Exploration of Plant-Microbe Interactions for Sustainable Agriculture in CRISPR Era
Abstract
:1. Introduction
2. Composition and Driving Factors of the Plant–Microbe (PM) Interactions
2.1. Composition
2.2. Factors Influencing Microbial Communities and PM Interactions
2.2.1. Biotic Factors
2.2.2. Abiotic Factors
3. Role of Plant Microbiota in Sustainable Agriculture
3.1. Beneficial PM Interactions in Agriculture
3.2. Harmful PM Interactions
4. Modern Tools to Explore PM Interactions
5. Components of the Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas System
5.1. Cas9 and Cpf1 Orthologs
5.2. Cas9 and Cpf1 Variants
5.3. RNA-Targeting Endonucleases
6. CRISPR-Based Programmed Tools and Applications
7. CRISPR-Mediated PM Applications in Agriculture
7.1. Understanding the Fundamentals of the PM Interactions
7.2. Plant Disease Resistance
7.3. Plant Growth Promotion and Nutrient Uptake
7.4. Metabolic Engineering
8. Limitations and Possible Solutions
8.1. Culture, Species Isolation, and Transformation Protocols
8.2. Delivery of CRISPR-Based Tools
8.3. Transgene-Free Applications
8.4. Off-Targets, Biosafety Laws, and Regulations
9. Conclusions and Future Directions
Author Contributions
Funding
Conflicts of Interest
References
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Host | Sampling | Key Findings | Ref. |
---|---|---|---|
Agave | Rhizosphere, whole plant | Microbial composition was mainly regulated by the plant compartment, while the fungal community composition was primarily determined by the plant host biogeography. | [9] |
Arabidopsis | Root, rhizosphere | The composition of rhizospheric microbiota was found reliant on the environment rather than host species. | [10] |
Arabidopsis | Leaf, root | Genome drafts of 400 isolates revealed a substantial overlap of genome-encoded functional capabilities between leaf- and root-derived bacteria with few significant differences. | [11] |
Arabidopsis | Root, rhizosphere | Explored genetic network controlling the phosphate stress response influences the structure of the root microbiome community, even under non-stress phosphate conditions. | [12] |
Arabidopsis | Roots, rhizosphere | Bacterial microbiota is indispensable for plant survival and protection against root-filamentous fungi. | [13] |
Barley | Root, rhizosphere | Rhizospheric and root microbiota affect plant growth. The interactions between microbe–microbe and plant–microbe drive distinct microbiota. | [14] |
Citrus | Root, rhizosphere | The core rhizosphere microbiome comprises several potential beneficial plant microbial species and detected over-represented microbial functional traits. | [15] |
Grapevine | Grape must | Environmental factors, variety, and regional origins determine the unique grapevine-associated microbiota. These factors are the key to the unique taste and wine quality. | [16] |
Grapevine | Rhizosphere, whole plant | Microbial composition of soil and root is primarily influenced by plant-selective pressure, soil C:N ratio, and pH. Leaf and fruit microbiota alterations correlated with soil carbon, cultivation practices, and geography. | [17] |
Maize | Roots, rhizosphere | Associated microbiota showed heritable variation in community composition of rhizosphere and significant field-specific heritable variation. | [18] |
Maize | Roots, rhizosphere | Assembled a simplified and representative synthetic bacterial model community containing seven dominant strains to study the community assembly dynamics that interfered with the growth of a plant-pathogenic fungus. | [19] |
Maize | Root, rhizosphere | Microbiome composition varies with plant genotype, plant age, and climate events. | [20] |
Petunia, Arabidopsis | Root, rhizosphere | Root microbiota composition and responses vary substantially in response to the varying phosphorus (P) application. | [21] |
Potato | Roots, rhizosphere | Early stages of the plant showed the cultivar-dependent composition of bacterial communities, but in the flowering and senescence stages, this was not the case. Furthermore, the population of some species flourished under different ecological conditions more than the other species. | [22] |
Rice | Root, rhizosphere | Endosphere, rhizoplane, and rhizosphere consist of a diverse microbiome. Cultivation practices influence the diversity of microbiome compositions at each compartment. | [23] |
Rice | Root, rhizosphere | Type of soil environment (i.e., rhizosphere versus bulk soil) is a driving factor of the structure of the microbial community than the plant age. | [24] |
Soybean, Wheat | Rhizosphere, root | Soil properties such as pH and nitrate content may influence the composition of root microbiome in agricultural fields. | [25] |
Sugar beet | Soil after harvesting | Identified crucial bacterial taxa and genes suppressing a fungal root pathogen and showed that plant protection depends on the rhizospheric microbial community. | [26] |
Sugarcane | Rhizosphere, whole plant | Microbial communities enter primarily from native rhizospheric soil and colonize plant organs in distinct patterns. | [27] |
Tomato | Rhizosphere, whole plant | Distinct microbial communities found associated with different plant organs. | [28] |
Tomato | Rhizosphere, whole plant | The study explored the protection role of rhizosphere microbiota against soil-borne pathogen causing wilt disease. | [29] |
Wheat, Cucumber | Roots from pots | Genus or species level differences observed between the rhizospheric microbiome from diverse plant species related to environmental factors. | [30] |
Wild mustard | Leaf and root | Leaf microbiome genetically controlled by the host and several bacterial species of leaf microbiomes shared with root microbiomes, suggesting acquisition from the soil. | [31] |
Pathogen | Disease | Host | Target Gene (plant or pathogen), Interaction | GE Tool | Ref. | |
---|---|---|---|---|---|---|
Bacteria | ||||||
1. | Xanthomonas oryzae pv. oryzae | Bacterial blight | Rice | OsSWEET14 (plant); Pathogen interacts with the promoter of gene and hijacks plant sugars | TALEN | [151] |
2. | Xanthomonas oryzae pv. oryzae | Bacterial blight | Rice | OsSWEET14 and OsSWEET11 (plant); Pathogen interacts with the promoter of gene and hijacks plant sugars | CRISPR/Cas9 | [152] |
3. | Xanthomonas oryzae pv. oryzae | Bacterial blight | Rice | OsSWEET13 (plant); Pathogen hijacks sucrose from plant cells | TALEN | [153] |
4. | Pseudomonas syringae pv. tomato, Xanthomonas spp., Phytophthora capsici | Bacterial speck, Blight, and spot | Tomato | SlDMR6-1 (plant); Knock-out of DMR6 increases salicylic acid levels that induces production of secondary metabolites and PR genes | CRISPR/Cas9 | [154] |
5. | Xanthomonas citri subsp. citri | Citrus canker | Citrus | CsLOB1 (plant); Susceptibility gene induced by pathogen | CRISPR/Cas9 | [155] |
6. | Xanthomonas citri subsp. citri | Citrus canker | Citrus | CsLOB1 (plant); Susceptibility gene induced by pathogen | CRISPR/Cas9 | [156] |
7. | Erwinia amylovora | Fire blight | Apple | DIPM-1, 2 and 4 (plant); Directly interact with the disease-specific gene of bacterial pathogen | CRISPR/Cas9 | [157] |
8. | Pseudomonas syringae pv. tomato (Pto) DC3000 | Bacterial speck | Tomato | SlJAZ2 (plant); Directly interact with coronatine produced by bacteria that helps in leaf colonization | CRISPR/Cas9 | [158] |
Fungi and Oomycetes | ||||||
9. | Magnaporthe grisea, Burkholderia glumae | Fungal blast, bacterial blight | Rice | OsMPK5 (plant); A negative regulator of rice defense response | CRISPR/Cas9 | [159] |
10. | Blumeria graminis f. sp. tritici | Powdery mildew | Wheat | MLO-A1, B1, and D1 (plant); Confer susceptibility to fungi | CRISPR/Cas9 | [160] |
11. | Uncinula necator | Powdery mildew | Grape | MLO-7 (plant); Confer susceptibility to a fungal pathogen | CRISPR/Cas9 | [157] |
12. | Ustilago maydis | Corn smut | Maize | bW2 and bE1 (microbe); To evaluate the CRISPR system. | CRISPR/Cas9 | [170] |
13. | Phytophthora tropicalis | Black pod disease | Cacao | Non-Expressor of Pathogenesis-Related3 (TcNPR3) gene (plant) | CRISPR/Cas9 | [171] |
14. | Blumeria graminis f. sp. tritici | Powdery mildew | Wheat | Three homologs of TaEDR1 (plant); Plays a negative role in plant immunity | CRISPR/Cas9 | [172] |
15. | Oidium neolycopersici | Powdery mildew | Tomato | SlMlo1 (plant); Confer susceptibility to fungi | CRISPR/Cas9 | [173] |
16. | Phytophthora sojae | Damping off | Soybean | Avr4/6 (microbe); Virulence proteins enter host cells and promote host susceptibility. | CRISPR/Cas9 | [174] |
17. | Magnaporthe oryzae | Rice blast | Rice | OsERF922 (plant); Negative regulator of blast fungus | CRISPR/Cas9 | [175] |
18. | Leptosphaeria maculans | Blackleg disease | Canola | Histidine kinase (microbe); To study resistance mechanism against a pesticide (Iprodione) | CRISPR/Cas9 | [176] |
19. | Alternaria alternata | Black molds | Sunflower | Phosphate decarboxylase pyrG, polyketide-synthase, pksA, and 1,3,8-THN reductase, brm2 (microbe); To establish a CRISPR system | CRISPR/Cas9 | [177] |
20. | Magnaporthe oryzae | Rice blast | Rice | Melanin biosynthetic polyketide synthase genes ALB1 and RSY1, succinate dehydrogenase enzyme SDI1 (microbe); Mutations to study the pathogenicity | CRISPR/Cas9 (RNP) | [161] |
21. | Sclerotinia sclerotiorum | White mold | Flowers, Vegetables | Oxalate biosynthesis gene Ssoah1 (microbe); Mutations to study the pathogenicity | CRISPR/Cas9 | [162] |
22. | Ustilaginoidea virens | False smut | Rice | USTA ustiloxin and UvSLT2 MAP kinase (microbe); To study the gene function | CRISPR/Cas9 | [163] |
23. | Magnaporthe oryzae | Rice blast | Rice | OsSEC3A (plant); participate in the exocyst complex and interact with defense proteins | CRISPR/Cas9 | [164] |
24. | Botrytis cinerea | Gray mold | Grape | WRKY52 (plant); Transcription factor involved in response to biotic stress | CRISPR/Cas9 | [165] |
25. | Fusarium oxysporum | Wilt | Tomato, legumes, cotton | Polyketide synthase PKS4 (microbe); To study gene function | CRISPR/Cas9 (RNP) | [166] |
26. | Phytophthora capsici and P. sojae | Powdery mildew, Damping-off | Vegetables, soybean | Oxysterol binding protein-related protein 1 (microbe); To study resistance mechanism against a pesticide (Oxathiapiprolin) | CRISPR/Cas9 | [167] |
27. | Fusarium oxysporum | Wilt | Tomato, legumes, cotton | FoSso1 and FoSso2 (microbe); For endogenous tagging of target genes | CRISPR/Cas9 | [168] |
28. | Peronophythora litchii | Downy blight | Lychee | Pectin acetylesterase, PAE4, and PAE5 (microbe); to study the pathogenicity | CRISPR/Cas9 | [169] |
Viruses | ||||||
29. | BSCTV | Viral (DNA) | Arabidopsis | Replication origin (microbe) | ZNF | [178] |
30. | TYLCCNV, TbCSV | Viral (DNA) | Tobacco | AC1 replication-associated (Rep) protein (microbe) | ZNF | [179] |
31. | TYCCNV, TbCSV, TLCYnV | Viral (DNA) | Tobacco | AC1 replication-associated (Rep) protein (microbe) | TALE | [186] |
32. | TuMV | Viral (RNA) | Arabidopsis | eIF4E/exon (plant); Directly interact with viral protein and helps viral replication | CRISPR/Cas9 | [187] |
33. | CVYV, ZYMV, PRSV-W | Viral (RNA) | Cucumber | eIF4E/exon (plant); Directly interact with viral protein and helps viral replication | CRISPR/Cas9 | [188] |
34. | RTSV | Tungro (RNA) | Rice | eIF4G (plant); Directly interact with viral protein and helps viral RNA replication | CRISPR/Cas9 | [189] |
35. | TYLCV, BCTV, MeMV | Viral (DNA) | Tobacco | Intergenic region of origin of replication (IR), capsid protein (CP), RCRII motif of Rep protein (microbe) | CRISPR/Cas9 | [190] |
36. | BeYDV | Viral (DNA) | Tobacco | Long intergenic region (LIR), Rep protein encoding gene (microbe) | CRISPR/Cas9 | [191] |
37. | BSCTV | Viral (DNA) | Arabidopsis, Tobacco | IR, CP and Rep (microbe) | CRISPR/Cas9 | [192] |
38. | CBSV | Brown streak (RNA) | Cassava | nCBP-1 & nCBP-2/exon (plant); Directly interact with viral protein and helps viral replication | CRISPR/Cas9 | [193] |
39. | TMV | Viral (RNA) | Arabidopsis, Tobacco | ORF1a, ORFCP, 3’- UTR (microbe) | CRISPR/Cas9 | [180] |
40. | TuMV | Viral (RNA) | Tobacco | TuMV-GFP, Helper component proteinase silencing suppressor (HC-Pro), coat protein genes (microbe) | CRISPR/Cas13a | [181] |
41. | WDV | Viral (DNA) | Barley | Rep, MP, LIR (microbe) | CRISPR/Cas9 | [182] |
42. | CYVV | Viral (DNA) | Arabidopsis | eIF4E1 gene (plant); Directly interact with viral protein and helps viral replication | Cas9- PmCDA1 | [183] |
43. | eBSV | Viral (DNA) | Banana | Three target sites in viral genome (microbe) | CRISPR/Cas9 | [184] |
44. | CLCuKoV, TYLCV, TYLCSV, MeMV, BCTV | Viral (DNA) | Tobacco | IR, coat protein and Rep (microbe) | CRISPR/Cas9 | [185] |
Trait | Present and Future Applications | Potential CRISPR Tools |
---|---|---|
Understanding the fundamentals of the PM interactions | Identification of genes involved in PM interactions | Genotyping, DNA barcoding, lineage tracing |
Study of gene function in microbe and plant | Cas9, Cpf1 (gene knock-in/knock-out, gene replacement) | |
Regulation of gene expression, promoter engineering | CRISPRa, CRISPRi (transcription regulation); DNA methylation, histone modification (epigenome editing) | |
Novel allele generation | EvolvR (diversification of target genomic locus) | |
Plant disease resistance | Functional characterization of pathogenesis-related factors | Cas9, Cpf1 (gene knock-in/knock-out) |
Phytopathogen identification | Cas13 (RNA editing tool), RNA base editors | |
Development of disease-resistant plant varieties | Cas9, Cpf1 (gene knock-in/knock-out, gene replacement), ABE/CBE (base editing) | |
Pyramiding of multiple disease-resistant traits | Multiplex GE | |
Pesticide resistance in crops | Cas9, Cpf1(gene knock-in/knock-out, gene replacement), ABE/CBE (base editing) | |
Plant growth promotion and nutrient uptake | Improvement of nutrient accessibility (biological nitrogen fixation, phosphate solubilization) | Cas9, Cpf1 (gene knock-in/knock-out, gene replacement) |
Application of nodulation in non-leguminous crops through pathway engineering | Cas9, Cpf1 (gene replacement, multiplex GE) | |
Improved stress resistance by signaling molecules | Cas9, Cpf1 (gene knock-in/knock-out, gene transfer/replacement) | |
Engineered microbes to reduce cost and chemical use | Cas9, Cpf1 (gene knock-in/knock-out, gene replacement, multiplex GE) | |
Metabolic engineering | Exploration of the novel plant metabolome pathways | Cas9, Cpf1 (gene knock-in/knock-out, gene replacement, multiplex GE) |
Secondary metabolites | Cas9, Cpf1 (gene knock-in/knock-out, gene replacement, multiplex GE) |
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Shelake, R.M.; Pramanik, D.; Kim, J.-Y. Exploration of Plant-Microbe Interactions for Sustainable Agriculture in CRISPR Era. Microorganisms 2019, 7, 269. https://doi.org/10.3390/microorganisms7080269
Shelake RM, Pramanik D, Kim J-Y. Exploration of Plant-Microbe Interactions for Sustainable Agriculture in CRISPR Era. Microorganisms. 2019; 7(8):269. https://doi.org/10.3390/microorganisms7080269
Chicago/Turabian StyleShelake, Rahul Mahadev, Dibyajyoti Pramanik, and Jae-Yean Kim. 2019. "Exploration of Plant-Microbe Interactions for Sustainable Agriculture in CRISPR Era" Microorganisms 7, no. 8: 269. https://doi.org/10.3390/microorganisms7080269