RNA Interference in Plant Protection from Fungal and Oomycet Infection

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Somente assinantes

Resumo

Phytopathogenic fungi pose a threat to food security, limiting the biological potential of agricultural crops and reducing the quality of products. New plant protection methods based on natural systemic and cellular phytoimmunity are being developed to date, where a unique mechanism, described by the term “RNA interference” (RNAi), occupies a special place. RNAi regulates the expression of target genes in a homologically dependent manner and, with the involvement of a protein complex designated as RISC (RNA-induced silencing complex), on the one hand, it protects plants from pathogens, but on the other hand, pathogens use it as a virulence factor. Cases of bilateral exchange of small RNAs between plants and pathogens affecting them through extracellular vesicles have been described. This review discusses the role of small RNAs, as well as DCL, AGO, and RdR proteins, in the infection of plants with pathogenic fungi and oomycetes, and the prospects for using RNAi in the development of environmentally friendly, modern plant protection products.

Sobre autores

I. Maksimov

Institute of Biochemistry and Genetics of Ufa Federal Research Center of Russian Academy of Sciences

Autor responsável pela correspondência
Email: igor.mak2011@yandex.ru
Russia, 450054, Ufa

M. Shein

Institute of Biochemistry and Genetics of Ufa Federal Research Center of Russian Academy of Sciences

Email: igor.mak2011@yandex.ru
Russia, 450054, Ufa

G. Burkhanova

Institute of Biochemistry and Genetics of Ufa Federal Research Center of Russian Academy of Sciences

Email: igor.mak2011@yandex.ru
Russia, 450054, Ufa

Bibliografia

  1. Fire A.Z. // Cell Death Differ. 2007. V. 14. P. 1998–2012.
  2. Romano N., Macino G. // Mol. Microbiol. 1992. V. 6. P. 3343–3353.
  3. Schuurs T.A., Schaeffer E.A., Wessels J.G. // Genetics. 1997. V. 147. P. 589–596.
  4. Hamada W., Spanu P.D. // Mol. Gen. Genet. 1998. V. 259. P. 630–638.
  5. Jorgensen R.A., Cluster P.D., English J., Que Q., Napoli C.A. // Plant Mol. Biol. 1996. V. 31. № 5. P. 957–973.
  6. Yang L., Mu X., Liu C., Cai J., Shi K., Zhu W., Yang Q. // J. Integr. Plant Mol. Biol. 2015. V. 57. № 12. P. 1078–1088.
  7. Huang C.Y., Wang H., Hu P., Hamby R., Jin H. // Cell Host Microbe. 2019. V. 26. № 2. P. 173–182.
  8. Wang J., Mei J., Ren G. // Front. Plant Sci. 2019. V. 10. Art. 360.
  9. Dutta S, Kumar D, Jha S, Prabhu K.V., Kumar M., Mukhopadhyay K. // Planta. 2017. V. 246. № 5. P. 939–957.
  10. Navarro L., Jay F., Nomura K., He S.Y., Voinnet O. // Science. 2008. V. 321. № 5891. P. 964–967.
  11. Katiyar-Agarwal S., Jin H. // Annu Rev Phytopathol. 2010. V. 48. P. 225–246.
  12. Zhang T., Zhao J.H., Fang Y.Y., Guo H.S., Jin Y. // Int. J. Mol. Sci. 2022. V. 23. № 5. Art. 2742.
  13. Tao Z., Liu H., Qiu D., Zhou Y., Li X., Xu C., Wang S. // Plant Physiology. 2009. V. 151. № 2. P. 936–948.
  14. Derbyshire M., Mbengue M., Barascud M., Navaud O., Raffaele S. // Mol. Plant Pathol. 2019. V. 20. № 9. P. 1279–1297.
  15. Zhang H., Tao Z., Hong H., Chen Z., Wu C., Li X., Xiao J., Wang S. // Nat Plants. 2016. V. 2. Art. 16016.
  16. Salamon S, Żok J, Gromadzka K, Błaszczyk L. // Pathogens. 2021. V. 10. № 11. Art. 1461.
  17. Li F., Pignatta D., Bendix C., Brunkard J.O., Cohn M.M., Tung J., Sun H., Kumar P., Baker B. // PNAS USA. 2012. V. 109. № 5. P. 1790–1795.
  18. Fukudome A., Kanaya A., Egami M., Nakazawa Y., Hiraguri A., Moriyama H., Fukuhara T. // RNA. 2011. V. 17. № 4. P. 750–760.
  19. Xiong Q., Ye W., Choi D., Wong J., Qiao Y., Tao K., Wang Y., Ma W. // Mol. Plant Microbe Interact. 2014. V. 27. № 12. P. 1379–89.
  20. Vetukuri R.R., Whisson S.C., Grenville-Briggs L.J. // Eur. J. Plant Pathol. 2017. V. 149. P. 771–777.
  21. de Vries S., de Vries J., Rose L.E. // Genes. 2019. V. 10. № 4. P. 310.
  22. Yin C., Ramachandran S.R., Zhai Y., Bu C., Pappu H.R., Hulbert S.H. // New Phytol. 2019. V. 222. № 3. P. 1561–1572.
  23. Wang B., Sun Y., Song N., Zhao M., Liu R., Feng H., Wang X., Kang Z. // New Phytol. 2017. V. 215. № 1. P. 338–350.
  24. Hou Y., Zhai Y., Feng L., Karimi H.Z., Rutter B.D., Zeng L. et al. // Cell Host Microbe. 2019. V. 25. P. 153–165.
  25. Natarajan B., Kalsi H.S., Godbole P., Malankar N., Thiagarayaselvam A., Siddappa S., et al. // J. Exp. Bot. 2018. V. 69. № 8. P. 2023.
  26. Luan Y., Cui J., Li J., Jiang N., Liu P., Meng J. // Planta 2018. V. 247. P. 127.
  27. Yang L., Jue D., Li W., Zhang R., Chen M., Yang Q. // PLoS ONE. 2013. V. 8. Art. e72840.
  28. Mu X.Y., Liu X.R., Cai J.H., Zhu W.J., Wang Z., Yang Q., You X. // Russ. J. Plant Physiol. 2018. V. 65. P. 203–210.
  29. Yu X., Hou Y., Chen W., Wang S., Wang P., Qu S. // Plant Cell Physiol. 2017. V. 58. № 9. P. 1541.
  30. Shen D., Suhrkamp I., Wang Y., Liu S., Menkhaus J., Verreet J.A., Fan L., Cai D. // New Phytol. 2014. V. 204. P. 577–594.
  31. Zhang H., Yu P., Zhao J., Jiang H., Wang H., Zhu Y. et al. // New Phytol. 2018. V. 217. P. 799–812.
  32. Cao J.Y., Xu Y.P., Zhao L., Li S.S., Cai X.Z. // Plant Mol. Biol. 2016. V. 92. P. 39–55.
  33. Yang L., Mu X., Liu C., Cai J., Shi K., Zhu W., Yang Q. // J. Integr. Plant Biol. 2015. V. 57. P. 1078–1088.
  34. Han G.Z. // New Phytol. 2019. V. 222. № 1. P. 70.
  35. Ouyang S., Park G., Atamian H.S., Han C.S., Stajich J.E., Kaloshian I., Borkovich K.A. // PLoS Pathog. 2014. V. 10. № 10. Art. e1004464.
  36. de Vries S., Kloesges T., Rose L.E. // Genome Biol Evol. 2015. V. 7. № 12. P. 3307–3321.
  37. Wu F., Xu J., Gao T., Huang D., Jin W. // BMC Plant Biol. 2021. V. 21. № 1. Art. 496.
  38. Han G., Cheng C., Zheng Y., Wang X., Xu Y., Wang W. et al. // Int. J. Mol. Sci. 2019. V. 20. Art. 4491.
  39. Zhang H., Chen X., Wang C., Xu Z., Wang Y., Liu X. et al. // Mol. Biol. Rep. 2013. V. 40. P. 6245–6253.
  40. Coursey T., Regedanz E., Bisaro D.M. // J. Virol. 2018. V. 92.
  41. Liu B., Li P., Li X., Liu C., Cao S., Chu C., Cao X. // Plant Physiol. 2005. V. 139. P. 296–305.
  42. Zhang B.S., Li Y.C., Guo H.S., Zhao J.H. // Front. Plant Sci. 2022. V. 13. Art. 847086.
  43. Wang Q., An B., Hou X., Guo Y., Luo H., He C. // Front. Microbiol. 2018. V. 8. Art. 2621.
  44. Yin C., Zhu H., Jiang Y., Shan Y., Gong L. // Cells. 2020. V. 9. P. 363
  45. Alazem M., Lon N.-Sh. // Curr. Opin. Vir. 2020. V. 42. P. 1.
  46. Matzke M.A., Kanno T., Matzke A.J. // Annu. Rev. Plant Biol. 2015. V.66. P. 243–267.
  47. Xin Y., Ma B., Zeng Q., He W., Qin M., He N. // Hortic Res. 2021. V. 8. № 1. Art. 154.
  48. Cambiagno D.A., Torres J.R., Alvarez M.E. // Front. Plant Sci. 2021. V. 12. Art. 703667.
  49. Lopez Sanchez A., Stassen J.H., Furci L., Smith L.M., Ton J. // Plant J. 2016. V. 88. P. 361–374.
  50. Luna E., Ton J. // Plant Signal. Behav. 2012. V. 7. P. 615–618.
  51. Schumann U., Lee J.M., Smith N.A., Zhong C., Zhu J.K., Dennis E.S. et al. // Epigenetics. 2019. V. 14. P. 1074–1087.
  52. Kong W., Xia X., Wang Q., Liu L.W., Zhang S., Ding L. et al. // Front. Genet. 2020. V. 11. Art. 460.
  53. Saripalli G., Sharma C., Gautam T., Singh K., Jain N., Prasad P. et al. // Mol. Biol. Rep. 2020. V. 47. P. 1339–1360.
  54. Geng S., Kong X., Song G., Jia M., Guan J., Wang F. et al. // Phytol. 2019. V. 221. P. 1023–1035.
  55. Morán-Diez M.E., Martínez de Alba Á.E., Rubio M.B., Hermosa R., Monte E. // J. Fungi. 2021. V. 7. P. 318–331.
  56. Srikant T., Drost H.G. // Front. Plant Sci. 2021. V. 11. Art. 606800.
  57. Kinoshita T., Seki M. // Plant Cell Physiol. 2014. V. 55. P. 1859–1863.
  58. Hubbard M., Germida J., Vujanovic V. // J. Appl. Microbiol. 2014. V. 116. № 1. P. 109–122.
  59. Espinas N.A., Saze H., Saijo Y. // Front. Plant Sci. 2016. V. 7. Art. 1201.
  60. Mallory A., Vaucheret H. // Plant Cell. 2010. V. 22. P. 3879–3889.
  61. Matzke M., Mosher R. // Nat. Rev. Genet. 2014. V. 15. P. 394–408.
  62. Astier-Manifacier S., Cornuet P. // Biochim. Biophys. Acta Nucleic Acids Protein Synth. 1971. V. 232. P. 484–493.
  63. Terefe-Ayana D., Yasmin A., Le T.L., Kaufmann H., Biber A., Kühr A., Linde M., Debener T. // Front. Plant Sci. 2011. V. 2. P. 35.
  64. Nunes C.C., Dean R.A. // Mol. Plant Pathol. 2012. V. 13. P. 519–529.
  65. Lewsey M.G., Hardcastle T.J., Melnyk C.W., Molnar A., Valli A.A., Urich M.A., Nery J.R., Baulcombe D.C., Ecker D.C. // PNAS USA. 2016. V. 113. Art. 801–810.
  66. Fang Y., Wang Z., Liu X., Tyler B.M. // Front. Microbiol. 2022. V. 13. Art. 817844.
  67. De Palma M., Ambrosone A., Leone A., Del Gaudio P., Ruocco M., Turiák L. et al // Plants. 2020. V. 9. P. 1777–1791.
  68. Zhang T., Zhao Y.L., Zhao J.H., Wang S., Jin Y., Chen Z.Q. et al. // Nat Plants. 2016. V. 2(10). Art. 16153.
  69. Rutter B.D., Innes R.W. // Plant Physiol. 2017. V. 173. P. 728–741.
  70. Jiao J., Peng D. // J. Plant Interact. 2018. V. 13. P. 514–521.
  71. Wang M., Weiberg A., Lin F.M., Thomma B.P., Huang H.D., Jin H. // Nature Plants. 2016. V. 2. № 10. Art. 16151.
  72. Ji H.M., Mao H.Y., Li S.J., Feng T., Zhang Z.Y., Cheng L. et al. // New Phytol. 2021. V. 232. № 2. P. 705–718.
  73. Wytinck N., Manchur C.L., Li V.H., Whyard S., Belmonte M.F. // Plants. 2020. V. 9. Art. 1780.
  74. Melnyk C.W., Molnar A., Baulcombe D.C. // EMBO J. 2011. V. 30. P. 3553–3563.
  75. Wang M., Dean R.A. // Mol. Plant Pathol. 2020. P. 21. P. 589–601.
  76. Liu G., Kang G., Wang S., Huang Y., Cai Q. // Front. Plant Sci. 2021. V. 12. Art. 757925.
  77. Villalobos–Escobedo J.M., Herrera–Estrella A., Carreras–Villaseñor N. // Mycologia. 2016. V. 108. № 3. P. 556–571.
  78. Lax C., Tahiri G., Patiño–Medina J.A., Cánovas–Márquez J.T., Pérez-Ruiz J.A., Osorio–Concepción M. et al. // Int. J. Mol. Sci. 2020. V. 21. № 24. Art. 9348.
  79. Qian X., Hamid F.M., El Sahili A., Darwis D.A., Wong Y.H., Bhushan S. et al. // J. Biol. Chem. 2016. V. 291. P. 9295–9309.
  80. Nguyen Q.B., Kadotani N., Kasahara S., Tosa Y., Mayama S., Nakayashiki H. // Mol. Microbiol. 2008. V. 68. P. 1348–1365.
  81. Kunej U., Jakše J., Radišek S., Štajner N. // Int. J. Mol. Sci. 2021. V. 22. Art. 4224.
  82. Chen Y., Gao Q., Huang M., Liu Y., Liu Z., Liu X., Ma Z. // Sci. Rep. 2015. V. 5. Art. 12500.
  83. Werner B.T., Koch A., Šečić E., Engelhardt J., Jelonek L., Steinbrenner J. et al. // PLoS ONE 2021. V. 16. № 8. Art. e0252365.
  84. Neupane A., Feng C., Mochama P.K., Saleem H., Lee Marzano S.Y. // Front. Plant Sci. 2019. V. 10. Art. 976.
  85. Mochama P., Jadhav P., Neupane A., Marzano S.Y.L. // Viruses. 2018. V. 10. Art. 214.
  86. Jo S.M., Ayukawa Y., Yun S.H., Komatsu K., Arie T. // J. Gen. Plant Pathol. 2018. V. 84. P. 395–398
  87. Campo S., Gilbert K.B., Carrington J.C. // PLoS Pathog. 2016. V. 12. Art. e1005640.
  88. Jeseničnik T., Štajner N., Radišek S., Mishra A.K., Košmelj K., Kunej U., Jakše J. // Int. J. Mol. Sci. 2022. V. 23. № 2. Art. 900.
  89. Feng H., Xu M., Liu Y., Gao X., Yin Z., Voegele R.T., Huang L. // For. Pathol. 2017. V. 47. Art. E12354.
  90. Borah M., Konakalla N.C. // Emerging Trends in Plant Pathology. Springer, Singapore. 2021. C. 561–575.
  91. Dunker F., Trutzenberg A., Rothenpieler J.S., Kuhn S., Pröls R., Schreiber T. et al // Elife. 2020. V. 9. Art. e56096
  92. Mascia T., Labarile R., Doohan F., Gallitelli D. // Sci. Rep. 2019. V. 9. Art. 2657.
  93. Ye W., Jiang J., Lin Y., Yeh K.-W., Lai Z., Xu X., Oelmüller R. // BMC Plant Biol. 2019. V. 19. P. 1–16.
  94. Raman V., Simon S.A., Demirci F., Nakano M., Meyers B.C., Donofrio N.M. // Mol. Plant-Microbe Interact. 2017. V. 30. P. 517–530.
  95. Wong-Bajracharya J., Singan V.R., Monti R., Plett K.L., Ng V., Grigoriev I.V. et al // PNAS USA. 2022. V. 119. № 3. Art. e2103527119.
  96. Bazin J., Khan G.A., Combier J.P., Bustos-Sanmamed P., Debernardi J.M., Rodriguez R. et al. // Plant J. 2013. V. 74. P. 920–934.
  97. Couzigou J.M., Lauressergues D., André O., Gutjahr C., Guillotin B., Bécard G., Combier J.P. // Cell Host Microbe. 2017. V. 21. P. 106–112.
  98. Etemadi M., Gutjahr C., Couzigou J.-M., Zouine M., Lauressergues D., Timmers A. et al // Plant Physiol. 2014. V. 166. P. 281–292.
  99. Wu P., Wu Y., Liu C.C., Liu L.W., Ma F.F., Wu X.Y. et al. // Front. Plant Sci. 2016. V. 7. Art. 429.
  100. Dang Y., Yang Q., Xue Z., Liu Y. // Eukaryotic Cell. 2011. V. 10. № 9. P. 1148–1155.
  101. Choi J., Kim K.T., Jeon J., Wu J., Song H., Asiegbu F.O., Lee Y.H. // BMC Genom. 2014. V. 15. Art. S14.
  102. Yadav V., Sun S., Billmyre R.B., Thimmappa B.C., Shea T., Lintner R. et al. // PNAS USA. 2018. V. 115. P. 3108–3113
  103. Третьякова П.Я., Соловьев А.А. // Экологическая генетика. 2020. Т. 18. № 4. С. 467–481.
  104. Matsuo Y., Novianti F., Takehara M., Fukuhara T., Arie T., Komatsu K. // Mol. Plant-Microbe Interac. 2019. V. 32. P. 1475.
  105. Lee W.S., Fu S.F., Li Z., Murphy A.M., Dobson E.A., Garland L. et al. // BMC Plant Biol. 2016. V. 16. Art. 15.
  106. Diao P., Zhang Q., Sun H., Ma W., Cao A., Yu R. et al. // Genes (Basel). 2019. V. 10. № 7. Art. 526.
  107. Hunter L.J.R., Brockington S.F., Murphy A.M., Pate A.E., Gruden K., MacFarlane S.A., Palukaitis P., Carr J.P. // Sci. Rep. 2016. V. 6: 23082.
  108. Qin L., Mo N., Zhang Y., Muhammad T., Zhao G., Zhang Y., Liang Y. // Front Plant Sci. 2017. V. 8. Art. 1068.
  109. Prakash V., Chakraborty S. // Physiol Mol Biol Plants. 2019 V. 25. № 4. P. 1055.
  110. Pradhan M., Pandey P, Baldwin I.T., Pandey S.P. // Plant Physiol. 2020. V. 184. № 2. P. 1128–1152.
  111. Dowen R.H., Pelizzola M., Schmitz R.J., Lister R., Dowen J.M., Nery J.R., Dixon J.E., Ecker J.R. // PNAS USA. 2012. V. 109. № 32. Art. E2183-91.
  112. Maksimov I.V. // Rus. J. Plant Physiol. 2009. T. 56. № 6. C. 742–752.
  113. Westwood J.H., Mccann L., Naish M., Dixon H., Murphy A.M., Stancombe M.A. et al. // Mol. Plant Pathol. 2013. V. 14. P. 158.
  114. Panwar V., McCallum B., Bakkeren G. // Plant Mol. Biol. 2013. V. 81. P. 595–608.
  115. Jahan S.N., Åsman A.K., Corcoran P., Fogelqvist J., Vetukuri R.R., Dixelius C. // J. Exp. Bot. 2015. V. 66. P. 2785–2794.
  116. Vega-Arreguin J.C., Jalloh A., Bos J.I., Moffett P. // Mol. Plant Microbe Interact. 2014. V. 27. P. 770–780.
  117. Song Y., Thomma B.P. // Mol. Plant Pathol. 2018. V. 19. P. 77–89.
  118. Coburn G.A., Cullen B.R. // J. Antimicrobial Chemotherapy. 2003. V. 51/ № 4. P. 753–756.
  119. Sang H., Kim J.-I. // Plant Biotechnol. Rep. 2020. V. 14. P. 1–8.
  120. Cheng W., Song X.-S., Li H-P., Cao L-H., Sun Ke., Qiu X.-L. et al // Plant Biotechnol. J. 2015. V. 9. P. 1335–1345.
  121. Tiwari I.M., Jesuraj A., Kamboj R., Devanna B.N., Botella J.R., Sharma T.R. // Sci. Rep. 2017. V. 7. Art. 7521.
  122. Panwar V., Jordan M., McCallum B., Bakkeren G. // Plant Biotechnol. J. 2018. V. 16. P. 1013–1023.
  123. Tetorya M., Rajam M.V. // 3 Biotech. 2021. V. 11. Art. 443.
  124. Zhang J., Khan S.A., Hasse C., Ruf S., Heckel D.G., Bock R. // Science. 2015. V. 347. P. 991–994.
  125. Qi T., Zhu X., Tan C., Liu P., Guo J., Kang Z., Guo J. // Plant Biotechnol. J. 2018. V. 16. P. 797–807.
  126. Nowara D., Gay A, Lacomme C., Shaw J., Ridout C., Douchkov D. et al. // Plant Cell. 2010. V. 22. P. 3130–3141.
  127. Acevedo-Garcia J., Spencer D., Thieron H, Reinstädler A., Hammond-Kosack K., Phillips A.L., Panstruga R. // Plant Biotechnol. J. 2017. V. 15. № 3. P. 367–378.
  128. Várallyay É., Giczey G., Burgyán J. // Arch. Virol. 2012. V. 157. P. 1345–1350.
  129. Wang Y., Cheng X., Shan Q., Zhang Y., Liu J., Gao C., Qiu J.-L. // Nat. Biotechnol. 2014. V. 32. P. 947–951.
  130. Yara A., Yaeno T., Hasegawa M., Seto H., Montillet J.L., Kusumi K., Seo S., Iba K. // Plant Cell Physiol. 2007. V. 48. P. 1263–1274.
  131. Xin M., Wang Y., Yao Y., Xie C., Peng H., Ni Z., Sun Q. // BMC Plant Biol. 2010. V. 10. P. 123–134.
  132. Kamthan A., Chaudhuri A., Kamthan M., Datta A. // Front. Plant Sci. 2015. V. 6. Art. 208.
  133. Kouzai Y., Nakajima K., Hayafune M., Ozawa K., Kaku H., Shibuya N.,et al. // Plant Mol Biol. 2014. V. 84. № 4-5. P. 519.
  134. Johnson E.T., Proctor R.H., Dunlap C.A., Busman M. // Mycotoxin Res. 2018. V. 34. Art. 29.
  135. Koch A., Wassenegger M. // New Phytol. 2021. V. 231. № 1. P. 54–59.
  136. Biedenkopf D., Will T., Knauer T., Jelonek L., Furch A.C.U., Busche T., Koch A. // ExRNA. 2020. V. 2. Art. 12.
  137. Song X.-S., Gu K.-X., Duan X.-X., Xiao X.-M., Hou Y.-P., Duan Y.-B. et al. // Pestic. Biochem. Physiol. 2018. V. 150. P. 1–9.
  138. Gebremichael D.E., Haile Z.M., Negrini F., Sabbadini S., Capriotti L., Mezzetti B., Baraldi E. // Plants 2021. V. 10. Art. 650.
  139. McLoughlin A.G., Wytinck N., Walker P.L., Girard I.J., Rashid K.Y., de Kievit T. et al. // Sci. Rep. 2018. V. 8. № 1. Art. 7320.
  140. Werner B.T., Gaffar F.Y., Schuemann J., Biedenkopf D., Koch A.M. // Front. Plant Sci. 2020. V. 11. P. 476.
  141. Nerva L., Sandrini M., Gambino G., Chitarra W. // Biomolecules. 2020. V. 10. Art. 200.
  142. Hernandez-Soto A., Chacon-Credas R. // Int. J. Mol. Sci. 2021. V. 22. Art. 12148.
  143. Casacuberta J.M., Devos Y., du Jardin P., Ramon M., Vaucheret H., Nogue F. // Trends Biotechnol. 2015. V. 33. P. 145–147.
  144. Gu K.X., Song X.S., Xiao X.M., Duan X.X., Wang J.X., Duan Y.B. et al. // Pest. Biochem. Physiol. 2019. V. 153. P. 36–46.
  145. Jiang P., Chen Y., Wilde H.D. // Sci. Hortic. 2016. V. 201. P. 225–229.
  146. Šečić E., Kogel K.H. // Cur. Opin. Biotechnol. 2021. V. 70. P. 136–142
  147. Mumbanza F.M., Kiggundu A., Tusiime G., Tushemereirwe W.K., Niblett C., Bailey A. // Pest Manag. Sci. 2013. V. 69. P. 1155–1162.
  148. Hasley J.A.R., Navet N., Tian M. // PLOS One. 2021. V. 16. Art. e0253245.
  149. Álvarez–Sánchez A.R., Romo-Quinones C., Rosas-Quijano R., Reyes A.G., Barraza A., Magallón–Barajas F. et al. // Aquac. Res. 2018. V. 49. P. 480–491.
  150. Guan R., Chu D., Han X., Miao X., Li H. // Front. Bioeng. Biotechnol. 2021. V. 9. Art. 753790.
  151. Niehl A., Soininen M., Poranen M.M., Heinlein M. // Plant Biotechnol. J. 2018. V. 16. P. 1679–1687.
  152. Drinnenberg I.A., Weinberg D.E., Xie K.T., Mower J.P., Wolfe K.H., Fink G.R., Bartel D.P. // Science. 2009. V. 326. P. 544–550.
  153. Ding F., Huang X., Gao X., Xie M., Pan G., Li Q. et al. // Nanoscale. 2019. V. 11. № 37. P. 17211–17215.
  154. Mitter N., Worrall E.A., Robinson K.E., Xu Z.P., Carroll B.J. // Curr. Opin. Virol. 2017. V. 26. P. 49–55.
  155. Jiang C., Fan Z., Li Z., Niu D., Li Y., Zheng M. et al. // Mol. Plant Pathol. 2020. V. 21. P. 854–870.
  156. Kang S., Sun D., Qin J., Guo L., Zhu L., Bai Y. et al. // J. Pest Sci. 2022. V. 95. P. 101–114.

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML
Baixar
2.

Baixar (41KB)
Metadados
3.

Baixar (198KB)
Metadados

Declaração de direitos autorais © И.В. Максимов, М.Ю. Шеин, Г.Ф. Бурханова, 2023

Este site utiliza cookies

Ao continuar usando nosso site, você concorda com o procedimento de cookies que mantêm o site funcionando normalmente.

Informação sobre cookies