PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2019, Vol. 54, № 3, p. 446-457.
(how to cite this article)

doi: 10.15389/agrobiology.2019.3.446eng

UDC: 631.461.52:581.557:581.138.1

Acknowledgements:
Supported financially by Russian Science Foundation (project № 16-16-10035)

 

PLANT CELL WALL IN SYMBIOTIC INTERACTIONS. PECTINS

A.V. Tsyganova, V.E. Tsyganov

All-Russian Research Institute for Agricultural Microbiology, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia, e-mail isaakij@mail.ru, tsyganov@arriam.spb.ru (✉ corresponding author)

ORCID:
Tsyganova A.V. orcid.org/0000-0003-3505-4298
Tsyganov V.E. orcid.org/0000-0003-3105-8689

Received January 22, 2019

 

Since plant cells, unlike animals, are immobile and limited by rigid cell walls, often the properties of the plant extracellular matrix play a crucial role in the plant development. The extracellular matrix, in particular the cell walls, are involved in the molecular dialogue between partners during the interaction of plants and microorganisms during the formation of legume-rhizobial symbiosis (N.J. Brewin, 2004; M.K. Rich et al., 2014). Legume-rhizobial symbiosis is a convenient model for studying changes in the composition of the plant cell wall caused by interactions with bacteria. Colonization of host cells with nodule bacteria, rhizobia, involves the sequential reorganization of the plant-microbial interface. The bacterial components of the symbiotic interface include various surface polysaccharides (A.V. Tsyganova et al., 2012). Plant components include the cell wall, the extracellular matrix and the plasma membrane. In this review, we have summarized the data demonstrating the involvement of pectins, the polysaccharides of the cell wall matrix, in the legume-rhizobial symbiosis (K.H. Caffall et al., 2009; M.A. Atmodjo et al., 2013; C.T. Anderson, 2015). The greatest progress has been made in the study of homogalacturonan, for which highly specific monoclonal antibodies have been obtained (J.P. Knox et al., 1990; Y. Verhertbruggen et al., 2009). The level of methyl-esterification of homogalacturonan determines its function in nodules. It was shown that low methyl-esterified homogalacturonan is involved in increasing the rigidity of the cell walls and walls of infection threads (K.A. VandenBosch et al., 1989; A.L. Rae et al., 1992) that is especially manifested in ineffective interaction with rhizobia (K.A. Ivanova et al., 2015) and during the action of abiotic factors (M. Redondo-Nieto et al., 2003, 2007; M. Sujkowska-Rybkowska et al., 2015). High methyl-esterified homogalacturonan is observed in the cell walls at all stages of nodule development (A.L. Rae et al., 1992; A.V. Tsyganova et al., 2019). The absence of well characterized antibodies complicates the study of rhamnogalacturonan-II (M.A. O’Neill et al., 2004). However, it was shown that in nodules rhamnogalacturonan-II is present in the cell wall at the border with the plasma membrane, in undifferentiated symbiosomes, and also in the matrix of infection threads (M. Redondo-Nieto et al., 2003, 2007; M. Reguera et al., 2010). Probably, rhamnogalacturonan-II in combination with boron and arabinogalactan-protein extensins promotes movement of rhizobia in the matrix of infectious threads (M. Reguera et al., 2010). Only recently, we conducted the first studies aimed at identifying the role of rhamnogalacturonan-I in the development of nodules (A.V. Tsyganova et al., 2019). It has been shown that rhamnogalacturonan-I is present in the cell wall of the meristem cells, vascular bundles and in the walls of the infectious threads. However, its precise function remains unknown, although it was suggested that rhamnogalacturonan-I is involved in the perception of rhizobia as pathogens during ineffective symbiosis (A.V. Tsyganova et al., 2019). Thus, to date, it has been shown that all types of pectins are involved in the development of a symbiotic nodule. It is important to note that plant plays a central role in the remodelling of the cell wall during symbiotic interaction and the construction of the plant-microbe interface.

Keywords: legume-rhizobial symbiosis, plant-microbe interface, cell wall, infection thread, homogalacturonan, rhamnogalacturonans.

 

 

REFERENCES

  1. Cosgrove D.J. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol., 2005, 6(11): 850-861 CrossRef
  2. Malinovsky F.G., Fangel J.U., Willats W.G.T. The role of the cell wall in plant immunity. Front. Plant. Sci., 2014, 5: 178 CrossRef
  3. Keegstra K. Plant cell walls. Plant Physiol., 2010, 154(2): 483-486 CrossRef
  4. Lionetti V., Cervone F., Bellincampi D. Methyl esterification of pectin plays a role during plant—pathogen interactions and affects plant resistance to diseases. J. Plant Physiol., 2012, 169(16): 1623-1630 CrossRef
  5. Palin R., Geitmann A. The role of pectin in plant morphogenesis. Biosystems, 2012, 109(3): 397-402 CrossRef
  6. Bellincampi D., Cervone F., Lionetti V. Plant cell wall dynamics and wall-related susceptibility in plant—pathogen interactions. Front. Plant. Sci., 2014, 5: 228 CrossRef
  7. Brewin N.J. Plant cell wall remodelling in the Rhizobium—legume symbiosis. Crit. Rev. Plant Sci., 2004, 23(4): 293-316 CrossRef
  8. Rich M.K., Schorderet M., Reinhardt D. The role of the cell wall compartment in mutualistic symbioses of plants. Front. Plant. Sci., 2014, 5: 238 CrossRef
  9. Parniske M. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr. Opin. Plant Biol., 2000, 3(4): 320-328 CrossRef
  10. Rae A.L., Bonfante-Fasolo P., Brewin N.J. Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum. Plant J., 1992, 2(3): 385-395 CrossRef
  11. Ivanova K.A., Tsyganova A.V., Brewin N.J., Tikhonovich I.A., Tsyganov V.E. Induction of host defences by Rhizobium during ineffective nodulation of pea (Pisum sativum L.) carrying symbiotically defective mutations sym40 (PsEFD), sym33 (PsIPD3/PsCYCLOPS) and sym42. Protoplasma, 2015, 252(6): 1505-1517 CrossRef
  12. Tsyganova A.V., Tsyganov V.E., Borisov A.Yu., Tikhonovich I.A., Brevin N.D. Ekologicheskaya genetika, 2009, 7(3): 3-9 (in Russ.).
  13. Bradley D.J., Wood E.A., Larkins A.P., Galfre G., Butcher G.W., Brewin N.J. Isolation of monoclonal antibodies reacting with peribacteriod membranes and other components of pea root nodules containing Rhizobium leguminosarum. Planta, 1988, 173(2): 149-160 CrossRef
  14. VandenBosch K.A., Bradley D.J., Knox J.P., Perotto S., Butcher G.W., Brewin N.J. Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J., 1989, 8(2): 335-341 CrossRef
  15. Vincken J.-P., Schols H.A., Oomen R.J., McCann M.C., Ulvskov P., Voragen A.G., Visser R.G. If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol., 2003, 132(4): 1781-1789 CrossRef
  16. Anderson C.T. We be jammin': an update on pectin biosynthesis, trafficking and dynamics. J. Exp. Bot., 2015, 67(2): 495-502 CrossRef
  17. Atmodjo M.A., Hao Z., Mohnen D. Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol., 2013, 64(1): 747-779 CrossRef
  18. Caffall K.H., Mohnen D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res., 2009, 344(14): 1879-1900 CrossRef
  19. Saffer A.M. Expanding roles for pectins in plant development. J. Integr. Plant. Biol., 2018, 60(10): 910-923 CrossRef
  20. Larskaya I.A., Gorshkova T.A. Plant oligosaccharides — outsiders among elicitors? Biochemistry (Moscow), 2015, 80(7): 881-900 CrossRef
  21. Willats W.G., Steele‐King C.G., Marcus S.E., Knox J.P. Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J., 1999, 20(6): 619-628 CrossRef
  22. Peaucelle A., Louvet R., Johansen J.N., Höfte H., Laufs P., Pelloux J., Mouille G. Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr. Biol., 2008, 18(24): 1943-1948 CrossRef
  23. McCartney L., Ormerod A.P., Gidley M.J., Knox J.P. Temporal and spatial regulation of pectic (1→4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J., 2000, 22(2): 105-113 CrossRef
  24. Mohnen D. Pectin structure and biosynthesis. Curr. Opin. Plant Biol., 2008, 11(3): 266-277 CrossRef
  25. Wolf S., Mouille G., Pelloux J. Homogalacturonan methyl-esterification and plant development. Mol. Plant, 2009, 2(5): 851-860 CrossRef
  26. Lievens S., Goormachtig S., Herman S., Holsters M. Patterns of pectin methylesterase transcripts in developing stem nodules of Sesbania rostrata. Mol. Plant-Microbe Interact., 2002, 15(2): 164-168 CrossRef
  27. Prade R.A., Zhan D., Ayoubi P., Mort A.J. Pectins, pectinases and plant-microbe interactions. Biotechnol. Genet. Eng. Rev., 1999, 16(1): 361-392 CrossRef
  28. Levesque-Tremblay G., Pelloux J., Braybrook S.A., Müller K. Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta, 2015, 242(4): 791-811 CrossRef
  29. Wolf S., Greiner S. Growth control by cell wall pectins. Protoplasma, 2012, 249(2): 169-175 CrossRef
  30. Pelloux J., Rustérucci C., Mellerowicz E.J. New insights into pectin methylesterase structure and function. Trends Plant Sci., 2007, 12(6): 267-277 CrossRef
  31. Lionetti V., Fabri E., De Caroli M., Hansen A.R., Willats W.G.T., Piro G., Bellincampi D. Three pectin methylesterase inhibitors protect cell wall integrity for Arabidopsis immunity to Botrytis. Plant Physiol., 2017, 173(3): 1844-1863 CrossRef
  32. Peaucelle A., Braybrook S.A., Le Guillou L., Bron E., Kuhlemeier C., Höfte H. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol., 2011, 21(20): 1720-1726 CrossRef
  33. Pogorelko G., Lionetti V., Bellincampi D., Zabotina O. Cell wall integrity: Targeted post-synthetic modifications to reveal its role in plant growth and defense against pathogens. Plant Signal Behav., 2013, 8(9): e25435 CrossRef
  34. Rodríguez-Llorente I.D., Pérez-Hormaeche J., Mounadi K.E., Dary M., Caviedes M.A., Cosson V., Kondorosi A., Ratet P., Palomares A.J. From pollen tubes to infection threads: recruitment of Medicago floral pectic genes for symbiosis. Plant J., 2004, 39(4): 587-598 CrossRef
  35. Fauvart M., Verstraeten N., Dombrecht B., Venmans R., Beullens S., Heusdens C., Michiels J. Rhizobium etli HrpW is a pectin-degrading enzyme and differs from phytopathogenic homologues in enzymically crucial tryptophan and glycine residues. Microbiology, 2009, 155(9): 3045-3054 CrossRef
  36. Muñoz J.A., Coronado C., Pérez-Hormaeche J., Kondorosi A., Ratet P., Palomares A.J. MsPG3, a Medicago sativa polygalacturonase gene expressed during the alfalfa—Rhizobium meliloti interaction. PNAS USA, 1998, 95(16): 9687-9692 CrossRef
  37. Xie F., Murray J.D., Kim J., Heckmann A.B., Edwards A., Oldroyd G.E.D., Downie J.A. Legume pectate lyase required for root infection by rhizobia. PNAS USA, 2012, 109(2): 633-638 CrossRef
  38. Knox J.P., Linstead P.J., King J., Cooper C., Roberts K. Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta, 1990, 181(4): 512-521 CrossRef
  39. Verhertbruggen Y., Marcus S.E., Haeger A., Ordaz-Ortiz J.J., Knox J.P. An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr. Res., 2009, 344(14): 1858-1862 CrossRef
  40. Guillemin F., Guillon F., Bonnin E., Devaux M.-F., Chevalier T., Knox J.P., Liners F., Thibault J.-F. Distribution of pectic epitopes in cell walls of the sugar beet root. Planta, 2005, 222(2): 355-371 CrossRef
  41. Tsyganova A.V., Seliverstova E.V., Ivanova K.A., Brewin N.J., Tsyganov V.E. Comparative analysis of remodelling of the plant—microbe interface in Pisum sativum and Medicago truncatula symbiotic nodules. Protoplasma, 2019, 256(4): 983-996 CrossRef
  42. Sherrier D.J., Taylor G.S., Silverstein K.A.T., Gonzales M.B., VandenBosch K.A. Accumulation of extracellular proteins bearing unique proline-rich motifs in intercellular spaces of the legume nodule parenchyma. Protoplasma, 2005, 225(1): 43-55 CrossRef
  43. Ivanov S., Fedorova E.E., Limpens E., De Mita S., Genre A., Bonfante P., Bisseling T. Rhizobium—legume symbiosis shares an exocytotic pathway required for arbuscule formation. PNAS USA, 2012, 109(21): 8316-8321 CrossRef
  44. Gavrin A., Chiasson D., Ovchinnikova E., Kaiser B.N., Bisseling T., Fedorova E.E. VAMP721a and VAMP721d are important for pectin dynamics and release of bacteria in soybean nodules. New Phytol., 2016, 210(3): 1011-1021 CrossRef
  45. Redondo-Nieto M., Pulido L., Reguera M., Bonilla I., Bolaños L. Developmentally regulated membrane glycoproteins sharing antigenicity with rhamnogalacturonan II are not detected in nodulated boron deficient Pisum sativum. Plant Cell Environ., 2007, 30(11): 1436-1443 CrossRef
  46. Redondo-Nieto M., Wilmot A.R., El-Hamdaoui A., Bonilla I., Bolaños L. Relationship between boron and calcium in the N2-fixing legume—rhizobia symbiosis. Plant Cell Environ., 2003, 26(11): 1905-1915 CrossRef
  47. Sujkowska-Rybkowska M., Borucki W. Pectins esterification in the apoplast of aluminum-treated pea root nodules. J. Plant Physiol., 2015, 184: 1-7 CrossRef
  48. Carpena R.O., Esteban E., Sarro M.J., Peñalosa J., Gárate A.N., Lucena J.J., Zornoza P. Boron and calcium distribution in nitrogen-fixing pea plants. Plant Sci., 2000, 151(2): 163-170 CrossRef
  49. O’Neill M.A., Ishii T., Albersheim P., Darvill A.G. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu. Rev. Plant Biol., 2004, 55(1): 109-139 CrossRef
  50. Redondo-Nieto M., Maunoury N., Mergaert P., Kondorosi E., Bonilla I., Bolaños L. Boron and calcium induce major changes in gene expression during legume nodule organogenesis. Does boron have a role in signalling? New Phytol., 2012, 195(1): 14-19 CrossRef
  51. Bolaños L., Brewin N.J., Bonilla I. Effects of Boron on Rhizobium-legume cell-surface interactions and nodule development. Plant Physiol., 1996, 110(4): 1249-1256 CrossRef
  52. Bolaños L., Cebrián A., Redondo-Nieto M., Rivilla R., Bonilla I. Lectin-like glycoprotein PsNLEC-1 is not correctly glycosylated and targeted in boron-deficient pea nodules. Mol. Plant-Microbe Interact., 2001, 14(5): 663-670 CrossRef
  53. Bolaños 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, 104(1): 85-90 CrossRef
  54. Bonilla I., Mergold-Villasenor C., Campos M.E., Sanchez N., Perez H., Lopez L., Cas-trejon L., Sanchez F., Cassab G.I. The aberrant cell walls of boron-deficient bean root nodules have no covalently bound hydroxyproline/proline-rich proteins. Plant Physiol., 1997, 115(4): 1329-1340 CrossRef
  55. Matoh T., Takasaki M., Takabe K., Kobayashi M. Immunocytochemistry of rhamno-galacturonan II in cell walls of higher plants. Plant Cell Physiol., 1998, 39(5): 483-491 CrossRef
  56. Reguera M., Abreu I., Brewin N.J., Bonilla I., Bolaños L. Borate promotes the formation of a complex between legume AGP-extensin and rhamnogalacturonan II and enhances production of Rhizobium capsular polysaccharide during infection thread development in Pisum sativum symbiotic root nodules. Plant Cell Environ., 2010, 33(12): 2112-2120 CrossRef
  57. Gorshkova T.A., Kozlova L.V., Mikshina P.V. Biokhimiya, 2013, 78(7): 1068-1088 (in Russ.).
  58. Mikshina P.V., Petrova A.A., Faizullin D.A., Zuev Yu.F., Gorshkova T.A. Biokhimiya, 2015, 80(7): 1088-1098 (in Russ.).
  59. Lee K.J.D., Cornuault V., Manfield I.W., Ralet M.-C., Knox P.J. Multi-scale spatial heterogeneity of pectic rhamnogalacturonan I (RG-I) structural features in tobacco seed endosperm cell walls. Plant J., 2013, 75(6): 1018-1027 CrossRef
  60. Jones L., Seymour G.B., Knox J.P. Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-b-D-galactan. Plant Physiol., 1997, 113(4): 1405-1412 CrossRef
  61. Moore P.J., Staehelin L.A. Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.; implication for secretory pathways. Planta, 1988, 174(4): 433-445 CrossRef
  62. Corral-Martínez P., García-Fortea E., Bernard S., Driouich A., Seguí-Simarro J.M. Ultra-structural immunolocalization of arabinogalactan protein, pectin and hemicellulose epitopes through anther development in Brassica napus. Plant Cell Physiol., 2016, 57(10): 2161-2174 CrossRef
  63. Liu J., Hou J., Chen H., Pei K., Li Y., He X.-Q. Dynamic changes of pectin epitopes in cell walls during the development of the procambium–cambium continuum in poplar. Int. J. Mol. Sci., 2017, 18(8): 1716 CrossRef
  64. Torode T.A., O’Neill R., Marcus S.E., Cornuault V., Pose S., Lauder R.P., Kračun S.K., Rydahl M.G., Andersen M.C., Willats W.G. Branched pectic galactan in phloem-sieve-element cell walls: implications for cell mechanics. Plant Physiol., 2018, 176(2): 1547-1558 CrossRef
  65. Lehner A., Dardelle F., Soret-Morvan O., Lerouge P., Driouich A., Mollet J.-C. Pectins in the cell wall of Arabidopsis thaliana pollen tube and pistil. Plant Signal Behav., 2010, 5(10): 1282-1285 CrossRef
  66. Tsyganova A.V., Seliverstova E.V., Brewin N.J., Tsyganov V.E. Bacterial release is accompanied by ectopic accumulation of cell wall material around the vacuole in nodules of Pisum sativum sym33-3 allele encoding transcription factor PsCYCLOPS/PsIPD3. Protoplasma, 2019 CrossRef [Epub ahead of print].
  67. Gorshkov V.Y., Daminova A.G., Mikshina P.V., Petrova O.E., Ageeva M.V., Salnikov V.V., Gorshkova T.A., Gogolev Y.V. Pathogen-induced conditioning of the primary xylem vessels — a prerequisite for the formation of bacterial emboli by Pectobacterium atrosepticum. Plant Biol., 2016, 18(4): 609-617 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)