Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Actinorhizal plant defence-related genes in response to symbiotic Frankia

Ana Ribeiro A , Inês Graça A , Katharina Pawlowski B and Patrícia Santos A C D
+ Author Affiliations
- Author Affiliations

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

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

C Department of Plant Pathology, Michigan State University, East Lansing, MI 48824, USA.

D Corresponding author. Email: psantos@msu.edu

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) 639-644 https://doi.org/10.1071/FP11012
Submitted: 14 January 2011  Accepted: 10 May 2011   Published: 16 August 2011

Abstract

Actinorhizal plants have become increasingly important as climate changes threaten to remake the global landscape over the next decades. These plants are able to grow in nutrient-poor and disturbed soils, and are important elements in plant communities worldwide. Besides that, most actinorhizal plants are capable of high rates of nitrogen fixation due to their capacity to establish root nodule symbiosis with N2-fixing Frankia strains. Nodulation is a developmental process that requires a sequence of highly coordinated events. One of these mechanisms is the induction of defence-related events, whose precise role in a symbiotic interaction remains to be elucidated. This review summarises what is known about the induction of actinorhizal defence-related genes in response to symbiotic Frankia and their putative function during symbiosis.

Additional keywords: defence genes, hypersensitive response, oxidative burst, pathogenesis, root nodule symbioses, stress responses.


References

Altenbach D, Robatzek S (2007) Pattern recognition receptors: from the cell surface to intracellular dynamics. Molecular Plant—Microbe Interactions 20, 1031–1039.
Pattern recognition receptors: from the cell surface to intracellular dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGktbw%3D&md5=0694c3775af1135a8badc4548f70927fCAS |

An CS, Kim HB, Lee SH, Jang-Hyun J, Oh CJ, Lee H (2005) Gene expression in root nodules of Elaeagnus umbellata. In ‘Biological nitrogen fixation, sustainable agriculture and the environment. Vol. 41’. (Eds YP Wang, M Lin, ZX Tian, WE Newton) pp. 207–208. (Springer: Dordrecht)

Anderson JP, Gleason CA, Foley RC, Thrall PH, Burdon JB, Singh KB (2010) Plants versus pathogens: an evolutionary arms race. Functional Plant Biology 37, 499–512.
Plants versus pathogens: an evolutionary arms race.Crossref | GoogleScholarGoogle Scholar |

Auguy F, Abdel-Lateif K, Doumas P, Badin P, Guerin V, Bogusz D, Hocher V (2011) Activation of the isoflavonoid pathway in actinorhizal symbioses. Functional Plant Biology 38, 720–726.
Activation of the isoflavonoid pathway in actinorhizal symbioses.Crossref | GoogleScholarGoogle Scholar |

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

Berry AM, McIntyre L, McCully ME (1986) Fine structure of root hair infection leading to nodulation in the Frankia–Alnus symbiosis. Canadian Journal of Botany 64, 292–305.
Fine structure of root hair infection leading to nodulation in the Frankia–Alnus symbiosis.Crossref | GoogleScholarGoogle Scholar |

Century K, Holub EB, Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and fungal pathogen. Proceedings of the National Academy of Sciences of the United States of America 92, 6597–6601.
NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and fungal pathogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmslOjs7Y%3D&md5=a96ca1a1b323343c6dc68915860f8b99CAS |

D’Haeze W, De Rycke R, Mathis R, Goormachtig S, Pagnotta S, Verplancke C, Capoen W, Holsters M (2003) Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proceedings of the National Academy of Sciences of the United States of America 100, 11 789–11 794.
Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFKmurk%3D&md5=a88a37c4342e096bdc5d7de81d1353fcCAS |

Dangl JL, Jones JD (2001) Plant pathogens and integrated defense responses to infection. Nature 411, 826–833.
Plant pathogens and integrated defense responses to infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksF2gu74%3D&md5=dcfe022a03fe8f2769d33881f455945bCAS |

Diem HG, Dommergues YR (1990) Current and potential uses and management of Casuarinaceae in the tropics. In ‘The biology of Frankia and actinorhizal plants’. (Eds CR Schwintzer, JD Tjepkema) pp. 317–342. (Academic Press: San Diego)

Fortunato A, Santos P, Graca I, Gouveia M, Martins S, Ricardo CPP, 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, Laplaze L, Duhoux E, Bogusz D (1998) Actinorhizal symbioses: recent advances in plant molecular and genetic transformation studies. Critical Reviews in Plant Sciences 17, 1–28.
Actinorhizal symbioses: recent advances in plant molecular and genetic transformation studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlSksrk%3D&md5=9012b4018f5e8423a3c91e3db3878b89CAS |

Franssen HJ, Nap J-P, Gloudemans T, Stiekema W, Van Dam H, Govers F, Louwerse J, Van Kammen A, Bisseling T (1987) Characterization of cDNA for nodulin-75 of soybean: a gene product involved in early stages of root nodule development. Proceedings of the National Academy of Sciences of the United States of America 84, 4495–4499.
Characterization of cDNA for nodulin-75 of soybean: a gene product involved in early stages of root nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXkvFWisbk%3D&md5=70b87e685e847469b79f02f89ac24e28CAS |

Gamas P, de Billy F, Truchet G (1998) Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins. Molecular Plant-Microbe Interactions 11, 393–403.
Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFynsLo%3D&md5=7637015b34c1fea5b5e36980d788daf0CAS |

Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (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 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 |

Goetting-Minesky MP, Mullin BC (1994) Differential gene expression in an actinorhizal symbiosis: evidence for a nodule-specific cysteine proteinase. Proceedings of the National Academy of Sciences of the United States of America 91, 9891–9895.
Differential gene expression in an actinorhizal symbiosis: evidence for a nodule-specific cysteine proteinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXht1Cmsbw%3D&md5=56f3e962b3e26662f3b28cf1356d6231CAS |

Goormachtig S, Lievens S, van de Velde W, van Montagu M, Holsters M (1998) Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. The Plant Cell 10, 905–915.

Guan C-H, Akkermans ADL, van Kammen A, Bisseling T, Pawlowski K (1997) ag13 is expressed in Alnus glutinosa nodules in infected cells during endosymbiont degradation and in the nodule pericycle. Physiologia Plantarum 99, 601–607.
ag13 is expressed in Alnus glutinosa nodules in infected cells during endosymbiont degradation and in the nodule pericycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVahtLo%3D&md5=8a7fbd9666ffe24e08aaa5a2db7ef9f6CAS |

Gucciardo S, Rathbun EA, Shanks M, Jenkyns S, Mak L, Durrant MC, Brewin NJ (2005) Epitope tagging of legume root nodule extensin modifies protein structure and crosslinking in cell walls of transformed tobacco leaves. Molecular Plant—Microbe Interactions 18, 24–32.
Epitope tagging of legume root nodule extensin modifies protein structure and crosslinking in cell walls of transformed tobacco leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsFKn&md5=6bf67d6099f9be4b65ee7ef9e936b470CAS |

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 |

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 156, 700–711.

Jacobsen-Lyon K, Jensen EO, Jorgensen J, Marcker KA, Peacock WJ, Dennis ES (1995) Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. The Plant Cell 7, 213–223.

Kasprzewska A (2003) Plant chitinases – regulation and functions. Cellular & Molecular Biology Letters 8, 809–824.

Katinakis P, Verma DPS (1985) Nodullin-24 of soybean codes for a peptide of the peribacteroid membrane and was generated by a tandem duplication of a sequence resembling an insertion element. Proceedings of the National Academy of Sciences of the United States of America 82, 4157–4161.
Nodullin-24 of soybean codes for a peptide of the peribacteroid membrane and was generated by a tandem duplication of a sequence resembling an insertion element.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXkvF2lsLk%3D&md5=707695faf2b49423cece34f8d39495c9CAS |

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 |

Kim HB, Oh CJ, Lee H, An CS (2003) A type-l chalcone isomerase mRNA is highly expressed in the root nodules of Elaeagnus umbellata. Journal of Plant Biology 46, 263–270.
A type-l chalcone isomerase mRNA is highly expressed in the root nodules of Elaeagnus umbellata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvVelsQ%3D%3D&md5=c0123d34f39f975c7887cf7946614c58CAS |

Kim YJ, Kim HB, Baek HE, Heu S, An CS (2005) Constitutive expression of two endochitinases from root nodules of Elaeagnus umbellata confers resistance on transgenic Arabidopsis plants against the fungal pathogen Botrytis cinerea. Journal of Plant Biology 48, 39–46.
Constitutive expression of two endochitinases from root nodules of Elaeagnus umbellata confers resistance on transgenic Arabidopsis plants against the fungal pathogen Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlektbk%3D&md5=0c2e1cfd0880026693ff0d5d2ecc5447CAS |

Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix JJ, Auguy F, Bogusz D, Duhoux E (1999) Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules. Plant Physiology 121, 113–122.
Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGlsLg%3D&md5=5b6afbbbeb32fef31bbdb3b676293ceeCAS |

Laplaze L, Ribeiro A, Franche C, Duhoux E, Auguy F, Bogusz D, Pawlowski K (2000) Characterization of a Casuarina glauca nodule-specific subtilisin-like protease gene, a homolog of Alnus glutinosa ag12. Molecular Plant—Microbe Interactions 13, 113–117.
Characterization of a Casuarina glauca nodule-specific subtilisin-like protease gene, a homolog of Alnus glutinosa ag12.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSgtQ%3D%3D&md5=f17bf8344120c66087f9dc51680fe7a0CAS |

Laplaze L, Gherbi H, Duhoux E, Pawlowski K, Auguy F, Guermache F, Franche C, Bogusz D (2002) Symbiotic and non-symbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca. Plant Molecular Biology 49, 81–92.
Symbiotic and non-symbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlemtLc%3D&md5=c81fccd561a37a3eb99fb3d6e3ae6adfCAS |

Lee SB, Ham BK, Park JM, Kim YJ, Paek KH (2006) BnNHL18A shows a localization change by stress-inducing chemical treatments. Biochemical and Biophysical Research Communications 339, 399–406.
BnNHL18A shows a localization change by stress-inducing chemical treatments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Ortr%2FI&md5=12d4dd8f8020b645167dd1a2104dc77dCAS |

Li Y, Zhou L, Li Y, Chen D, Tan X, Lei L, Zhou J (2008) A nodule-specific plant cysteine proteinase, AsNODF32, is involved in nodule senescence and nitrogen fixation activity of the green manure legume Astragalus sinicus. New Phytologist 180, 185–192.
A nodule-specific plant cysteine proteinase, AsNODF32, is involved in nodule senescence and nitrogen fixation activity of the green manure legume Astragalus sinicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ait7bJ&md5=4d6e33ddaaf9fcd1becbdf7e36426f27CAS |

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
Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria.Crossref | GoogleScholarGoogle Scholar |

Newcomb W, Wood SM (1987) Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal root nodules. International Review of Cytology 109, 1–88.
Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal root nodules.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hsVCitw%3D%3D&md5=e868d6a931f28d4c2fbf13179e792858CAS |

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 |

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

Pawlowski K, Twigg P, Dobritsa S, Guan C, Mullin B (1997) A nodule-specific gene family from Alnus glutinosa encodes glycine and histidine-rich proteins expressed in the early stages of actinorhizal nodule development. Molecular Plant—Microbe Interactions 10, 656–664.
A nodule-specific gene family from Alnus glutinosa encodes glycine and histidine-rich proteins expressed in the early stages of actinorhizal nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvFOrtrk%3D&md5=17490dc1fddb8aef5f8b1abf6141353aCAS |

Pawlowski K, Bogusz D, Ribeiro A, Berry AM (2011) Progress on research on actinorhizal plants. Functional Plant Biology 38, 633–638.
Progress on research on actinorhizal plants.Crossref | GoogleScholarGoogle Scholar |

Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.
A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvVekuw%3D%3D&md5=76f31e76959f86d5ac7495aee6075da1CAS |

Ramu SK, Peng HM, Cook DR (2002) Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Molecular Plant—Microbe Interactions 15, 522–528.
Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlSntr0%3D&md5=44bcdd39dc8bce9d46dc800a538f39a8CAS |

Ribeiro A, Akkermans A, van Kammen A, Bisseling T, Pawlowski K (1995) A nodule-specific gene encoding a subtilisin-like protease is involved in early stages of actinorhizal nodule development. The Plant Cell 7, 785–794.

Rodríguez-Concepción M, Pérez-García A, Beltrán JP (2001) Up-regulation of genes encoding novel extracellular proteins during fruit set in pea. Plant Molecular Biology 46, 373–382.
Up-regulation of genes encoding novel extracellular proteins during fruit set in pea.Crossref | GoogleScholarGoogle Scholar |

Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher RA, Lange J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Molecular Plant—Microbe Interactions 13, 763–777.
Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkt1ahtb4%3D&md5=74649d9d38ce35af54c35345c520a5b2CAS |

Salzer P, Feddermann N, Wiemken A, Boller T, Staehelin C (2004) Sinorhizobium meliloti-induced chitinase gene expression in Medicago truncatula ecotype R108–1: a comparison between symbiosis-specific class V and defense-related class IV chitinases. Planta 219, 626–638.
Sinorhizobium meliloti-induced chitinase gene expression in Medicago truncatula ecotype R108–1: a comparison between symbiosis-specific class V and defense-related class IV chitinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Cqur0%3D&md5=2e5703754bbf501bb71c519973de265aCAS |

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 |

Santos P, Fortunato A, Ribeiro A, Pawlowski K (2008) Chitinases in root nodules. Plant Biotechnology 25, 299–307.
Chitinases in root nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVajt7bN&md5=ffec314ea8e166bed4121fff46711d6cCAS |

Santos P, Fortunato A, Graca I, Martins S, Gouveia M, Auguy F, Bogusz D, Ricardo CPP, Pawlowski K, Ribeiro A (2010) Characterization of four defense-related genes up-regulated in root nodules of Casuarina glauca. Symbiosis 50, 27–35.
Characterization of four defense-related genes up-regulated in root nodules of Casuarina glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFyisLjJ&md5=5486949310f832fb0f20af6abbec8f19CAS |

Schaller A (2004) A cut above the rest: the regulatory function of plant proteases. Planta 220, 183–197.
A cut above the rest: the regulatory function of plant proteases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVensrfK&md5=6e1ba736ef5e63becc1ad0468931e488CAS |

Sheokand S, Brewin NJ (2003) Cysteine proteases in nodulation and nitrogen fixation. Indian Journal of Experimental Biology 41, 1124–1132.

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 |

Soto MJ, Dominguez-Ferreras A, Pérez-Mendoza D, Sanjuán J, Olivares J (2009) Mutualism versus pathogenesis: the give-and-take in plant–bacteria interactions. Cellular Microbiology 11, 381–388.
Mutualism versus pathogenesis: the give-and-take in plant–bacteria interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVaqu7k%3D&md5=09ecc5a9d3b5da6a0878b3cb9f239437CAS |

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 |

Staehelin C, Müller J, Mellor RB, Wiemken A, Boller T (1992) Chitinase and peroxidase in effective (Fix+) and ineffective (Fix−) soybean nodules. Planta 187, 295–300.
Chitinase and peroxidase in effective (Fix+) and ineffective (Fix) soybean nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1ygtL0%3D&md5=adebdd32a017ce18728dce010ca48abeCAS |

Staehelin C, Schultze M, Kondorosi E, Kondorosi A (1995) Lipochitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa. Plant Physiology 108, 1607–1614.

Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends in Plant Science 12, 282–285.
Distinct, crucial roles of flavonoids during legume nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslWlu70%3D&md5=fc33516d219b33c2583b67ef7db3ba39CAS |

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.
cg12 Expression is specifically linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvF2kurY%3D&md5=155585aa1d51d56d48a548792916529dCAS |

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 |

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 |

Tellström V, Usadel B, Thimm O, Stitt M, Küster H, Niehaus K (2007) The lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula. Plant Physiology 143, 825–837.
The lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |

Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaître B, Alunni B, Bourge M, Kucho K, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122–1126.
Plant peptides govern terminal differentiation of bacteria in symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlaisrw%3D&md5=2546d7be73884a30357d0fb4a08e0396CAS |

Vasse J, de Billy F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti–alfalfa symbiotic interactions is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566.
Abortion of infection during the Rhizobium meliloti–alfalfa symbiotic interactions is accompanied by a hypersensitive reaction.Crossref | GoogleScholarGoogle Scholar |

Wall LG, Berry AM (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In ‘Nitrogen-fixing actinorhizal symbioses’. (Eds K. Pawlowski, WE Newton) pp. 147–166. (Springer: Dordrecht)

Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signalling and fungal resistance in Arabidopsis. The Plant Cell 20, 471–481.
A LysM receptor-like kinase plays a critical role in chitin signalling and fungal resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslSiur8%3D&md5=d914d4696e248f0b896e9bcb8e64b4baCAS |

Wilson RC, Long F, Maruoka EM, Cooper J (1994) A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. The Plant Cell 6, 1265–1275.

Zheng MS, Takahashi H, Miyazaki A, Hamamoto H, Shah J, Yamaguchi I, Kusano T (2004) Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement. Planta 218, 740–750.
Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslGjsbo%3D&md5=8db290624aaea82997e16293dcb4a89aCAS |