The symbiosis-related ERN transcription factors act in concert to coordinate rhizobial host root infection

Plant Physiology

Volumn 171, Issue 2, 2016, Pages 1037-1054

  Cerri, Marion R ^a,e   Frances, Lisa ^a   Kelner, Audrey ^a   Fournier, Joëlle ^a   Middleton, Patrick H ^b   Auriac, Marie Christine ^a   Mysore, Kirankumar S ^c   Wen, Jiangqi ^c   Erard, Monique ^d   Barker, David G ^a   Oldroyd, Giles E ^b   de Carvalho Niebel, Fernanda ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b JOHN INNES CENTRE   (United Kingdom)

^c Samuel Roberts Noble Foundation   (United Kingdom)

^d INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ALLELE; AMINO ACID SEQUENCE; BARREL MEDIC; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; MYCORRHIZA; NITROGEN FIXATION; NODULATION; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PHYSIOLOGY; PLANT DISEASE; PLANT EPIDERMIS; PLANT ROOT; PROMOTER REGION; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS; ULTRASTRUCTURE;

ALLELES; AMINO ACID SEQUENCE; BASE SEQUENCE; GENE EXPRESSION REGULATION, PLANT; MEDICAGO TRUNCATULA; MUTATION; MYCORRHIZAE; NITROGEN FIXATION; ORGANOGENESIS; PLANT DISEASES; PLANT EPIDERMIS; PLANT PROTEINS; PLANT ROOTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RHIZOBIUM; ROOT NODULES, PLANT; SIGNAL TRANSDUCTION; SYMBIOSIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84973618747     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00230     Document Type: Article

References (76)

1. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17: 5484-5496
2. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, 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
3. Antolín-Llovera M, Ried MK, Parniske M (2014) Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE ectodomain promotes complex formation with Nod factor receptor 5. Curr Biol 24: 422-427
4. Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé JC, Dénarié 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
5. Arrighi JF, Godfroy O, de Billy F, Saurat O, Jauneau A, Gough C (2008) The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection. Proc Natl Acad Sci USA 105: 9817-9822
6. Berrabah F, Bourcy M, Eschstruth A, Cayrel A, Guefrachi I, Mergaert P, Wen J, Jean V, Mysore KS, Gourion B, et al (2014) A nonRD receptorlike kinase prevents nodule early senescence and defense-like reactions during symbiosis. New Phytol 203: 1305-1314
7. Bourcy M, Brocard L, Pislariu CI, Cosson V, Mergaert P, Tadege M, Mysore KS, Udvardi MK, Gourion B, Ratet P (2013) Medicago truncatula DNF2 is a PI-PLC-XD-containing protein required for bacteroid persistence and prevention of nodule early senescence and defense-like reactions. New Phytol 197: 1250-1261
8. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ, et al (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci USA 109: 13859-13864
9. Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ané JM, et al (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci USA 108: 14348-14353
10. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12: 1647-1666
11. Cerri MR, Frances L, Laloum T, Auriac MC, Niebel A, Oldroyd GE, Barker DG, Fournier J, 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
12. Charpentier M, Oldroyd G (2010) How close are we to nitrogen-fixing cereals? Curr Opin Plant Biol 13: 556-564
13. Charron D, Pingret JL, Chabaud M, Journet EP, Barker DG (2004) Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression. Plant Physiol 136: 3582-3593
14. Chen DS, Liu CW, Roy S, Cousins D, Stacey N, Murray JD (2015) Identification of a core set of rhizobial infection genes using data from single cell-types. Front Plant Sci 6: 575
15. Czaja LF, Hogekamp C, Lamm P, Maillet F, Martinez EA, Samain E, Dénarié J, Küster H, Hohnjec N (2012) Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol 159: 1671-1685
16. Delaux P-M, Bécard G, Combier J-P (2013) NSP1 is a component of the Myc signaling pathway. New Phytol 199: 59-65
17. Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535
18. Dupont L, Alloing G, Pierre O, El Msehli S, Hopkins J, Hérouart D, Frendo P (2012) The legume root nodule: from symbiotic nitrogen fixation to senescence. In Senescence, Ed. Tetsuji Nagata, Intech Publisher doi: 10.5772/34438: 137-157
19. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673-681
20. Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG (2015) Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol 167: 1233-1242
21. Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29: 593-617
22. Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (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. Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545-557
24. Hogekamp C, Küster H (2013) A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis. BMC Genomics 14: 306
25. Horváth B, Yeun LH, Domonkos A, Halász G, Gobbato E, Ayaydin F, Miró K, Hirsch S, Sun J, Tadege M, et al (2011) Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant Microbe Interact 24: 1345-1358
26. Hossain MS, Umehara Y, Kouchi H (2006) A novel fix- symbiotic mutant of Lotus japonicus, Ljsym105, shows impaired development and premature deterioration of nodule infected cells and symbiosomes. Mol Plant Microbe Interact 19: 780-788
27. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, 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
28. Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, et al (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786-1789
29. Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszynski A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH, et al (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523: 308-312
30. Kumagai H, Hakoyama T, Umehara Y, Sato S, Kaneko T, Tabata S, Kouchi H (2007) A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiol 143: 1293-1305
31. Laloum T, Baudin M, Frances L, Lepage A, Billault-Penneteau B, Cerri MR, Ariel F, Jardinaud MF, Gamas P, de Carvalho-Niebel F, et al (2014) Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis. Plant J 79: 757-768
32. Laporte P, Lepage A, Fournier J, Catrice O, Moreau S, Jardinaud MF, Mun JH, Larrainzar E, Cook DR, Gamas P, et al (2014) The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection. J Exp Bot 65: 481-494
33. Larrainzar E, Riely BK, Kim SC, Carrasquilla-Garcia N, Yu H-J, Hwang H-J, Oh M, Kim GB, Surendrarao AK, Chasman D, et al (2015) Deep sequencing of the Medicago truncatula root transcriptome reveals a massive and early interaction between nodulation factor and ethylene signals. Plant Physiol 169: 233-265
34. Le Signor C, Savois V, Aubert G, Verdier J, Nicolas M, Pagny G, Moussy F, Sanchez M, Baker D, Clarke J, et al (2009) Optimizing TILLING populations for reverse genetics in Medicago truncatula. Plant Biotechnol J 7: 430-441
35. Libault M, Joshi T, Benedito VA, Xu D, Udvardi MK, Stacey G (2009) Legume transcription factor genes: what makes legumes so special? Plant Physiol 151: 991-1001
36. Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199: 639-649
37. Lindner SE, De Silva EK, Keck JL, LlinásM(2010) Structural determinants of DNA binding by a P. falciparum ApiAP2 transcriptional regulator. J Mol Biol 395: 558-567
38. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1: 10
39. Magori S, Kawaguchi M (2009) Long-distance control of nodulation: molecules and models. Mol Cells 27: 129-134
40. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63
41. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144: 324-335
42. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rougé P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, et al (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20: 912-921
43. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, et al (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19: 1221-1234
44. Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie JA, Kawaguchi M, Kawasaki S (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
45. Murray JD (2011) Invasion by invitation: rhizobial infection in legumes. Mol Plant Microbe Interact 24: 631-639
46. Murray JD, Muni RR, Torres-Jerez I, Tang Y, Allen S, Andriankaja M, Li G, Laxmi A, Cheng X, Wen J, et al (2011) Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 65: 244-252
47. Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11: 252-263
48. Ovchinnikova E, Journet EP, Chabaud M, Cosson V, Ratet P, Duc G, Fedorova E, Liu W, den Camp RO, Zhukov V, et al (2011) IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago Spp. Mol Plant Microbe Interact 24: 1333-1344
49. Pandey B, Sharma P, Tyagi C, Goyal S, Grover A, Sharma I (2015) Structural modeling and molecular simulation analysis of HvAP2/EREBP from barley. J Biomol Struct Dyn 19: 1-17
50. Pislariu CI, Murray JD, Wen J, Cosson V, Muni RR, Wang M, Benedito VA, Andriankaja A, Cheng X, Jerez IT, et al (2012) A Medicago truncatula tobacco retrotransposon insertion mutant collection with defects in nodule development and symbiotic nitrogen fixation. Plant Physiol 159: 1686-1699
51. Popp C, Ott T (2011) Regulation of signal transduction and bacterial infection during root nodule symbiosis. Curr Opin Plant Biol 14: 458-467
52. Quandt HJ, Puhler A, Boer 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
53. Ratet P, Porcedu A, Tadege M, Myosore K (2010). Insertional mutagenesis in Medicago truncatula using Tnt1 retrotransposon. In Medicago truncatula Handbook. http://www.noble.org/Global/medicagohandbook/pdf/InsertionalMutagenesis.pdf
54. Roux B, Rodde N, Jardinaud MF, Timmers T, Sauviac L, Cottret L, Carrère S, Sallet E, Courcelle E, Moreau S, 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
55. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682
56. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675
57. Shoji T, Mishima M, Hashimoto T (2013) Divergent DNA-binding specificities of a group of ETHYLENE RESPONSE FACTOR transcription factors involved in plant defense. Plant Physiol 162: 977-990
58. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, Barker DG (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197-1206
59. Singh S, Katzer K, Lambert J, Cerri M, Parniske M (2014) CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15: 139-152
60. Singh S, Parniske M (2012) Activation of calcium- and calmodulindependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr Opin Plant Biol 15: 444-453
61. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791
62. Soyano T, Hayashi M (2014) Transcriptional networks leading to symbiotic nodule organogenesis. Curr Opin Plant Biol 20: 146-154
63. Soyano T, Shimoda Y, Hayashi M (2015) NODULE INCEPTION antagonistically regulates gene expression with nitrate in Lotus japonicus. Plant Cell Physiol 56: 368-376
64. Suganuma N, Nakamura Y, Yamamoto M, Ohta T, Koiwa H, Akao S, Kawaguchi M (2003) The Lotus japonicus Sen1 gene controls rhizobial differentiation into nitrogen-fixing bacteroids in nodules. Mol Genet Genomics 269: 312-320
65. Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M, et al (2008) Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J 54: 335-347
66. Tripathi P, Rabara RC, Choudhary MK, Miller MA, Huang YS, Shen QJ, Blachon S, Rushton PJ (2015) The interactome of soybean GmWRKY53 using yeast 2-hybrid library screening to saturation. Plant Signal Behav 10: e1028705
67. van de Velde W, Guerra JC, De Keyser A, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141: 711-720
68. Vernié T, Kim J, Frances L, Ding Y, Sun J, Guan D, Niebel A, Gifford M, de Carvalho-Niebel F, Oldroyd GED (2015) The NIN transcription factor coordinates diverse nodulation programmes in different tissues of the root. Plant Cell 27: 3410-3424
69. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64: 5004-5007
70. Xiao TT, Schilderink S, Moling S, Deinum EE, Kondorosi E, Franssen H, Kulikova O, Niebel A, Bisseling T (2014) Fate map of Medicago truncatula root nodules. Development 141: 3517-3528
71. Yamaguchi N, Winter CM, Wu MF, Kwon CS, William DA, Wagner D (2014) PROTOCOLS: chromatin immunoprecipitation from Arabidopsis tissues. Arabidopsis Book 12: e0170
72. Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2012) DNAbinding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18: 267-276
73. Yano K, Yoshida S, Müller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, et al (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105: 20540-20545
74. Yoro E, Suzaki T, Toyokura K, Miyazawa H, Fukaki H, 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
75. Young ND, Debellé F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H, et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524
76. Zhao Y, Cheng S, Song Y, Huang Y, Zhou S, Liu X, Zhou DX (2015) The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell 27: 2469-2483