The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals

New Phytologist

Volumn 208, Issue 3, 2015, Pages 887-903

  Clavijo, Fernando ^a   Diedhiou, Issa ^a,b,c   Vaissayre, Virginie ^a   Brottier, Laurent ^a,d   Acolatse, Jennifer ^a   Moukouanga, Daniel ^a   Crabos, Amandine ^a   Auguy, Florence ^a   Franche, Claudine ^a   Gherbi, Hassen ^a,d   Champion, Antony ^a,b,c   Hocher, Valerie ^a,d   Barker, David ^e   Bogusz, Didier ^a   Tisa, Louis S ^f   Svistoonoff, Sergio ^a,b,c,d  

^a University of Montpellier 2   (France)

^b Centre de Recherche de Bel Air   (Senegal)

^c UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^d UNIV MONTPELLIER   (France)

^e LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^f UNIVERSITY OF NEW HAMPSHIRE   (United States)

Author keywords

Actinorhiza; Biological nitrogen fixation; Mycorrhiza; Nodule inception; Plant microbe signalling; Root hair deformation; Root nodule symbioses

Indexed keywords

ACTINORHIZA; DICOTYLEDON; GENE EXPRESSION; INFECTIVITY; LEGUME; MYCORRHIZA; NITROGEN; NITROGEN FIXATION; NODULATION; PHENOTYPE; PHYLOGENETICS; RHIZOBACTERIUM; ROOT SYSTEM; SYMBIONT; TRANSGENIC PLANT;

BACTERIA (MICROORGANISMS); CASUARINA; CASUARINA GLAUCA; FRANKIA;

NIN PROTEIN, LOTUS JAPONICUS; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANGIOSPERM; FABACEAE; FRANKIA; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; NODULATION; PHYSIOLOGY; SEQUENCE HOMOLOGY; SYMBIOSIS;

AMINO ACID SEQUENCE; ANGIOSPERMS; FABACEAE; FRANKIA; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PLANT PROTEINS; PLANT ROOT NODULATION; ROOT NODULES, PLANT; SEQUENCE HOMOLOGY, AMINO ACID; SYMBIOSIS;

EID: 84945475060     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13506     Document Type: Article

References (66)

1. Abdel-Lateif K, Vaissayre V, Gherbi H, Verries C, Meudec E, Perrine-Walker F, Cheynier V, Svistoonoff S, Franche C, Bogusz D et al. 2013. Silencing of the chalcone synthase gene in Casuarina glauca highlights the important role of flavonoids during nodulation. New Phytologist 199: 1012-1021.
2. 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.
3. Boisnard-Lorig C, Colon-Carmona A, Bauch M, Hodge S, Doerner P, Bancharel E, Dumas C, Haseloff J, Berger F. 2001. Dynamic analyses of the expression of the HISTONE:YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 13: 495.
4. Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14: 695-700.
5. Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, Batagov AO, Sandal N, Mortensen A, Schauser L, Ellis N et al. 2003. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiology 131: 1009-1017.
6. 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: 1647-1665.
7. Cullimore JV, Ranjeva R, Bono JJ. 2001. Perception of lipo-chitooligosaccharidic Nod factors in legumes. Trends in Plant Science 6: 24-30.
8. Curtis MD, Grossniklaus U. 2003. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133: 462-469.
9. Demina IV, Persson T, Santos P, Plaszczyca M, Pawlowski K. 2013. Comparison of the nodule vs. root transcriptome of the actinorhizal plant Datisca glomerata: actinorhizal nodules contain a specific class of defensins. PLoS ONE 8: e72442.
10. Diagne N, Escoute J, Lartaud M, Verdeil JL, Franche C, Kane A, Bogusz D, Diouf D, Duponnois R, Svistoonoff S. 2011. Uvitex2B: a rapid and efficient stain for detection of arbuscular mycorrhizal fungi within plant roots. Mycorrhiza 21: 315-321.
11. Diédhiou I, Tromas A, Cissoko M, Gray K, Parizot B, Crabos A, Alloisio N, Fournier P, Carro L, Svistoonoff S et al. 2014. Identification of potential transcriptional regulators of actinorhizal symbioses in Casuarina glauca and Alnus glutinosa. BMC Plant Biology 14: 342.
12. Diouf D, Gherbi H, Prin Y, Franche C, Duhoux E, Bogusz D. 1995. Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree. Molecular Plant-Microbe Interactions 8: 532-537.
13. Doyle JJ. 2011. Phylogenetic perspectives on the origins of nodulation. Molecular Plant-Microbe Interactions 24: 1289-1295.
14. Esseling JJ, Emons AMC. 2004. Dissection of Nod factor signalling in legumes: cell biology, mutants and pharmacological approaches. Journal of Microscopy 214: 104-113.
15. Esseling JJ, Lhuissier FGP, Emons AMC. 2004. A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16: 933-944.
16. Fliegmann J, Canova S, Lachaud C, Uhlenbroich S, Gasciolli V, Pichereaux C, Rossignol M, Rosenberg C, Cumener M, Pitorre D et al. 2013. Lipo-chitooligosaccharidic symbiotic signals are recognized by LysM Receptor-Like Kinase LYR3 in the legume Medicago truncatula. ACS Chemical Biology 8: 1900-1906.
17. Fox J. 2005. The R Commander: a basic-statistics graphical user interface to R. Journal of Statistical Software 14: 1-42.
18. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C et al. 2008. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proceedings of the National Academy of Sciences, USA 105: 4928-4932.
19. Gleave AP. 1992. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20: 1203-1207.
20. Helliwell CA, Wesley SV, Wielopolska AJ, Waterhouse PM. 2002. High-throughput vectors for efficient gene silencing in plants. Functional Plant Biology 29: 1217-1225.
21. Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P et al. 2011. Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiology 156: 700-711.
22. Hocher V, Auguy F, Argout X, Laplaze L, Franche C, Bogusz D. 2006. Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytologist 169: 681-688.
23. Jouanin L, Tourneur J, Tourneur C, Casse-Delbart F. 1986. Restriction maps and homologies of the three plasmids of Agrobacterium rhizogenes strain A4. Plasmid 16: 124-134.
24. 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. Molecular Plant-Microbe Interactions 14: 737-748.
25. Karimi M, Bleys A, Vanderhaeghen R, Hilson P. 2007. Building blocks for plant gene assembly. Plant Physiology 145: 1183-1191.
26. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772-780.
27. Konishi M, Yanagisawa S. 2013. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nature Communications 4: 1617.
28. Kosuta S, Held M, Hossain MS, Morieri G, MacGillivary A, Johansen C, Antolín-Llovera M, Parniske M, Oldroyd GED, Downie AJ. 2011. Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant Journal 67: 929-940.
29. Kumagai H, Kouchi H. 2003. Gene silencing by expression of hairpin RNA in Lotus japonicus roots and root nodules. Molecular Plant-Microbe Interactions 16: 663-668.
30. Laplaze L, Duhoux E, Franche C, Frutz T, Svistoonoff S, Bisseling T, Bogusz D, Pawlowski K. 2000. Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells. Molecular Plant-Microbe Interactions 13: 107-112.
31. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J. 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781-784.
32. Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E, Colot V, Meyer C, Krapp A. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications 4: 1713.
33. Markmann K, Giczey G, Parniske M. 2008. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biology 6: e68.
34. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GED. 2007. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiology 144: 324-335.
35. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115: 495-501.
36. Oldroyd GED. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews. Microbiology 11: 252-263.
37. Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JSS, Kudrna D, Wing R, Untergasser A et al. 2011. LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331: 909-912.
38. Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D et al. 2007. Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiology 144: 1852-1862.
39. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N et al. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585-592.
40. Schauser L, Roussis A, Stiller J, Stougaard J. 1999. A plant regulator controlling development of symbiotic root nodules. Nature 402: 191-195.
41. Schauser L, Wieloch W, Stougaard J. 2005. Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. Journal of Molecular Evolution 60: 229-237.
42. Sheen J. 2002. A transient expression assay using Arabidopsis mesophyll protoplasts. [WWW document] URL http://genetics.mgh.harvard.edu/sheenweb/ [accessed 23 December 2013].
43. 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.
44. Smith SA, Beaulieu JM. 2009. Life history influences rates of climatic niche evolution in flowering plants. Proceedings of the Royal Society B: Biological Sciences 276: 4345-4352.
45. Smith SA, Donoghue MJ. 2008. Rates of molecular evolution are linked to life history in flowering plants. Science 322: 86-89.
46. Smouni A, Laplaze L, Bogusz D, Guermache F, Auguy F, Duhoux E, Franche C. 2002. The 35S promoter is not constitutively expressed in the transgenic tropical actinorhizal tree, Casuarina glauca. Functional Plant Biology 29: 649-656.
47. Soyano T, Hayashi M. 2014. Transcriptional networks leading to symbiotic nodule organogenesis. Current Opinion in Plant Biology 20: 146-154.
48. Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M. 2014. NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proceedings of the National Academy of Sciences, USA 111: 14607-14612.
49. Soyano T, Kouchi H, Hirota A, Hayashi M. 2013. NODULE INCEPTION directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genetics 9: e1003352.
50. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
51. Suzaki T, Kawaguchi M. 2014. Root nodulation: a developmental program involving cell fate conversion triggered by symbiotic bacterial infection. Current Opinion in Plant Biology 21: 16-22.
52. Suzuki W, Konishi M, Yanagisawa S. 2013. The evolutionary events necessary for the emergence of symbiotic nitrogen fixation in legumes may involve a loss of nitrate responsiveness of the NIN transcription factor. Plant Signaling & Behavior 8: e25975.
53. Svistoonoff S, Benabdoun FM, Nambiar-Veetil M, Imanishi L, Vaissayre V, Cesari S, Diagne N, Hocher V, de Billy F, Bonneau J et al. 2013. The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. PLoS ONE 8: e64515.
54. Svistoonoff S, Hocher V, Gherbi H. 2014. Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation? Current Opinion in Plant Biology 20: 11-18.
55. Svistoonoff S, Laplaze L, Auguy F, Runions J, Duponnois R, Haseloff J, Franche C, Bogusz D. 2003. cg12 expression is specifically linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development. Molecular Plant-Microbe Interactions 16: 600-607.
56. Svistoonoff S, Laplaze L, Liang J, Ribeiro A, Gouveia MC, Auguy F, Fevereiro P, Franche C, Bogusz D. 2004. Infection-related activation of the cg12 promoter is conserved between actinorhizal and legume-rhizobia root nodule symbiosis. Plant Physiology 136: 3191-3197.
57. Svistoonoff S, Sy M-O, Diagne N, Barker DG, Bogusz D, Franche C. 2010. Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation. Molecular Plant-Microbe Interactions 23: 740-747.
58. Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564-577.
59. Torrey JG. 1976. Initiation and development of root nodules of Casuarina (Casuarinaceae). American Journal of Botany 63: 335-344.
60. Vancanneyt G, Schmidt R, O'Connor-Sanchez A, Willmitzer L, Rocha-Sosa M. 1990. Construction of an intron-containing marker gene: splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation. Molecular & General Genetics 220: 245-250.
61. Vierheilig H, Coughlan AP, Wyss U, Piché Y. 1998. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64: 5004-5007.
62. Yokota K, Hayashi M. 2011. Function and evolution of nodulation genes in legumes. Cellular and Molecular Life Sciences 68: 1341-1351.
63. Yokota K, Soyano T, Kouchi H, Hayashi M. 2010. Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice. Plant & Cell Physiology 51: 1436-1442.
64. Yoo S-D, Cho Y-H, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2: 1565-1572.
65. 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 Physiology 165: 747-758.
66. Zhang Z, Lopez MF, Torrey JG. 1984. A comparison of cultural characteristics and infectivity of Frankia isolates from root nodules of Casuarina species. Plant and Soil 78: 79-90.