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Host-induced Gene Advanced article Article Contents Silencing for • Introduction • HIGS of Nematodes Pest/Pathogen Control • HIGS of Insect Pests • HIGS of Fungi and Oomycetes Michael Nagle, Oregon State University, Corvallis, Oregon, USA • Future Directions Jared M LeBoldus, Oregon State University, Corvallis, Oregon, USA Online posting date: 22nd January 2018 AmyLKlocko, University of Colorado Colorado Springs, Colorado Springs, Col- orado, USA Host-induced gene silencing (HIGS) is an approach growth of the juvenile forms of coleopteran and lepidopteran that shows promise for the control of a variety insects. Farmers commonly grow Bt varieties of many large com- of problematic crop-damaging organisms, rang- modity crops, such as Zea mays (corn) and Gossypium hirsutum ing from nematodes and insects, to fungi and (cotton). As with other approaches to insect control, emerging et al parasitic plants. In general, HIGS utilises ribonu- resistance to Bt crops is becoming problematic (Tabashnik ., 2013), leading to interest in more effective utilisation of this cleic acid interference (RNAi) molecules produced technology, such as the combination of Bt fields with non-Bt by the plant, which then target key genes in refuge plantings and the development of alternate approaches to pests/pathogens, ideally leading to improved resis- pest control. tance of the plant and a reduction in damage. As One of these alternatives, a distinctive genetic engineering this area of research is still very much in develop- approach that has demonstrated effectiveness for controlling pests ment, the possible off-target and nontarget effects and pathogens, is host-induced gene silencing (HIGS). This need to be assessed, as do the long-term stabil- approach is unique as the host plant’s resistance is improved ity and effectiveness. Practical implementation of by RNA (ribonucleic acid)-mediated silencing of genes in the HIGS to commercial crop production will rely on pest/pathogen. Examples of some of the successes of this system extensive field-testing, as well as regulatory and in protecting various plant species against pests and pathogens marketplace acceptance of new varieties. can be found in Table 1. In this system, the host plant expresses RNAs that are designed to interfere with the expression of spe- cific pest/pathogen genes. Regulation of genes by RNAs ispart of a highly conserved biological process – for further reading see Introduction RNA Interference (RNAi) and MicroRNAs. HIGS utilises the ribonucleic acid interference (RNAi) pathway, a process by which Crop loss owing to damage by pests and pathogens is a signifi- translation of messenger ribonucleic acids (mRNAs) is reduced cant issue. For example, damage to Triticum aestivum (wheat) and by RNA-mediated neutralisation of the mRNAs, or where tran- Hordeum vulgare (barley) in the USA alone owing to Fusarium script production is reduced following epigenetic modifications, species was estimated to be 2.7 billion dollars between 1998 and via RNA-induced transcriptional silencing (RITS). An overview 2000 (Nganje et al., 2004). There are a variety of possible strate- of the molecular interactions between plants and fungi or insects gies for pest and pathogen control, including seeking naturally during HIGS is shown in Figure 1. resistant cultivars, breeding for improved resistance of suscepti- RNAi can lead to inhibition of gene expression by these ble cultivars, the application of commercial pesticides, crop rota- two distinct mechanisms (reviewed by Wilson and Doudna, tion and genetic engineering of resistance. These approaches can 2013). Following transcription, double-stranded ribonucleic acid be integrated as part of pest management strategies. For further (dsRNA) or microRNA precursors are cleaved by the ribonu- reading see Integrated Pest Management. clease DICER or DICER-like homologs into short interfering Genetic engineered resistance can take the form of expressed ribonucleic acid (siRNA) or miRNA fragments no more than 26 proteins, such as those from the bacterial species Bacillus nucleotides (nt) in length. These short RNAs may be amplified thuringiensis (commonly known as Bt proteins) to inhibit the by an RNA-dependent RNA polymerase, leading to a stronger silencing effect. By post-transcriptional gene silencing, siRNAs eLS subject area: Plant Science or miRNAs complex with enzymes including the nuclease ARG- ONAUTE (AGO) to form the RNA-induced silencing complex How to cite: Nagle, Michael; LeBoldus, Jared M; and Klocko, Amy L (January (RISC), which catalyses degradation of transcripts complemen- 2018) Host-induced Gene Silencing for Pest/Pathogen Control. tary to the bound RNA. In pretranscriptional gene silencing, RNA In: eLS. John Wiley & Sons, Ltd: Chichester. complexes with AGO and de novo DNA (deoxyribonucleic acid) DOI: 10.1002/9780470015902.a0023726 methyltransferases, leading to DNA methylation and epigenetic eLS © 2018, John Wiley & Sons, Ltd. www.els.net 1 Host-induced Gene Silencing for Pest/Pathogen Control Table 1 Summary of example HIGS studies cited Transgenic host Target species Target gene(s) Role(s) of Reference target(s) gene(s) HIGS targeting nematodes Arabidopsis thaliana Meloidogyne incognita, 16D10 Effector Huang et al. (2006) (Arabidopsis) Meloidogyne javanica, Meloidogyne arenaria, Meloidogyne hapla (root-knot nematode) Arabidopsis thaliana Meloidogyne chitwoodi 16D10 Effector Dinh et al. (2014) (Arabidopsis) (root-knot nematode) Solanum tuberosum Meloidogyne chitwoodi 16D10 Effector Dinh et al. (2014) (potato) (root-knot nematode) Vitis vinifera cv. Meloidogyne incognita 16D10 Effector Yang et al. (2013) Chardonnay (root-knot nematode) (chardonnay grape) Nicotiana tabacum Meloidogyne incognita Isocitrate lyase Metabolism Lourenco-Tessutti (tobacco) (root knot nematode) et al. (2015) Nicotiana tabacum Meloidogyne incognita Heat shock protein 90 Chaperone protein Lourenco-Tessutti (tobacco) (root-knot nematode) et al. (2015) Glycine max (soybean) Meloidogyne incognita Tyrosine phosphatase Metabolism Ibrahim et al. (2011) (root-knot nematode) Glycine max (soybean) Heterodera glycines Major sperm protein Sperm motility Steeves et al. (2006) (soybean cyst nematode) Glycine max (soybean) Heterodera glycines L-Lactate dehydrogenase Metabolism Youssef et al. (2013) (soybean cyst nematode) Glycine max (soybean) Heterodera glycines J15 Actin-related protein Tian et al. (2016) (soybean cyst nematode) Glycine max (soybean) Heterodera glycines J20 Signal transduction Tian et al. (2016) (soybean cyst nematode) Glycine max (soybean) Heterodera glycines J23 Actin-binding protein Tian et al. (2016) (soybean cyst nematode) Solanum melongena Meloidogyne incognita msp-18 Pharyngeal gland-specific Shivakumara et al. (eggplant) (southern root-knot effector (2017) nematode) Solanum melongena Meloidogyne incognita msp-20 Pharyngeal gland-specific Shivakumara et al. (eggplant) (southern root-knot effector (2017) nematode) HIGS targeting insects Hordeum vulgare (barley) Sitobion avenae (grain Sheath protein Salivary channel integrity Abdellatef et al. (2015) aphid) Arabidopsis thaliana Helicoverpa armigera CYP6AE14 Gossypol metabolism Mao et al. (2007) (Arabidopsis) (cotton bollworm) Zea mays (maize) Diabrotica virgifera H + ATPase Proton pump Baum et al. (2007) virgifera (western corn rootworm) Zea mays (maize) Diabrotica virgifera Snf7 Signal transduction for Bachman et al. (2013) virgifera (western corn regulation of lysozyme rootworm) formation 2 eLS © 2018, John Wiley & Sons, Ltd. www.els.net Host-induced Gene Silencing for Pest/Pathogen Control Table 1 (continued) Transgenic host Target species Target gene(s) Role(s) of Reference target(s) gene(s) HIGS targeting fungi and oomycetes Arabidopsis thaliana Blumeria graminis (barley Avirulence a10 Effector Nowara et al. (2010) (Arabidopsis) powdery mildew) Solanum tuberosum Phytophthora infestans Avirulence protein 3a Effector, virulence factor Bos et al. (2010) (potato) (potato blight) Triticum aestivum (wheat) Puccinia triticina (wheat MAP kinase (PtMAPK1) Predicted pathogenicity or Panwar et al. (2013) leaf rust) cyclophilin (PtCYC1) virulence calcineurin B (PtCNB) Solanum tuberosum Phytophthora infestans G protein β-subunit Signal transduction Jahan et al. (2015) (potato) (potato blight) (GPB1) associated with sporangium development Solanum tuberosum Phytophthora infestans Cellulose synthase A2 Synthesis of cellulose for Jahan et al. (2015) (potato) (potato blight) oomycete cell walls Solanum tuberosum Phytophthora infestans Pectinesterase Degradation of pectins in Jahan et al. (2015) (potato) (potato blight) plant cell walls Solanum tuberosum Phytophthora infestans Glyceraldehyde Glycolysis Jahan et al. (2015) (potato) (potato blight) 3-phosphate dehydrogenase Arabidopsis thaliana Fusarium graminearum Cytochrome P450 51A, Ergosterol biosynthesis Koch et al. (2013) (Arabidopsis), (fusarium ear blight) 51B and 51C Hordeum vulgare (barley) Hordeum vulgare (barley) Blumeria graminis (barley Eight candidate effectors, Unknown Pliego et al. (2013) powdery mildew) including two ribonucleases Musa musa x paradisiaca Fusarium oxysporum f. sp. Velvet Regulation of Ghag et al. (2014) (banana) cubense (fusarium wilt) development, mycotoxin production Musa musa x paradisiaca Fusarium oxysporum f. sp. Fusarium transcription Regulation of gene Ghag et al. (2014) (banana) cubense (fusarium wilt) factor 1 expression Arabidopsis thaliana Verticillium dahliae Ave1, SIX gene expression Transcription factor, Song and Thomma (Arabidopsis)
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