Lipo-chitooligosaccharide Nodulation Signals from Rhizobium meliloti Induce Their Rapid Degradation by the Host Plant Alfalfa

Extracellular enzymes from alfalfa (Medicago sativa L.) involved in the degradation of nodulation (Nod) factors could be distinguished by their different cleavage specificities and were separated by lectin affinity chromatography. A particular glycoprotein was able to release an acylated lipo-disaccharide from all tested Nod factors having an oligosaccharide chain length of four or five residues. Structural modifications of the basic lipo-chitooligosaccharide did not affect the cleavage site and had only weak influence on the cleavage efficiency of Nod factors tested. The acylated lipo-trisaccharide was resistant to degradation. When alfalfa roots were preincubated with Nod factors at nanomolar concentrations, the activity of the dimer-forming enzyme was stimulated up to 6-fold within a few hours. The inducing activity of Nod factors decreased in the order NodRm-IV(C16:2,Ac,S) > NodRm-IV(C16:2,S) and NodRm-V(C16:2,Ac,S) > NodRm-V(C16:2,S) > NodRm-IV(C16:0,S) > NodRm-IV(C16:2). Pretreatment with NodRm-III(C16:2) as well as unmodified chitooligosaccharides did not stimulate the dimer-forming enzyme. Roots preincubated with Rhizobium meliloti showed similar stimulation of the dimer-forming activity. Mutant strains unable to produce Nod factors did not enhance the hydrolytic activity. These results indicate a rapid feedback inactivation of Nod signals after their perception by the host plant alfalfa.

[1]  J. Dénarié,et al.  Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. , 1996, Annual review of biochemistry.

[2]  G. Stacey,et al.  The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. , 1994, Molecular plant-microbe interactions : MPMI.

[3]  M. Crespi,et al.  enod40, a gene expressed during nodule organogenesis, codes for a non‐translatable RNA involved in plant growth. , 1994, The EMBO journal.

[4]  H. Hirt,et al.  Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. , 1994, The Plant cell.

[5]  E. Journet,et al.  Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. , 1994, The Plant journal : for cell and molecular biology.

[6]  T. Bisseling,et al.  Root Hair Deformation Activity of Nodulation Factors and Their Fate on Vicia sativa , 1994, Plant physiology.

[7]  M. Crespi,et al.  Alfalfa Enod12 Genes Are Differentially Regulated during Nodule Development by Nod Factors and Rhizobium Invasion , 1994, Plant physiology.

[8]  E. Kondorosi,et al.  Biosynthesis of lipooligosaccharide nodulation factors: Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Mellor,et al.  Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  R. Mellor,et al.  Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases , 1994 .

[11]  Z. Magyar,et al.  Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. , 1994, The EMBO journal.

[12]  J. Thomas-Oates,et al.  Nodulation protein NodL of Rhizobium leguminosarum O‐acetylates lipo‐oligosaccharides, chitin fragments and N‐acetylglucosamine in vitro , 1994, Molecular microbiology.

[13]  M. Parniske,et al.  Plant defense responses of host plants with determinate nodules induced by eps-defective exob mutants of bradyrhizobium-japonicum , 1994 .

[14]  E. Kondorosi,et al.  Cell and Molecular Biology of Rhizobium-Plant , 1994 .

[15]  M. Crespi,et al.  Effects of Nod Factors on Plants , 1994 .

[16]  J. Mikkelsen,et al.  Plant chitinases. , 2008, The Plant journal : for cell and molecular biology.

[17]  J. Dénarié,et al.  Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. , 1993, The Journal of biological chemistry.

[18]  Jean Dénarié,et al.  Lipo-oligosaccharide nodulation factors: A new class of signaling molecules mediating recognition and morphogenesis , 1993, Cell.

[19]  J. Vasse,et al.  Abortion of infection during the Rhizobium meliloti—alfalfa symbiotic interaction is accompanied by a hypersensitive reaction , 1993 .

[20]  B. Staskawicz,et al.  Prokaryotic plant parasites , 1993, Cell.

[21]  T. Bisseling,et al.  Rhizobium Lipooligosaccharides Rescue a Carrot Somatic Embryo Mutant. , 1993, The Plant cell.

[22]  E. Kondorosi,et al.  The Sulfate Group on the Reducing End Protects Nod Signals of R. Meliloti Against Hydrolysis by Medicago Chitinases , 1993 .

[23]  E. Journet,et al.  Expression of the Medicago Truncatula ENOD12 Gene in Response to R. Meliloti Nod Factors and during Spontaneous Nodulation in Transgenic Alfalfa , 1993 .

[24]  T. Heitz,et al.  Plant 'pathogenesis-related' proteins and their role in defense against pathogens. , 1993, Biochimie.

[25]  R. Palacios,et al.  New Horizons in Nitrogen Fixation , 1993, Current Plant Science and Biotechnology in Agriculture.

[26]  T. Boller,et al.  Genes Involved in Plant Defense , 1994, Plant Gene Research.

[27]  A. Hirsch.  Developmental biology of legume nodulation. , 1992, The New phytologist.

[28]  D. Ehrhardt,et al.  Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. , 1992, Science.

[29]  R. Mellor,et al.  Partial purification and characterization of trehalase from soybean nodules , 1992 .

[30]  Shuhei Tanaka,et al.  Induction Patterns of Chitinases in Yam Callus by Inoculation with Autoclaved Fusarium oxysporum, Ethylene, and Chitin and Chitosan Oligosaccharides. , 1992, Bioscience, biotechnology, and biochemistry.

[31]  J. Ryals,et al.  The Primary Structure of Plant Pathogenesis-related Glucanohydrolases and Their Genes , 1992 .

[32]  E. Kondorosi,et al.  Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[33]  P. Lerouge,et al.  Molecular basis of symbiotic host specificity in rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals , 1991, Cell.

[34]  H. Inui,et al.  Induction of Chitinases in Rice Callus Treated with Chitin Derivatives , 1991 .

[35]  P. Lerouge,et al.  Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa , 1991, Nature.

[36]  G. Caetano-Anollés,et al.  Plant genetic control of nodulation. , 1991, Annual review of microbiology.

[37]  Philippe Roche,et al.  Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal , 1990, Nature.

[38]  J. Gyuris,et al.  Positive and negative control of nod gene expression in Rhizobium meliloti is required for optimal nodulation , 1989, The EMBO journal.

[39]  D. Roby,et al.  Chitin oligosaccharides as elicitors of chitinase activity in melon plants. , 1987, Biochemical and biophysical research communications.

[40]  A. A. N. Brussel,et al.  Small leguminosae as test plants for nodulation of Rhizobium leguminosarum and other rhizobia and agrobacteria harbouring a leguminosarum sym-plasmid , 1982 .

[41]  E. Vincze,et al.  Genetic and Biochemical Analysis of Mutants Affected in Nitrate Reduction in Rhizobium meliloti , 1979 .