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Discovery of an extended bundle sheath in Ricinus communis L. and its role as a temporal storage compartment for the iron chelator nicotianamine

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Abstract

The extended bundle sheath (EBS) is a specialized layer of cells that enhances the lateral transport of photoassimilates within the leaf. This little-known tissue is often considered to be legume-specific. We identified an EBS in cotyledons and leaves of the non-legume Ricinus communis L. By means of cytological and immunological studies and using the localization of the iron-chelator nicotianamine as an established indicator for mass transport, we confirmed its role as a transport tissue and a temporal sink. Observations on cotyledons of Ricinus seedlings further proved that the EBS carries out these tasks from a very early stage of development onwards. This is the first time that information has been obtained on the physiological role of an EBS in a non-legume. Our results support the idea of its widespread occurrence among higher plants.

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Fig. 1a, b. Fig. 2a, b.
Fig. 3a–i.
Figs. 4–8. Fig. 5a–c. Fig. 6a–c. Fig. 7a–c. Fig. 8a–c.
Fig. 9a–d.

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Abbreviations

EBS:

extended bundle sheath

NA:

nicotianamine

PVM:

paraveinal mesophyll

References

  • Bewley JD, Black M (1994) Seeds. Physiology of development and germination, 2nd edn. Plenum Press, New York

  • Brubaker CL, Lersten NR (1995) Paraveinal mesophyll: review and survey of the subtribe Erythrininae (Phaseoleae, Papilionoideae, Leguminosae). Plant Syst Evol 196:31–62

    Google Scholar 

  • Fischer DG (1967) An unusual layer of cells in the mesophyll of the soybean leaf. Bot Gaz 128:215–218

    Article  Google Scholar 

  • Franceschi VR, Giaquinta RT (1983a) The paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation: I. Ultrastructure and histochemistry during vegetative development. Planta 157:411–421

    Google Scholar 

  • Franceschi VR, Giaquinta RT (1983b) The paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation: II. Structural, metabolic, and compartmental changes during reproductive growth. Planta 157:422–431

    CAS  Google Scholar 

  • Franceschi VR, Giaquinta RT (1983c) Specialized cellular arrangements in legume leaves in relation to assimilate transport and compartmentation: comparison of the paraveinal mesophyll. Planta 159:415–422

    Google Scholar 

  • Haberlandt G (1896) Physiologische Pflanzenanatomie, 2nd edn. Engelmann, Leipzig

  • Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551

    PubMed  Google Scholar 

  • Kevekordes KG, McCully ME, Canny MJ (1987) The occurrence of an extended bundle sheath system (paraveinal mesophyll) in the legumes. Can J Bot 66:94–100

    Google Scholar 

  • Klauer SF, Franceschi VR (1997) Mechanism of transport of vegetative storage proteins to the vacuole of the paraveinal mesophyll of soybean leaf. Protoplasma 200:174–185

    CAS  Google Scholar 

  • Klauer SF, Franceschi VR, Ku MSB, Zhang D (1996) Identification and localization of vegetative storage proteins in legume leaves. Am J Bot 83:1–10

    CAS  Google Scholar 

  • Köhler J (1992) Die Bedeutung der verschiedenen Gewebe des Keimblattes von Ricinus communis L. für die Aufnahme von Saccharose und anderer im Phloem transportierter Stoffe. PhD thesis, Bayreuth, Germany

  • Köpff F (1892) Ueber die anatomische Charaktere der Dalbergieen, Sophoreen und Swartzieen. Dissertation, Friedrich-Alexander-Universität, Erlangen

  • Kriedemann P, Beevers H (1967) Sugar uptake and translocation in the castor bean seedling. I. Characteristics of transfer in intact and excised seedlings. Plant Physiol 42:161–173

    CAS  Google Scholar 

  • Krüger C (2001) Phloembeladung und -transport von Eisen und anderen Mikronährstoffen in Keimpflanzen von Ricinus communis L. Dissertation, Martin-Luther-Universität, Halle/Saale

  • Lansing AJ, Franceschi VR (2000) The paraveinal mesophyll: a specialized path for intermediary transport of assimilates in legume leaves. Aust J Plant Physiol 27:757–767

    Article  CAS  Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11:587–599

    Article  CAS  PubMed  Google Scholar 

  • Napp-Zinn K (1973) Anatomie des Blattes II A, 1. In: Zimmermann W, Carlquist S, Ozenda PG, Wulff HD (eds) Encyclopedia of plant anatomy. Bornträger, Berlin

  • Pich A, Hillmer S, Manteuffel R, Scholz G (1997) First immunohistochemical localization of the endogenous Fe-chelator nicotianamine. J Exp Bot 48:759–767

    CAS  Google Scholar 

  • Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Fe homeostasis in plant cells: Does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentrations? Planta 213:967–976

    CAS  PubMed  Google Scholar 

  • Radlkofer L (1890) Ueber die Gliederung der Familie der Sapindaceen. Sitzungsber Bayer Akad Wiss Math Naturwiss Kl 20:105–379

    Google Scholar 

  • Russin WA, Evert RF (1984) Studies on the leaf of Populus deltoides (Salicaceae): morphology and anatomy. Am J Bot 71:1398–1415

    Google Scholar 

  • Scholz G, Becker R, Pich A, Stephan UW (1992) Nicotianamine—a common constituent of strategies I and II of iron acquisition by plants. A review. J Plant Nutr 15:1647–1665

    CAS  Google Scholar 

  • Stephan UW, Scholz G (1993) Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiol Plant 88:522–529

    Article  CAS  Google Scholar 

  • Stephan UW, Schmidke I, Pich A (1994) Phloem translocation of Fe, Cu, Mn and Zn in Ricinus seedlings in relation to the concentrations of nicotianamine, an endogenous chelator of divalent metal ions, in different seedling parts. Plant Soil 165:181–188

    CAS  Google Scholar 

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Acknowledgement

The authors gratefully acknowledge Dr. R. Manteuffel (IPK Gatersleben, Germany) for kindly providing the antibody against nicotianamine and for helpful discussions.

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Correspondence to T. Rutten.

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Rutten, T., Krüger, C., Melzer, M. et al. Discovery of an extended bundle sheath in Ricinus communis L. and its role as a temporal storage compartment for the iron chelator nicotianamine. Planta 217, 400–406 (2003). https://doi.org/10.1007/s00425-003-1010-y

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