Multi-component symbiosis of Legumes with beneficial soil microbes: genetic and evolutionary basis of application in sustainable crop production

Abstract

Leguminous plants have a genetic system that provides interaction with different beneficial soil microorganisms (BSM). The system has been formed on the basis of the genetic mechanisms that had arisen during the co-evolution of plants with arbuscular-mycorrhizal (AM) fungi and appeared to provide pre-adaptations for further evolution of interaction with various BSM. A concept of the use of BSM in sustainable agriculture is proposed, which postulates an establishment of the multi-component beneficial plant-microbe communities based on varieties of legumes with high potential for interaction with the BSM. 

Keywords

GLOMEROMYCOTA

References

[1] Борисов А. Ю., Наумкина Т. С., Штарк О. Ю. и др., 2004. Эффективность использования совместной инокуляции гороха посевного (Pisum sativum L.) грибами арбускулярной микоризы и клубеньковыми бактерия-ми для повышения продуктивности растений в устойчивом экологически ориентированном земледелии//Докл. РАСХН. № 2. С. 12-14.

[2] Борисов А. Ю., Цыганов В. Е., Штарк О. Ю. и др., 2002. Каталог мировой коллекции ВИР. Вып. 728. Горох (Симбиотическая эффективность)/Под ред.И. А. Тихоновича, М. А. Вишняковой, СПб.: ВИР, 29 с.

[3] Жуков В. А., Штарк О. Ю., Борисов А. Ю., Тихонович И. А., 2009. Молекулярно-генетические механизмы контроля растением ранних стадий развития взаимовыгодных (мутуалистических) симбиозов бобовых//Генетика. Т. 45. С. 1449-1460.

[4] Игнатов В. В. (ред.), 2005. Молекулярные основы взаимоотношений ассоциативных микроорганизмов с растениями. М.: Наука, 262 с.

[5] Кожемяков А. П., Чеботарь В. К., 2005. Биопрепараты для земледелия//Биопрепараты в сельском хозяйстве (Методология и практика применения микроорганизмов в растениеводстве и кормопроизводстве)/Под ред. И. А. Тихоновича, Ю. В. Круглова, М., С. 18-54.

[6] Лабутова Н. М., 2009. Взаимоотношения эндомикоризных грибов с микроорганизмами ризосферы//Ми-кол. Фитопатол. Т. 43. № 1. С. 3-19.

[7] Лабутова Н. М., Левина Р. Л., 2008. Динамика подвижных форм макроэлементов в ризосфере бобовых растений при функционировании различных симбиотических систем//Материалы Межрегиональной научно-практической конференции «Почвенные ресурсы Северо-Запада России: их состояние, охрана и рациональное использование», СПб., С. 135-140.

[8] Лабутова Н. М., Поляков А. И., Лях В. А., Гор-дон В. Л., 2004. Влияние инокуляции клубеньковы-ми бактериями и эндомикоризным грибом Glomus intraradices на урожай различных сортов сои и содержание белка и масла в семенах//Докл. РАСХН. № 2. C. 10-12.

[9] Проворов Н. А., Воробьев Н. И., Андронов Е. Е., 2008. Макро-и микроэволюция бактерий в системах симбиоза//Генетика. Т. 44. С. 12-28.

[10] Проворов Н. А., 2009. Растительно-микробные симбиозы как эволюционный континуум//Ж. Общ. Биол. Т. 70. № 1. С. 10-34.

[11] Чеботарь В. К., Казаков А. Е., Ерофеев С. В. и др., 2008. Способ получения комплексного микробиологического удобрения. Патент № 2318784 от 10.03.2008.

[12] Штарк О. Ю., Данилова Т. Н., Наумкина Т. С. и др., 2006. Анализ исходного материала гороха посевного (Pisum sativum L.) для селекции сортов с высоким симбиотическим потенциалом и выбор параметров для его оценки//Экол. Генет. T. 4. № 2. С. 22-28.

[13] Якоби Л. М., Кукалев А. С., Ушаков К. В. и др., 2000. Полиморфизм форм гороха посевного по эффективности симбиоза с эндомикоризным грибом Glomus sp. в условиях инокуляции ризобиями//Сельхоз. Биол. 2000. №3. C. 94-102.

[14] Akiyama K., Matsuzaki K., Hayashi H., 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi//Nature. Vol. 435. P. 824-827.

[15] Ané J. M., Kiss G. B., Riely B. K. et al., 2004. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes//Science. Vol. 303. P. 1364-1367.

[16] Artursson V., Finlay R. D., Jansson J. K., 2006. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth//Environ. Microbiol. Vol. 8. P. 1-10.

[17] Bakker P. A. H. M., Raaijmakers J. M., Bloemberg G. et al. (eds.), 2007. New perspectives and approaches in plant growth-promoting rhizobacteria research (Reprinted from Eropean Journal of Plant Pathology, 119:2, 2007). Dordrecht: Springer. 126 p.

[18] Balachandar D., Raja P., Kumar K., Sundaram S. P., 2007. Non-rhizobial nodulation in legumes//Biotechnol. Molec. Biol. Rev. Vol. 2. P. 49-57.

[19] Barea J.-M., Pozo M.-J., Azcon R., Azcon-Aguilar C., 2005. Microbial cooperation in the rhizosphere//J. Exp. Botany. Vol. 56, N. 14, P. 1761-1788.

[20] Barker S. J., Tagu D., 2000. The role of auxins and cytokinins in mycorrhizal symbiosis//J. Plant Growth Regul. Vol. 19. P. 144-154.

[21] Belimov A. A., Kunakova A. M., Safronova V. I. et al., 2000. Interaction between associative bacteria and barley under environmental stresses: input of partner genotypes and growth conditions//New approaches and techniques in breeding sustainable fodder crops and amenity grasses/Eds. N. A. Provorov et al., St-Petersburg: VIRA Press. P. 146-148.

[22] Bleecker A. B., Kende H., 2000. Ethylene: a gaseous signal molecule in plants//Annu. Rev. Cell Dev. Biol. Vol. 16. P. 1-18.

[23] Borisov A. Y., Danilova T. N., Shtark O. Y. et al., 2008. Tripartite symbiotic system of pea (Pisum sativum L.): applications in sustainable agriculture//Biological Nitrogen Fixation: Towards Poverty Alleviation through Sustainable Agriculture. Proceedings of 15th International Congress on Nitrogen Fixation & 12th International Conference of the African Association for Biological Nitrogen Fixation/Eds. F. D. Dakora et al., Dordrecht: Springer. P. 15-17.

[24] Brewin N. J., 2004. Plant cell wall remodeling in the Rhizobium-legume symbiosis//Crit. Rev. Plant. Sci. Vol. 23. P. 1-24.

[25] Brockwell J., Bottomley P. J., Thies J. E., 1995. Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment//Plant Soil. Vol. 174. P 143-180.

[26] Brundrett M. C., 2002. Coevolution of roots and mycorrhizas of land plants//New Phytol. Vol. 154. P. 275-304.

[27] Caetano-Anolles G., Gresshoff P. M., 1991. Plant genetic control of nodulation//Annu. Rev. Microbiol. Vol. 45. P. 345-382.

[28] Chen C., Ane J-M. Zhu H., 2008. OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice//New Phytol. Vol. 180. P. 311-315.

[29] Compant S., Duffy B., Nowak J., Clément C., Barka E. A., 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects//Appl. Environ. Microbiol. Vol. 71. P. 4951-4959.

[30] Cronk Q. C. B., Bateman R. M., Hawkins J. A., 2002. Developmental genetics and plant evolution. Boca Raton: CRC Press. 543 p.

[31] D'Haeze W., Holsters M., 2002. Nod factor structures, responses, and perception during initiation of nodule development//Glycobiol. Vol. 12. P. 79-105.

[32] Dilworth M. J., James E. K., Sprent J. I., Newton W. E. (eds.), 2008. Nitrogen-fixing leguminous symbioses. Dordrecht: Springer. 404 p.

[33] Dolgikh E. A., Leppyanen I. V., Osipova M. A. et al., 2011. Genetic dissection of Rhizobium-induced infection and nodule organogenesis in pea based on ENOD12A and ENOD5 expression analysis//Plant Biol. V. 13. P. 285-296.

[34] Downie J. A., 2010. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots//FEMS Microbiol. Rev. Vol. 34. P. 150-170.

[35] Duc G., Messager A., 1989. Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation//Plant Sci. Vol. 60. P. 207-213.

[36] Endre G., Kereszt A., Kevei Z. et al., 2002. A receptor kinase gene regulating symbiotic nodule development//Nature. Vol. 417. P. 962-966.

[37] Fournier J., Timmers A. C. J., Sieberer B. J. et al., 2008. Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization//Plant Physiol. Vol. 148. P. 1985-1995.

[38] Garcia-Garrido J. M., Ocampo J. A., 2002. Regulation of the plant defence response in arbuscular mycorrhizal symbiosis//J. ExP. Bot. Vol. 53. P. 1377-1386.

[39] Geil R. D., Peterson L., Guinel F. C., 2001. Morphological alterations of pea (Pisum sativum cv. Sparkle) arbuscular mycorrhizas as a result of exogenous ethylene treatment//Mycorrhiza. Vol. 11. P. 137-143.

[40] Genre A., Bonfante P., 2005. Building a mycorrhizal cell: how to reach compatibility between plants and arbuscular mycorrhizal fungi//J. Plant Interact. Vol. 1. N. 1. P. 3-13.

[41] Genre A., Chabaud M., Timmers T. et al., 2005. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection//Plant Cell. Vol. 17. P. 3489-3499.

[42] Gianinazzi-Pearson V., 1996. Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis//Plant Cell. Vol. 8. P. 1871-1883.

[43] Graham P. H., Vance C. P., 2003. Legumes: importance and constraints to greater use//Plant Physiology. Vol. 131. P. 872-877.

[44] Gresshoff P. M, Lohar D., Chan P.-K. et al., 2009. Genetic analysis of ethylene regulation of legume nodulation//Plant Signaling & Behavior. Vol. 4. P. 818-823.

[45] Hildebrandt U., Ouziad F., Marner F. J., Bothe H., 2006. The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores//FEMS Microbiol. Lett. Vol. 254. P. 258-267.

[46] Hirsch A. M., Lum M. R., Downie J. A., 2001. What makes the rhizobia-legume symbiosis so special?//Plant Physiol. 2001. Vol. 127. P. 1484-1492.

[47] Imaizumi-Anraku H., Takeda N., Charpentier M. et al., 2005. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots//Nature. Vol. 433. P. 527-531.

[48] Jacobsen E., 1984. Modification of symbiotic interaction of pea (Pisum sativum L.) and Rhizobium leguminosarum by induced mutations//Plant Soil. Vol. 82. P. 427-438.

[49] Jones K. M., Kobayashi H., Davies B. W. et al., 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model//Nat. Rev. Microbiol. Vol. 5. P. 619-633.

[50] Jones K. M., Sharopova N., Lohar D. P. et al., 2008. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant//PNAS. Vol. 105. P. 704-709.

[51] Kalo P., Gleason C., Edwards A. et al., 2005. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators//Science. Vol. 308. P. 1786-1789.

[52] Kistner C., Winzer T., Pitzschke A. et al., 2005. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis//Plant Cell. Vol. 17. P. 2217-2229.

[53] Koltai H., Kapulnik Y. (eds.), 2010. Arbuscular mycorrhizas: physiology and function. Dordrecht: Springer. 623 p.

[54] Kosuta S., Chabaud M., Lougnon G. et al., 2003. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula//Plant Physiol. Vol. 131. P. 952-962.

[55] Krusell L., Madsen L. H., Sato S. et al., 2002. Shoot control of root development and nodulation is mediated by a receptor-like kinase//Nature. Vol. 420. P. 422-426.

[56] Kumagai H., Kinoshita E., Ridge R. W., Kouchi H., 2006. RNAi knock-down of ENOD40s leads to significant suppression of nodule formation in Lotus japonicus//Plant Cell Physiol. Vol. 47. P. 1102-1111.

[57] Küster H., Vieweg M. F., Manthey K. et al., 2007. Identification and expression regulation of symbiotically activated legume gene//Phytochem. Vol. 68. P. 8-18.

[58] Lie T. A., 1971. Temperature-dependent root-nodule formation in pea cv. Iran//Plant Soil. Vol. 34. P. 751-752.

[59] Limpens E., Mirabella R., Fedorova E. et al., 2005. Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2//PNAS. Vol. 102. P. 10375-10380.

[60] Madsen E. B., Madsen L. H., Radutoiu S. et al., 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals//Nature. Vol. 425. P. 637-640.

[61] Madsen L. H., Tirichine L., Jurkiewicz A. et al., 2010. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus//Nature Communications. 1:10. doi: 10. 1038/ncomms1009 (2010).

[62] Maillet F., Poinsot V., André O. et al., 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza//Nature. Vol. 469. P. 58-64.

[63] Markmann K., Parniske M., 2009. Evolution of root endosymbiosis with bacteria: how novel are nodules?//Trends Plant Sci. Vol. 14. P. 77-86.

[64] Messinese E., Mun J. H., Yeun L. H., 2007. A novel nuclear protein interacts with the symbiotic DMI3 calcium-and calmodulin-dependent protein kinase of Medicago truncatula//Mol. Plant-Microbe Interact. Vol. 20. P. 912-921.

[65] Minerdi D., Bianciotto V., Bonfante P., 2002. Endosymbiotic bacteria in mycorrhizal fungi: from their morphology to genomic sequences//Plant Soil. Vol. 244. P. 211-219.

[66] Mitra R. M., Gleason C. A., Edwards A. et al., 2004. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning//PNAS. Vol. 101. P. 4701-4705.

[67] Morandi D., Sagan M., Prado-Vivant E., Duc G., 2000. Influence of genes determining supernodulation on root colonisation by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants//Mycorrhiza. Vol. 10. P. 37-42.

[68] Murakami Y., Miwa H., Imaizumi-Anraku H. et al., 2006. Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation//DNA Res. Vol. 13. P. 255-265.

[69] Murray J. D., Karas B. J., Sato S. et al., 2007. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis//Science. Vol. 315. P. 101-104.

[70] Nagahashi G., Douds J. D. D., 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots//New Phytol. Vol. 136. P. 299-304.

[71] Navazio L., Moscatiello R., Genre A. et al., 2007. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells//Plant Physiol. Vol. 144. P. 673-681.

[72] Nishimura R., Hayashi M., Wu G. J. et al., 2002. HAR1 mediates systemic regulation of symbiotic organ development//Nature. Vol. 420. P. 426-429.

[73] Nutman P. S., 1946. Genetic factors concerned in the symbiosis of clover and nodule bacteria//Nature. Vol. 151. P. 463-465.

[74] Ovchinnikova E., Limpens E., Borisov A. et al., 2010. Intracellular accommodation of Rhizobium bacteria is controlled by the common symbiotic signaling pathway//Abstract book of the 9th European Nitrogen Fixation Conference, 6-10 Sept. 2010, Geneva, Switzerland. P. 214.

[75] Parniske M., 2000. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease?//Curr. Opin. Plant Biol. Vol. 3. P. 320-328.

[76] Parniske M., 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses//Nature Rev. Microbiol. Vol. 6. P. 763-775.

[77] Preston G. M., 2004. Plant perceptions of plant growthpromoting Pseudomonas//Phil. Trans. R. Soc. Lond. B. Vol. 359. P. 907-918.

[78] Provorov N. A., Shtark O. Y., Zhukov V. A. et al., 2010. Developmental genetics of plant-microbe symbioses. -NY, USA: Nova Science Publishers. 152 p.

[79] Provorov N. A., Tikhonovich I. A., 2003. Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis//Genet. Resources and Crop Evolution. Vol. 50. P. 89-99.

[80] Provorov N. A., Vorobyov N. I., 2009. Host plant as an organizer of microbial evolution in the beneficial symbioses//Phytochem. Rev. Vol. 8. P. 519-534.

[81] Radutoiu S., Madsen L. H., Madsen E. B. et al., 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases//Nature. Vol. 425. P. 585-592.

[82] Redecker D., 2002. Molecular identification and phylogeny of arbuscular mycorrhizal fungi//Plant Soil. Vol. 244. P. 67-73.

[83] Remy W., Taylor T. N., Hass H., Kerp H., 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizas//PNAS. Vol. 91. P. 11841-11843.

[84] Requena N., Jimenez J., Toro M., Barea J. M., 1997. Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for re-vegetation in Mediterranean semi-arid ecosystems//New Phytol. Vol. 136. P. 667-677.

[85] Requena N., Perez-Solis E., Azcón-Aguilar C. et al., 2001. Management of indigenous plant-microbe symbioses aids restoration of decertified ecosystems//Appl. Environ. Microbiol. Vol. 67. P. 495-498.

[86] Sanchez L., Weidmann S., Arnould C. et al., 2005. Pseudomonas fluorescens and Glomus mosseae trigSanchez L., Weidmann S., Arnould C. et al., 2005. Pseudomonas fluorescens and Glomus mosseae trig

[87] Sandhu H. S., Gupta V. V. S. R., Wratten S. D., 2010. Evaluating the economic and social impact of soil microbes//Soil microbiology and sustainable crop production/Eds. G. R. Dixon, E. L. Tilston. Dordrecht: Springer. P. 399-417.

[88] Schnabel E., Journet E. P., de Carvalho-Niebel F. et al., 2005. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length//Plant Mol. Biol. Vol. 58. P. 809-822.

[89] Schulz B., Boyle S., Sieber T. (eds.), 2006. Microbial root endophytes. Dordrecht: Springer. 367 p. 90. Schüßler A., Schwarzott D., Walker C., 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution//Mycol. Res. Vol. 105. P. 1413-1297.

[90] Sessitsch A., Howieson J. G., Perret X. et al., 2002. Advances in Rhizobium research//Crit. Rev. Plant Sci. Vol. 21. P. 323-378.

[91] Shtark O. Y., Borisov A. Y., Zhukov V. A. et al., 2010. Intimate associations of beneficial soil microbes with the host plants//Soil microbiology and sustainable crop production/Eds. G. R. Dixon, E. L. Tilston, Dordrecht: Springer. P. 119-196.

[92] Smith K. P., Goodman R. M., 1999. Host variation for interactions with beneficial plant-associated microbes//Annu. Rev. Phytopathol. Vol. 37. P. 473-491.

[93] Smith S. E., Read D. J., 2008. Mycorrhizal symbiosis, 3nd ed. Maryland Heights, USA: Elsevier, Academic Press. 800 p.

[94] Sprent J. I., 2001. Nodulation in Legumes. Kew, Royal Botanical Gardens: Cromwell Press Ltd. 146 p.

[95] Sprent J. I., 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation.//New Phytol. Vol. 174. P. 11-25.

[96] Stracke S., Kistner C., Yoshida S. et al., 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis//Nature. Vol. 417. P. 959-962.

[97] Suzaki T., Sato M., Ashikari M. et al., 2004. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1//Development. Vol. 131. P. 5649-5657.

[98] Tikhonovich I. A., Provorov N. A., 2007. Cooperation of plants and microorganisms: getting closer to the genetic construction of sustainable agro-systems//Biotechnol. J. Vol. 2. P. 833-848.

[99] Timmers A. C. J., Vallotton P., Heym C., Menzel D., 2007. Microtubule dynamics in root hairs of Medicago truncatula//Eur. J. Cell Biol. Vol. 86. P. 69-83.

[100] Tirichine L., Imaizumi-Anraku H., Yoshida S. et al., 2006. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development//Nature. Vol. 441. P. 1153-1156.

[101] Tirichine L., Sandal N., Madsen L. H. et al., 2007. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis//Science. Vol. 315. P. 104-107.

[102] Tokala R. K., Strap J. L., Jung C. M. et al., 2002. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum)//Appl. Environ. Microbiol. Vol. 68. P. 2161-2171.

[103] Vallad E., Goodman R. M., 2004. Systemic acquired resistance and induced systemic resistance in conventional agriculture // Crop Sci. Vol. 44. P. 1920-1934. 105. van Brussel A. A. N., Bakhuizen R., van Spronsen P. C. et al., 1992. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium // Science. Vol. 257. P. 70-72.

[104] Vance C. P., 2001. Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in the world of declining renewable resources//Plant Physiol. Vol. 127. P. 390-397.

[105] Vavilov N. I., 1922. The law of homologous series in variation//J. Genet. Vol. 12. N 1. P. 47-89.

[106] Wan X., Hontelez J., Lillo A. et al., 2007. Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development//J. Exp. Bot. Vol. 58. P. 2033-2041.

[107] Yano K., Yoshida S., Muller J. et al., 2008. CYCLOPS, a mediator of symbiotic intracellular accommodation//PNAS. Vol. 105. P. 20540-20545.

[108] Yokota K., Takashi S., Kouchi H., Hayashi M., 2010. Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice//Plant Cell Physiol. Vol. 51. P. 1436-1442.

[109] Young N. D., Udvardi M., 2009. Translating Medicago truncatula genomics to crop legumes//Curr. Opin. Plant Biol. Vol. 12. P. 193-201.

[110] Zhu H., Choi H. K., Cook D. R., Shoemaker R. C., 2005. Bridging model and crop legumes through comparative genomics//Plant Physiol. Vol. 137. P. 1189-1196.

RIGHTS & PERMISSIONS

Shtark O.Y., Borisov A.U., Zhukov V.A., Nemankin T.A., Tikhonovich I.A.