Abstract
Casuarina glauca is a fast-growing multipurpose tree belonging to the Casuarinaceae family and native to Australia. It requires limited use of chemical fertilizers due to the symbiotic association with the nitrogen-fixing actinomycete Frankia and with mycorrhizal fungi, which help improve phosphorous and water uptake by the root system. C. glauca can grow in difficult sites, colonize eroded lands and improve their fertility, thereby enabling the subsequent growth of more demanding plant species. As a result, this tree is increasingly used for reforestation and reclamation of degraded lands in tropical and subtropical areas such as China and Egypt. Many tools have been developed in recent years to explore the molecular basis of the interaction between Frankia and C. glauca. These tools include in vitro culture of the host and genetic transformation with Agrobacterium, genome sequencing of Frankia and related studies, isolation of plant symbiotic genes combined with functional analyses (including knock-down expression based on RNA interference), and transcriptome analyses of roots inoculated with Frankia or Rhizophagus irregularis. These efforts have been fruitful since recent results established that many common molecular mechanisms regulate the nodulation process in actinorhizal plants and legumes, thus providing new insights into the evolution of nitrogen-fixing symbioses.
Similar content being viewed by others
References
Abdel-Lateif K, Vaissayre V, Gherbi H, Verries C, Meudec E, Perrine-Walker F, Cheynier V, Svistoonoff S, Franche C, Bogusz D and Hocher V 2013 The silencing of the Chalcone Synthase (CHS) gene in Casuarina glauca highlights the important role of flavonoids during nodulation. New Phytol. doi: 10.1111/nph.12326
Auguy F, Abdel-Lateif K, Doumas P, Badin P, Guerin V, Bogusz D and Hocher V 2011 Isoflavonoids pathway activation in actinorhizal symbioses. Funct. Plant Biol. 38 690–696
Badran DA, El-Lakany MH, El-Osta ML and Abu Gazia HA 1979 Breeding and improving casuarina trees. 1. Taxonomy and morphological characteristics of Casuarina spp. growing in Egypt. Alex. J. Agric. Res. 24 603–684
Benabdoun M, Nambiar-Veetil M, Imanishi L, Svistoonoff S, Ykhlef N, Gherbi H and Franche C 2011 Composite Actinorhizal Plants with Transgenic Roots for the Study of Symbiotic Associations with Frankia. J. Bot. doi:10.1155/2011/702947
Benson DR and Clawson ML 2000 Evolution of the actinorhizal plant symbioses ; in Prokaryotic nitrogen fixation: A model system for analysis of biological process (ed) EW Triplett (Wymondham: Horizon Scientific Press) pp 207–224
Berg RH and McDowell L 1987 Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136 104–117
Berry AM and Sunnel LA 1990 The infection process and nodule development ; in The biology of Frankia and Actinorhizal plants (eds) CR Schwintzer and JD Tjepkema (New York Academic Press) pp 61–81
Delaux P-M, Sejalon-Delmas N, Bécard G and Ané J-M 2013 Evolution of the plant-microbe symbiotic tool-kit. Trends Plant Sci. 18 298–304
Diem HG, Gauthier D and Dommergues Y 1983 An effective strain of Frankia from Casuarina. Can. J. Bot. 61 2815–2821.
Diem HG and Dommergues YR 1990 Current and potential uses and management of Casuarinaceae in the tropics and subtropics ; in The biology of Frankia and Actinorhizal plants (eds) CR Schwintzer and JD Tjepkema (New York: Academic Press) pp 317–342
Diouf D, Gherbi H, Franche C, Duhoux E and Bogusz D 1995 Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree. Mol. Plant-Microbe Interact. 8 532–537
Diouf D, Sy M-O, Gherbi H, Bogusz D and Franche C 2008 Casuarinaceae ; in Compendium of transgenic crop plants: transgenic forest tree species vol 9 (eds) CR Kole, RScorza and TC Hall (Oxford: Blackwell Publishing) pp 279–292
Duhoux E, Franche C, Bogusz D, Diouf D, Le VQ, Gherbi H, Sougoufara B, Le Roux C and Dommergues Y 1996 Casuarina and Allocasuarina ; in Biotechnology in Agriculture and Forestry vol 35 Tree V (ed) YPS Bajaj (Berlin: Springer-Verlag) pp 76–94
El-Lakany MH 1983 Breeding and improving of casuarina: a promising multipurpose tree for arid region in Egypt ; in Casuarina ecology, management and utilization (eds) SJ Midgley, JW Turnbull and RD Johnston (Melbourne: CSIRO) pp 58–65
El-Lakany MH, Omran TA and Shehata MS 1989 Variation in seed characteristics of Casuarina as affected by species, season of collection and position on tree crown. Intern. Tree Crops J. 5 237–245
Fernandez MP, Meugnier H, Grimont PAD and Bardin R 1989 Deoxyribonucleic acid relatedness among members of the genus Frankia. Int. J. Syst. Bacteriol. 39 424–429
Franche C, Diouf D, Le QV, N'Diaye A, Gherbi H, Bogusz D, Gobé C and Duhoux E 1997 Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens. Plant J. 11 897–904
Franche C, Diouf D, Laplaze L, Auguy F, Rio M, Frutz T, Duhoux E and Bogusz D 1998 The soybean (lbc3), Parasponia and Trema hemoglobin gene promoters retain their symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae. Implications for the evolution of hemoglobin genes and root nodule symbioses. Mol. Plant Microbe Interact. 11 887–894
Franche C and Bogusz D 2012 Signaling and communication in the actinorhizal symbiosis; in Signaling and communication in plant symbiosis (eds) S Perotto and F Baluska (Berlin: Springer) pp 73–92
Gherbi H, Franche C, Duhoux E and Bogusz D 1997 Cloning of a full-lengh symbiotic hemoglobin cDNA and in-situ localization of hemoglobin mRNA in Casuarina glauca and Allocasuarina verticillata root nodule. Physiol. Plant. 99 608–616
Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, et al. 2008a SymRK defines a common genetic basis for plant root endosymbioses with AM fungi, rhizobia and Frankia bacteria. Proc. Natl. Acad. Sci. USA 105 4928–32
Gherbi H, Nambiar-Veetil M, Zhong C, Félix J, Autran D, Girardin R, Vaissayre V, Auguy F, Bogusz D and Franche C 2008b Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Mol. Plant-Microbe Interact. 21 518–524
Hahn D 2008 Polyphasic taxonomy of the genus Frankia ; in Nitrogen-fixing actinorhizal symbioses. Nitrogen fixation: Origins, applications, and research progress, vol. 6 (eds) K Pawlowski, WE Newton (Dordrecht: Springer) pp 25–47
He X H and Critchley C 2008 Frankia nodulation, mycorrhization and interactions between Frankia and mycorrhizal fungi in Casuarina plants. in Mycorrhiza (ed) A Varma (Berlin Heidelberg: Springer-Verlag) pp 767–781
Hocher V, Auguy F, Argout X, Laplaze L, Franche C and Bogusz D 2006 Expressed sequence tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytol. 169 681–688
Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P and Bogusz D 2011 Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol. 156 700–711
Jacobsen-Lyon K, Jensen EO, Jorgensen J-E, Marcker KA, Peacock WJ and Dennis ES 1995 Symbiotic and non-symbiotic hemoglobin genes of Casuarina glauca. Plant Cell 7 213–222
Jefferson RA, Kavanagh TA and Bevan MW 1987 GUS fusion: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6 3901–3907
Kucho K, Kakoi K, Yamaura M, Higashi S, Uchiumi T and Abe M 2009 Transient transformation of Frankia by fusion marker genes in liquid culture. Microbes Environ 24 231–240
Kumagai H, Kinoshita E, Ridge RW and Kouchi H 2006 RNAi knock-down of ENOD40s leads to significant suppression of nodule formation in Lotus japonicus. Plant Cell Physiol. 47 1102–1111
Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix JJ, Auguy F, Bogusz D and Duhoux E 1999 Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules. Plant Physiol. 121 113–122
Laplaze L, Ribeiro A, Franche C, Duhoux E, Auguy F, Bogusz D and Pawlowski K 2000 Characterization of a Casuarina glauca nodule-specific subtilisin-like protease gene, a homologue of Alnus glutinosa ag12. Mol. Plant-Microbe Interact. 13 113–117
Laplaze L, Gherbi H, Duhoux E, Pawlowski K, Auguy F, Guermache F, Franche C and Bogusz D 2002 Symbiotic and nonsymbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca. Plant Mol. Biol. 49 81–92
Le QV, Bogusz D, Gherbi H, Lappartient A, Duhoux E and Franche C 1996 Agrobacterium tumefaciens gene transfer to Casuarina glauca, a tropical nitrogen-fixing tree. Plant Science 118 57–69
Liang Z and Chen B 1982 Vegetative propagation method on Pseudomonas solanacearum resistant clones of casuarina plants. Sci. Silvae Sinica 18 199–202
Nambiar-Veetil M, Nair DN, Selvakesavan RK, Jayaraj RSC, Roopesh M, Prabhu SJ, Balasubramanian A, Venkatachalam R, et al. 2011 Development of an in silico gene bank for plant abiotic stresses: towards its utilization for molecular analysis of salt tolerant and susceptible Casuarina equisetifolia clones ; in Improving smallholder livelihoods through improved casuarina productivity (eds) C Zhong, K Pinyopusarerk, A Kalinganire and C Franche (China Forestry Publishing House, Beijing) pp144–151
Mansour SR 2003 Survival of Frankia strains under different soil condition. Online J. Biol. Sci. 3 618–626
Mansour SR and Megahed M 2002 Interaction of soil and different Frankia strains on nodulation and mass production of three Casuarina species. Eg. J. Microbiol. 37 323–342
Narayanan C, Dudzinski M, Sharma JK and Mohanan C 1996 The Extent, recognition and management of blister bark disease; in Recent Casuarina research and development (Eds) K Pinyopusarerk, JW Turnbull and SJ Midgley (Canberra, Australia: CSIRO Forestry and Forest Products) pp 74–79
Narayanan C, Sharma JK and Minter DW 2003 Subramanianospora vesiculosa: a hyphomycete causing wilt disease of Casuarina equisetifolia. Indian Phytopathology 56 159–163
National Research Council 1984 Casuarinas: nitrogen-fixing trees for adverse sites (Washington: National Academic Press)
Normand P and Fernandez MP 2009 Evolution and diversity of Frankia. Mol. Monogr. 8 103–125
Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L and Misra AK 1996 Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int. J. Syst. Bacteriol. 46 1–9
Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, et al. 2007a Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res. 17 7–15
Normand P, Queiroux C, Tisa LS, Benson DR, Rouy Z, Cruveiller S and Medigue C 2007b Exploring the genomes of Frankia. Physiol. Plant. 130 331–343
Obertello M, Wall L, Laplaze L, Nicole M. Auguy F, Gherbi H, Bogusz D and Franche C 2007 Functional analysis of the metallothionein gene CgMT1 isolated from the actinorhizal tree Casuarina glauca. Mol. Plant-Microbe Interact. 20 1231–1240
Oldroyd ED 2013 Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Com. 11 252–263
Olivares J, Bedmar EJ and Sanjuan J 2013 Biological nitrogen fixation in the context of global change. Mol. Plant-Microbe Interact. 26 486–494
Pappas KM and Cevallos MA 2011 Plasmids of the Rhizobiaceae and Their Role in Interbacterial and Transkingdom Interactions. Soil Biol. 23 295–337
Parnishke M 2008 Arbuscular mycorrhiza : the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6 763–775
Pawlowski K and Demchenko KN 2012 The diversity of actinorhizal symbiosis. Protoplasma doi: 10.1007/s00709–012–0388–4.
Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, et al. 2007 Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiol. 144 1852–1862
Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T and Bennett MJ 2009 Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14 399–408
Perrine-Walker F, Doumas F, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, et al. 2010 Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiol. 154 1372–1380
Rawnsley T and Tisa LS 2007 Development of a physical map for three Frankia strains and a partial genetic map for Frankia EuI1c. Physiol. Plant. 130 427–439
Sen A, Sur S, Bothra AK, Benson DR, Normand P and Tisa LS 2008 The implication of life style on codon usage patterns and predicted highly expressed genes for three Frankia genomes. Anton. Van Leeuw. 93 335–46
Santi C, Swistoonoff S, Constans L, Auguy F, Duhoux E, Bogusz D and Franche C 2002 Choosing a reporter for gene expression studies in transgenic actinorhizal plants of the Casuarinaceae family. Plant Soil 254 229–237
Santi C, von Groll U, Chiurazzi M, Auguy F, Bogusz D, Franche C and Pawlowski K 2003 Comparison of nodule induction in legume and actinorhizal symbiosis : the induction of actinorhizal nodules does not involve ENOD40. Mol. Plant-Microbe Interact. 16 808–816
Santi C, Bogusz D and Franche C 2013 Nitrogen fixation in non legumes. Ann. Bot. 111 743–767
Smouni A, Laplaze L, Bogusz D, Auguy F, Duhoux E and Franche C 2002 The 35S promoter is not constitutively expressed in the transgenic tropical actinorhizal tree, Casuarina glauca. Funct. Plant Biol. 29 649–656
Svistoonoff S, Laplaze L, Auguy F, Runions CJ, Duponnois R, Haseloff J, Franche C and 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. Mol. Plant-Microbe Interact. 16 600–607
Svistoonoff S, Laplaze L, Liang J, Ribeiro A, Gouveia MC, Auguy F, Fevereiro P, Franche C and Bogusz D 2004 Infection-related activation of the cg12 promoter is conserved between actinorhizal and legume-rhizobia root nodule symbioses. Plant Physiol. 136 3191–3197
Svistoonoff S, Gherbi H, Nambiar-Veetil M, Zhong C, Michalak Z, Laplaze L, Vaissayre V, Auguy F, et al. 2010a Contribution of transgenic Casuarinaceae to our knowledge of the actinorhizal symbioses. Symbiosis 50 3–11
Svistoonoff S, Sy M-O, Diagne N, Barker D, Bogusz D and Franche C 2010b Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene during actinorhizal root nodulation. Mol. Plant-Microbe Interact. 23 740–747
Svistoonoff S, Benabdoun F-M, Nambiar-Veetil M, Imanishi L, Vaissayre V, Cesari S, Diagne N, Hocher V, et al. 2013 The independent acquisition of root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. PLoS ONE 8 e64515
Sy M-O, Constans L, Obertello M, Geney C, Laplaze L, Auguy F, Bogusz D and Franche C 2007 The PsEnod12B promoter from the early nodulin gene of Pisum sativum does not drive gene expression during the early stages of actinorhizal nodule development in transgenic Casuarinaceae. Plant Soil 281 279–287
Tromas A, Parizot B, Diagne N, Champion C, Hocher V, Cissoko M, Crabos A, Lahouse B, Bogusz D, Laplaze L and Svistoonoff S 2012 Heart of endosymbioses: transcriptomics reveals a conserved genetic programme among arbuscular mycorrhizal, actinorhizal, and legume-Rhizobium symbioses. PLoS ONE 7 e44742
Turnbull JW and Martensz PN 1982 Seed production, collection and germination of Casuarinaceae. Austr. For. Res. 12 281–294
Venkateshwaran M, Volkening JD, Sussman MR and Ané J-M 2012 Symbiosis and the social network of higher plants. Curr. Opin. Plant Biol. 16 1–10
Wall LG and Berry AM 2008 Early interactions, infection and nodulation in actinorhizal symbiosis. in Nitrogen-fixing actinorhizal symbioses (eds) K Pawlowski and WE (Newton Dordrecht: Springer) pp 147–166
Zhong C and Zhang Y 2003 Introduction, cultivation and management of casuarinas in China. China Forest. Sci. Technol. 17 3–5
Zhong C, Zhang Y, Chen Y, Jiang Q, Chen Z, Liang J, Pinyopusarerk K, Franche C and Bogusz D 2010 Casuarina research in China. Symbiosis 1 107–114
Acknowledgements
Research on actinorhizal plants was supported by the Research Institute of Tropical Forestry, the Chinese Academy of Forestry, the Suez Canal University, the Institut of Forest Genetics and Tree Breeding, the Institute de Recherche pour le Développement (IRD), the Montpellier University 2, the Agence Nationale de la Recherche (ANR) Blanc project NewNod (ANR-06-BLAN-0095) and SESAM (BLAN-1708-01), and the PHC-IMHOTEP 27467SA. We thank Jocelyne Bonneau (IRD) for help with the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
[Zhong C, Mansour S, Nambiar-Veetil M, Bogusz D and Franche C 2013 Casuarina glauca: A model tree for basic research in actinorhizal symbiosis. J. Biosci. 38 1–9] DOI10.1007/s12038-013-9370-3
Rights and permissions
About this article
Cite this article
Zhong, C., Mansour, S., Nambiar-Veetil, M. et al. Casuarina glauca: A model tree for basic research in actinorhizal symbiosis. J Biosci 38, 815–823 (2013). https://doi.org/10.1007/s12038-013-9370-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-013-9370-3