. Tiwari, S.B., Shen, Y., Chang, H.-C., et al. (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57-66.
43. Voinnet, O., Rivas, S., Mestre, P., and, Baulcombe, D., (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956. (Pubitemid 36339384)
44. Xie, F., Murray, J.D., Kim, J., Heckmann, A.B., Edwards, A., Oldroyd, G.E., and, Downie, J.A., (2012) Legume pectate lyase required for root infection by rhizobia. Proc. Natl Acad. Sci. USA, 109, 633-638.
45. Yano, K., Yoshida, S., Müller, J., et al. (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl Acad. Sci. USA, 105, 20540-20545.
46. Yoro, E., Suzaki, T., Toyokura, K., Miyazawa, H., Fukaki, H., and, Kawaguchi, M., (2014) A positive regulator of nodule organogenesis, NODULE INCEPTION, acts as a negative regulator of rhizobial infection in Lotus japonicus. Plant Physiol. 165, 747-758.
47. Young, N.D., and, Bharti, A.K., (2012) Genome-enabled insights into legume biology. Annu. Rev. Plant Biol. 63, 283-305.
48. Young, N.D., Debelle, F., Oldroyd, G.E.D., et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature, 480, 520-524.
49. Zanetti, M.E., Blanco, F.A., Beker, M.P., Battaglia, M., and, Aguilar, O.M., (2010) A C subunit of the plant nuclear factor NF-Y required for rhizobial infection and nodule development affects partner selection in the common bean-rhizobium etli symbiosis. Plant Cell, 22, 4142-4157.