Skip to main content

Advertisement

SpringerLink
Log in

Biotic stress triggered small RNA and RNAi defense response in plants

  • Review
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The yield of crops is largely affected by different types of biotic stresses. To minimize the damage, crop plants adapted themselves to overcome the stress conditions through gene expression reprogramming at transcriptional and post-transcriptional levels. With a better knowledge of plants’ responses in adverse environments, new methodologies and strategies have been applied to develop better stress-tolerant plants. In this manner, small RNAs (micro RNA and small-interfering RNA) are reported to play a central role to combat biotic stresses in plants. Depending upon the stress stimuli, these small RNAs can up or down regulate the genes expression, that indicate their potential role in overcoming the stress. These stress-induced small RNAs may reduce the expression of the target gene(s) that might negatively influence plants’ response to the adverse conditions. Contrariwise, miRNA, a class of small RNA, can downregulate its expression to upregulate the expression of the target gene(s), which might positively aid to the stress adaptation. Along with this, benefits of RNA interference (RNAi) have also been stated in functional genomic research on insects, fungi and plant pathogens. RNAi is involved in the safe transport of dsRNA to the targeted mRNA(s) in the biotic stress-causing agents (for example fungi and insects) and saves the plant from damage, which is a safer approach compared to use of chemical pesticides. The current review summarizes the role of small RNAs and the use of RNAi to save the plants from biotic stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Ali M, Hasan H, Bux H, Gul A, Memon HMU, Khan A, Munir F, Tawseen HB, Shakoor M, Majid M (2020) Role of transcription factors in drought mediating pathways in wheat. In: Ozturk M, Gul A (eds) Climate change and food security with emphasis on wheat, 1st edn. Academic Press, London, pp 177–192

    Google Scholar 

  2. Hasan H, Ali M, Javaid A, Liaqat A, Hussain S, Siddique R, Fayaz T, Gul A (2020) Cellular mechanism of salinity tolerance in wheat. In: Ozturk M, Gul A (eds) Climate change and food security with emphasis on wheat, 1st edn. Academic Press, London, pp 55–76

    Google Scholar 

  3. Ali M, Gul A, Hasan H, Gul S, Fareed A, Nadeem M, Siddique R, Jan SU, Jamil M (2020) Cellular mechanisms of drought tolerance in wheat. In: Ozturk M, Gul A (eds) Climate change and food security with emphasis on wheat, 1st edn. Academic Press, London, pp 155–167

    Google Scholar 

  4. Ali M, Gul A, Hasan H, Alipour H, Abbasi AA, Abbas S, Fatima T, Taimoor Z (2020) LEA proteins and drought stress in wheat. In: Ozturk M, Gul A (eds) Climate change and food security with emphasis on wheat, 1st edn. Academic Press, London, pp 193–205

    Google Scholar 

  5. Muhammad T, Zhang F, Zhang Y, Liang Y (2019) RNA interference: a natural immune system of plants to counteract biotic stressors. Cells 8(1):38

    CAS  PubMed Central  Google Scholar 

  6. Budak H, Zhang B (2017) MicroRNAs in model and complex organisms. Springer, New York

    Google Scholar 

  7. Phillips T (2008) Small non-coding RNA and gene expression. Nat Educ 1(1):115

    Google Scholar 

  8. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    CAS  PubMed  Google Scholar 

  9. Huang J, Yang M, Zhang X (2016) The function of small RNAs in plant biotic stress response. J Integr Plant Biol 58(4):312–327

    CAS  PubMed  Google Scholar 

  10. Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16(12):727–741

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Baulcombe D (2004) RNA silencing in plants. Nature 431(7006):356

    CAS  PubMed  Google Scholar 

  12. Brant EJ, Budak H (2018) Plant small non-coding RNAs and their roles in biotic stresses. Front Plant Sci 9:1038

    PubMed  PubMed Central  Google Scholar 

  13. Pattanayak D, Solanke AU, Kumar PA (2013) Plant RNA interference pathways: diversity in function, similarity in action. Plant Mol Biol Rep 31(3):493–506

    CAS  Google Scholar 

  14. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62(5):742–759

    CAS  PubMed  Google Scholar 

  15. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    CAS  PubMed  Google Scholar 

  16. Sunkar R, Chinnusamy V, Zhu J, Zhu J-K (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12(7):301–309

    CAS  PubMed  Google Scholar 

  17. Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233(3):471–484

    CAS  PubMed  Google Scholar 

  18. Budak H, Kantar M, Bulut R, Akpinar BA (2015) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13

    CAS  PubMed  Google Scholar 

  19. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11(8):539

    CAS  PubMed  Google Scholar 

  20. Agrawal N, Dasaradhi P, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK (2003) RNA interference: biology, mechanism, and applications. Microbiol Mol Biol Rev 67(4):657–685

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Sajid IA, Tabassum B, Yousaf I, Khan A, Adeyinka OS, Shahid N, Nasir IA, Husnain T (2019) In vivo gene silencing of potato virus X by small interference RNAs in transgenic potato. Potato Res. https://doi.org/10.1007/s11540-019-09433-0

    Article  Google Scholar 

  22. Tabassum B, Nasir IA, Khan A, Aslam U, Tariq M, Shahid N, Husnain T (2016) Short hairpin RNA engineering: in planta gene silencing of potato virus Y. Crop Prot 86:1–8

    CAS  Google Scholar 

  23. Boyd LA, Ridout C, O'Sullivan DM, Leach JE, Leung H (2013) Plant–pathogen interactions: disease resistance in modern agriculture. Trends Genet 29(4):233–240

    CAS  PubMed  Google Scholar 

  24. Gautam HR, Bhardwaj ML, Kumar R (2013) Climate change and its impact on plant diseases. Curr Sci 105(12):1685–1691

    Google Scholar 

  25. Islam W, Noman A, Qasim M, Wang L (2018) Plant responses to pathogen attack: small RNAs in focus. Int J Mol Sci 19(2):515

    PubMed Central  Google Scholar 

  26. Borovsky D (2005) Guest editorial. Phytoparasitica 33(2):109–112

    Google Scholar 

  27. Gordon KH, Waterhouse PM (2007) RNAi for insect-proof plants. Nat Biotechnol 25(11):1231

    CAS  PubMed  Google Scholar 

  28. Adeyinka OS, Tabassum B, Nasir IA, Yousaf I, Sajid IA, Shehzad K, Batcho A, Husnain T (2019) Identification and validation of potential reference gene for effective dsRNA knockdown analysis in Chilo partellus. Sci Rep 9(1):1–11

    CAS  Google Scholar 

  29. Quan G, Kanda T, Tamura T (2002) Induction of the white egg 3 mutant phenotype by injection of the double-stranded RNA of the silkworm white gene. Insect Mol Biol 11(3):217–222

    CAS  PubMed  Google Scholar 

  30. Ohnishi A, Hull JJ, Matsumoto S (2006) Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. Proc Natl Acad Sci USA 103(12):4398–4403

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Tomoyasu Y, Denell RE (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev Genes Evol 214(11):575–578

    CAS  PubMed  Google Scholar 

  32. Fujita K, Shimomura K, Yamamoto K-i, Yamashita T, Suzuki K (2006) A chitinase structurally related to the glycoside hydrolase family 48 is indispensable for the hormonally induced diapause termination in a beetle. Biochem Biophys Res Commun 345(1):502–507

    CAS  PubMed  Google Scholar 

  33. Arakane Y, Li B, Muthukrishnan S, Beeman RW, Kramer KJ, Park Y (2008) Functional analysis of four neuropeptides, EH, ETH, CCAP and bursicon, and their receptors in adult ecdysis behavior of the red flour beetle Tribolium castaneum. Mech Dev 125(11–12):984–995

    CAS  PubMed  Google Scholar 

  34. Konopova B, Jindra M (2008) Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development 135(3):559–568

    CAS  PubMed  Google Scholar 

  35. Minakuchi C, Namiki T, Shinoda T (2009) Krüppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Dev Biol 325(2):341–350

    CAS  PubMed  Google Scholar 

  36. Parthasarathy R, Palli SR (2009) Molecular analysis of juvenile hormone analog action in controlling the metamorphosis of the red flour beetle, Tribolium castaneum. Arch Insect Biochem Physiol 70(1):57–70

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Roignant J-Y, Carré C, Mugat B, Szymczak D, Lepesant J-A, Antoniewski C (2003) Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 9(3):299–308

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J (2006) Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog 2(2):e14

    PubMed  PubMed Central  Google Scholar 

  39. Miller SC, Brown SJ, Tomoyasu Y (2008) Larval RNAi in Drosophila? Dev Genes Evol 218(9):505–510

    CAS  PubMed  Google Scholar 

  40. Lehane M, Billingsley P (2012) Biology of the insect midgut. Springer Science & Business Media, Berlin

    Google Scholar 

  41. Hakim RS, Baldwin K, Smagghe G (2010) Regulation of midgut growth, development, and metamorphosis. Annu Rev Entomol 55:593–608

    CAS  PubMed  Google Scholar 

  42. Uslu VV, Wassenegger M (2020) Critical view on RNA silencing-mediated virus resistance using exogenously applied RNA. Curr Opin Virol 42:18–24

    CAS  PubMed  Google Scholar 

  43. Bolognesi R, Ramaseshadri P, Anderson J, Bachman P, Clinton W, Flannagan R, Ilagan O, Lawrence C, Levine S, Moar W (2012) Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoS ONE 7(10):e47534

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    CAS  PubMed  Google Scholar 

  45. Dzitoyeva S, Dimitrijevic N, Manev H (2001) Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol Psychiatry 6(6):665

    CAS  PubMed  Google Scholar 

  46. Timmons L, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263(1):103–112

    CAS  PubMed  Google Scholar 

  47. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25(11):1322

    CAS  PubMed  Google Scholar 

  48. Mao Y-B, Cai W-J, Wang J-W, Hong G-J, Tao X-Y, Wang L-J, Huang Y-P, Chen X-Y (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25(11):1307

    CAS  PubMed  Google Scholar 

  49. Nejat N, Mantri N (2017) Plant immune system: crosstalk between responses to biotic and abiotic stresses the missing link in understanding plant defence. Signal 2:O2

    Google Scholar 

  50. Khaled SK, Abdel-Tawab FM, Fahmy EM, Ahmed E, Khaled KA (2019) The impact of siRNA features on its fidelity and ef-ficiency in targeting soluble acid invertase gene in sugarcane. Egypt J Genet Cytol 47(2)

  51. Zhang H, Zhang J, Yan J, Gou F, Mao Y, Tang G, Botella JR, Zhu J-K (2017) Short tandem target mimic rice lines uncover functions of miRNAs in regulating important agronomic traits. Proc Natl Acad Sci 114(20):5277–5282

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang F, Ren X, Zhang F, Qi M, Zhao H, Chen X, Ye Y, Yang J, Li S, Zhang Y (2019) A R2R3-type MYB transcription factor gene from soybean, GmMYB12, is involved in flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis. Plant Biotechnol Rep 13:1–15

    Google Scholar 

  53. Jalmi SK, Bhagat PK, Verma D, Noryang S, Tayyeba S, Singh K, Sharma D, Sinha AK (2018) Traversing the links between heavy metal stress and plant signaling. Front Plant Sci 9:12

    PubMed  PubMed Central  Google Scholar 

  54. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2(2):e219

    PubMed  PubMed Central  Google Scholar 

  55. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229(4):1009–1014

    CAS  PubMed  Google Scholar 

  56. Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L). BMC Plant Biol 10(1):123

    PubMed  PubMed Central  Google Scholar 

  57. Kulcheski FR, de Oliveira LF, Molina LG, Almerão MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimarães FC (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12(1):307

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Ludwig-Müller J (2015) Bacteria and fungi controlling plant growth by manipulating auxin: balance between development and defense. J Plant Physiol 172:4–12

    PubMed  Google Scholar 

  59. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    CAS  PubMed  Google Scholar 

  60. Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4(2):205–217

    CAS  PubMed  Google Scholar 

  62. Lu S, Sun YH, Amerson H, Chiang VL (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J 51(6):1077–1098

    CAS  PubMed  Google Scholar 

  63. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39(8):1033–1037

    CAS  PubMed  Google Scholar 

  64. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312(5772):436–439

    CAS  PubMed  Google Scholar 

  65. Khraiwesh B, Zhu J-K (1819) Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta Gene Regul Mech 2:137–148

    Google Scholar 

  66. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15(6):394–408

    CAS  PubMed  Google Scholar 

  67. Martínez de Alba AE, Moreno AB, Gabriel M, Mallory AC, Christ A, Bounon R, Balzergue S, Aubourg S, Gautheret D, Crespi MD (2015) In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs. Nucleic Acids Res 43(5):2902–2913

    PubMed  PubMed Central  Google Scholar 

  68. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136(4):642–655

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Banerjee S, Sirohi A, Ansari AA, Gill SS (2017) Role of small RNAs in abiotic stress responses in plants. Plant Gene 11:180–189

    CAS  Google Scholar 

  70. Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457(7228):413–420

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Sampey GC, Guendel I, Das R, Jaworski E, Klase Z, Narayanan A, Kehn-Hall K, Kashanchi F (2012) Transcriptional gene silencing (TGS) via the RNAi machinery in HIV-1 infections. Biology 1(2):339–369

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Casacuberta JM, Devos Y, Du Jardin P, Ramon M, Vaucheret H, Nogue F (2015) Biotechnological uses of RNAi in plants: risk assessment considerations. Trends Biotechnol 33(3):145–147

    CAS  PubMed  Google Scholar 

  73. Machado AK, Brown NA, Urban M, Kanyuka K, Hammond-Kosack KE (2018) RNAi as an emerging approach to control Fusarium head blight disease and mycotoxin contamination in cereals. Pest Manag Sci 74(4):790–799

    CAS  PubMed  Google Scholar 

  74. Ding S-W, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130(3):413–426

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Zrachya A, Kumar PP, Ramakrishnan U, Levy Y, Loyter A, Arazi T, Lapidot M, Gafni Y (2007) Production of siRNA targeted against TYLCV coat protein transcripts leads to silencing of its expression and resistance to the virus. Transgenic Res 16(3):385–398

    CAS  PubMed  Google Scholar 

  76. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, Zhu J-K, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci 103(47):18002–18007

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21(23):3123–3134

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38:S31

    CAS  PubMed  Google Scholar 

  79. Navarro L, Jay F, Nomura K, He SY, Voinnet O (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321(5891):964–967

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Zhang X, Zhao H, Gao S, Wang W-C, Katiyar-Agarwal S, Huang H-D, Raikhel N, Jin H (2011) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393∗-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42(3):356–366

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Zhu C, Liu T, Chang Y-N, Duan C-G (2019) Small RNA functions as a trafficking effector in plant immunity. Int J Mol Sci 20(11):2816

    CAS  PubMed Central  Google Scholar 

  82. Yi H, Richards EJ (2007) A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19(9):2929–2939

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Zotti M, dos Santos EA, Cagliari D, Christiaens O, Taning CNT, Smagghe G (2018) RNA interference technology in crop protection against arthropod pests, pathogens and nematodes. Pest Manag Sci 74(6):1239–1250

    CAS  PubMed  Google Scholar 

  84. Filipowicz W (2005) RNAi: the nuts and bolts of the RISC machine. Cell 122(1):17–20

    CAS  PubMed  Google Scholar 

  85. Wilson RC, Doudna JA (2013) Molecular mechanisms of RNA interference. Ann Rev Biophys 42:217–239

    CAS  Google Scholar 

  86. Zotti M, Smagghe G (2015) RNAi technology for insect management and protection of beneficial insects from diseases: lessons, challenges and risk assessments. Neotropical Entomol 44(3):197–213

    CAS  Google Scholar 

  87. Joga MR, Zotti MJ, Smagghe G, Christiaens O (2016) RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front Physiol 7:553

    PubMed  PubMed Central  Google Scholar 

  88. Bonfim K, Faria JC, Nogueira EO, Mendes ÉA, Aragão FJ (2007) RNAi-mediated resistance to bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol Plant Microbe Interact 20(6):717–726

    CAS  PubMed  Google Scholar 

  89. Dolgov S, Mikhaylov R, Serova T, Shulga O, Firsov A (2010) Pathogen-derived methods for improving resistance of transgenic plums (Prunus domestica L.) for Plum pox virus infection. Julius-Kühn-Archiv (427):133

  90. Scorza R, Callahan A, Dardick C, Ravelonandro M, Polak J, Malinowski T, Zagrai I, Cambra M, Kamenova I (2013) Genetic engineering of Plum pox virus resistance:‘HoneySweet’plum—from concept to product. Plant Cell, Tissue Organ Cult 115(1):1–12

    CAS  Google Scholar 

  91. Siomi H, Siomi MC (2009) On the road to reading the RNA-interference code. Nature 457(7228):396

    CAS  PubMed  Google Scholar 

  92. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957

    PubMed  Google Scholar 

  93. Guedes R, Smagghe G, Stark J, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62

    CAS  PubMed  Google Scholar 

  94. Douglas AE (2018) Strategies for enhanced crop resistance to insect pests. Annu Rev Plant Biol 69:637–660

    CAS  PubMed  Google Scholar 

  95. Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10(2):126

    CAS  PubMed  Google Scholar 

  96. Kolliopoulou A, Santos D, Taning CNT, Wynant N, Vanden Broeck J, Smagghe G, Swevers L (2019) PIWI pathway against viruses in insects. Wiley Interdisc Rev RNA 10(6):e1555

    Google Scholar 

  97. Nandety RS, Kuo Y-W, Nouri S, Falk BW (2015) Emerging strategies for RNA interference (RNAi) applications in insects. Bioengineered 6(1):8–19

    CAS  PubMed  Google Scholar 

  98. Ozata DM, Gainetdinov I, Zoch A, O’Carroll D, Zamore PD (2019) PIWI-interacting RNAs: small RNAs with big functions. Nat Rev Genet 20(2):89–108

    CAS  PubMed  Google Scholar 

  99. Gammon DB, Mello CC (2015) RNA interference-mediated antiviral defense in insects. Curr Opin Insect Sci 8:111–120

    PubMed  PubMed Central  Google Scholar 

  100. Marques JT, Imler J-L (2016) The diversity of insect antiviral immunity: insights from viruses. Curr Opin Microbiol 32:71–76

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Swevers L, Liu J, Smagghe G (2018) Defense mechanisms against viral infection in Drosophila: RNAi and non-RNAi. Viruses 10(5):230

    PubMed Central  Google Scholar 

  102. Christiaens O, Dzhambazova T, Kostov K, Arpaia S, Joga MR, Urru I, Sweet J, Smagghe G (1424E) Literature review of baseline information on RNAi to support the environmental risk assessment of RNAi-based GM plants. EFSA Support Publ 15(5):1424E

    Google Scholar 

  103. Niu J, Shen G, Christiaens O, Smagghe G, He L, Wang J (2018) Beyond insects: current status and achievements of RNA interference in mite pests and future perspectives. Pest Manag Sci 74(12):2680–2687

    CAS  PubMed  Google Scholar 

  104. Christiaens O, Swevers L, Smagghe G (2014) DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 53:307–314

    CAS  PubMed  Google Scholar 

  105. Guan R-B, Li H-C, Fan Y-J, Hu S-R, Christiaens O, Smagghe G, Miao X-X (2018) A nuclease specific to lepidopteran insects suppresses RNAi. J Biol Chem 293(16):6011–6021

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Wang K, Peng Y, Pu J, Fu W, Wang J, Han Z (2016) Variation in RNAi efficacy among insect species is attributable to dsRNA degradation in vivo. Insect Biochem Mol Biol 77:1–9

    PubMed  Google Scholar 

  107. Kolliopoulou A, Taning CN, Smagghe G, Swevers L (2017) Viral delivery of dsRNA for control of insect agricultural pests and vectors of human disease: prospects and challenges. Front Physiol 8:399

    PubMed  PubMed Central  Google Scholar 

  108. Swevers L, Vanden Broeck J, Smagghe G (2013) The possible impact of persistent virus infection on the function of the RNAi machinery in insects: a hypothesis. Front Physiol 4:319

    PubMed  PubMed Central  Google Scholar 

  109. Brigneti G, Garcia-Mas J, Baulcombe D (1997) Molecular mapping of the potato virus Y resistance gene Rysto in potato. Theor Appl Genet 94(2):198–203

    CAS  Google Scholar 

  110. Kasschau KD, Carrington JC (1998) A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95(4):461–470

    CAS  PubMed  Google Scholar 

  111. Frizzi A, Huang S (2010) Tapping RNA silencing pathways for plant biotechnology. Plant Biotechnol J 8(6):655–677

    CAS  PubMed  Google Scholar 

  112. Webster CL, Waldron FM, Robertson S, Crowson D, Ferrari G, Quintana JF, Brouqui J-M, Bayne EH, Longdon B, Buck AH (2015) The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol 13(7):e1002210

    PubMed  PubMed Central  Google Scholar 

  113. Remnant EJ, Shi M, Buchmann G, Blacquière T, Holmes EC, Beekman M, Ashe A (2017) A diverse range of novel RNA viruses in geographically distinct honey bee populations. J Virol 91(16):e00158–e1117

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Yu XD, Liu ZC, Huang SL, Chen ZQ, Sun YW, Duan PF, Ma YZ, Xia LQ (2016) RNAi-mediated plant protection against aphids. Pest Manag Sci 72(6):1090–1098

    CAS  PubMed  Google Scholar 

  115. Fishilevich E, Vélez AM, Storer NP, Li H, Bowling AJ, Rangasamy M, Worden SE, Narva KE, Siegfried BD (2016) RNAi as a management tool for the western corn rootworm Diabrotica virgifera virgifera. Pest Manag Sci 72(9):1652–1663

    CAS  PubMed  Google Scholar 

  116. Palli SR (2014) RNA interference in Colorado potato beetle: steps toward development of dsRNA as a commercial insecticide. Curr Opin Insect Sci 6:1–8

    PubMed  PubMed Central  Google Scholar 

  117. Killiny N, Hajeri S, Tiwari S, Gowda S, Stelinski LL (2014) Double-stranded RNA uptake through topical application, mediates silencing of five CYP4 genes and suppresses insecticide resistance in Diaphorina citri. PLoS ONE 9(10):e110536

    PubMed  PubMed Central  Google Scholar 

  118. Wang M, Jin H (2017) Spray-induced gene silencing: a powerful innovative strategy for crop protection. Trends Microbiol 25(1):4–6

    CAS  PubMed  Google Scholar 

  119. Luan J-B, Ghanim M, Liu S-S, Czosnek H (2013) Silencing the ecdysone synthesis and signaling pathway genes disrupts nymphal development in the whitefly. Insect Biochem Mol Biol 43(8):740–746

    CAS  PubMed  Google Scholar 

  120. Yoon J-S, Gurusamy D, Palli SR (2017) Accumulation of dsRNA in endosomes contributes to inefficient RNA interference in the fall armyworm, Spodoptera frugiperda. Insect Biochem Mol Biol 90:53–60

    CAS  PubMed  Google Scholar 

  121. Christiaens O, Tardajos MG, Reyna M, Zarel L, Dash M, Dubruel P, Smagghe G (2018) Increased RNAi efficacy in Spodoptera exigua via the formulation of dsRNA with guanylated polymers. Front Physiol 9:316

    PubMed  PubMed Central  Google Scholar 

  122. Gillet F-X, Garcia RA, Macedo LL, Albuquerque EV, Silva M, Grossi-de-Sa MF (2017) Investigating engineered ribonucleoprotein particles to improve oral RNAi delivery in crop insect pests. Front Physiol 8:256

    PubMed  PubMed Central  Google Scholar 

  123. Taning CNT, Christiaens O, Berkvens N, Casteels H, Maes M, Smagghe G (2016) Oral RNAi to control Drosophila suzukii: laboratory testing against larval and adult stages. J Pest Sci 89(3):803–814

    Google Scholar 

  124. Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GM, Xu ZP (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat Plants 3(2):1–10

    Google Scholar 

  125. Cooper AM, Silver K, Zhang J, Park Y, Zhu KY (2019) Molecular mechanisms influencing efficiency of RNA interference in insects. Pest Manag Sci 75(1):18–28

    CAS  PubMed  Google Scholar 

  126. Dang Y, Yang Q, Xue Z, Liu Y (2011) RNA interference in fungi: pathways, functions, and applications. Eukaryot Cell 10(9):1148–1155

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel K-H (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci 110(48):19324–19329

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Wang M, Weiberg A, Lin F-M, Thomma BP, Huang H-D, Jin H (2016) Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat Plants 2(10):16151

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Khajuria C, Ivashuta S, Wiggins E, Flagel L, Moar W, Pleau M, Miller K, Zhang Y, Ramaseshadri P, Jiang C (2018) Development and characterization of the first dsRNA-resistant insect population from western corn rootworm Diabrotica virgifera virgifera LeConte. PLoS ONE 13(5):e0197059

    PubMed  PubMed Central  Google Scholar 

  130. Sugahara R, Tanaka S, Jouraku A, Shiotsuki T (2017) Geographic variation in RNAi sensitivity in the migratory locust. Gene 605:5–11

    CAS  PubMed  Google Scholar 

Download references

Funding

No funding was received from any source during this study.

Author information

Authors and Affiliations

  1. School of Life Sciences, University of Science and Technology of China (USTC), Hefei, 230027, Anhui, China

    Mohsin Ali & Ayesha Javaid

  2. Department of Bioinformatics & Biotechnology, International Islamic University, Islamabad, 44000, Pakistan

    Mohsin Ali & Sajid Hassan Naqvi

  3. Division of Plant Sciences, Faculty of Agriculture and Environmental Science, Catholic University of the West Africa, Cotonou, Benin

    Anicet Batcho

  4. Department of Plant Breeding, Swedish University of Agricultural Sciences, PO Box 101, 23053, Alnarp, Sweden

    Waqas Khan Kayani

  5. Department of Integrative Biotechnology, Sungkyunkwan University Natural Sciences Campus, Suwon, Gyeonggi-do, 16419, South Korea

    Aamir Lal

  6. Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

    Imtiaz Ahmad Sajid

  7. Pathology Section, Department of Forest Conservation and Protection, Forestry Research Institute of Nigeria, Ibadan, Nigeria

    Joy O. Nwogwugwu

Authors
  1. Mohsin Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ayesha Javaid
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sajid Hassan Naqvi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anicet Batcho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Waqas Khan Kayani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aamir Lal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Imtiaz Ahmad Sajid
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Joy O. Nwogwugwu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohsin Ali.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ali, M., Javaid, A., Naqvi, S.H. et al. Biotic stress triggered small RNA and RNAi defense response in plants. Mol Biol Rep 47, 5511–5522 (2020). https://doi.org/10.1007/s11033-020-05583-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-020-05583-4

Keywords

Search

Navigation