Ecological geneticsEcological geneticsЭкологическая генетика1811-09322411-9202Eco-Vector62460710.17816/ecogen624607Genetic basis of ecosystems evolutionГенетические основы эволюции экосистемResearch ArticleEffect of mutations in the Sym7, Sym19 and Sym34 genes on the interaction of pea (Pisum sativum L.) with the arbuscular mycorrhizal fungus Rhizophagus irregularisВлияние мутаций в генах Sym7, Sym19 и Sym34 на взаимодействие гороха (Pisum sativum L.) с арбускулярно-микоризным грибом Rhizophagus irregularishttps://orcid.org/0000-0002-3656-455921935113900J-4063-20184934-4465ShtarkOksana Y.ШтаркОксана Юрьевна
Russian Federation

Cand. Sci. (Biology)

канд. биол. наук

oshtark@yandex.ruhttps://orcid.org/0000-0001-8961-9317ZhernakovAleksandr I.ЖернаковАлександр Игоревич
Russian Federation
azhernakov@gmail.comhttps://orcid.org/0000-0002-6568-7988KichiginaNatalia E.КичигинаНаталья Евгеньевна
Russian Federation
n.kichigina@arriam.ruhttps://orcid.org/0000-0001-7957-36931714-8554AkhtemovaGulnara A.АхтемоваГульнара Асановна
Russian Federation

Cand. Sci. (Biology)

канд. биол. наук

ahgulya@yandex.ruhttps://orcid.org/0000-0002-2300-857X4906-1159SulimaAnton S.СулимаАнтон Сергеевич
Russian Federation

Cand. Sci. (Biology)

канд. биол. наук

asulima@arriam.ruhttps://orcid.org/0000-0001-5666-30205048-0203ZorinEvgeny A.ЗоринЕвгений Андреевич
Russian Federation

Cand. Sci. (Biology)

канд. биол. наук

kjokkjok8@gmail.comhttps://orcid.org/0000-0002-2411-9191353259579002610-3670ZhukovVladimir A.ЖуковВладимир Александрович
Russian Federation

Candidate of Biological Sciences, Head of the Laboratory of Genetics of Plant-Microbe Interactions

Кандидат биологических наук, заведующий лабораторией генетики растительно-микробных взаимодействий

vzhukov@arriam.ruAll-Russia Research Institute for Agricultural MicrobiologyВсероссийский научно-исследовательский институт сельскохозяйственной микробиологии26082024290920242232252421412202326082024Copyright ©; 2024, Eco-VectorCopyright ©; 2024, Эко-Вектор2024Eco-VectorЭко-Векторhttps://journals.eco-vector.com/ecolgenet/article/view/624607

BACKGROUND: Within the pea (Pisum sativum L.) species, genotypes with high and low responsiveness to inoculation with arbuscular mycorrhizal fungi can be distinguished.

AIM: The aim of this study was to test the hypothesis that pea responsiveness to arbuscular mycorrhizal fungi inoculation may be inversely correlated with root colonization levels.

MATERIALS AND METHODS: The wild-type line Finale with low responsiveness to arbuscular mycorrhizal fungi inoculation and symbiotic mutants obtained on its basis were used. Plants were grown under controlled climatic conditions with a deficiency of available phosphorus; the fungus Rhizophagus irregularis was used for inoculation. Parameters of plant growth and development of reproductive organs were determined 52 and 71 days after inoculation, which corresponded to the flowering and pod filling stages, respectively.

RESULTS: All mutant lines under conditions without inoculation had generally reduced parameters compared to the original line Finale. Inoculation led to a decrease in many parameters in the line Finale. Mutations in the Sym7 and Sym34 genes, which led to a decrease or delay in the start of mycorrhization, respectively, contributed to the manifestation of a positive plant response to inoculation. The mutant in the Sym19 gene almost completely lacked intrartadical colonization, while inoculation had no effect on the growth and development of above-ground organs.

CONCLUSIONS: The study results support the idea that reducing mycorrhization levels can have a positive effect on pea plants.

В пределах вида горох посевной (Pisum sativum L.) можно выделить генотипы с высокой и низкой отзывчивостью на инокуляцию арбускулярно-микоризными грибами. Цель данного исследования — проверка предположения о том, что отзывчивость гороха на инокуляцию арбускулярно-микоризными грибами может иметь обратную корреляцию с уровнем колонизации корней. В работе использована линия дикого типа Finale с невысокой отзывчивостью на инокуляцию арбускулярно-микоризными грибами и полученные на ее основе симбиотические мутанты. Растения выращивали в контролируемых климатических условиях при дефиците доступного фосфора; для инокуляции использовали гриб Rhizophagus irregularis. Параметры роста растений и развития репродуктивных органов определяли через 52 и 71 день после инокуляции, что соответствовало стадиям цветения и наполнения бобов соответственно. Все мутантные линии в условиях без инокуляции имели, в основном, пониженные параметры по сравнению с исходной линией Finale. Инокуляция привела к снижению многих параметров у этой линии. Мутации в генах Sym7 и Sym34, приводящие к снижению или замедлению начала микоризации, соответственно, способствовали проявлению положительной реакции растений на инокуляцию. У мутанта по гену Sym19 практически полностью отсутствовала внутрикорневая колонизация, при этом инокуляция не оказала влияния на рост и развитие надземных органов. Результаты исследования подтверждают идею, что снижение уровня микоризации может иметь положительное влияние на растения гороха.

peaPisum sativum L.arbuscular mycorrhizasymbiotic mutantssymbiotic effectivenessгорох посевнойPisum sativum L.арбускулярная микоризасимбиотические мутантысимбиотическая эффективностьРоссийский научный фондRussian Science Foundation (RSF)22-16-00109Smith SE, Read DJ. Mycorrhizal symbiosis. 3rd edition. San Diego, London: Academic Press; 2008. doi: 10.1016/B978-0-12-370526-6.X5001-6Smith S.E., Read D.J. Mycorrhizal symbiosis. 3rd edition. San Diego, London: Academic Press, 2008. doi: 10.1016/B978-0-12-370526-6.X5001-6Keymer A., Gutjahr C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Curr Opin Plant Biol. 2018;44: 137–144. doi: 10.1016/j.pbi.2018.04.005Keymer A., Gutjahr C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond // Curr Opin Plant Biol. 2018. Vol. 44. P. 137–144. doi: 10.1016/j.pbi.2018.04.005Salmeron-Santiago IA, Martínez-Trujillo M, Valdez-Alarcón JJ, et al. An updated review on the modulation of carbon partitioning and allocation in arbuscular mycorrhizal plants. Microorganisms. 2022;10(1):75. doi: 10.3390/microorganisms10010075Salmeron-Santiago I.A., Martínez-Trujillo M., Valdez-Alarcón J.J., et al. An updated review on the modulation of carbon partitioning and allocation in arbuscular mycorrhizal plants // Microorganisms. 2022. Vol. 10, N 1. ID 75. doi: 10.3390/microorganisms10010075Nadal M, Paszkowski U. Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol. 2013;16(4):473–479. doi: 10.1016/j.pbi.2013.06.005Nadal M., Paszkowski U. Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis // Curr Opin Plant Biol. 2013. Vol. 16, N 4. P. 473–479. doi: 10.1016/j.pbi.2013.06.005Luginbuehl LH, Oldroyd GED. Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Curr Biol. 2017;27(17): R952–R963. doi: 10.1016/j.cub.2017.06.042Luginbuehl L.H., Oldroyd G.E.D. Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants // Curr Biol. 2017. Vol. 27, N 17. P. R952–R963. doi: 10.1016/j.cub.2017.06.042Fester T, Sawers R. Progress and challenges in agricultural applications of arbuscular mycorrhizal fungi. CRC Crit Rev Plant Sci. 2011;30(5):459–470. doi: 10.1080/07352689.2011.605741Fester T., Sawers R. Progress and challenges in agricultural applications of arbuscular mycorrhizal fungi // CRC Crit Rev Plant Sci. 2011. Vol. 30, N 5. P. 459–470. doi: 10.1080/07352689.2011.605741Ahanger MA, Hashem A, Abd-Allah EF, Ahmad P. Chapter 3. Arbuscular mycorrhiza in crop improvement under environmental stress. In: Emerging technologies and management of crop stress tolerance. Vol. 2. Academic Press; 2014. P. 69–95. doi: 10.1016/B978-0-12-800875-1.00003-XAhanger M.A., Hashem A., Abd-Allah E.F., Ahmad P. Chapter 3. Arbuscular mycorrhiza in crop improvement under environmental stress. В кн.: Emerging technologies and management of crop stress tolerance. Vol. 2. Academic Press, 2014. P. 69–95. doi: 10.1016/B978-0-12-800875-1.00003-XLatef AAHA, Hashem A, Rasool S, et al. Arbuscular mycorrhizal symbiosis and abiotic stress in plants: A review. J Plant Biology. 2016;59(5):407–426. doi: 10.1007/s12374-016-0237-7Latef A.A.H.A., Hashem A., Rasool S., et al. Arbuscular mycorrhizal symbiosis and abiotic stress in plants: A review // J Plant Biology. 2016. Vol. 59, N 5. P. 407–426. doi: 10.1007/s12374-016-0237-7Rivero J, Álvarez D, Flors V, et al. Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytologist. 2018;220(4):1322–1336. doi: 10.1111/nph.15295Rivero J., Álvarez D., Flors V., et al. Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato // New Phytologist. 2018. Vol. 220, N 4. P. 1322–1336. doi: 10.1111/nph.15295Jakobsen I, Smith SE, Smith FA. Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. In: van der Heijden MGA, Sanders IR, editors. Mycorrhizal ecology. Ecological studies. Vol. 157. Berlin: Springer, Heidelberg; 2003. P. 75–92. doi: 10.1007/978-3-540-38364-2_3Jakobsen I., Smith S.E., Smith F.A. Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. В кн.: Mycorrhizal ecology. Ecological studies. Vol. 157 / M.G.A. van der Heijden, I.R. Sanders, editors. Berlin: Springer, Heidelberg, 2003. P. 75–92. doi: 10.1007/978-3-540-38364-2_3Van Der Heijden MGA. Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. In: van der Heijden MGA, Sanders IR, editors. Mycorrhizal ecology. Ecological studies. Vol. 157. Berlin: Springer, Heidelberg; 2003. P. 243–265. doi: 10.1007/978-3-540-38364-2_10Van Der Heijden M.G.A. Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. В кн.: Mycorrhizal ecology. Ecological studies. Vol. 157 / M.G.A. van der Heijden, I.R. Sanders, editors. Berlin: Springer, Heidelberg, 2003. P. 243–265. doi: 10.1007/978-3-540-38364-2_10Klironomos JN. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology. 2003;84(9):2292–2301. doi: 10.1890/02-0413Klironomos J.N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi // Ecology. 2003. Vol. 84, N 9. P. 2292–2301. doi: 10.1890/02-0413Konvalinková T, Jansa J. Lights off for arbuscular mycorrhiza: On its symbiotic functioning under light deprivation. Front Plant Science. 2016;7:782. doi: 10.3389/fpls.2016.00782Konvalinková T., Jansa J. Lights off for arbuscular mycorrhiza: On its symbiotic functioning under light deprivation // Front Plant Science. 2016. Vol. 7. ID 782. doi: 10.3389/fpls.2016.00782Kosterin OE. Pea (Pisum sativum L.): the uneasy fate of the first genetical object. Vavilov journal of genetics and breeding. 2015;19(1):13–26. EDN: TWQXOZКостерин О.Э. При царе горохе (Pisum sativum L.): непростая судьба первого генетического объекта // Вавиловский журнал генетики и селекции. 2015. Т. 19, № 1. С. 13–26. EDN: TWQXOZSinyushin AA, Gostimsky SA. Achievements and prospects of using pea (Pisum sativum) as a model object in plant development genetics. Biology Bulletin Reviews. 2008;128(6):531–541. EDN: JUPCZN (In Russ.)Синюшин А.А., Гостимский С.А. Достижения и перспективы использования гороха посевного (Pisum sativum) в качестве модельного объекта в генетике развития растений // Успехи современной биологии. 2008. Т. 128, № 6. С. 531–541. EDN: JUPCZNYakobi LM, Kukalev AS, Ushakov KV, et al. Polymorphism of seed pea forms on the efficiency of symbiosis with the endomycorrhizal fungus Glomus sp. under conditions of rhizobium inoculation. Agricultural biology. 2000;(3):94–102. EDN: YLBAPD (In Russ.)Якоби Л.М., Кукалев А.С., Ушаков К.В., и др. Полиморфизм форм гороха посевного по эффективности симбиоза с эндомикоризным грибом Glomus sp. в условиях инокуляции ризобиями // Сельскохозяйственная биология. 2000. № 3. С. 94–102. EDN: YLBAPDZhukov VA, Zhernakov AI, Sulima AS, et al. Association study of symbiotic genes in pea (Pisum sativum L.) cultivars grown in symbiotic conditions. Agronomy. 2021;11(11):2368. doi: 0.3390/agronomy11112368Zhukov V.A., Zhernakov A.I., Sulima A.S., et al. Association study of symbiotic genes in pea (Pisum sativum L.) cultivars grown in symbiotic conditions // Agronomy. 2021. Vol. 11, N 11. ID 2368. doi: 0.3390/agronomy11112368Rivera-Becerril F, Calantzis C, Turnau K, et al. Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot. 2002;53(371):1177–1185. doi: 10.1093/jexbot/53.371.1177Rivera-Becerril F., Calantzis C., Turnau K., et al. Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes // J Exp Bot. 2002. Vol. 53, N 371. P. 1177–1185. doi: 10.1093/jexbot/53.371.1177Xavier LJC, Germida JJ. Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils. 2003;37(5):161–167. doi: 10.1007/s00374-003-0605-6Xavier L.J.C., Germida J.J. Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition // Biol Fertil Soils. 2003. Vol. 37, N 5. P. 161–167. doi: 10.1007/s00374-003-0605-6Borisov AYu, Naumkina TS, Shtark OYu, et al. Effectiveness of combined inoculation of pea (Pisum sativum L.) with arbuscularmycorrhizal fungu and rhizobia. Bulletin of the Russian Academy of Agricultural Sciences. 2004;(2):12–13. EDN: PKBJBDБорисов А.Ю., Наумкина Т.С., Штарк О.Ю., и др. Эффективность использования совместной инокуляции гороха посевного грибами арбускулярной микоризы и клубеньковыми бактериями // Доклады Российской академии сельскохозяйственных наук. 2004. № 2. С. 12–13. EDN: PKBJBDSchweiger R, Baier MC, Persicke M, Müller C. High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nat Commun. 2014;5:3886. doi: 10.1038/ncomms4886Schweiger R., Baier M.C., Persicke M., Müller C. High specificity in plant leaf metabolic responses to arbuscular mycorrhiza // Nat Commun. 2014. Vol. 5. ID 3886. doi: 10.1038/ncomms4886Desalegn G, Turetschek R, Kaul H-P, Wienkoop S. Microbial symbionts affect Pisum sativum proteome and metabolome under Didymella pinodes infection. J Proteomics. 2016;143:173–187. doi: 10.1016/j.jprot.2016.03.018Desalegn G., Turetschek R., Kaul H.-P., Wienkoop S. Microbial symbionts affect Pisum sativum proteome and metabolome under Didymella pinodes infection // J Proteomics. 2016. Vol. 143. P. 173–187. doi: 10.1016/j.jprot.2016.03.018Zhukov VA, Akhtemova GA, Zhernakov AI, et al. Evaluation of the symbiotic effectiveness of pea (Pisum sativum L.) genotypes in pot experiment. Agricultural Biology. 2017;52(3):607–614. EDN: YZKVLX doi: 10.15389/agrobiology.2017.3.607engЖуков В.А., Ахтемова Г.А., Жернаков А.И., и др. Симбиотическая эффективность генотипов гороха посевного (Pisum sativum L.) при моделировании в вегетационном эксперименте // Сельскохозяйственная биология. 2017. Т. 52, № 3. С. 607–614. EDN: YZKVLX doi: 10.15389/agrobiology.2017.3.607engShtark OY, Puzanskiy RK, Avdeeva GS, et al. Metabolic alterations in pea leaves during arbuscular mycorrhiza development. PeerJ. 2019;7: e7495. doi: 10.7717/peerj.7495Shtark O.Y., Puzanskiy R.K., Avdeeva G.S., et al. Metabolic alterations in pea leaves during arbuscular mycorrhiza development // PeerJ. 2019. Vol. 7. ID e7495. doi: 10.7717/peerj.7495Yurkov AP, Lactionov YuV, Kojemyakov AP, Stepanova GV. Symbiotic efficiency of bacterial and fungal preparations for forage crops according to seed harvest. Kormoproizvodstvo. 2017;(3):16–21. EDN: YGUNSXЮрков А.П., Лактионов Ю.В., Кожемяков А.П., Степанова Г.В. Анализ симбиотической эффективности бактериальных и грибных препаратов на кормовых культурах по данным урожайности семян // Кормопроизводство. 2017. № 3. С. 16–21. EDN: YGUNSXMüller LM, Harrison MJ. Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol. 2019;50:132–139. doi: 10.1016/j.pbi.2019.05.004Müller L.M., Harrison M.J. Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis // Curr Opin Plant Biol. 2019. Vol. 50. P. 132–139. doi: 10.1016/j.pbi.2019.05.004Engvild KC. Nodulation and nitrogen fixation mutants of pea, Pisum sativum. Theor Appl Genet. 1987;74(6):711–713. doi: 10.1007/BF00247546Engvild K.C. Nodulation and nitrogen fixation mutants of pea, Pisum sativum // Theor Appl Genet. 1987. Vol. 74, N 6. P. 711–713. doi: 10.1007/BF00247546Borisov AY, Danilova TN, Koroleva TA, Naumkina TS. Pea (Pisum sativum L.) regulatory genes controlling development of nitrogen-fixing nodule and arbuscular mycorrhiza: fundamentals and application. Biologia (Bratisl). 2004;59(S13):137–144.Borisov A.Y., Danilova T.N., Koroleva T.A., Naumkina T.S. Pea (Pisum sativum L.) regulatory genes controlling development of nitrogen-fixing nodule and arbuscular mycorrhiza: fundamentals and application // Biologia (Bratisl). 2004. Vol. 59, N S13. P. 137–144.Kistner C, Winzer T, Pitzschke A, et al. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell. 2005;17(8):2217–2229. doi: 10.1105/tpc.105.032714Kistner C., Winzer T., Pitzschke A., et al. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis // Plant Cell. 2005. Vol. 17, N 8. P. 2217–2229. doi: 10.1105/tpc.105.032714Shtark OY, Zhukov VA, Provorov NA, et al. Intimate associations of beneficial soil microbes with host plants. In: Dixon G, Tilston E, editors. Soil microbiology and sustainable crop production. Springer; 2010. P. 119–196. EDN: SLALLN doi: 10.1007/978-90-481-9479-7_5Shtark O.Y., Zhukov V.A., Provorov N.A., et al. Intimate associations of beneficial soil microbes with host plants. В кн.: Soil microbiology and sustainable crop production / G. Dixon, E. Tilston, editors. Springer, 2010. P. 119–196. EDN: SLALLN doi: 10.1007/978-90-481-9479-7_5Kaló P, Gleason C, Edwards A, et al. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science. 2005;308(5729):1786–1789. doi: 10.1126/science.1110951Kaló P., Gleason C., Edwards A., et al. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators // Science. 2005. Vol. 308, N 5729. P. 1786–1789. doi: 10.1126/science.1110951Dolgikh EA, Leppyanen IV, Osipova MA, et al. Genetic dissection of Rhizobium-induced infection and nodule organogenesis in pea based on ENOD12A and ENOD5 expression analysis. Plant Biol. 2011;13(2):285–296. doi: 10.1111/j.1438-8677.2010.00372.xDolgikh E.A., Leppyanen I.V., Osipova M.A., et al. Genetic dissection of Rhizobium-induced infection and nodule organogenesis in pea based on ENOD12A and ENOD5 expression analysis // Plant Biol. 2011. Vol. 13, N 2. P. 285–296. doi: 10.1111/j.1438-8677.2010.00372.xShtark OY, Sulima AS, Zhernakov AI, et al. Arbuscular mycorrhiza development in pea (Pisum sativum L.) mutants impaired in five early nodulation genes including putative orthologs of NSP1 and NSP2. Symbiosis. 2016;68(1–3):129–144. doi: 10.1007/s13199-016-0382-2Shtark O.Y., Sulima A.S., Zhernakov A.I., et al. Arbuscular mycorrhiza development in pea (Pisum sativum L.) mutants impaired in five early nodulation genes including putative orthologs of NSP1 and NSP2 // Symbiosis. 2016. Vol. 68, N 1–3. P. 129–144. doi: 10.1007/s13199-016-0382-2Liu W, Kohlen W, Lillo A, et al. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell. 2011;23(10):3853–3865. doi: 10.1105/tpc.111.089771Liu W., Kohlen W., Lillo A., et al. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2 // Plant Cell. 2011. Vol. 23, N 10. P. 3853–3865. doi: 10.1105/tpc.111.089771Maillet F, Poinsot V, André O, et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature. 2011;469(7328):58–63. doi: 10.1038/nature09622Maillet F., Poinsot V., André O., et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza // Nature. 2011. Vol. 469, N 7328. P. 58–63. doi: 10.1038/nature09622Delaux P-M, Bécard G, Combier J-P. NSP 1 is a component of the Myc signaling pathway. New Phytologist. 2013;199(1):59–65. doi: 10.1111/nph.12340Delaux P.-M., Bécard G., Combier J.-P. NSP 1 is a component of the Myc signaling pathway // New Phytologist. 2013. Vol. 199, N 1. P. 59–65. doi: 10.1111/nph.12340Endre G, Kereszt A, Kevei Z, et al. A receptor kinase gene regulating symbiotic nodule development. Nature. 2002;417(6892): 962–966. doi: 10.1038/nature00842Endre G., Kereszt A., Kevei Z., et al. A receptor kinase gene regulating symbiotic nodule development // Nature. 2002. Vol. 417, N 6892. P. 962–966. doi: 10.1038/nature00842Stracke S, Kistner C, Yoshida S, et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature. 2002;417(6892):959–962. doi: 10.1038/nature00841Stracke S., Kistner C., Yoshida S., et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis // Nature. 2002. Vol. 417, N 6892. P. 959–962. doi: 10.1038/nature00841Marsh JF, Schultze M. Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytologist. 2001;150(3):525–532. doi: 10.1046/j.1469-8137.2001.00140.xMarsh J.F., Schultze M. Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants // New Phytologist. 2001. Vol. 150, N 3. P. 525–532. doi: 10.1046/j.1469-8137.2001.00140.xDemchenko K, Winzer T, Stougaard J, et al. Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytologist. 2004;163(2):381–392. doi: 10.1111/j.1469-8137.2004.01123.xDemchenko K., Winzer T., Stougaard J., et al. Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation // New Phytologist. 2004. Vol. 163, N 2. P. 381–392. doi: 10.1111/j.1469-8137.2004.01123.xMuromtsev GS, Marshunova GA, Jacobi LM. Certificate of author No. 1501509 to invention: A strain of endomycorrhizal fungus Glomus mosseae Nic. & Gerd., increasing the yield of agricultural plants and improving their mineral nutrition. (In Russ.)Муромцев Г.С., Маршунова Г.А., Якоби Л.М. Авторское свидетельство № 1501509 на изобретение: «Штамм эндомикоризного гриба Glomus mosseae Nic. & Gerd., повышающий урожай cельскохозяйственных растений и улучшающий их минеральное питание».Knott CM. A key for stages of development of the pea (Pisum sativum). Ann Appl Biol. 1987;111(1):233–245. doi: 10.1111/j.1744-7348.1987.tb01450.xKnott C.M. A key for stages of development of the pea (Pisum sativum) // Ann Appl Biol. 1987. Vol. 111, N 1. P. 233–245. doi: 10.1111/j.1744-7348.1987.tb01450.xFox J. Applied regression analysis and generalized linear models. Sage Publications; 2015. 816 p.Fox J. Applied regression analysis and generalized linear models. Sage Publications, 2015. 816 p.Vierheilig H, Coughlan AP, Wyss U, Piché Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol Am Soc Microbiol. 1998;64(12):5004–5007. doi: 10.1128/AEM.64.12.5004-5007.1998Vierheilig H., Coughlan A.P., Wyss U., Piché Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi // Appl Environ Microbiol Am Soc Microbiol. 1998. Vol. 64, N 12. P. 5004–5007. doi: 10.1128/AEM.64.12.5004-5007.1998Trouvelot A, Kough JL, Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S, editors. Physiological and genetical aspects of mycorrhizae. Paris: INRA, 1986. P. 217–221.Trouvelot A., Kough J.L., Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. В кн.: Gianinazzi-Pearson V., Gianinazzi S., editors. Physiological and genetical aspects of mycorrhizae. Paris: INRA, 1986. P. 217–221.Little TM, Hills FJ. Agricultural experimentation. Design and analysis. New York: John Wiley and Sons United States; 1978. 350 p.Little T.M., Hills F.J. Agricultural experimentation. Design and analysis. New York: John Wiley and Sons United States, 1978. 350 p.Kuznetsova E, Seddas-Dozolme PMA, Arnould C, et al. Symbiosis-related pea genes modulate fungal and plant gene expression during the arbuscule stage of mycorrhiza with Glomus intraradices. Mycorrhiza. 2010;20(6):427–443. doi: 10.1007/s00572-009-0292-8Kuznetsova E., Seddas-Dozolme P.M.A., Arnould C., et al. Symbiosis-related pea genes modulate fungal and plant gene expression during the arbuscule stage of mycorrhiza with Glomus intraradices // Mycorrhiza. 2010. Vol. 20, N 6. P. 427–443. doi: 10.1007/s00572-009-0292-8Nagae M, Takeda N, Kawaguchi M. Common symbiosis genes CERBERUS and NSP1 provide additional insight into the establishment of arbuscular mycorrhizal and root nodule symbioses in Lotus japonicus. Plant Signal Behav. 2014;9(5):e28544. doi: 10.4161/psb.28544Nagae M., Takeda N., Kawaguchi M. Common symbiosis genes CERBERUS and NSP1 provide additional insight into the establishment of arbuscular mycorrhizal and root nodule symbioses in Lotus japonicus // Plant Signal Behav. 2014. Vol. 9, N 5. ID e28544. doi: 10.4161/psb.28544Shtark OY, Zhukov VA, Tikhonovich IA, et al. Strigolactones as regulators of symbiotrophy of plants and microorganisms. Russian Journal of Plant Physiology. 2018;65(2):83–100. EDN: YSSSHV doi: 10.7868/S001533031802001XШтарк O.Ю., Шишова М.Ф., Повыдыш М.Н., и др. Стриголактоны — регуляторы симбиотрофии растений и микроорганизмов // Физиология растений. 2018. Т. 65, № 2. С. 83–100. EDN: YSSSHV doi: 10.7868/S001533031802001XSmith SE, Jakobsen I, Grønlund M, Smith FA. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol Am Soc Plant Biol. 2011;156(3):1050–1057. doi: 10.1104/pp.111.174581Smith S.E., Jakobsen I., Grønlund M., Smith F.A. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition // Plant Physiol Am Soc Plant Biol. 2011. Vol. 156, N 3. P. 1050–1057. doi: 10.1104/pp.111.174581