Diffusible factors from Frankia modify nodulation kinetics in Discaria trinervis, an intercellular root-infected actinorhizal symbiosis
Luciano Andrés Gabbarini A and Luis Gabriel Wall A BA Programa Interacciones Biológicas, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, R. Sáenz Peña 352, B1876BXD Bernal, Argentina.
B Corresponding author. Email: lgwall@unq.edu.ar
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) 662-670 https://doi.org/10.1071/FP11015
Submitted: 15 January 2011 Accepted: 5 May 2011 Published: 16 August 2011
Abstract
Frankia BCU110501 induces nitrogen-fixing root nodules in Discaria trinervis (Gillies ex Hook. & Arn.) Reiche (Rhamnaceae) via intercellular colonisation, without root hair deformation. It produces diffusible factors (DFs) that might be involved in early interactions with the D. trinervis roots, playing a role in the nodulation process. The induction of root nodule development in actinorhizal symbiosis would depend on the concentration of factors produced by the bacteria and the plant. A detailed analysis of nodulation kinetics revealed that these DFs produce changes at the level of initial rate of nodulation and also in nodulation profile. Diluted Frankia BCU110501 inoculum could be activated in less than 96 h by DFs produced by Frankia BCU110501 cells that had been previously washed. Biochemical characterisation showed that Frankia BCU110501 DFs have a molecular weight of <12 kDa, are negatively charged at pH 7.0 and seem to contain a peptide bond necessary for their activity. Frankia BCU110501, belonging to Frankia Clade 3, does not induce nodules in Alnus acuminata H.B.K. ssp. acuminata but is able to deform root hairs, as do Frankia strains from Clade 1. The root hair deforming activity of Frankia BCU110501 DFs show the same biochemical characteristics of the DFs involved in nodulation of D. trinervis. These results suggest that Frankia symbiotic factors have a basic structure regardless of the infection pathway of the host plant.
Additional keywords: actinorhiza, intercellular infection, nitrogen fixation, root hair deformation.
References
Akkermans ADL, Hirsch AM (1997) A reconsideration of terminology in Frankia research: a need for congruence. Physiologia Plantarum 99, 574–578.| A reconsideration of terminology in Frankia research: a need for congruence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVahsL0%3D&md5=73450aba144cac4bbafd123305a39278CAS |
Benson DR, Clawson ML (2000) Evolution of the actinorhizal plant symbiosis. In ‘Prokaryotic nitrogen fixation: a model system for the analysis of a biological process’. (Ed. E Triplett) pp. 207–224. (Horizon Scientific Press: Norfolk)
Berry A, Torrey JG (1979) Isolation and characterization in vivo and in vitro of an actimyceteous endophyte from Alnus rubra Bong. In ‘Symbiotic nitrogen fixation in the management of temperate forests’. (Eds J Gordon, C Wheeler, D Perry) pp. 69–83. (Oregon State University, Forest Research Laboratory: Corvallis)
Burggraaf A, Van Der Linden J, Tak T (1983) Studies on the localization of infectible cells on Alnus glutinosa roots. Plant and Soil 74, 175–188.
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.
Chaia E (1998) Isolation of an effective strain of Frankia from nodules of Discaria trinervis (Rhamnaceae). Plant and Soil 205, 99–102.
Chaia EE, Fontenla SB, Vobis G, Wall LG (2006) Infectivity of soilborne Frankia and mycorrhizae in Discaria trinervis along a vegetation gradient in Patagonian soil. Journal of Basic Microbiology 46, 263–274.
| Infectivity of soilborne Frankia and mycorrhizae in Discaria trinervis along a vegetation gradient in Patagonian soil.Crossref | GoogleScholarGoogle Scholar |
Gabbarini LA, Wall LG (2008) Analysis of nodulation kinetics in Frankia–Discaria trinervis symbiosis reveals different factors involved in the nodulation process. Physiologia Plantarum 133, 776–785.
| Analysis of nodulation kinetics in Frankia–Discaria trinervis symbiosis reveals different factors involved in the nodulation process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1OitL0%3D&md5=c1551cd06edb7b44379a086733858ba6CAS |
González JE, Marketon MM (2003) Quorum sensing in nitrogen-fixing rhizobia. Microbiology and Molecular Biology Reviews 67, 574–592.
| Quorum sensing in nitrogen-fixing rhizobia.Crossref | GoogleScholarGoogle Scholar |
Huss-Danell K (1978) Nitrogenase activity measurements in intact plants of Alnus incana. Physiologia Plantarum 43, 372–376.
| Nitrogenase activity measurements in intact plants of Alnus incana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXlvFert7g%3D&md5=115f06bf4b948ed6785b78c5368dba1eCAS |
Knowlton S, Dawson JO (1982) Effects of Pseudomona cepacia and cultural factors on the nodulation of Alnus rubra roots by Frankia. Canadian Journal of Botany 61, 2877–2882.
| Effects of Pseudomona cepacia and cultural factors on the nodulation of Alnus rubra roots by Frankia.Crossref | GoogleScholarGoogle Scholar |
Madsen L, Tirichine L, Jurkiewicz A, Sullivan J, Heckmann A, Bek A, Ronson C, James E, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Communications 1, 1–12.
| The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1ChsbzM&md5=2e0fe52e5d07e02a41e562981afbe778CAS |
Murry MA, Fontaine MS, Torrey JG (1984) Growth kinetics and nitrogenase induction in Frankia sp. HFPArI 3 grown in batch culture. Plant and Soil 78, 61–78.
| Growth kinetics and nitrogenase induction in Frankia sp. HFPArI 3 grown in batch culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1Sgt7c%3D&md5=eb538079f008eb95a56b8465470e6f5bCAS |
Nittayajarn A, Baker D (1989) Methods for the quantification of Frankia cell biomass. Plant and Soil 118, 199–204.
| Methods for the quantification of Frankia cell biomass.Crossref | GoogleScholarGoogle Scholar |
Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, et al (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 |
Otero Casal A, Muñoz Crego A, Bernárdez Hermida M, Fábregas Casal J (2005) ‘Quorum sensing: el lenguaje de las bacterias.’ (Acribia, S.A.: Zaragoza)
Solans M (2007) Discaria trinervis–Frankia symbiosis promotion by saprophytic actinomycetes. Journal of Basic Microbiology 47, 243–250.
| Discaria trinervis–Frankia symbiosis promotion by saprophytic actinomycetes.Crossref | GoogleScholarGoogle Scholar |
Solans M, Vobis G, Wall L (2009) Saprophytic actinomycetes promote nodulation in Medicago sativa–Sinorhizobium meliloti symbiosis in the presence of high N. Journal of Plant Growth Regulation 28, 106–114.
| Saprophytic actinomycetes promote nodulation in Medicago sativa–Sinorhizobium meliloti symbiosis in the presence of high N.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslyitrw%3D&md5=925d083d20618be796a8895c508cd403CAS |
Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiology 144, 575–581.
| Legume evolution: where do nodules and mycorrhizas fit in?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvValsLg%3D&md5=44db221b8a934345cbc338366cc906d9CAS |
Swensen SM, Mullin BC (1997) Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbioses. Physiologia Plantarum 99, 565–573.
| Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVWqsb8%3D&md5=0af2513a01fb9876524f72dd553f2121CAS |
Takano E, Chakraburtty R, Nihira T, Yamada Y, Bibb M (2001) A complex role for the g-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Molecular Microbiology 41, 1015–1028.
| A complex role for the g-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlGhs7g%3D&md5=a971e4b5ebc69c2d52a36411fb9cdc4aCAS |
Valverde C, Wall L (1999a) Regulation of nodulation in Discaria trinervis (Rhamnaceae)–Frankia symbiosis. Canadian Journal of Botany 77, 1302–1310.
Valverde C, Wall LG (1999b) Time course of nodule development in the Discaria trinervis (Rhamnaceae)–Frankia symbiosis. New Phytologist 141, 345–354.
| Time course of nodule development in the Discaria trinervis (Rhamnaceae)–Frankia symbiosis.Crossref | GoogleScholarGoogle Scholar |
Valverde C, Wall L, Huss-Danell K (2000) Regulation of nodulation and nodule mass relative to nitrogenase activity and nitrogen demandin seedlings of Discaria trinervis (Rhamnaceae). Symbiosis 19, 167–182.
Valverde C, Ferrari A, Wall LG (2002) Phosphorus and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis (Rhamnaceae) and Frankia BCU110501. New Phytologist 153, 43–51.
| Phosphorus and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis (Rhamnaceae) and Frankia BCU110501.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1ykug%3D%3D&md5=cbed9840bf74cf2cf9448abeb80b15bdCAS |
Van Ghelue M, Løvaas E, Ringø 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.
| Early interactions between Alnus glutinosa and Frankia strain ArI3. Production and specificity of root hair deformation factor(s).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVahsbc%3D&md5=5988bfb665fa18eb92c427fd76384278CAS |
Wall LG (2000) The actinorhizal symbiosis. Journal of Plant Growth Regulation 19, 167–182.
Wall L, Berry A (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In ‘Nitrogen-fixing actinorhizal symbioses’. (Eds K Pawlowski, W Newton) pp. 147–166. (Springer: Dordrecht)
Wall LG, Huss-Danell K (1997) Regulation of nodulation in Alnus incana–Frankia symbiosis. Physiologia Plantarum 99, 594–600.
| Regulation of nodulation in Alnus incana–Frankia symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVahtL4%3D&md5=802751bfa7947815ce0bc3d01734952eCAS |
Wall LG, Valverde C, Huss-Danell K (2003) Regulation of nodulation in the absence of N2 is different in actinorhizal plants with different infection pathways. Journal of Experimental Botany 54, 1253–1258.
| Regulation of nodulation in the absence of N2 is different in actinorhizal plants with different infection pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFCju7Y%3D&md5=419f16e454acc29dd0cb2806ab023334CAS |