Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca

New Phytologist

Volumn 209, Issue 1, 2016, Pages 86-93

  Chabaud, Mireille ^a   Gherbi, Hassen ^b   Pirolles, Elodie ^b   Vaissayre, Virginie ^b   Fournier, Joëlle ^a   Moukouanga, Daniel ^b   Franche, Claudine ^b   Bogusz, Didier ^b   Tisa, Louis S ^c   Barker, David G ^a   Svistoonoff, Sergio ^b,d,e  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY OF NEW HAMPSHIRE   (United States)

^d Centre de Recherche de Bel Air   (Senegal)

^e UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

Author keywords

Actinorhiza; Chitinase resistance; Frankia culture supernatant; NIN gene expression; Nuclear ca2+ spiking; Plant microbe signaling; Transgenic casuarina glauca

Indexed keywords

ACTINORHIZA; CALCIUM; ENZYME ACTIVITY; EVERGREEN TREE; GENE EXPRESSION; HOST PLANT; LEGUME; MICROBIAL ACTIVITY; NODULATION; POLYSACCHARIDE; RHIZOBACTERIUM; SIGNALING; TRANSGENIC PLANT;

CASUARINA GLAUCA; FRANKIA;

BACTERIAL PROTEIN; CALCIUM; CHITINASE; PHOTOPROTEIN; PLANT PROTEIN; RECOMBINANT PROTEIN; YELLOW CAMELEON 2.1;

ANGIOSPERM; CHEMICAL PHENOMENA; FRANKIA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MYCORRHIZA; NODULATION; PHYSIOLOGY; PLANT ROOT; REPORTER GENE; SYMBIOSIS; TRANSGENIC PLANT;

ANGIOSPERMS; BACTERIAL PROTEINS; CALCIUM; CHITINASE; FRANKIA; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LUMINESCENT PROTEINS; MYCORRHIZAE; PLANT PROTEINS; PLANT ROOT NODULATION; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT PROTEINS; SYMBIOSIS;

EID: 84949267238     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13732     Document Type: Article

References (28)

1. Beauchemin NJ, Furnholm T, Lavenus J, Svistoonoff S, Doumas P, Bogusz D, Laplaze L, Tisa LS. 2012. Casuarina root exudates alter the physiology, surface properties and plant infectivity of Frankia sp. strain CcI3. Applied and Environmental Microbiology 78: 575-580.
2. Cérémonie H, Cournoyer B, Maillet F, Normand P, Fernandez MP. 1998. Genetic complementation of rhizobial nod mutants with Frankia DNA: artefact or reality? Molecular and General Genetics 260: 115-119.
3. Cérémonie H, Debellé F, Fernandez MP. 1999. Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Canadian Journal of Botany 77: 1293-1301.
4. Chaia EE. 1998. Isolation of an effective strain of Frankia from nodules of Discaria trinervis (Rhamnaceae). Plant and Soil 205: 99-102.
5. Clavijo F, Diedhiou I, Vaissayre V, Brottier L, Acolatse J, Moukouanga D, Crabos A, Auguy F, Franche C, Gherbi H et al. 2015. The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytologist 208: 887-903.
6. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist 198: 190-202.
7. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche D 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.
8. Granqvist E, Sun J, Op den Camp R, Pujic P, Hill L, Normand P, Morris RJ, Downie JA, Geurts R, Oldroyd GED. 2015. Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and non-legumes. New Phytologist 207: 551-558.
9. 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.
10. Normand P, Lalonde M. 1982. Evaluation of Frankia strains isolated from provenances of two Alnus species. Canadian Journal of Microbiology 28: 1133-1142.
11. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N et al. 2007. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Research 17: 7-15.
12. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK. 1996. Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. International Journal of Systematic Bacteriology 46: 1-9.
13. Oldroyd GE. 2013. Speak, friend, and enter: signaling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology 11: 252-263.
14. Oldroyd GE, Downie JA. 2006. Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 9: 351-357.
15. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6: 763-775.
16. Pawlowski K, Sprent JI. 2008. Comparison between actinorhizal and legume symbiosis. In: Pawlowski K, Newton WE, eds. Nitrogen-fixing actinorhizal symbioses. Dordrecht, the Netherlands: Springer, 261-288.
17. Persson T, Battenberg K, Demina IV, Vigil-Stenman T, Vanden Heuvel B, Pujic P, Facciotti MT, Wilbanks EG, O'Brien A, Fournier P et al. 2015. Candidatus Frankia Datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS ONE 10: e0127630.
18. Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce DC, Detter C, Tapia R et al. 2011. Genome sequence of 'Candidatus Frankia datiscae' Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. Journal of Bacteriology 193: 7017-7018.
19. Roche P, Lerouge P, Ponthus C, Promé J-C. 1991. Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti-alfalfa symbiosis. Journal of Biological Chemistry 266: 10933-10940.
20. Santi C, Bogusz D, Franche C. 2013. Biological nitrogen fixation in non-legume plants. Annals of Botany 111: 743-767.
21. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiology 151: 1197-1206.
22. 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.
23. 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.
24. Svistoonoff S, Sy MO, 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.
25. Van Ghelue M, Løvaas E, Ring E, Solheim B. 1997. Early interactions between Alnus glutinosa and Frankia strain ArI3: production and specificity of root hair deformation factor(s). Physiologia Plantarum 99: 579-587.
26. Wall LG, Berry AM. 2008. Early interactions, infection and nodulation in actinorhizal symbiosis. In: Pawlowski K, Newton WE, eds. Nitrogen-fixing actinorhizal symbioses. Dordrecht, the Netherlands: Springer, 147-166.
27. 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.
28. Zhong C, Mansour S, Nambiar-Veetil M, Bogusz D, Franche C. 2013. Casuarina glauca: a model tree for basic research in actinorhizal symbiosis. Journal of Biosciences 38: 815-823.