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Plant function and evolutionary biology
REVIEW

Progress on research on actinorhizal plants

Katharina Pawlowski A E , Didier Bogusz B , Ana Ribeiro C and Alison M. Berry D
+ Author Affiliations
- Author Affiliations

A Department of Botany, Stockholm University, 10691 Stockholm, Sweden.

B Groupe Rhizogenèse, Unité Mixte de Recherche Diversité et Adaptation des Plantes Cultivées, Institut de Recherche pour le Développement, 911 avenue Agropolis, BP 5045, 34394 Montpellier Cedex 5, France.

C ECO-BIO/Tropical Research Institute, Av. da República (EAN), Quinta do Marquês, 2784-505 Oeiras, Portugal.

D Department of Plant Sciences, University of California, Davis, CA 95616, USA.

E Corresponding author. Email: pawlowski@botan.su.se

This paper originates from a presentation at the 16th International Meeting on Frankia and Actinorhizal Plants, Oporto, Portugal, 5–8 September 2010.

Functional Plant Biology 38(9) 633-638 https://doi.org/10.1071/FP11066
Submitted: 10 March 2011  Accepted: 10 May 2011   Published: 16 August 2011

Abstract

In recent years, our understanding of the plant side of actinorhizal symbioses has evolved rapidly. No homologues of the common nod genes from rhizobia were found in the three Frankia genomes published so far, which suggested that Nod factor-like molecules would not be used in the infection of actinorhizal plants by Frankia. However, work on chimeric transgenic plants indicated that Frankia Nod factor equivalents signal via the same transduction pathway as rhizobial Nod factors. The role of auxin in actinorhizal nodule formation differs from that in legume nodulation. Great progress has been made in the analysis of pathogenesis-related and stress-related gene expression in nodules. Research on nodule physiology has shown the structural and metabolic diversity of actinorhizal nodules from different phylogenetic branches. The onset of large-scale nodule transcriptome analysis in different actinorhizal systems will provide access to more information on the symbiosis and its evolution.

Additional keywords: Alnus, Casuarina, Datisca, Discaria, Elaeagnus, Frankia, infected cells.


References

Alloisio N, Queiroux C, Fournier P, Pujic P, Normand P, Vallenet D, Médigue C, Yamaura M, Kakoi K, Kucho K (2010) The Frankia alni symbiotic transcriptome. Molecular Plant-Microbe Interactions 23, 593–607.
The Frankia alni symbiotic transcriptome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltFSltL4%3D&md5=3d6cc4cd0af8ee3938f02ad55ed0f22fCAS |

Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiologia Plantarum 109, 372–381.
Reactive oxygen species and antioxidants in legume nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsl2ju7s%3D&md5=2f3dd7f97fb553ecbf0e1c35b1f361adCAS |

Beckwith J, Tjepkema JD, Cashon RE, Schwintzer CR, Tisa LS (2002) Hemoglobin in five genetically diverse Frankia strains. Canadian Journal of Microbiology 48, 1048–1055.
Hemoglobin in five genetically diverse Frankia strains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlGitbw%3D&md5=c0db8065151543d6a59808807e13550dCAS |

Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiological Reviews 57, 293–319.

Berg RH (1999) Frankia forms infection threads. Canadian Journal of Botany 77, 1327–1333.

Berg RH, McDowell L (1987) Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136, 104–117.
Endophyte differentiation in Casuarina actinorhizae.Crossref | GoogleScholarGoogle Scholar |

Berg RH, McDowell L (1988) Cytochemistry of the wall of infected cells in Casuarina actinorhizae. Canadian Journal of Botany 66, 2038–2047.

Berg RH, Langenstein B, Silvester WB (1999) Development in the Datisca–Coriaria nodule type. Canadian Journal of Botany 77, 1334–1350.

Berry AM, Kahn RKS, Booth MC (1989) Identification of indole compounds secreted by Frankia HFPArI3 in defined culture medium. Plant and Soil 118, 205–209.
Identification of indole compounds secreted by Frankia HFPArI3 in defined culture medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXmt1yltr4%3D&md5=0c70c85ea13ec49c799fa2b69ef5f377CAS |

Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proceedings of the National Academy of Sciences of the United States of America 90, 6091–6094.
Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlGitbY%3D&md5=4f8ea0165b1749f00529d309bc923ea0CAS |

Berry AM, Murphy TM, Okubara PA, Jacobsen KR, Swensen SM, Pawlowski K (2004) Novel expression pattern of cytosolic Gln synthetase in nitrogen-fixing root nodules of the actinorhizal host, Datisca glomerata. Plant Physiology 135, 1849–1862.
Novel expression pattern of cytosolic Gln synthetase in nitrogen-fixing root nodules of the actinorhizal host, Datisca glomerata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqt7k%3D&md5=cac609c23f5680ae9e95b382843bdbe7CAS |

Berry AM, Mendoza-Herrera A, Guo Y-Y, Hayashi J, Persson T, Barabote R, Demchenko K, Zhang S, Pawlowski K (2011) New perspectives on nodule nitrogen assimilation in actinorhizal symbioses. Functional Plant Biology 38, 645–652.
New perspectives on nodule nitrogen assimilation in actinorhizal symbioses.Crossref | GoogleScholarGoogle Scholar |

Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti G, Rotino GL, Campion B, Defez R (2008) Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Archives of Microbiology 190, 67–77.
Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVSks7Y%3D&md5=f12d3dbe663f97fe6fd62df810ea20d5CAS |

Céremonie H, Debelle 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.

Coats V, Schwintzer CR, Tjepkema JD (2009) Truncated hemoglobins in Frankia CcI3: effects of nitrogen source, oxygen concentration, and nitric oxide. Canadian Journal of Microbiology 55, 867–873.
Truncated hemoglobins in Frankia CcI3: effects of nitrogen source, oxygen concentration, and nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSjsr3J&md5=d9d4d18903497b7586ae5bbea2441f7fCAS |

Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. The Plant Journal 39, 487–512.
Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus.Crossref | GoogleScholarGoogle Scholar |

Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Science Signaling 1, re11
De novo organ formation from differentiated cells: root nodule organogenesis.Crossref | GoogleScholarGoogle Scholar |

De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Molecular Biology 60, 871–887.
Lateral root initiation or the birth of a new meristem.Crossref | GoogleScholarGoogle Scholar |

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.
Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1ahtbs%3D&md5=87152587faba3e8559079bd11f4cce40CAS |

Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiology 131, 900–910.
The rest of the iceberg. Legume diversity and evolution in a phylogenetic context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFemtbo%3D&md5=793d94b3668845c492ad2ac1d2f5eaa0CAS |

Fortunato A, Santos P, Graça I, Gouveia MM, Martins SM, Ricardo CP, Pawlowski K, Ribeiro A (2007) Isolation and characterization of cgchi3, a nodule-specific gene from Casuarina glauca encoding a class III chitinase. Physiologia Plantarum 130, 418–426.
Isolation and characterization of cgchi3, a nodule-specific gene from Casuarina glauca encoding a class III chitinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Oqu7o%3D&md5=3ed4d8b0ef41c4b415fa8b33e42139b1CAS |

Franche C, Diouf D, Le QV, Bogusz D, N’Diaye A, Gherbi H, Gobé C, Duhoux E (1997) Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens. The Plant Journal 11, 897–904.
Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1Cksr4%3D&md5=2b2ddd4972ebca5701b02d7826d8b102CAS |

Franche C, Diouf D, Laplaze L, Auguy F, Frutz T, Rio M, Duhoux E, Bogusz D (1998) Soybean (lbc3), Parasponia, and Trema hemoglobin gene promoters retain symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae: implications for hemoglobin gene evolution and root nodule symbioses. Molecular Plant-Microbe Interactions 11, 887–894.
Soybean (lbc3), Parasponia, and Trema hemoglobin gene promoters retain symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae: implications for hemoglobin gene evolution and root nodule symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXls1SjsLc%3D&md5=aebc63d0974334f8adeae18f966bbb0eCAS |

Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008a) 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 of the United States of America 105, 4928–4932.
SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktlSjsbo%3D&md5=3de9c59f7472f502b25ec523a87e7187CAS |

Gherbi H, Nambiar-Veetil M, Zhong C, Félix J, Autran D, Girardin R, Vaissayre V, Auguy F, Bogusz D, Franche C (2008b) Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Molecular Plant-Microbe Interactions 21, 518–524.
Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltFSqs7c%3D&md5=787d53fbf6baab0d3ef5b2262ab9ea4cCAS |

Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Verméglio A, Médigue C, Sadowsky M (2007) Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316, 1307–1312.
Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia.Crossref | GoogleScholarGoogle Scholar |

Günther C, Schlereth A, Udvardi M, Ott T (2007) Metabolism of reactive oxygen species is attenuated in leghemoglobin-deficient nodules of Lotus japonicus. Molecular Plant-Microbe Interactions 20, 1596–1603.
Metabolism of reactive oxygen species is attenuated in leghemoglobin-deficient nodules of Lotus japonicus.Crossref | GoogleScholarGoogle Scholar |

Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin R, Berry AM, Normand P, Domenach AM (2003) A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia. Plant and Soil 254, 193–205.
A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVKhur8%3D&md5=7595687247afe18add70ecc62f7d6683CAS |

Heckmann AB, Hebelstrup KH, Larsen K, Micaelo NM, Jensen EØ (2006) A single hemoglobin gene in Myrica gale retains both symbiotic and non-symbiotic specificity. Plant Molecular Biology 61, 769–779.
A single hemoglobin gene in Myrica gale retains both symbiotic and non-symbiotic specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnslSgsr0%3D&md5=9f2106452140886c02eef1b76cb12972CAS |

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.
Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root.Crossref | GoogleScholarGoogle Scholar |

Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P, Bogusz D (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiology
Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade.Crossref | GoogleScholarGoogle Scholar | in press.

Horchani F, Prevot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi-Smiti S, Puppo A, Brouquisse R (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiology
Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules.Crossref | GoogleScholarGoogle Scholar | in press.

Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytologist 136, 375–405.
Actinorhizal symbioses and their N2 fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXls1ent7w%3D&md5=abe032bef40a47675eb10ecf9b2e99ddCAS |

Jacobsen-Lyon K, Jensen EO, Jorgensen J-E, Marcker KA, Peacock WJ, Dennis ES (1995) Symbiotic and non-symbiotic hemoglobin genes of Casuarina glauca. The Plant Cell 7, 213–222.

Journet E, van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer MJ, Niebel A, Schiex T, Jaillon O, Chatagnier O, Godiard L, Micheli F, Kahn D, Gianinazzi-Pearson V, Gamas P (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Research 30, 5579–5592.
Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis.Crossref | GoogleScholarGoogle Scholar |

Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends in Plant Science 14, 373–382.
Linking development to defense: auxin in plant-pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVajs74%3D&md5=ab1b90aa6397868e4bab54bb4116d919CAS |

Kim HB, An CS (2002) Differential expression patterns of an acidic chitinase and a basic chitinase in the root nodule of Elaeagnus umbellata. Molecular Plant-Microbe Interactions 15, 209–215.
Differential expression patterns of an acidic chitinase and a basic chitinase in the root nodule of Elaeagnus umbellata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitF2gtLc%3D&md5=aefde029aee1d71dcfccf54a77147578CAS |

Knowlton S, Berry AM, Torrey JG (1980) Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Canadian Journal of Microbiology 26, 971–977.
Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7htFKisg%3D%3D&md5=6877b0ff08c2c7ead8cf467521688517CAS |

Kouchi H, Shimomura K, Hata S, Hirota A, Wu GJ, Kumagai H, Tajima S, Suganuma N, Suzuki A, Aoki T, Hayashi M, Yokoyama T, Ohyama T, Asamizu E, Kuwata C, Shibata D, Tabata S (2004) Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Research 11, 263–274.
Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVWltL4%3D&md5=8bc1d9f6c050b5d2bf7adc35ed6a0b29CAS |

Lancelle SA, Torrey JG (1984) Early development of Rhizobium-induced root nodules of Parasponia rigida. 1. lnfection and early nodule initiation. Protoplasma 123, 26–37.
Early development of Rhizobium-induced root nodules of Parasponia rigida. 1. lnfection and early nodule initiation.Crossref | GoogleScholarGoogle Scholar |

Lancelle SA, Torrey JG (1985) Early development of Rhizobium-induced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development. Canadian Journal of Botany 63, 25–35.
Early development of Rhizobium-induced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development.Crossref | GoogleScholarGoogle Scholar |

Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63.
Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitl2lsg%3D%3D&md5=ee6bf8aded20c8e755ddac038dda1fb8CAS |

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

Mathesius U (2008) Auxin: at the root of nodule development? Functional Plant Biology 35, 651–668.
Auxin: at the root of nodule development?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFartL%2FN&md5=bdc07fd0afbcd1929f4ae4f617e1e515CAS |

Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. The Plant Journal 14, 23–34.
Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtV2is7o%3D&md5=3f68f72ce832665d92244d34132f6565CAS |

Meesters TM, Van Vliet WM, Akkermans ADL (1987) Nitrogenase is restricted to the vesicles in Frankia strain EAN1pec. Physiologia Plantarum 70, 267–271.
Nitrogenase is restricted to the vesicles in Frankia strain EAN1pec.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltFahu70%3D&md5=6b877a05b1a07bcdc3ba2f2324beaa48CAS |

Miller IM, Baker DD (1985) The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae). Protoplasma 128, 107–119.
The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae).Crossref | GoogleScholarGoogle Scholar |

Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biology and Biochemistry 29, 881–888.
Regulation of oxygen diffusion in legume nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks1WqsrY%3D&md5=c6dbaaa7cb10595d8d1b6ba3331601a3CAS |

Naisbitt T, James EK, Sprent JI (1992) The evolutionary significance of the legume genus Chamaecrista, as determined by nodule structure. New Phytologist 122, 487–492.
The evolutionary significance of the legume genus Chamaecrista, as determined by nodule structure.Crossref | GoogleScholarGoogle Scholar |

Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Research 17, 7–15.
Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography.Crossref | GoogleScholarGoogle Scholar |

Obertello M, Wall L, Laplaze L, Nicole M, Auguy F, Gherbi H, Bogusz D, Franche C (2007) Functional analysis of the metallothionein gene cgMT1 isolated from the actinorhizal tree Casuarina glauca. Molecular Plant-Microbe Interactions 20, 1231–1240.
Functional analysis of the metallothionein gene cgMT1 isolated from the actinorhizal tree Casuarina glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKqsbzI&md5=ee0a0290572f2179c999fc7bb2ebbb01CAS |

Oldroyd GE, Harrison MJ, Paszkowski U (2009) Reprogramming plant cells for endosymbiosis. Science 324, 753–754.
Reprogramming plant cells for endosymbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVelu7s%3D&md5=b95470b087079ee3b51742f1b908991dCAS |

Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331, 909–912.
LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFSjt7c%3D&md5=6115e4c6ccf3ee41185e6f02c113b8a8CAS |

Pacios-Bras C, Schlaman HRM, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Molecular Biology 52, 1169–1180.
Auxin distribution in Lotus japonicus during root nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVCqtL4%3D&md5=6b06debd161a686e1621c41401b22bb4CAS |

Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6, 763–775.
Arbuscular mycorrhiza: the mother of plant root endosymbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWitL3J&md5=5a4ee5ca91ab8398e46f97106f291bf3CAS |

Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? The Plant Cell 8, 1899–1913.

Pawlowski K, Jacobsen KR, Alloisio N, Denison RF, Klein M, Winzer T, Sirrenberg A, Guan C, Berry AM (2007) Truncated hemoglobins in actinorhizal nodules of Datisca glomerata. Plant Biology 9, 776–785.
Truncated hemoglobins in actinorhizal nodules of Datisca glomerata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslCksg%3D%3D&md5=a867ff57197ff658243366fb3a46b6dbCAS |

Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D, Bennett M, Laplaze L (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiology 144, 1852–1862.
Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca.Crossref | GoogleScholarGoogle Scholar |

Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Péret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, Laplaze L (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiology 154, 1372–1380.
Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2ntrzM&md5=31c768773620c289b511ccc842f0825eCAS |

Prell J, Poole P (2006) Metabolic changes of rhizobia in legume nodules. Trends in Microbiology 14, 161–168.
Metabolic changes of rhizobia in legume nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Gltrg%3D&md5=99da0e377c594b1c5bd6700426e7d4fcCAS |

Racette S, Torrey JG (1989) Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpll. Canadian Journal of Botany 67, 2873–2879.
Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpll.Crossref | GoogleScholarGoogle Scholar |

Ribeiro A, Graça I, Pawlowski K, Santos P (2011) Actinorhizal plant defence-related genes in response to symbiotic Frankia. Functional Plant Biology 38, 639–644.
Actinorhizal plant defence-related genes in response to symbiotic Frankia.Crossref | GoogleScholarGoogle Scholar |

Samac DA, Graham MA (2007) Recent advances in legume-microbe interactions: recognition, defense response, and symbiosis from a genomic perspective. Plant Physiology 144, 582–587.
Recent advances in legume-microbe interactions: recognition, defense response, and symbiosis from a genomic perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvValsLk%3D&md5=231d367d0f8257163574a939506347c1CAS |

Sasakura F, Uchiumi T, Shimoda Y, Suzuki A, Takenouchi K, Higashi S, Abe M (2006) A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide. Molecular Plant-Microbe Interactions 19, 441–450.
A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVagtbw%3D&md5=7862ab96ccc6ba45bd685fd5006e42a0CAS |

Schubert M, Melnikova AN, Mesecke N, Zubkova EK, Fortte R, Batashev DR, Barth I, Sauer N, Gamalei YuV, Mamushina NS, Tietze L, Voitsekhovskaja OV, Pawlowski K (2010) Two novel disaccharides, rutinose and methylrutinose, are involved in carbon metabolism in Datisca glomerata. Planta 231, 507–521.
Two novel disaccharides, rutinose and methylrutinose, are involved in carbon metabolism in Datisca glomerata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslWnsg%3D%3D&md5=7a44f6b35c93c4b91a07bdd2ea3dbd42CAS |

Schubert M, Koteeva NK, Wabnitz PW, Santos P, Büttner M, Sauer N, Demchenko K, Pawlowski K (2011) Carbon partitioning in roots and nitrogen-fixing root nodules of Datisca glomerata. Planta 233, 139–152.
Carbon partitioning in roots and nitrogen-fixing root nodules of Datisca glomerata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12g&md5=908394989c171327d3d8ad7eab15dabeCAS |

Smouni A, Laplaze L, Bogusz D, 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.
The 35S promoter is not constitutively expressed in the transgenic tropical actinorhizal tree, Casuarina glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFSgtr8%3D&md5=442b762827fe618bc69d36fcb20ab568CAS |

Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 92, 2647–2651.
Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXksl2rs7o%3D&md5=d2d5cd2236f8fe6f20f9d367391ba827CAS |

Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective of the occurrence of nodulation. New Phytologist 174, 11–25.
Evolving ideas of legume evolution and diversity: a taxonomic perspective of the occurrence of nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVKms7w%3D&md5=775b98fcf38525fc51129d0896d33e80CAS |

Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. The Plant Cell 21, 1495–1511.
Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVCqtL8%3D&md5=8ab4fe13de32d8ede1d574c23fbcdaa4CAS |

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.
Infection-related activation of the cg12 promoter is conserved between actinorhizal and legume-rhizobia root nodule symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVyms7s%3D&md5=981747f428fef352ec01b51b719387f3CAS |

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.
Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1ensbs%3D&md5=771a3718e8dcd1f957eb22880ed9974eCAS |

Swensen SM (1996) The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. American Journal of Botany 83, 1503–1512.
The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association.Crossref | GoogleScholarGoogle Scholar |

Tavares F, Santos CL, Sellstedt A (2007) Reactive oxygen species in legume and actinorhizal nitrogen-fixing symbioses: the microsymbiont’s response to an unfriendly reception. Physiologia Plantarum 130, 344–356.
Reactive oxygen species in legume and actinorhizal nitrogen-fixing symbioses: the microsymbiont’s response to an unfriendly reception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Oqurg%3D&md5=7b51f5904da4d902ab77fea72afd838bCAS |

Tjepkema JD, Cashon RE, Beckwith J, Schwintzer CR (2002) Hemoglobin in Frankia, a nitrogen-fixing actinomycete. Applied and Environmental Microbiology 68, 2629–2631.
Hemoglobin in Frankia, a nitrogen-fixing actinomycete.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFKjsr4%3D&md5=cb4b895b71851d2be657dff4b788a44cCAS |

Vieweg MF, Hohnjec N, Küster H (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220, 757–766.
Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVSqs7s%3D&md5=e36547470fefb7dd01d5b730f0c835f5CAS |

Zdyb A, Demchenko K, Heumann J, Mrosk C, Grzeganek P, Göbel C, Feussner I, Pawlowski K, Hause B (2011) Jasmonate biosynthesis in legume and actinorhizal nodules. New Phytologist 189, 568–579.
Jasmonate biosynthesis in legume and actinorhizal nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlChtbo%3D&md5=a60e8eb86c960eefc6e840d8fdee4a42CAS |

Zhu XY, Chase MW, Qiu YL, Kong HZ, Dilcher DL, Li JH, Chen ZD (2007) Mitochondrial matR sequences help to resolve deep phylogenetic relationships in rosids. BMC Evolutionary Biology 7, 217
Mitochondrial matR sequences help to resolve deep phylogenetic relationships in rosids.Crossref | GoogleScholarGoogle Scholar |