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. 1997 Dec;115(4):1329–1340. doi: 10.1104/pp.115.4.1329

The aberrant cell walls of boron-deficient bean root nodules have no covalently bound hydroxyproline-/proline-rich proteins.

I Bonilla 1, C Mergold-Villaseñor 1, M E Campos 1, N Sánchez 1, H Pérez 1, L López 1, L Castrejón 1, F Sánchez 1, G I Cassab 1
PMCID: PMC158598  PMID: 9414547

Abstract

B-deficient bean (Phaseolus vulgaris L.) nodules examined by light microscopy showed dramatic anatomical changes, mainly in the parenchyma region. Western analysis of total nodule extracts examined by sodium dodecyl sulfate-polyacrylamide gel electrophoresis showed that one 116-kD polypeptide was recognized by antibodies raised against hydroxyproline-rich glycoproteins (HRGPs) from the soybean (Glycine max) seed coat. A protein with a comparable molecular mass of 116 kD was purified from the cell walls of soybean root nodules. The amino acid composition of this protein is similar to the early nodulin (ENOD2) gene. Immunoprecipitation of the soybean ENOD2 in vitro translation product showed that the soybean seed coat anti-HRGP antibodies recognized this early nodulin. Furthermore, we used these antibodies to localize the ENOD2 homolog in bean nodules. Immunocytochemistry revealed that in B-deficient nodules ENOD2 was absent in the walls of the nodule parenchyma. The absence of ENOD2 in B-deficient nodules was corroborated by performing hydroxyproline assays. Northern analysis showed that ENOD2 mRNA is present in B-deficient nodules; therefore, the accumulation of ENOD2 is not affected by B deficiency, but its assembly into the cell wall is. B-deficient nodules fix much less N2 than control nodules, probably because the nodule parenchyma is no longer an effective O2 barrier.

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Selected References

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  1. Averyhart-Fullard V., Datta K., Marcus A. A hydroxyproline-rich protein in the soybean cell wall. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1082–1085. doi: 10.1073/pnas.85.4.1082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bolanos L., Brewin N. J., Bonilla I. Effects of Boron on Rhizobium-Legume Cell-Surface Interactions and Nodule Development. Plant Physiol. 1996 Apr;110(4):1249–1256. doi: 10.1104/pp.110.4.1249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bolanos L., Esteban E., De Lorenzo C., Fernandez-Pascual M., De Felipe M. R., Garate A., Bonilla I. Essentiality of Boron for Symbiotic Dinitrogen Fixation in Pea (Pisum sativum) Rhizobium Nodules. Plant Physiol. 1994 Jan;104(1):85–90. doi: 10.1104/pp.104.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonilla I., Garcia-González M., Mateo P. Boron requirement in cyanobacteria : its possible role in the early evolution of photosynthetic organisms. Plant Physiol. 1990 Dec;94(4):1554–1560. doi: 10.1104/pp.94.4.1554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boudart G., Dechamp-Guillaume G., Lafitte C., Ricart G., Barthe J. P., Mazau D., Esquerré-Tugayé M. T. Elicitors and suppressors of hydroxyproline-rich glycoprotein accumulation are solubilized from plant cell walls by endopolygalacturonase. Eur J Biochem. 1995 Sep 1;232(2):449–457. doi: 10.1111/j.1432-1033.1995.tb20830.x. [DOI] [PubMed] [Google Scholar]
  6. Cohen M. S. Effect of boron on cell elongation and division in squash roots. Plant Physiol. 1977 May;59(5):884–887. doi: 10.1104/pp.59.5.884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Datta K., Schmidt A., Marcus A. Characterization of two soybean repetitive proline-rich proteins and a cognate cDNA from germinated axes. Plant Cell. 1989 Sep;1(9):945–952. doi: 10.1105/tpc.1.9.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drózdz M., Kucharz E., Szyja J. A colorimetric micromethod for determination of hydroxyproline in blood serum. Z Med Labortech. 1976 Aug 4;17(4):163–171. [PubMed] [Google Scholar]
  9. Francisco S. M., Tierney M. L. Isolation and characterization of a proline-rich cell wall protein from soybean seedlings. Plant Physiol. 1990 Dec;94(4):1897–1902. doi: 10.1104/pp.94.4.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Franssen H. J., Nap J. P., Gloudemans T., Stiekema W., Van Dam H., Govers F., Louwerse J., Van Kammen A., Bisseling T. Characterization of cDNA for nodulin-75 of soybean: A gene product involved in early stages of root nodule development. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4495–4499. doi: 10.1073/pnas.84.13.4495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hong J. C., Cheong Y. H., Nagao R. T., Bahk J. D., Cho M. J., Key J. L. Isolation and characterization of three soybean extensin cDNAs. Plant Physiol. 1994 Feb;104(2):793–796. doi: 10.1104/pp.104.2.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hong J. C., Nagao R. T., Key J. L. Characterization and sequence analysis of a developmentally regulated putative cell wall protein gene isolated from soybean. J Biol Chem. 1987 Jun 15;262(17):8367–8376. [PubMed] [Google Scholar]
  13. Kobayashi M., Matoh T., Azuma Ji. Two Chains of Rhamnogalacturonan II Are Cross-Linked by Borate-Diol Ester Bonds in Higher Plant Cell Walls. Plant Physiol. 1996 Mar;110(3):1017–1020. doi: 10.1104/pp.110.3.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Loomis W. D., Durst R. W. Chemistry and biology of boron. Biofactors. 1992 Apr;3(4):229–239. [PubMed] [Google Scholar]
  16. Mackown C. T., Van Sanford D. A. Postanthesis nitrate assimilation in winter wheat : in situ flag leaf reduction. Plant Physiol. 1986 May;81(1):17–20. doi: 10.1104/pp.81.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Memelink J., Swords K. M., de Kam R. J., Schilperoort R. A., Hoge J. H., Staehelin L. A. Structure and regulation of tobacco extensin. Plant J. 1993 Dec;4(6):1011–1022. doi: 10.1046/j.1365-313x.1993.04061011.x. [DOI] [PubMed] [Google Scholar]
  18. Scheres B., Van De Wiel C., Zalensky A., Horvath B., Spaink H., Van Eck H., Zwartkruis F., Wolters A. M., Gloudemans T., Van Kammen A. The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell. 1990 Jan 26;60(2):281–294. doi: 10.1016/0092-8674(90)90743-x. [DOI] [PubMed] [Google Scholar]
  19. Showalter A. M. Structure and function of plant cell wall proteins. Plant Cell. 1993 Jan;5(1):9–23. doi: 10.1105/tpc.5.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sánchez F., Campos F., Padilla J., Bonneville J. M., Enríquez C., Caput D. Purification, cDNA Cloning, and Developmental Expression of the Nodule-Specific Uricase from Phaseolus vulgaris L. Plant Physiol. 1987 Aug;84(4):1143–1147. doi: 10.1104/pp.84.4.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wilson R. C., Long F., Maruoka E. M., Cooper J. B. A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. Plant Cell. 1994 Sep;6(9):1265–1275. doi: 10.1105/tpc.6.9.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. van de Wiel C., Scheres B., Franssen H., van Lierop M. J., van Lammeren A., van Kammen A., Bisseling T. The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J. 1990 Jan;9(1):1–7. doi: 10.1002/j.1460-2075.1990.tb08073.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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