Skip to main content
Log in

Morphology and anatomy of root nodules of Retama monosperma (L.)Boiss.

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

In spite of the importance of Retama species for dune stabilization and re-vegetation and the contribution to the bio-fertilization of semi-arid and arid ecosystems, the symbiotic interaction of Retama species with rhizobia remains largely unstudied. In this paper, we aim to provide the first detailed study on nodule morphology and anatomy of Retama monosperma.

Methods

We collected nodules from coastal areas nearby Oran (Algeria) and studied in detail their anatomy and ultrastructure by light and electron microscopy.

Results

First, we confirmed the likely identity of the microsymbiont as B. retamae and found that nodules of R. monosperma belong to the genistoid type of indeterminate nodules. Infection threads, typical for most nodules of legumes, are absent in nodules of R. monosperma and bacterial spread is associated with plant cell division. The nitrogen fixation zone is homogenous with only invaded cells and a network of non-invaded cells found in many nodules, is absent. Moreover, endoreduplication does not take place in bacteroids in nodules of R. monosperma.

Conclusions

The features observed in this study are compared to the morphology and anatomy of nodules of other legumes and the possible consequences for nodule functioning and the mode of infection during the establishment of the interaction are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bergersen FJ (1982) Root nodules of legumes: structure and functions. Reseach Studies Press Ltd., Baldock, 164p

    Google Scholar 

  • Boulila F, Depret G, Boulila A, Belhadi D, Benallaoua S, Laguerre G (2009) Retama species growing in different ecological-climatic areas of north eastern Algeria have a narrow range of Rhizobia that form a novel phylogenetic clade within the Bradyrhizobium genus. Syst Appl Microbiol 32:245–255

    Article  PubMed  Google Scholar 

  • Caravaca F, Alguacil MM, Figueroa D, Barea JM, Roldan A (2003a) Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area. For Ecol Manage 182:49–58

    Article  Google Scholar 

  • Caravaca F, Figueroa D, Alguacil MM, Roldan A (2003b) Application of composted urban residue enhanced the performance of afforested shrub species in degraded semiarid land. Bioresour Technol 90:65–70

    Article  CAS  PubMed  Google Scholar 

  • Chomczynski P, Rymaszewski M (2006) Alkaline polyethylene glycol-based method for direct PCR from bacteria, eukaryotic tissue samples, and whole blood. Biotechniques 40:454, 456, 458

    Article  CAS  PubMed  Google Scholar 

  • de Velde V, 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

    Article  PubMed  Google Scholar 

  • Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051

    Article  CAS  PubMed  Google Scholar 

  • Golinowski W, Kopcinska J, Borucki W (1987) The morphogenesis of lupine root nodules during infection by Rhizobium lupini. Acta Soc Bot Pol 61:307–318

    Article  Google Scholar 

  • Gonzalez-Sama A, Lucas M, de Felipe MR, Pueyo JJ (2004) An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus). New Phytol 163:371–380

    Article  Google Scholar 

  • Gough C, Cullimore J (2011) Lipo-chitoologosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24:867–878

    Article  CAS  PubMed  Google Scholar 

  • Guerrouj K, Ruíz-Díez B, Chahboune R, Ramírez-Bahena MH, Abdelmoumen H, Quinones MA, El Idrissi MM, Velázquez E, Fernández-Pascual M, Bedmar EJ, Peix A (2013) Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp.nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol 36:218–223

    Article  CAS  PubMed  Google Scholar 

  • Haase P, Pugnaire FI, Fernández EM, Puigdefábregas J, Clark SC, Incoll LD (1996) Investigation of rooting depth in the semi-arid shrub Retama sphaerocarpa (L.) Boiss. by labelling of ground water with a chemical tracer. J Hydrol 177:23–31

    Article  CAS  Google Scholar 

  • Held M, Hossain MS, Yokota K, Bonfante P, Stougaard J, Szczyglowski K (2010) Common and not so common symbiotic entry. Trends Plant Sci 15:540–545

    Article  CAS  PubMed  Google Scholar 

  • Kalita M, Stepkowski T, Łotocka B, Malek W (2006) Phylogeny and nodulation genes and symbiotic properties of Genista tinctoria bradyrhizobia. Arch Microbiol 186:87–97

    Article  CAS  PubMed  Google Scholar 

  • Łotocka B, Kopcinska J, Skalniak M (2012) Review article: the meristem in indeterminate root nodules of Faboideae. Symbiosis 58:63–72

    Article  PubMed Central  PubMed  Google Scholar 

  • Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun. doi:10.1038/ncomms1009

    PubMed Central  PubMed  Google Scholar 

  • McRae DG, Miller RW, Berndt WB, Joy K (1989) Transport of C4-dicarboxylates and amino acids by Rhizobium meliloti bacteroids. Mol Plant–Microbe Interact 2:273–278

    Article  Google Scholar 

  • Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A, Kondorosi E (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small secreted polypeptides with conserved cysteine motifs. Plant Physiol 132:161–173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Rev 11:252–263

    CAS  Google Scholar 

  • Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Ozenda P (1977) Flore et végétation du Sahara. Ed. CNRS Paris. 622p

  • Popp C, Ott T (2011) Regulation of signal transduction and bacterial infection during root nodule symbiosis. Curr Opin Plant Biol 14:458–467

    Article  CAS  PubMed  Google Scholar 

  • Renier A, De Faria SM, Jourand P, Giraud E, Dreyfus B, Rapior S, Prin Y (2011) Nodulation of Crotalaria podocarpa DC. by Methylobacterium nodulans displays very unusual features. J Exp Bot 62:3693–3697

    Article  CAS  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biology 17:208–212

    Article  CAS  Google Scholar 

  • Rodríguez-Echeverría S, Pérez-Fernández MA (2003) Soil fertility and herb facilitation mediated by Retama sphaerocarpa. J Veg Sci 14:807–814

    Article  Google Scholar 

  • Rodríguez-Echeverría S, Pérez-Fernández MA (2005) Potential use of Iberian shrubby legumes and rhizobia inoculation in revegetation projects under acidic soil conditions. Appl Soil Ecol 29:203–208

    Article  Google Scholar 

  • Sajnaga E, Malek W, Łotocka B, Stepkowski T, Legocki A (2001) The root-nodule symbiosis between Sarothamnus scoparius L. and its microsymbionts. A van Leeuwenhoek 79:385–391

    Article  CAS  Google Scholar 

  • Schubert KR (1986) Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Ann Rev Plant Physiol 37:539–574

    Article  CAS  Google Scholar 

  • Selker JML, Newcomb EH (1985) Spatial relationships between uninfected and infected cells in root nodules of soybean. Planta 165:446–454

    Article  CAS  PubMed  Google Scholar 

  • Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25

    Article  CAS  PubMed  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–42

    Article  CAS  PubMed  Google Scholar 

  • Sutton WD (1983) Nodule development and senescence. In: Broughton WJ (ed) Nitrogen fixation. Vol 3. Legumes. Clarendon Press, Oxford, pp 144–212

    Google Scholar 

  • Tang C, Robson AD, Dilworth MJ, Kuo J (1992) Microscopic evidence on how iron deficiency limits initiation in Lupinus augustifolius L. New Phytol 121:457–467

    Article  CAS  Google Scholar 

  • Timmers ACJ, Soupène E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G (2000) Saprophytic intracellular rhizobia in alfalfa nodules. Mol Plant-Microbe Interact 13:1204–1213

    Article  CAS  PubMed  Google Scholar 

  • Valladares F, Villar-Salvador P, Domínguez S, Fernández-Pascual PJL, Pugnaire FI (2002) Enhancing the early performance of the leguminous shrub Retama sphaerocarpa (L.) Boiss.: fertilisation versus Rhizobium inoculation. Plant Soil 240:253–262

    Article  CAS  Google Scholar 

  • Vega-Hernández MC, Pérez-Galdona R, Dazzo FB, Jarabo-Lorenzo A, Alfayate MC, León-Barrios M (2001) Novel infection process in the indeterminate root nodule symbiosis between Chamaecytisus proliferus (tagasaste) and Bradyrhizobium sp. New Phytol 150:707–721

    Article  Google Scholar 

  • Vinuesa P, Silva C, Werner D, Martínez-Romero E (2005) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 34:29–54

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Frédéric Debellé for critically reading the manuscript. This work was supported by the French Laboratory of Excellence project “TULIP” (ANR-10-LABX-41); ANR-11-IDEX-0002-02).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ton Timmers.

Additional information

Responsible Editor: Euan K. James.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1

Sequences from 16S rRNA, atpD, glnII and RecA obtained from Retama monosperma nodules in FASTA format (PDF 24 kb)

Online resource 2

Blastn Alignments of 16S rRNA, atpD, glnII and RecA sequences with the homologous sequences of Bradyrhizobium retamae strain R7Q2. (PDF 42 kb)

Online resource 3

Semithin section of the apical region of a nodule of R. monosperma observed by fluorescence microscopy under UV excitation (ex: 365/12, em: LP397). The outer cortical cell walls have a strong autofluorescence indicative of lignification. The nodule endodermis also fluoresces strongly and is multilayered. Scale bar 400 μm. (JPEG 823 kb)

Online resource 4

Semithin sections of peripheral regions of nodules of R. monosperma showing the nodule endodermis under UV excitation (ex: 365/12, em: LP397) in A to C and the corresponding DIC images in D to E. A. Apical region close to the meristem. B. The middle region of the nodule. C. The basal part of the nodule close to the root. Scale bar 75 μm. (JPEG 1247 kb)

Online resource 5

Ploidy profiles of different organs of R. monosperma determined by flow cytometry. Only in nodules a low level of DNA endoreduplication is observed. (JPEG 675 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Selami, N., Auriac, MC., Catrice, O. et al. Morphology and anatomy of root nodules of Retama monosperma (L.)Boiss.. Plant Soil 379, 109–119 (2014). https://doi.org/10.1007/s11104-014-2045-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2045-5

Keywords

Navigation