NODULE INCEPTION Directly Targets Subunit Genes to Regulate Essential Processes of Root Nodule Development in
The interactions of legumes with symbiotic nitrogen-fixing bacteria cause the formation of specialized lateral root organs called root nodules. It has been postulated that this root nodule symbiosis system has recruited factors that act in early signaling pathways (common SYM genes) partly from the ancestral mycorrhizal symbiosis. However, the origins of factors needed for root nodule organogenesis are largely unknown. NODULE INCEPTION (NIN) is a nodulation-specific gene that encodes a putative transcription factor and acts downstream of the common SYM genes. Here, we identified two Nuclear Factor-Y (NF-Y) subunit genes, LjNF-YA1 and LjNF-YB1, as transcriptional targets of NIN in Lotus japonicus. These genes are expressed in root nodule primordia and their translational products interact in plant cells, indicating that they form an NF-Y complex in root nodule primordia. The knockdown of LjNF-YA1 inhibited root nodule organogenesis, as did the loss of function of NIN. Furthermore, we found that NIN overexpression induced root nodule primordium-like structures that originated from cortical cells in the absence of bacterial symbionts. Thus, NIN is a crucial factor responsible for initiating nodulation-specific symbiotic processes. In addition, ectopic expression of either NIN or the NF-Y subunit genes caused abnormal cell division during lateral root development. This indicated that the Lotus NF-Y subunits can function to stimulate cell division. Thus, transcriptional regulation by NIN, including the activation of the NF-Y subunit genes, induces cortical cell division, which is an initial step in root nodule organogenesis. Unlike the legume-specific NIN protein, NF-Y is a major CCAAT box binding protein complex that is widespread among eukaryotes. We propose that the evolution of root nodules in legume plants was associated with changes in the function of NIN. NIN has acquired functions that allow it to divert pathways involved in the regulation of cell division to root nodule organogenesis.
Vyšlo v časopise:
NODULE INCEPTION Directly Targets Subunit Genes to Regulate Essential Processes of Root Nodule Development in. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003352
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003352
Souhrn
The interactions of legumes with symbiotic nitrogen-fixing bacteria cause the formation of specialized lateral root organs called root nodules. It has been postulated that this root nodule symbiosis system has recruited factors that act in early signaling pathways (common SYM genes) partly from the ancestral mycorrhizal symbiosis. However, the origins of factors needed for root nodule organogenesis are largely unknown. NODULE INCEPTION (NIN) is a nodulation-specific gene that encodes a putative transcription factor and acts downstream of the common SYM genes. Here, we identified two Nuclear Factor-Y (NF-Y) subunit genes, LjNF-YA1 and LjNF-YB1, as transcriptional targets of NIN in Lotus japonicus. These genes are expressed in root nodule primordia and their translational products interact in plant cells, indicating that they form an NF-Y complex in root nodule primordia. The knockdown of LjNF-YA1 inhibited root nodule organogenesis, as did the loss of function of NIN. Furthermore, we found that NIN overexpression induced root nodule primordium-like structures that originated from cortical cells in the absence of bacterial symbionts. Thus, NIN is a crucial factor responsible for initiating nodulation-specific symbiotic processes. In addition, ectopic expression of either NIN or the NF-Y subunit genes caused abnormal cell division during lateral root development. This indicated that the Lotus NF-Y subunits can function to stimulate cell division. Thus, transcriptional regulation by NIN, including the activation of the NF-Y subunit genes, induces cortical cell division, which is an initial step in root nodule organogenesis. Unlike the legume-specific NIN protein, NF-Y is a major CCAAT box binding protein complex that is widespread among eukaryotes. We propose that the evolution of root nodules in legume plants was associated with changes in the function of NIN. NIN has acquired functions that allow it to divert pathways involved in the regulation of cell division to root nodule organogenesis.
Zdroje
1. DownieJA, WalkerSA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2: 483–489.
2. MadsenEB, MadsenLH, RadutoiuS, OlbrytM, RakwalskaM, et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637–640.
3. RadutoiuS, MadsenLH, MadsenEB, FelleHH, UmeharaY, et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585–592.
4. ArrighiJF, BarreA, Ben AmorB, BersoultA, SorianoLC, et al. (2006) The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265–279.
5. RadutoiuS, MadsenLH, MadsenEB, JurkiewiczA, FukaiE, et al. (2007) LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26: 3923–3935.
6. SmitP, LimpensE, GeurtsR, FedorovaE, DolgikhF, et al. (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145: 183–191.
7. EhrhardtDW, WaisR, LongSR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673–681.
8. OldroydGED, DownieJA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59: 519–546.
9. KistnerC, ParniskeM (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7: 511–518.
10. HayashiT, BanbaM, ShimodaY, KouchiH, HayashiM, et al. (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 63: 141–154.
11. MadsenLH, TirichineL, JurkiewiczA, SullivanJT, HeckmannAB, et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Commun 1: 10.
12. GleasonC, ChaudhuriS, YangT, MuñozA, PoovaiahBW, et al. (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441: 1149–1152.
13. TirichineL, Imaizumi-AnrakuH, YoshidaS, MurakamiY, MadsenLH, et al. (2006) Deregulation of a Ca2+ calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441: 1153–1156.
14. TirichineL, SandalN, MadsenLH, RadutoiuS, AlbrektsenAS, et al. (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315: 104–107.
15. MurrayJD, KarasBJ, SatoS, TabataS, AmyotL, et al. (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315: 101–104.
16. HwangI, SheenJ, MullerB (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63: 353–80.
17. PletJ, WassonA, ArielF, Le SignorC, BakerD, et al. (2011) MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J 65: 622–633.
18. HeckmannAB, SandalN, BekAS, MadsenLH, JurkiewiczA, et al. (2011) Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant-Microbe Interact 24: 1385–1395.
19. SchauserL, RoussisA, StillerJ, StougaardJ (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402: 191–195.
20. CatoiraR, GaleraC, de BillyF, PenmetsaRV, JournetEP, et al. (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647–1665.
21. OldroydGED, LongSR (2003) Identification and characterization of Nodulation-Signaling Pathway 2, a Gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol 131: 1027–1032.
22. HeckmannAB, LombardoF, MiwaH, PerryJA, BunnewellS, et al. (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142: 1739–1750.
23. MurakamiY, MiwaH, Imaizumi-AnrakuH, KouchiH, DownieJA, et al. (2006) Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation. DNA Res 13: 255–265.
24. MailletF, PoinsotV, AndréO, Puech-PagésV, HaouyA, et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58–63.
25. LiuW, KohlenW, LilloA, Op den CampR, IvanovS, et al. (2011) Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell 23: 3853–3865.
26. KalóP, GleasonC, EdwardsA, MarshJ, MitraRM, et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786–1789.
27. SmitP, RaedtsJ, PortyankoV, DebelléF, GoughC, et al. (2005) NSP1 of the GRAS protein family is essential for Rhizobial Nod factor–induced transcription. Science 308: 1789–1791.
28. MarshJF, RakocevicA, MitraRM, BrocardL, SunJ, et al. (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144: 324–335.
29. MaekawaT, Maekawa-YoshikawaM, TakedaN, Imaizumi-AnrakuH, MurookaY, et al. (2009) Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J 58: 183–194.
30. HirschS, KimJ, MuñozA, HeckmannAB, DownieJA, et al. (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545–557.
31. MantovaniR (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239: 15–27.
32. CombierJP, FrugierF, de BillyF, BoualemA, El-YahyaouiF, 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.
33. SchauserL, WielochW, StougaardJ (2005) Evolution of NIN-like proteins in Arabidopsis, Rice, and Lotus japonicus. J Mol Evol 60: 229–237.
34. XieF, MurrayJD, KimJ, HeckmannAB, EdwardsA, et al. (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109: 633–638.
35. CastaingsL, CamargoA, PocholleD, GaudonV, TexierY, et al. (2008) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57: 426–435.
36. HaseloffJ (1999) GFP variants for multispectral imaging in living cells. Methods Cell Biol 58: 139–151.
37. HøgslundN, RadutoiuS, KrusellL, VoroshilovaV, HannahMA, et al. (2009) Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS ONE 4: e6556 doi:10.1371/journal.pone.0006556
38. ZanettiME, BlancoFA, BekerMP, BattagliaM, AguilarOM (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.
39. ElkonR, LinhartC, SharanR, ShamirR, ShilohY (2003) Genome-wide in silico identification of transcriptional regulators controlling the cell cycle in human cells. Genome Res 13: 773–780.
40. HuQ, LuJF, LuoR, SenS, MaitySN (2006) Inhibition of CBF/NF-Y mediated transcription activation arrests cells at G2/M phase and suppresses expression of genes activated at G2/M phase of the cell cycle. Nucleic Acids Res 34: 6272–6285.
41. GrskovicM, ChaivorapolC, Gaspar-MaiaA, LiH, Ramalho-SantosM (2007) Systematic identification of cis-regulatory sequences active in mouse and human embryonic stem cells. PLoS Genet 3: e145 doi:10.1371/journal.pgen.0030145
42. BenattiP, DolfiniD, ViganòA, RavoM, WeiszA, et al. (2011) Specific inhibition of NF-Y subunits triggers different cell proliferation defects. Nucleic Acids Res 39: 5356–5368.
43. MaekawaT, KusakabeM, ShimodaY, SatoS, TabataS, et al. (2008) Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol Plant-Microbe Interact 21: 375–382.
44. ThirumuruganT, ItoY, KuboT, SerizawaA, KurataN (2008) Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genomics 279: 279–289.
45. YanoK, YoshidaS, MüllerJ, SinghS, BanbaM, et al. (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105: 20540–20545.
46. MinamiE, KouchiH, CohnJR, OgawaT, StaceyG (1996) Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J 10: 23–32.
47. NiwaS, KawaguchiM, Imaizumi-AnrakuH, ChechetkaSA, IshizakaM, et al. (2001) Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. Mol Plant-Microbe Interact 14: 848–856.
48. TakedaN, OkamotoS, HayashiM, MurookaY (2005) Expression of LjENOD40 genes in response to symbiotic and non-symbiotic signals: LjENOD40–1 and LjENOD40–2 are differentially regulated in Lotus japonicus. Plant Cell Physiol 46: 1291–1298.
49. Op den CampRH, De MitaS, LilloA, CaoQ, LimpensE, et al. (2011) A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol 157: 2013–2022.
50. MortierV, Den HerderG, WhitfordR, Van de VeldeW, RombautsS, et al. (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153: 222–237.
51. PenmetsaRV, CookDR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527–530.
52. HeidstraR, YangWC, YalcinY, PeckS, EmonsAM, et al. (1997) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124: 1781–1787.
53. PenmetsaRV, FrugoliJA, SmithLS, LongSR, CookDR (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol 131: 998–1008.
54. LaursenNB, LarsenK, KnudsenJY, HoffmannHJ, PoulsenC, et al. (1994) A protein binding AT-rich sequence in the soybean leghemoglobin c3 promoter is a general cis element that requires proximal DNA elements to stimulate transcription. Plant Cell 6: 659–668.
55. FehlbergV, ViewegMF, DohmannEN, HohnjecN, PühlerA, et al. (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. J Exp Bot 56: 799–806.
56. AndriankajaA, Boisson-DernierA, FrancesL, SauviacL, JauneauA, et al. (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.
57. AsamizuE, ShimodaY, KouchiH, TabataS, SatoS (2008) A positive regulatory role for LjERF1 in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant Physiol 147: 2030–2040.
58. CombierJP, de BillyF, GamasP, NiebelA, RivasS (2008) Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev 22: 1549–1559.
59. HocherV, AlloisioN, AuguyF, FournierP, DoumasP, et al. (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant physiol 156: 700–711.
60. de SilvioA, ImbrianoC, MantovaniR (1999) Dissection of the NF-Y transcriptional activation potential. Nucleic Acids Res 27: 2578–2584.
61. DonatiG, GattaR, DolfiniD, FossatiA, CeribelliM, et al. (2008) An NF-Y-dependent switch of positive and negative histone methyl marks on CCAAT promoters. PLoS ONE 3: e2066 doi:10.1371/journal.pone.0002066
62. GurtnerA, FuschiP, MagiF, ColussiC, GaetanoC, et al. (2008) NF-Y dependent epigenetic modifications discriminate between proliferating and postmitotic tissue. PLoS ONE 3: e2047 doi:10.1371/journal.pone.0002047
63. YamamotoA, KagayaY, ToyoshimaR, KagayaM, TakedaS, et al. (2009) Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J 58: 843–856.
64. LiuJX, HowellSH (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.
65. BanbaM, GutjahrC, MiyaoA, HirochikaH, PaszkowskiU, et al. (2008) Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation signaling pathway. Plant Cell Physiol 49: 1659–1671.
66. YokotaK, SoyanoT, KouchiH, HayashiM (2010) Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice. Plant Cell Physiol 51: 1436–1442.
67. YokotaK, HayashiM (2011) Function and evolution of nodulation genes in legumes. Cell Mol. Life Sci 68: 1341–1351.
68. KöszegiD, JohnstonAJ, RuttenT, CzihalA, AltschmiedL, et al. (2011) Members of the RKD transcription factor family induce an egg cell-like gene expression program. Plant J 67: 280–291.
69. WakiT, HikiT, WatanabeR, HashimotoH, NakajimaK (2011) The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 21: 1277–1281.
70. HirschAM, LarueTA, DoyleJ (1997) Is the legume nodule a modified root or stem or an organ sui generis? Crit Rev Plant Sci 16: 361–392.
71. Díaz CL, Grønlund M, Schlaman HRM, Spaink HP (2005) Induction of hairy roots for symbiotic gene expression studies. In: Marquez AJ. Editor. Lotus japonicus Handbook. Dordrecht: Springer. pp. 261–277.
72. CurtisMD, GrossniklausU (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469.
73. WaadtR, SchmidtLK, LohseM, HashimotoK, BockR, et al. (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56: 505–516.
74. AoyamaT, ChuaNH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11: 605–612.
75. KarimiM, InzéD, DepickerA (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193–195.
76. FlemetakisE, KavroulakisN, QuaedvliegNE, SpainkHP, DimouM, et al. (2000) Lotus japonicus contains two distinct ENOD40 genes that are expressed in symbiotic, nonsymbiotic, and embryonic tissues. Mol Plant–Microbe Interact 13: 987–994.
77. WangH, TangW, ZhuC, PerrySE (2002) A chromatin immunoprecipitation (ChIP) approach to isolate genes regulated by AGL15, a MADS domain protein that preferentially accumulates in embryos. Plant J 32: 831–843.
78. LohmannGV, ShimodaY, NielsenMW, JørgensenFG, GrossmannC, et al. (2010) Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol Plant-Microbe Interact 23: 510–521.
79. RzhetskyA, NeiM (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9: 945–967.
80. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
81. Colón-CarmonaA, YouR, Haimovitch-GalT, DoernerP (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20: 503–508.
82. KouchiH, SekineM, HataS (1995) Distinct classes of mitotic cyclins are differentially expressed in the soybean shoot apex during the cell cycle. Plant Cell 7: 1143–1155.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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