Simbiogenetics of microbe-plant interactions



Cite item

Full Text

Abstract

We present the concept of symbiogenetics defined as a branch of general genetics which investigates the Super-Organism Genetic Systems (SOGS) formed due to functional integration of partners' genes during symbiotic interactions. The minimal hereditary unit within SOGS involves no less than a pair of genes that belong to different partners and interact according to the models of complementation or epistasis. Using the examples of plant-microbe interactions we demonstrate that the integrity of SOGS is maintained due to tight signal interactions between partners and is manifested as formation of common biochemical pathways and as development of special symbiotic structures. Using the models of nodule development we demonstrate that the origin of SOGS involves recruiting of genes, which performed diverse functions in free-living organisms, into the symbiotic regulatory networks. The progressive evolution of nodule structures in different dicot lineages was based on the parallel recruiting of genes from the ancestral gene pool into symbiotic regulatory networks. The majority of mutualistic and antagonistic plant-microbe symbioscs represent the components of an evolutionary continuum that originated early in land plants and underwent intensive transformations due to high plasticity of SOGS based on inter- and intra-gene recombination.

About the authors

Igor A Tikhonovich

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: arriam@arriam.spb.ru. contact@arriam.spb.ru Podbelskiy Ch., 3, Saint-Petersburg, Pushkin-8

Nikolay A Provorov

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: provorov@newmail.ru

References

  1. Дьяков Ю.Т., Озерецковская О.Л., Джавахия В.Г., Багирова С.Ф. Общая и молекулярная фитопатология.-М: Общество фитопатологов, 2001. -302 с.
  2. Козо-Полянский Б.М. Основной биогенетический закон с ботанической точки зрения. Воронежское областное книгоиздательство, 1937. -25:5 с.
  3. Лобашов М.Е. Генетика.-2-е издание.-Л.: Изд-во ЛГУ, 1967.-751 с.
  4. Лутова Л.А., Пропоров НА., Тиходеев ОН. и др. Генетика развития растений/Под ред. С.Г. Ингс-Всчтомова. -СПб.: Наука, 2000. -539 с.
  5. Любищев А.А. Из переписки СВ. Мсйсна и А.А. Любищсва (1968-1972)//Природа.-1990. -№ 4.-С. 81.
  6. Проворов НА. Гснстико-эволюционные основы учения о симбиозе//Журн. Общей биологии. -2001. -Т. 62. -JVs 6.-С. 472-495.
  7. Тихонович И.А., Проворов НА. (ред.). Генетика симбиотической азотфиксации с основами селекции.-СПб.: Наука, 1998.-194 с.
  8. Akita M., Andersson R.A. Pirhonen M. ct al. Moss as a model system for studies on plant-palhogcn interactions//Biology of Plant-Microbe Interactions. Vol. 4./Eds. Tikhonovich I.A., Lugtcnbcrg B.J.J., Provorov N.A. St.-Pctcrsburg: 1S-MPMI, 2004 (in press).
  9. Bulandreau J., Viallard V., Cournoyer B. ct al. Bwkholderia cepacia Gcnomovar III is a common plant-associated bacterium//Appl. Environ. Microbiol. -2001. -Vol. 67. -N 2. -P. 982-985.
  10. Baumann P., Moran N.A., Baumann L. The evolution and genetics of aphid endosymbionts//BioSci. -1997.-Vol. 47, N 1.-P. 12-20.
  11. Biancioito V., Lumini E., Lanfranco L. ct al. Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaccac//Appl. Environ. Microbiol. -2000. -Vol. 66. -P. 4503-4509.
  12. Boddey R.M., Reis V.M., Urquigava S. ct al. N2 fixation in sugar cane: the role of Acetobacter diazolrophicus II Nitrogen Fixation: Fundamentals and Applications/Eds. Tikhonovich I.A., Provorov N.A., Romanov V.I., Newton B.E. Dordrecht: Kluwcr Academic Publishers, 1995.-P. 641-646.
  13. Borisov A.Y., Madsen L.H., Tsyganov V.E. ct al. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus II Plant Physiol. -2003. -Vol. 131. -P. 1009-1017.
  14. Brewin N.J. Tissue and cell invasion by Rhizobium: the structure and development of infection threads and symbiosomes//The Rhizobiaccac/Eds. Spaink H., Konodorosi A., Hooykaas PJ. Dordrecht, Boston, London: Kluwcr Acad. Publ. -1998. -P. 417-429.
  15. Buttner D., Bonas U. Common infection strategics of plant and animal pathogenic bacteria//Current Opinions in Plant Biology. -2003. -Vol. 6.-P. 312-319.
  16. Charles T.C., Shouguang J., Nester E.W. Two-component sensory transduction systems in phytobactcria//Ann. Rev. Phytopathol. -1992. -Vol. 30. -P. 463-484.
  17. Cook D.R. Medicago truncutula-a model for making!//Current Opinions in Plant Biology. -1999. -Vol. 2. -P. 301-304.
  18. Denarie J., Debelle F, Rosenberg C. Signaling and host range variation in nodulation//Annu. Rev. Microbiol. -1992.-Vol. 46.-P. 497-531.
  19. Flor H.H. Genetics of pathogenicity in Melampsora lini II J. Agric. Res. -1946. -Vol. 73. -P. 335-357.
  20. Franken P., Requena N. Analysis of gene expression in arbuscular mycorrhizas: new approaches and challenges//New Phyto-logist. -2001. -Vol. 150.-P. 517-523.
  21. Franssen H.J., Nap J.P., Bisseling T. Nodulins in root nodule development//Biological Nitrogen Fixation/Eds. Staccy G., Burris R.H., Evans H.J. New York, London: Chapman and Hall. -1992. -P. 598-624.
  22. Gianinazzi-Pearson V. Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis//The Plant Cell. -1996, -Vol. 8.-P. 1871-1883.
  23. Gresshoj] P.M., Buzas D.M., Laniya T. ct al. Systemic regulation of nodulation by a leaf-controlled LRR-rcccptor kinase//Biology of Plant-Microbe Interactions. V. 4./Eds. Tikhonovich I.A., Lugtcn-bcrg B.J.J., Provorov N.A. St.-Petersburg: IS-MPMI, 2004 (in press).
  24. Gualtieri G., Bisseling T. The evolution of nodulation//Plant Mol. Biol. -2000. -Vol. 42. -P. 181-194.
  25. Guinel F.C., Geil R.D. A model for the development of the rhizobial and arbuscular mycorrhizal symbioscs in legumes and its use to understand the roles of ethylene in the establishment of these two symbioscs//Canad. J. Bot. -2002. -Vol. 80. -P. 695-720.
  26. Herd S., Christensen M.J., Saunders K. ct al. Quantitative assessment of in planta distribution of metabolic activity and gene expression of an endophytic fungus//Microbiology.-1997. -Vol. 143.-P. 267-275.
  27. Kaminski P.A., Balut J., Boistard P. A survay of symbiotic nitrogen fixation by rhizobia//The Rhizobiaccac/Eds. Spaink H., Konodorosi A., Hooykaas P.J.J. Dordrecht; Boston; London: Kluwcr Acad. Publ.-1998.-P. 431-460
  28. Kannenberg E.L., Reuhs B.L., Forsberg L.S., Carlson R.W. Lipopolysaccharidcs and K-antigcns: their structures, biosynthesis and functions//The Rhizobiaccac/Eds. Spaink H., Konodorosi A., Hooykaas P.J. Dordrecht, Boston, London: Kluwcr Acad. Publ.-1998,-P. 119-154.
  29. Kapulnik Y, Volpin H., Itzhaki H. ct al. Suppression of defense responses in mycorrhizal alfalfa and tobacco roots//New Phyto-logist. -1996. -Vol. 133. -P. 59-64.
  30. Kistner C, Pamiske M. Evolution of signal transduction in intracellular symbiosis//Trends in Plant Sci. -2002. -Vol. 7. -N 11, -P. 511-518.
  31. Kondorosi A., Vinardell J.-M., Nikovics K. ct al. Plant-microbe interactions -a tool for studying plant development//Biology of Plant-Microbe Interactions. V. 4./Eds. Tikhonovich I.A., Lugtcnbcrg B.J.J., Provorov N.A. St.-Petersburg: IS-MPMI, 2004 (in press).
  32. Lang B.F., Gray M.W., Burger G. Mitochondrial genome evolution and the origin of cukaryotcs//Annu. Rev. Genet.-1999.-Vol. 33,-P. 351-397.
  33. Loegering W.Q. Current concepts of intcrorganismal genetics//Annu. Rev. Phytopathol. -1978. -Vol. 16. -P. 309-320.
  34. Marsh J.F., Schultze M. Analysis of arbuscular mycorrhizas using symbiosis defective plant mutants//New Phytologist. -2001. -Vol. 150.-P. 525-532.
  35. Minerdi D., Fani R., Gallo R. ct al. Nitrogen fixation genes in an endosymbiotic Burkholderia strain//Appl. Environ. Microbiol. -2001. -Vol. 67. -P. 725-732.
  36. Moulin L., Munive A., Dreyfus В., Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Prcotcobactcria//Nature.-2001.-Vol. 411.-P. 948-950
  37. Nester E., WoodD., Panloja M., Liu P. Agrobacterium-plmt interactions: unfinished business and continuing surprises//Biology of Plant-Microbe Interactions.-Vol. 4./Eds. Tikhonovich I.A., Lugtcnbcrg B.J.J., Provorov N.A. St.-Petersburg: IS-MPMI, 2004 (in press).
  38. Niehaus K., Kapp D., Puhler A. Plant defence and delayed infection of alfalfa pscudonodulcs induced by an exopo-lysaccharidc (EPS-l)-dcficient Rhizobium meliloti mutant//Planta. -1993. -Vol. 190. -P. 415-425.
  39. Nutman PS. Genetic factors concerned in the symbiosis of clover and nodule bacteria//Nature,-1946.-Vol. 157.-N 3989.-P. 463-465.
  40. Person C, Samborski D.J., Rohringer R. The genc-for-gene concept//Nature. -1962. -Vol. 194. -P. 561-562
  41. Provorov N.A., Borisov A. Y, Tikhonovich LA. Developmental genetics and evolution of symbiotic structures in nitrogen-fixing nodules and arbuscular mycorrhiza//J. Thcor. Biol. -2002. -Vol. 214. -N 2.-P. 215-232.
  42. Quispel A. Evolutionary aspects of symbiotic adaptations: Rhizobium contribution to evolution of associations//The Rhizobiaccac/Eds Spaink H.P., Kondorosi A., Hooykaas P.J.J. Dordrecht: Kluwcr Acad. Publ.-1998. -P. 487-507.
  43. Renzel Z. Breeding for better symbiosis//Plant and Soil. -2002. -Vol. 245. -N 1. -P. 147-162.
  44. Ruse M. Limits to our knowledge of evolution//Evolutionary Biology. Vol. 32/Eds. Clcgg M.T., Hccht M.K., Macinryrc R.J. Kluwcr Acad. Plenum Publ. New York, 2000. -P. 3-33
  45. Schauser L., Roussis A., Stiller J., Stoiigaard J. A plant regulator controlling development of symbiotic root nodules//Nature. -1999.-Vol. 402. -P. 191-195.
  46. Schultze M., Kondorosi A. Regulation of symbiotic root nodule development//Annu. Rev. Genet. -1998. -Vol. 32. -P. 33-57.
  47. Shiztliffe S.J. Vessey J.K. A nodulation (Nod+/Fix-) mutant of Phaseolus vulgaris L. has nodule-like structures lacking pcriphcrial vascular bundles (Pvb-) and is resistant to mycorrhizal infection (Мус-)//Plant Sci. -1996. -Vol. 118. -P. 209-220.
  48. Simonsen A.C. W., Rosendahl L. Origin of de novo synthesized proteins in the different compartments of pca-Rliizobium sp. symbiosomes//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -N 4. -P. 319-327.
  49. Smith S.E., Read D.J. Mycorrhizal Symbiosis (second edition). San Diego, London, New York, Boston, Sydney, Tokyo, Toronto: Academic Press, 1997. -590 p.
  50. Spaink LLP. The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogencsis//Annu. Rev. Phytopathol. -1995. -Vol. 33. -P. 345-368.
  51. Sprenl J.I. Nodulation in legumes. Cromwell Press Ltd. Royal Botanical Gardens, Kcw, 2001. -146 p.
  52. Steinert M., Hentschel U., Hacker J. Symbiosis and pathogenesis: evolution of the microbe-host interaction//Naturwis-senschaftcn. -2000. -Vol. 87. -P. 1-11.
  53. Tsyganov V.E. Voroshilova V.A., Priefer U.B. ct al. Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium -pea (Pisum sativum L.) symbiosis//Annals of Botany. -2002. -Vol. 89. -P. 357-366
  54. Turmel M., Otis С, Lemieux С. The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineages that lead to land plants//Proc. Natl. Acad. Sci. USA. -2002. -Vol. 99. -N 17. -P. 11275-11280.
  55. Van der Hoist PPG., Gronlund M., Stougaard J., Spaink HP. Symbiosis and defense: two sides of one coin//Biology of Plant-Microbe Interactions. V. 4./Eds. Tikhonovich I.A., Lugtcnbcrg B.J.J., Provorov N.A. St.-Pctcrsburg: IS-MPMI, 2004 (in press).
  56. Vivian A., Murillo J., Jackson R.W. The roles of plasmids in phytopathogenic bacteria: mobile arsenals//Microbiology. -2001. -Vol. 147. -P. 763-780.
  57. Walker S.A., Viprey V., Downie J.A. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers//Proc. Natl. Acad. Sci. USA. -2000. -Vol. 97. -N 24. -P. 13413-13418.
  58. Wall L.G. The actinorhizal symbiosis//J. Plant Growth Rcgul. -2000,-Vol. 19,-P. 167-182.
  59. Wilkinson DM. At cross purposes. How do we cope with scientific terms that have two different definitions?//Nature. -2001. -Vol. 412.-P. 485.
  60. Williamson V.M., Gleason C.A. Plant-ncmatodc interactions//Current Opinions in Plant Biology. -2003. -Vol. 6. -P. 327-333.
  61. Winzer Т., Baii-I A., binder M. ct al. A novel 53-kDa nodulinc of the symbiosomc membrane of soybean nodules, controlled by Bradyrhizobium japonicum II Mol. Plant-Microbe Interact. -1999. -Vol. 12. -N 3. -P. 218-226.
  62. Zerges W. Does complexity constrain organelle evolution?//Trends in Plant Science. -2002. -Vol. 7. -N 4. -P. 175-182.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2003 Tikhonovich I.A., Provorov N.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 65617 от 04.05.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies