Микоризные грибы: cовременные представления их значимости в минеральном питании растений и как натуральных биоудобрений

  • Я.С. Камельчук (Y.S. Кamelchuk) Полесский государственный университет, г. Пинск, Республика Беларусь
Ключевые слова: микоризные грибы, микобионты, абиотический и биотический стресс, питательные элементы, in vitro, биоудобрения, инокуляция

Аннотация

Микоризосфера является специфической почвенной микрозоной, формирующейся вокруг микоризированных корней растений и состоит из корня, гиф микобионта (непосредственно связанного с ним), ассоциированных с ними микроорганизмов почвы. Сами же корни растений содержат большое количество микроорганизмов, которые наряду с качеством почвы и климатическими условиями являются основными факторами, влияющими на жизнеспособность растения, его рост и развитие. Микроорганизмы, такие как микоризные грибы, могут способствовать более эффективному использованию плодородия почвы, обеспечивать оптимальные условия для роста растений, выступая тем самым в роли натуральных биоудобрений. Ключевую роль для жизнеспособности растения играют необходимые мутуалистические арбускулярные микоризные грибы (АМГ), которые являются связующим звеном между корнями растения-хозяина и почвенными питательными элементами в минеральной форме, доставляют растению воду и минеральные питательные вещества в обмен на продукты фотосинтеза, обеспечивают защиту от болезнетворных микроорганизмов. Таким образом, АМГ, являясь органическими компонентами почвы, в случае их отсутствия, могут привести к менее эффективному функционированию экосистемы. Процесс микоризации может стать действительной альтернативой обычным методам внесения удобрений, при этом успех пока сложно предсказуем, так как различные виды растений по-разному реагируют на одинаковые разновидности микоризных грибов. В данной статье предлагается обзор по минеральному питанию растений в симбиозе с микоризными грибами, по использованию микоризных грибов в сельском хозяйстве, в садоводстве, при адаптации растений in vitro; созданию инокулята на основе микоризных грибов и внесению биологических удобрений на основе микоризы, уделяя особое внимание некоторым важным факторам, которые могли бы увеличить успех процесса инокуляции.

Литература

1. Brundrett, M.C. Diversity and classification of mycorrhizal association / M.C. Brundrett // Biol. Rev. – 2004. Vol. 79. – P. 473–495.

2. Read, D.J. The structure and function of the vegetative mycelium of mycorrhizal roots / D.J. Read // D.H. Jennings, A.D.M. Rayner (eds.). The ecology and physiology of the fungal mycelium. – Cambridge: Cambridge University Press, 1984. – P. 215–240.

3. Prasad, R. Introduction to mycorrhiza: historical development in Mycorrhiza / Eds. Varma A., Prasad R., Tuteja N. (Cham: Springer), 2017. – P. 1–7. DOI: org/10.1007/978–3–319–53064–2_1.

4. Koide, R.T. A history of research on arbuscular mycorrhizal / R.T. Koide, B. Mosse // Mycorrhiza. – 2004. – № 14. – P. 145–163.

5. Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defense mechanisms / M.J. Pozo [et al.] // Arbuscular mycorrhizas: physiology and function. – 2010. – Chapter 9. – P. 193– 207.

6. Влияние арбускулярных микоризных грибов на рост и развитие растений / З.М. Алещенкова [и др.] // Наука и инновации – 2011. – № 2 (96). – С. 59–63.

7. Эндофитные микроорганизмы как промоутеры роста растений в культуре in vitro / Л.С. Cамарина [и др.] // Сельскохозяйственная биология, 2017. – Сочи, Россия. – Т. 52, № 5. – С. 917–927.

8. Соловьева, Е. Арбускулярные микоризные грибы в почвенно–климатических условиях Беларуси / Е. Соловьева, З. Алещенкова // Мат–лы 22–ой Междунар. науч.–практ.конф. «Human and Nature Safety» 4–6 мая 2016г. – АСУ, Каунасский р., 2016. – С. 152–156.

9. Jansa, J. In vitro and post vitro inoculation of micropropagated Rhododendrons with ericoid mycorrhizal fungi / Appl. Soil Ecol. / J. Jansa. – 2000. – № 15. – P.125–136.

10. Jakobsen, I. Transport of phosphorus and carbon in arbuscular mycorrhiza / I. Jakobsen // Mycorrhiza: structure, function, molecular biology and biotechnology // 2nd ed. Berlin: Springer. – 1999. – P. 305–332.

11. Kumawat, N. Role of Biofertilizers in Agriculture / N. Kumawat // Popular kheti. – Vol. 5(4). – 2017. – P. 63–66.

12. Bonfante, P. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis / P. Bonfante // Nat Commun. – Vol. 1(48). – 2010. DOI: org/10.1038/ncomms1046.

13. Friesen, M.I. Microbialy mediated plant functional traits. Annual Review of Ecology, Evolution, and Systematics / M.I. Friesen. – 2011. – Vol. 42. – P. 23–46. DOI: org/10.1146/annurev–ecolsys–102710–145039.

14. Santander, C. Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance / C. Santander // J. Soil Sci. Plant Nutr. – № 19 (2). – 2019. – P. 321–331. DOI: org/10.1007/s42729–019–00032–z.

15. Normand, L. Rooting and acclimatization of micropropagated cuttings are enhanced by the ectomycorrhizal fungi / L. Normand // Physiologia Plantatum, – Vol.98. – 1996. – P. 759–766. DOI: org/10.1111/j.1399–3054.1996.tb06682.

16. Lehmann, A. Arbuscular mycorrhizal influence on zinc nutrition in crop plants – A meta–analysis / A. Lehmann // Soil Biol. Biochem. – Vol.69, – 2014. – P. 123–131. DOI: org/10.1016/j.soilbio.2013.11.001.

17. Singh, L. Unraveling the role of fungal symbionts in plant abiotic stress tolerance / L. Singh // Plant Signaling & Behavior. – Vol.6 (2). – 2011. – P. 175–191. DOI: org/10.4161/psb.6.2.14146.

18. Mohammad, M. Effect of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts / M. Mohammad // J. Plant Nutr. – Vol. 26. – 2011. – P. 125–137. DOI: org/10.1081/PLN–120016500.

19. Marschner, H. Nutrient uptake in mycorrhizal symbiosis / H. Marschner // Plant & Soil. – Vol. 159. – 1994. – P. 89–102.

20. Johnson, D. In situ (CO2)–C–13 pulse labeling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhiza to the soil / D. Johnson // New Phitol. – Vol. 153. –2002. – P. 327–334.

21. Nehls, U. Carbohydrate metabolism in ectomycorrhizas gene expression, monosaccharide transport and metabolic control / U. Nehls // New Phitol. – Vol. 150. – 2001. – P. 533–541.

22. Buscot, F. Recent advances in exploring physiology and biodiversity of ectomycorrhizas highlight the functioning of these symbioses in ecosystems / F. Buscot // FEMS Microbiol. Rev. – Vol. 24. – 2000. – P. 601–614.

23. Azcon, R. Differential contribution of arbuscular mycorrhizal fungi to plant nitrate uptake (15N) under increasing N supply to the soil / R. Azcon // Can. J. Bot. – 2001. – Vol.79. – P. 1175–1180.

24. Hestrin, R. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition / R. Hestrin // Commun. Biol. – Vol. 2. – 2019. – 233 p. DOI: org/10.1038/s42003–019–0481–8.

25. Bucher, M. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces / M. Bucher // New Phytol. – № 173(1) – 2007. – P.11–26. DOI: org/10.1111/j.14698137.2006.01935.x.

26. Paterson, E. Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralization / E. Paterson // Plant Soil. – Vol. 408. – 2016. – P. 243–254. DOI: org/10.1007/s11104–016–2928–8.

27. Jones, M. D. Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? / M.D. Jones // Can. J. Bot. – Vol. 82. – 2004. – P. 1089–1109.

28. Casieri, L. Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without Sulphur stress / L. Casieri // Planta – Vol. 235. – 2012. – P. 1431–1447. DOI: org/10.1007/s00425–012–1645–7.

29. Jiang, Y. N. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi / Y. N. Jiang // Science – Vol. 356. – 2017. – P. 1172–1175. DOI: org/10.1126/science.aam9970.

30. Garcia, K. The role of mycorrhizal associations in plant potassium nutrition. / K.Garcia, S.D. Zimmermann // Front. Plant Sci. – 2014. – p. 337. DOI: org/10.3389/fpls.2014.00337.

31. Pallon, J. Symbiotic fungi that are essential for plant nutrient uptake in vesti gated with NMP. / J. Pallon // Nucl. Instrum. Methods Phys. Res. Sect., B 260. – 2007. – P. 149–152. DOI: org/ 10.1016/j.nimb.2007.02.018.

32. Olsson, P.A. Phosphorus availability influences elemental uptake in the mycorrhizal fungus Glomus intraradices, as revealed by particle–induced X–ray emission analysis / P.A. Olsson // Appl. Environ. Microbiol. – Vol.74. – 2007. – P. 4144–4148. DOI: org/10.1128/AEM.0 0376–08.

33. Olsson, P.A. Elemental composition in vesicles of an arbuscular mycorrhizal fungus, as revealed by PIXE analysis / P.A. Olsson // Fungal Biol. – Vol. 115. – 2011. – P. 643–648. DOI: org/10.1016/j.funbio.2011.03.008.

34. Pellegrino, E. Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi / E. Pellegrino // Soil Biol. Biochem. – Vol. 68. – 2014. – P. 429–439. DOI: org/10.1016/j.soilbio.2013.09.030.

35. Lehmann, A. Arbuscular mycorrhizal influence on zinc nutrition in crop plants – A meta–analysis / A. Lehmann // Soil Biol. Biochem. – Vol. 69. – 2014. – P. 123–131. DOI: org/10.1016/j.soilbio.2013.11.001.

36. Kwapata, M.B. Effects of moisture regime and phosphorus on mycorrhizal infection, nutrient uptake, and growth of cowpeas [Vigna unquiculata (L.) Walp] / M.B. Kwapata // Field Crops Res. – 1985. – Р. 241–250.

37. Walder, F.A. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis / F.Walder, M.G. van der Heijden, // Nat. Plants – № 1. – 2015. DOI: org/10.1038/nplants.2015.159.

38. Nouri, E. Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in petunia hybrid / E. Nouri // PLoS ONE – № 9. – 2014. DOI: org/10.1371/journal.pone.0090841.

39. Berruti, A. Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes / A. Berruti // Front Microbiol. – Vol. 6. – 2016. – P. 2–13. DOI: org/10.3389/fmicb.2015.01559.

40. Novak, J. Benefits of in vitro “biotization” of plant tissue cultures with microbial inoculants / J. Novak // In Vitro Cell. Dev. Biol. – Plant. – Vol. 34. – 1998. – P. 122–130. DOI: org/10.1007/BF02822776.

41. Jansa, J. In vitro and post vitro inoculation of micropropageted Rhododendrons with ericoid mycorrhizal fungi / J. Jansa // Appl. Soil. Ecol. – Vol.15. – 2000. – P. 125–136. DOI: org/10.1016/S0929–1393(00)00088–3.

42. Rai, M. Current advances in mecorrhization in micropropagation / M. Rai // In Vitro Cell. Dev. Biol. – Plant. – Vol. 37. – 2001. – P. 158–167. DOI: org/10.1079/IVP2000163/

43. Mucciarelli, M. In vitro and in vivo pepper–mint growth promotion by nonmycorrhizal fungal colonization / M. Mucciarelli // New Phytologist. – Vol. 158. – 2003. – P. 579–591. DOI: org/10.1046/j.1469–8137.2003.00762.x.

44. Kappor, R. Arbuscular mycorrhizae in micropropagation systems and their potential application / R. Kappor // Science Horticulturae. – Vol. 116. – 2008. – P. 227–239 DOI: org/10.1016/j.scienta.2008.02.002.

45. Дунаева, С.Е. Бактериальные микроорганизмы, ассоциированные с тканями растений в культуре in vitro: идентификация и возможная роль / С.Е Дунаева // Сельскохоз. Биология. – № 50(1). – 2015. – С. 3–15. DOI: org/10.15389/agrobiology.2015.1.3rus.

46. Srivastava, P.S. Role of Mycorrhiza in In Vitro Micropropagation of Plants / P.S. Srivastava // Techniques in Mycorrhizal Studies. Springer. – Dordrecht. – 2002. – P. 443–468. DOI: org/10.1007/978–94–017–3209–3_23.

47. Kokkoris, V. The role of in vitro cultivation on asymbiotic trait variation in a single species of arbuscular mycorrhizal fungus / V. Kokkoris // Fungal Biol. – Vol. 123. – 2019. – P. 307–317. DOI: org/10.1016/j.funbio.2019.01.005.

48. Sun, Z. Arbuscular mycorrhizal fungal proteins 14–3–3– are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis / Z. Sun // Front. Microbiol. – 2018. – № 5. – P. 9–19. DOI: org/10.3389/fmicb.2018.00091.

49. Ceballos, I. The in vitro mass–produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava / I. Ceballos // PLoS ONE 8 (8). – 2013. DOI: org/10.1371/journal.pone.0070633.

50. Rouphael, Y. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. / Y. Rouphael // Sci. Hortic (Amsterdam). – Vol. 196. – 2016. – P. 91–108. DOI: org/10.1016/j.scienta.2016.09.002.

51. Berruti, A. AMF components from a microbial inoculum fail to colonize roots and lack soil persistence in an arable maize field / A. Berruti // Symbiosis. – Vol. 72 (1). – 2016. – P. 73–80.

52. Siddiqui, Z. Effect of plant growth promoting bacterium, an AM fungus and soil types on the morphometrics and reproduction of Meloidogyne javanica on tomato / Z. Siddiqui // Appl. Soil Ecol. – № 8. – 1998. – P. 77–84.

53. Berruti, A. Application of laser microdissection to identify the mycorrhizal fungi that establish arbuscules inside root cells / A. Berruti // Front Plant Sci. – Vol. 4. – 2013. – P. 1–13. DOI: org/10.3389/fpls.2013.00135.

54. Rodriguez, A. The role of community and population ecology in applying mycorrhizal fungi for improved food security / A. Rodriguez // The ISME Journal. – № 9 (5). – P. 1053–1061. DOI: org/10.1038/ismej.2014.207.

55. Thirkell, T. Are mycorrhizal fungi our sustainable saviours considerations for achieving food security / T. Thirkell // J. Ecol. – № 105. – 2018. – P. 921–929. DOI: org/10.1111/1365–2745.12788.

56. Koltai, H. Mycorrhiza in floriculture: difficulties and opportunities / H. Koltai // Symbiosis. – Vol. 52. – 2010. – P. 55–63. DOI: org/10.1007/s13199–010–0090–2.

57. Berruti, A. Screening of plant growth retardants for growth control in Camellia / A. Berruti // Acta Hortic. – № 937. – 2012. – P. 265–270. DOI: org/10.17660/ActaHortic.2012.937.32.

58. Berruti, A. Application of nonspecific commercial AMF inocula results in poor mycorrhization in Camellia japonica / A. Berruti // Symbiosis. – Vol. 61 (2). – 2013. – P. 63–76. DOI: org/10.1007/s13199–013–0258–7.

59. Lazzara, S. Arbuscular mycorrhizal fungi altered the hypericin, pseudohypericin, and hyperforin content in flowers of Hypericum perforatum grown under contrasting P availability in a highly organic substrate / S. Lazzara // Mycorrhiza. – Vol. 27 (4). – 2017. – P. 345–354. DOI: org/10.1007/s00572–016–0756–6.

60. Htistozkova, M. Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development / M. Htistozkova // Appl. Soil Ecol. – Vol. 101. – 2016. – P. 57–63.

61. Borriello, R. Edaphic factors trigger diverse AM fungal communities associated to exotic camellias in closely located Lake Maggiore (Italy) sites / R. Borriello // Mycorrhiza. – Vol. 25 (4). – 2015. – P. 253–265.

62. Bagheri, S. Terpenoids and phenolic compounds production of mint genotypes in response to mycorrhizal bio–elicitors / S. Bagheri // Tech. J. Eng. Appl. – Sci. 4. – 2014. – P. 339–348.

63. Sbrana, C. Beneficial mycorrhizal symbionts affecting the production of health‐promoting phytochemicals / C. Sbrana // Electrophoresis. – Vol. 35 (11). – 2014. – P. 1535–1546.

64. Vosátka, M. Development of arbuscular mycorrhizal biotechnology and industry: current achievements and bottlenecks / M. Vosátka // Symbiosis. – Vol. 58. – 2013. – P. 29–37. DOI: org/10.1007/s13199–0120208–9.

65. van der Heijden Mycorrhizal ecology and evolution: the past, the present, and the future / van der Heijden // New Phytol. – № 205. – 2015. – P. 1406–1423. DOI: org/10.1111/nph.13288.

66. Allen, M. F. Ecology of vesicular–arbuscular mycorrhizae in an arid ecosystem: use of natural processes promoting dispersal and establishment / M. F. Allen // Mycorrhizae Decade Practical Applications and Research Priorities 7th NACOM IFAS. – Gainesville, FL. – 2018. – P. 133–135.

67. Verbruggen, E. Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success / E. Verbruggen // New Phytol. – № 197. – 2013. – P. 1104–1109. DOI: org/10.1111/j.14698137.2012.04348.x.

68. Corkidi, L. Assessing the in fectivity of commercial mycorrhizal inoculants in plant nursery conditions / L. Corkidi // J. Environ. Hortic. – № 22. – 2004. – P. 149–154.

69. Tarbell, T.J. Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium / J. Tarbell, TR.E. Koske // Mycorrhiza. – Vol. 18. – 2015. – P. 51–56. DOI: org/10.1007/s00572–007–0152–3.

70. Gosling, P. Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management / P. Gosling // Mycorrhiza. – Vol. 24. – 2015. – P. 47–59. DOI: org/10.1007/s00572–015–0651–6.

71. Faye, A. Evaluation of commercial arbuscular mycorrhizal inoculants / A. Faye // Can. J. Plant Sci. – № 93. – 2013. – P. 1201–1208. DOI: org/10.4141/cjps2013–326.

72. Leyval, C. Potential of arbuscular mycorrhizal fungi for bioremediation / C. Leyval // Mycorrhizal Technology in Agriculture. – № 8. – 2013. – P. 175–186.

73. van der Heijden Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity / van der Heijden // Nature. – № 396. – 2015. – P. 69–72. DOI: org/10.1038/23932.

74. Declerck, S. Monoxenic culture of the intraradical forms of glomus sp. Isolated from a tropical ecosystem: a proposed methodology for germplasm collection / S. Declerck // Mycologia. – № 90. –1998. – P. 579–585. DOI: org/10.2307/3761216.

75. Bécard, G. Early events of vesicular–arbuscular mycorrhiza formation on Ri T–DNA transformed roots / G. Bécard, J.A. Fortin // New Phytol. – № 108. – 1988. – P. 211–218. DOI: org/10.1111/j.1469–8137.1988.tb03698.x.

76. IJdo, M. Methods for large–scale production of AM fungi: past, present, and future / M. IJdo // Mycorrhiza. – Vol.21. – 2011. – P. 1–16. DOI: org/10.1007/s00572–010–0337–z.

77. Dalpé, Y. Arbuscular mycorrhiza inoculum to support sustainable cropping systems / Y. Dalpé, M. Monreal // Crop Manag. – № 10. – 2004. – P. 1094–1104. DOI: org/10.1094/CM2004–0301–09–RV.

78. Douds, D.D.Jr. On–farm production and utilization of arbuscular mycorrhizal fungus inoculum / D.D.Jr. Douds // Can. J. Plant Sci. – №85. – 2005. – P.15–21. DOI: org/10.4141/P03–168.

79. Pellegrino, E. Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components / E. Pellegrino // New Phytol. – № 194. – 2012. – P. 810–822. DOI: org/10.1111/j.1469–8137.2012.04090.x.

80. Mitra, D. Role of mycorrhiza and its associated bacteria on plant growth promotion and nutrient management in sustainable agriculture / D. Mitra // Int. J. Life Sci. – Appl. Sci. №1. – 2019. – P. 1–10.

81. Declerck, S. Monoxenic culture of the intraradical forms of glomus sp. Isolated from a tropical ecosystem: a proposed methodology for germplasm collection / S. Declerck // Mycologia. – № 90. – 1998. – P. 579–585. DOI: org/10.2307/3761216.

References

1. Brundrett M.C. Diversity and classification of mycorrhizal association. Biological reviews. 2004, vol. 79, pp. 473–495.

2. Read D.J., Jennings, D.H., Rayner A.D.M. The structure and function of the vegetative mycelium of mycorrhizal roots. Cambridge: Cambridge University Press, 1984, pp. 215–240.

3. Prasad R., Varma, A., Prasad, R., Tuteja, N. Introduction to mycorrhiza: historical development in Mycorrhiza. Springer, 2017, pp.1–7. DOI: org/10.1007/978–3–319–53064–2_1

4. Koide R.T., Mosse, B. A history of research on arbuscular mycorrhizal. Mycorrhiza. 2004, no.14, pp. 145–163.

5. Pozo M.J., Jung, S.C., Lopez–Raez, J.A. Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defense mechanisms. Arbuscular mycorrhizas: physiology and function, 2010, ch. 9, pp.193–207.

6. Aleshchenkova Z.M., Safronova, G., Solov'eva, E., Fedorenchik A. Vliyanie arbuskulyarnykh mikoriznykh gribov na rost i razvitie rastenii [The influence of arbuscular mycorrhizal fungi on the growth and development of plants]. Nauka i innovatsii. [Science and Innovation], 2011, no. 2, pp. 59–63 (In Russian)

7. Camarina, L.S. Endofitnye mikroorganizmy kak promoutery rosta rastenii v kul'ture in vitro. [Endophytic microorganisms as promoters of plant growth in vitro culture]. Sel'skokhozyaistvennaya biologiya. [Agricultural biology], Sochi, 2017, Rossiya, vol. 52, no. 5, pp. 917–927 (In Russian)

8. Solov'eva E., Aleshchenkova Z. Arbuskulyarnye mikoriznye griby v pochvenno–klimaticheskikh usloviyakh Belarusi. [Arbuscular mycorrhizal fungi in the soil–climatic conditions of Belarus]. Materialy 22–oi Mezhdunarodnoi nauchno–prakticheskoi konferentsii «Human and Nature Safety» [Materials of the 22nd International Scientific and Practical Conference «Human and Nature Safety»]. Kaunas, 2016, pp. 152–156 (In Russian)

9. Jansa J. In vitro and post vitro inoculation of micropropagated Rhododendrons with ericoid mycorrhizal fungi. Applied Soil Ecology, 2000, no.15, pp.125–136.

10. Jakobsen I. Transport of phosphorus and carbon in arbuscular mycorrhiza. Mycorrhiza: structure, function, molecular biology and biotechnology, 2nd ed., Springer–Verlag Berlin, 1999, pp. 305–332.

11. Kumawat N. Role of Biofertilizers in Agriculture. Popular Kheti, 2017, vol. 5(4), pp. 63–66.

12. Bonfante P. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun, 2010, vol. 1(48). DOI: org/10.1038/ncomms1046

13. Friesen M.I. Microbialy mediated plant functional traits. Annual Review of Ecology, Evolution, and Systematics, 2011, vol. 42, pp. 23–46. DOI: org/10.1146/annurev–ecolsys–102710–145039

14. Santander C. Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance. Journal of Soil Science and Plant Nutrition, 2019, no. 19(2), pp. 321–331. DOI: org/10.1007/s42729–019–00032–z

15. Normand L. Rooting and acclimatization of micropropagated cuttings are enhanced by the ectomycorrhizal fungi. Physiologia Plantatum, 1996, vol. 98, pp. 759–766. DOI: org/10.1111/j.1399–3054.1996.tb06682

16. Lehmann A. Arbuscular mycorrhizal influence on zinc nutrition in crop plants. A meta–analysis. Soil Biology and Biochemistry, 2014, vol.69, pp. 123–131. DOI: org/10.1016/j.soilbio.2013.11.001

17. Singh L. Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signaling & Behavior. 2011, vol. 6 (2), pp. 175–191. DOI: org/10.4161/psb.6.2.14146

18. Mohammad M. Effect of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts, Journal of Plant Nutrition, 2011, vol.26, pp. 125–137. DOI: org/10.1081/PLN–120016500).

19. Marschner H. Nutrient uptake in mycorrhizal symbiosis. Plant & Soil. 1994, vol. 159, pp. 89–102.

20. Johnson D. In situ (CO2)–C–13 pulse labeling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhiza to the soil. New Phytologist, 2002, vol. 153, pp. 327–334.

21. Nehls U. Carbohydrate metabolism in ectomycorrhizas gene expression, monosaccharide transport and metabolic control. New Phytologist, 2001, vol.150, pp. 533–541.

22. Buscot F. Recent advances in exploring physiology and biodiversity of ectomycorrhizas highlight the functioning of these symbioses in ecosystems. FEMS Microbiology Review, 2000, vol. 24, pp. 601–614.

23. Azcon R. Differential contribution of arbuscular mycorrhizal fungi to plant nitrate uptake (15N) under increasing N supply to the soil. Canadian Journal of Botany, 2001, vol. 79, pp. 1175–1180.

24. Hestrin R. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Communications Biology – Nature, 2019, vol. 2, p. 233. DOI: org/10.1038/s42003–019–0481–8

25. Bucher M. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist, 2007, vol. 173 (1), pp. 11–26. DOI: org/10.1111/j.14698137.2006.01935.x

26. Paterson E. Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralization. Plant & Soil. 2016, vol. 408, pp. 243–254. DOI: org/10.1007/s11104–016–2928–8

27. Jones M.D. Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Canadian Journal of Botany, 2004, vol. 82, pp. 1089–1109.

28. Casieri L. Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without Sulphur stress. Planta, 2012, vol. 235, pp. 1431–1447. DOI: org/10.1007/s00425–012–1645–7.

29. Jiang Y.N. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science, 2017, vol. 356, pp.1172–1175. DOI: org/10.1126/science.aam9970

30. Garcia K. and Zimmermann S.D. The role of mycorrhizal associations in plant potassium nutrition. Frontiers in Plant Science, 2014, p. 337. DOI: org/10.3389/fpls.2014.00337

31. Pallon J. Symbiotic fungi that are essential for plant nutrient uptake in vesti gated with NMP. Section B of Nuclear Instruments and Methods in Physics Research, 2007, pp. 149–152.DOI: org/10.1016/j.nimb.2007.02.018

32. Olsson P.A. Phosphorus availability influences elemental uptake in the mycorrhizal fungus Glomus intraradices, as revealed by particle–induced X–ray emission analysis. Applied and Environmental Microbiology, 2007, vol. 74, pp. 4144–4148. DOI: org/10.1128/AEM.0 0376–08

33. Olsson P.A. Elemental composition in vesicles of an arbuscular mycorrhizal fungus, as revealed by PIXE analysis. Fungal Biology Reviews, 2011, vol. 115, pp. 643–648. DOI: org/10.1016/j.funbio.2011.03.008

34. Pellegrino E. Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry, 2014, vol. 68, pp. 429–439. DOI: org/10.1016/j.soilbio.2013.09.030

35. Lehmann A. Arbuscular mycorrhizal influence on zinc nutrition in crop plants – A meta–analysis. Biology and Biochemistry, 2014, vol. 69, pp. 123–131. DOI: org/10.1016/j.soilbio.2013.11.001

36. Kwapata M.B. Effects of moisture regime and phosphorus on mycorrhizal infection, nutrient uptake, and growth of cowpeas [Vigna unquiculata (L.) Walp]. Field Crops Research, 1985, pp. 241–250.

37. Walder F. and van der Heijden M.G.A. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants, 2015, no. 1. DOI: org/10.1038/nplants.2015.159

38. Nouri E. Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in petunia hybrid. PLoS ONE, 2014, no. 9. DOI: org/10.1371/journal.pone.0090841

39. Berruti A. Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiology, 2016, vol. 6, pp. 2–13. DOI: org/10.3389/fmicb.2015.01559

40. Novak J. Benefits of in vitro “biotization” of plant tissue cultures with microbial inoculants. In Vitro Cellular & Developmental Biology – Plant, 1998, vol. 34, pp. 122–130. DOI: org/10.1007/BF02822776

41. Jansa J. In vitro and post vitro inoculation of micropropageted Rhododendrons with ericoid mycorrhizal fungi. Applied Soil Ecology, 2000, vol. 15, pp. 125–136. DOI: org/10.1016/S0929–1393(00)00088–3

42. Rai M. Current advances in mecorrhization in micropropagation. In Vitro Cellular & Developmental Biology – Plant, 2001, vol. 37, pp. 158–167. DOI: org/10.1079/IVP2000163

43. Mucciarelli M. In vitro and in vivo pepper–mint growth promotion by nonmycorrhizal fungal colonization. New Phytologist, 2003, vol. 158, pp. 579–591.
DOI: org/10.1046/j.1469–8137.2003.00762.x

44. Kappor R. Arbuscular mycorrhizae in micropropagation systems and their potential application. Science Horticulturae, 2008, vol. 116, pp. 227–239 DOI: org/10.1016/j.scienta.2008.02.002

45. Dunaeva S.E. Bakterial'nye mikroorganizmy, associirovannye s tkanjami rastenij v kul'ture in vitro: identifikacija i vozmozhnaja rol' [Bacterial microorganisms associated with plant tissues in an in vitro culture: identification and possible role]. Sel'skohozjajstvennaja Biologija [Agricultural Biology]. 2015, no. 50 (1), pp. 3–15. DOI: org/10.15389/agrobiology.2015.1.3rus

46. Srivastava P.S. Role of Mycorrhiza in In Vitro Micropropagation of Plants. Techniques in Mycorrhizal Studies. Springer. Dordrecht, 2002, pp. 443–468.
DOI: org/10.1007/978–94–017–3209–3_23

47. Kokkoris V. The role of in vitro cultivation on asymbiotic trait variation in a single species of arbuscular mycorrhizal fungus. Fungal Biology Reviews, 2019, vol. 123, pp. 307–317.DOI: org/10.1016/j.funbio.2019.01.005

48. Sun Z. Arbuscular mycorrhizal fungal proteins 14–3–3– are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis. Frontiers in Microbiology, 2018, no. 5, pp. 9–19. DOI: org/10.3389/fmicb.2018.00091

49. Ceballos I. The in vitro mass–produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS ONE, 2013, no. 8 (8). DOI: org/10.1371/journal.pone.0070633

50. Rouphael Y. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Scientia Horticulturae. Amsterdam, 2016, vol. 196, pp. 91–108. DOI: org/10.1016/j.scienta.2016.09.002

51. Berruti A. AMF components from a microbial inoculum fail to colonize roots and lack soil persistence in an arable maize field. Symbiosis, 2016, vol. 72 (1), pp. 73–80.

52. Siddiqui Z. Effect of plant growth promoting bacterium, an AM fungus and soil types on the morphometrics and reproduction of Meloidogyne javanica on tomato. Applied Soil Ecology, 1998, no. 8, pp. 77–84.

53. Berruti A. Application of laser microdissection to identify the mycorrhizal fungi that establish arbuscules inside root cells. Frontiers in Plant Science, 2013, vol. 4, pp. 1–13. DOI: org/10.3389/fpls.2013.00135

54. Rodriguez A. The role of community and population ecology in applying mycorrhizal fungi for improved food security. The ISME Journal, 2014, no. 9 (5), pp.1053–1061. DOI: org/10.1038/ismej.2014.207

55. Thirkell T. Are mycorrhizal fungi our sustainable saviours considerations for achieving food security. Journal of Ecology, 2018, no. 105, pp. 921–929. DOI: org/10.1111/1365–2745.12788

56. Koltai H. Mycorrhiza in floriculture: difficulties and opportunities. Symbiosis, 2010, vol. 52, pp. 55–63. DOI: org/10.1007/s13199–010–0090–2

57. Berruti A. Screening of plant growth retardants for growth control in Camellia. Acta Horticulturae, 2012, no. 937, pp. 265–270. DOI: org/10.17660/ActaHortic.2012.937.32

58. Berruti A. Application of nonspecific commercial AMF inocula results in poor mycorrhization in Camellia japonica. Symbiosis, 2013, vol. 61 (2), pp. 63–76. DOI: org/10.1007/s13199–013–0258–7

59. Lazzara S. Arbuscular mycorrhizal fungi altered the hypericin, pseudohypericin, and hyperforin content in flowers of Hypericum perforatum grown under contrasting P availability in a highly organic substrate. Mycorrhiza, 2017, vol. 27 (4), pp. 345–354. DOI: org/10.1007/s00572–016–0756–6

60. Htistozkova M. Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development. Applied Soil Ecology, 2016, vol. 101, pp. 57–63.

61. Borriello R. Edaphic factors trigger diverse AM fungal communities associated to exotic camellias in closely located Lake Maggiore (Italy) sites. Mycorrhiza, 2015, vol. 25 (4), pp. 253–265.

62. Bagheri S. Terpenoids and phenolic compounds production of mint genotypes in response to mycorrhizal bio–elicitors. Applied Science and Engineering Progress, 2016, vol. 18, sci. 4, pp. 339–348.

63. Sbrana C. Beneficial mycorrhizal symbionts affecting the production of health‐promoting phytochemicals. Electrophoresis, 2014, vol. 35 (11), pp.1535–1546.

64. Vosátka M. Development of arbuscular mycorrhizal biotechnology and industry: current achievements and bottlenecks. Symbiosis, 2013, vol. 58, pp. 29–37. DOI: org/10.1007/s13199–0120208–9

65. van der Heijden Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist, 2015, no. 205, pp. 1406–1423. DOI: org/10.1111/nph.13288

66. Allen M.F. Ecology of vesicular–arbuscular mycorrhizae in an arid ecosystem: use of natural processes promoting dispersal and establishment. Mycorrhizae Decade Practical Applications and Research Priorities 7th NACOM IFAS. Gainesville, FL., 2018, pp.133–135.

67. Verbruggen E. Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success, New Phytologist, 2013, no. 197, pp. 1104–1109. DOI: org/10.1111/j.14698137.2012.04348.x

68. Corkidi L. Assessing the in fectivity of commercial mycorrhizal inoculants in plant nursery conditions. // Journal of Environmental Horticulture, 2004, no. 22, pp. 149–154.

69. Tarbell T.J., Koske R.E. Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza, 2015, vol. 18, pp. 51–56. DOI: org/10.1007/s00572–007–0152–3

70. Gosling P. Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management. Mycorrhiza, 2015, vol. 24, pp. 47–59. DOI: org/10.1007/s00572–015–0651–6

71. Faye A. Evaluation of commercial arbuscular mycorrhizal inoculants. Canadian Journal of Plant Science, 2013, no. 93, pp. 1201–1208. DOI: org/10.4141/cjps2013–326

72. Leyval C. Potential of arbuscular mycorrhizal fungi for bioremediation. Mycorrhizal Technology in Agriculture, 2013, no. 8, pp.175–186.

73. Van der Heijden Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 2015, no. 396, pp. 69–72. DOI: org/10.1038/23932

74. Declerck S. Monoxenic culture of the intraradical forms of glomus sp. Isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia, 1998, no. 90, pp. 579–585. DOI: org/10.2307/3761216

75. Bécard G., Fortin J.A. Early events of vesicular–arbuscular mycorrhiza formation on Ri T–DNA transformed roots. New Phytologist, 1988, no. 108, pp. 211–218. DOI: org/10.1111/j.1469–8137.1988.tb03698.x

76. IJdo M. Methods for large–scale production of AM fungi: past, present, and future. Mycorrhiza, 2011, vol. 21, pp. 1–16. DOI: org/10.1007/s00572–010–0337–z

77. Dalpé Y., Monreal M. Arbuscular mycorrhiza inoculum to support sustainable cropping systems. Crop Management, 2004, no. 10, pp. 1094–1104. DOI: org/10.1094/CM2004–0301–09–RV

78. Douds D.D.Jr. On–farm production and utilization of arbuscular mycorrhizal fungus inoculum. Canadian Journal of Plant Science, 2005, no. 85, pp. 15–21. DOI: org/10.4141/P03–168

79. Pellegrino E. Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytologist, 2012, no. 194, pp. 810–822. DOI: org/10.1111/j.1469–8137.2012.04090.x

80. Mitra D. Role of mycorrhiza and its associated bacteria on plant growth promotion and nutrient management in sustainable agriculture. International Journal of Health and Life Sciences, no.1, 2019, pp. 1–10.

81. Declerck S. Monoxenic culture of the intraradical forms of glomus sp. Isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia, 1998, no. 90, pp. 579–585. DOI: org/10.2307/3761216
Опубликован
2020-06-23
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Биологические науки