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Differential accumulation of hydroxyproline-rich glycoproteins in bean root nodule cells infected with a wild-type strain or a C4-dicarboxylic acid mutant of Rhizobium leguminosarum bv. phaseoli

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Abstract

An antiserum raised against deglycosylated hydroxyproline-rich glycoproteins (HPGPs) from melon (Cucumis melo L.) was used to study the relationship between Rhizobium infection and induction of HRGPs in bean (Phaseolus vulgaris L.) root nodule cells infected with either the wild-type or a C4-dicarboxylic acid mutant strain of Rhizobium leguminosarum bv. phaseoli. In effective nodules, where fixation of atmospheric dinitrogen is taking place, HRGPs were found to accumulate mainly in the walls of infected cells and in peribacteroid membranes surrounding groups of bacteroids. Internal ramifications of the peribacteroid membrane were also enriched in HRGPs whereas the peribacteroid space as well as the bacteroids themselves were free of these glycoproteins. In mutant-induced root nodules, HRGPs were specifically associated with the electron-dense, laminated structures formed in plastids as a reaction to infection by this mutant. The presence of HRGPs was also detected in the host cytoplasm. The aberrant distribution of HRGPs in infected cells of mutant-induced nodules likely reflects one aspect of the altered host metabolism in relation to peribacteroid-membrane breakdown. The possibility that the antiserum used for HRGP localization may have cross-reacted with ENOD 2 gene products is discussed in relation to amino-acid sequences and sites of accumulation.

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Abbreviations

GAR gold antibodies:

gold-conjugated goat antiserum to rabbit immunoglobulins

HRP:

deglycosylated hydroxyproline-rich glycoprotein

HRGP:

hydroxyproline-rich glycoprotein

PHB:

poly-B-hydroxybutyrate

PBS:

phosphate-buffered saline

TFMS:

trifluoromethane sulfonic acid

WT:

wild-type

B :

bacteroid

Cy :

cytoplasm

HCW :

host cell wall

IS :

intercellular space

IT :

infection thread

LS :

laminated structure

N :

nucleus

P :

peroxisome

PHB :

poly-β-hydroxybutyrate

PM :

peribacteroid membrane

PS :

peribacteroid space

S :

starch grain

Va :

vacuole

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Authors and Affiliations

  1. Département de phytologie, Université Laval, G1K 7P4, Sainte-Foy, Qué, Canada

    Nicole Benhamou

  2. Département des sols, Faculté des sciences de l'agriculture et de l'alimentation, Université Laval, G1K 7P4, Sainte-Foy, Qué, Canada

    Pierre J. Lafontaine

  3. Centre de Physiologie végétale, UA 241, CNRS, Université Paul Sabatier, 118, route de Narbonne, F-31062, Toulouse Cedex, France

    Dominique Mazau & Marie-Thérèse Esquerré-Tugayé

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  1. Nicole Benhamou
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  2. Pierre J. Lafontaine
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  3. Dominique Mazau
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  4. Marie-Thérèse Esquerré-Tugayé
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Additional information

This study was supported by grants from the National Research Council of Canada and from the Ministère de l'Éducation du Québec (FCAR). The authors thank S. Noël for excellent technical assistance and C. Parent for typing this manuscript.

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Benhamou, N., Lafontaine, P.J., Mazau, D. et al. Differential accumulation of hydroxyproline-rich glycoproteins in bean root nodule cells infected with a wild-type strain or a C4-dicarboxylic acid mutant of Rhizobium leguminosarum bv. phaseoli . Planta 184, 457–467 (1991). https://doi.org/10.1007/BF00197893

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