Acknowledgements requested in publications
« This work of the Interdisciplinary Thematic Institute IMCBio, as part of the ITI 2021-2028 program of the University of Strasbourg, CNRS and Inserm, was supported by IdEx Unistra (ANR-10-IDEX-0002), and by SFRI-STRAT’US project (ANR 20-SFRI-0012) and EUR IMCBio (ANR-17-EURE-0023) under the framework of the French Investments for the Future Program. »
2024
M., THIEME; N., MINADAKIS; C., HIMBER; B., KELLER; W., XU; K., RUTOWICZ; C., MATTEOLI; M., BÖHRER; B., RYMEN; D., LAUDENCIA-CHINGCUANCO; J., VOGEL; R., SIBOUT; C., STRITT; T., BLEVINS; A.C., ROULIN
Transposition of HOPPLA in siRNA-deficient plants suggests a limited effect of the environment on retrotransposon mobility in Brachypodium distachyon Actes
2024.
@proceedings{nokey,
title = {Transposition of HOPPLA in siRNA-deficient plants suggests a limited effect of the environment on retrotransposon mobility in Brachypodium distachyon},
author = {THIEME M. and MINADAKIS N. and HIMBER C. and KELLER B. and XU W. and RUTOWICZ K. and MATTEOLI C. and BÖHRER M. and RYMEN B. and LAUDENCIA-CHINGCUANCO D. and VOGEL J. and SIBOUT R. and STRITT C. and BLEVINS T. and ROULIN A.C.},
doi = {10.1101/2023.09.25.559196 },
year = {2024},
date = {2024-03-01},
urldate = {2024-03-01},
journal = {PLoS Genet},
abstract = {Long terminal repeat retrotransposons (LTR-RTs) are powerful mutagens regarded as a major source of genetic novelty and important drivers of evolution. Yet, the uncontrolled and potentially selfish proliferation of LTR-RTs can lead to deleterious mutations and genome instability, with large fitness costs for their host. While population genomics data suggest that an ongoing LTR-RT mobility is common in many species, the understanding of their dual roles in evolution is limited. Here, we harness the genetic diversity of 320 sequenced natural accessions of the Mediterranean grass Brachypodium distachyon to characterize how genetic and environmental factors influence plant LTR-RT dynamics in the wild. When combining a coverage-based approach to estimate global LTR-RT copy number variations with mobilome-sequencing of nine accessions exposed to eight different stresses, we find little evidence for a major role of environmental factors in LTR-RT accumulations in B. distachyon natural accessions. Instead, we show that loss of RNA polymerase IV (Pol IV), which mediates RNA-directed DNA methylation in plants, results in high transcriptional and transposition activities of RLC_BdisC024 (HOPPLA) LTR-RT family elements, and that these effects are not stress- specific. This work supports findings indicating an ongoing mobility in B. distachyon and reveals that host RNA-directed DNA methylation rather than environmental factors controls their mobility in this wild grass model.},
keywords = {},
pubstate = {published},
tppubtype = {proceedings}
}
G, Mohannath; A, McKinlay; R, Enganti; NV, Puppala; GP, Saradadevi; CS, Pikaard; T., Blevins
DNA hypermethylation and condensed chromatin correlate with chromosome-specific rRNA gene silencing in Arabidopsis Actes
2024.
@proceedings{nokey,
title = {DNA hypermethylation and condensed chromatin correlate with chromosome-specific rRNA gene silencing in Arabidopsis},
author = {Mohannath G and McKinlay A and Enganti R and Puppala NV and Saradadevi GP and Pikaard CS and Blevins T.},
doi = {10.1101/2023.02.03.526984},
year = {2024},
date = {2024-03-01},
journal = {bioRxiv},
abstract = {In eukaryotes, hundreds of ribosomal RNA (rRNA) genes are clustered at chromosomal loci called nucleolus organizer regions (NORs). Arabidopsis thaliana has two NORs, one on chromosome 2 (NOR2) and the other on chromosome 4 (NOR4). Each NOR consists of ∼ 400 rRNA gene copies. We recently showed that rRNA gene subtypes that map to NOR2 are silenced during development, whereas those that map to NOR4 are active. In several DNA methylation mutants of Arabidopsis, we show disruption of the NOR2 gene silencing to varying degrees. Significantly, the highest disruption of NOR2 gene silencing correlates with a maximum loss of cytosine methylation in the CHH context followed by the CG context, independent of RNA-directed DNA methylation (RdDM). Next, we show in Col-0 that NOR2 genes are relatively hypermethylated and NOR4 genes are hypomethylated using multiple methylation analysis of genomic DNA carried out with different types of methylation-sensitive restriction enzymes. We demonstrate similar differential methylation status between NOR2 and NOR4 genes in an introgression line named ColSf-NOR4, which carries NOR2 from Col-0 and NOR4 from ecotype Sf-2. Lastly, using Tn5 transposon-mediated transposition into native chromatin, we show that NOR2 gene chromatin is in more condensed state than NOR4 gene chromatin.},
keywords = {},
pubstate = {published},
tppubtype = {proceedings}
}
Kohl, Maximilian P; Chane-Woon-Ming, Béatrice; Bahena-Ceron, Roberto; Jaramillo-Ponce, Jose; Antoine, Laura; Herrgott, Lucas; Romby, Pascale; Marzi, Stefano
Ribosome Profiling Methods Adapted to the Study of RNA-Dependent Translation Regulation in Staphylococcus aureus Article de journal
Dans: Methods Mol Biol, vol. 2741, p. 73–100, 2024, ISSN: 1940-6029.
@article{pmid38217649,
title = {Ribosome Profiling Methods Adapted to the Study of RNA-Dependent Translation Regulation in Staphylococcus aureus},
author = {Maximilian P Kohl and Béatrice Chane-Woon-Ming and Roberto Bahena-Ceron and Jose Jaramillo-Ponce and Laura Antoine and Lucas Herrgott and Pascale Romby and Stefano Marzi},
doi = {10.1007/978-1-0716-3565-0_5},
issn = {1940-6029},
year = {2024},
date = {2024-01-01},
urldate = {2024-01-01},
journal = {Methods Mol Biol},
volume = {2741},
pages = {73--100},
abstract = {Noncoding RNAs, including regulatory RNAs (sRNAs), are instrumental in regulating gene expression in pathogenic bacteria, allowing them to adapt to various stresses encountered in their host environments. Staphylococcus aureus is a well-studied model for RNA-mediated regulation of virulence and pathogenicity, with sRNAs playing significant roles in shaping S. aureus interactions with human and animal hosts. By modulating the translation and/or stability of target mRNAs, sRNAs regulate the synthesis of virulence factors and regulatory proteins required for pathogenesis. Moreover, perturbation of the levels of RNA modifications in two other classes of noncoding RNAs, rRNAs, and tRNAs, has been proposed to contribute to stress adaptation. However, the study of how these various factors affect translation regulation has often been restricted to specific genes, using in vivo reporters and/or in vitro translation systems. Genome-wide sequencing approaches offer novel perspectives for studying RNA-dependent regulation. In particular, ribosome profiling methods provide a powerful resource for characterizing the overall landscape of translational regulation, contributing to a better understanding of S. aureus physiopathology. Here, we describe protocols that we have adapted to perform ribosome profiling in S. aureus.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Baldaccini, Morgane; Gaucherand, Léa; Chane-Woon-Ming, Béatrice; Messmer, Mélanie; Gucciardi, Floriane; Pfeffer, Sébastien
The helicase domain of human Dicer prevents RNAi-independent activation of antiviral and inflammatory pathways Article de journal
Dans: EMBO J, 2024, ISSN: 1460-2075.
@article{pmid38287188,
title = {The helicase domain of human Dicer prevents RNAi-independent activation of antiviral and inflammatory pathways},
author = {Morgane Baldaccini and Léa Gaucherand and Béatrice Chane-Woon-Ming and Mélanie Messmer and Floriane Gucciardi and Sébastien Pfeffer},
doi = {10.1038/s44318-024-00035-2},
issn = {1460-2075},
year = {2024},
date = {2024-01-01},
urldate = {2024-01-01},
journal = {EMBO J},
abstract = {In mammalian somatic cells, the relative contribution of RNAi and the type I interferon response during viral infection is unclear. The apparent inefficiency of antiviral RNAi might be due to self-limiting properties and mitigating co-factors of the key enzyme Dicer. In particular, the helicase domain of human Dicer appears to be an important restriction factor of its activity. Here, we study the involvement of several helicase-truncated mutants of human Dicer in the antiviral response. All deletion mutants display a PKR-dependent antiviral phenotype against certain viruses, and one of them, Dicer N1, acts in a completely RNAi-independent manner. Transcriptomic analyses show that many genes from the interferon and inflammatory response pathways are upregulated in Dicer N1 expressing cells. We show that some of these genes are controlled by NF-kB and that blocking this pathway abrogates the antiviral phenotype of Dicer N1. Our findings highlight the crosstalk between Dicer, PKR, and the NF-kB pathway, and suggest that human Dicer may have repurposed its helicase domain to prevent basal activation of antiviral and inflammatory pathways.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Nerantzaki, Maria; Husser, Claire; Ryckelynck, Michael; Lutz, Jean-François
Exchanging and Releasing Information in Synthetic Digital Polymers Using a Strand-Displacement Strategy Article de journal
Dans: J Am Chem Soc, 2024, ISSN: 1520-5126.
@article{pmid38286022,
title = {Exchanging and Releasing Information in Synthetic Digital Polymers Using a Strand-Displacement Strategy},
author = {Maria Nerantzaki and Claire Husser and Michael Ryckelynck and Jean-François Lutz},
doi = {10.1021/jacs.3c13953},
issn = {1520-5126},
year = {2024},
date = {2024-01-01},
urldate = {2024-01-01},
journal = {J Am Chem Soc},
abstract = {Toehold-mediated strand displacement (TMSD) was tested as a tool to edit information in synthetic digital polymers. Uniform DNA-polymer biohybrid macromolecules were first synthesized by automated phosphoramidite chemistry and characterized by HPLC, mass spectrometry, and polyacrylamide gel electrophoresis (PAGE). These precursors were diblock structures containing a synthetic poly(phosphodiester) (PPDE) segment covalently attached to a single-stranded DNA sequence. Three types of biohybrids were prepared herein: a substrate containing an accessible toehold as well as input and output macromolecules. The substrate and the input macromolecules contained noncoded PPDE homopolymers, whereas the output macromolecule contained a digitally encoded segment. After hybridization of the substrate with the output, incubation in the presence of the input led to efficient TMSD and the release of the digital segment. TMSD can therefore be used to erase or rewrite information in self-assembled biohybrid superstructures. Furthermore, it was found in this work that the conjugation of DNA single strands to synthetic segments of chosen lengths greatly facilitates the characterization and PAGE visualization of the TMSD process.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
2021
Lalaouna, D; Fochesato, S; Harir, M; Ortet, P; Schmitt-Kopplin, P; Heulin, T; Achouak, W
Amplifying and Fine-Tuning Rsm sRNAs Expression and Stability to Optimize the Survival of Pseudomonas brassicacerum in Nutrient-Poor Environments Article de journal
Dans: Microorganisms, vol. 9, no. 2, 2021, ISBN: 33530561, (2076-2607 (Print) 2076-2607 (Linking) Journal Article).
@article{nokey,
title = {Amplifying and Fine-Tuning Rsm sRNAs Expression and Stability to Optimize the Survival of Pseudomonas brassicacerum in Nutrient-Poor Environments},
author = {D Lalaouna and S Fochesato and M Harir and P Ortet and P Schmitt-Kopplin and T Heulin and W Achouak},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=33530561},
doi = {10.3390/microorganisms9020250},
isbn = {33530561},
year = {2021},
date = {2021-01-01},
journal = {Microorganisms},
volume = {9},
number = {2},
abstract = {In the beneficial plant root-associated Pseudomonas brassicacearum strain NFM421, the GacS/GacA two-component system positively controls biofilm formation and the production of secondary metabolites through the synthesis of rsmX, rsmY and rsmZ. Here, we evidenced the genetic amplification of Rsm sRNAs by the discovery of a novel 110-nt long sRNA encoding gene, rsmX-2, generated by the duplication of rsmX-1 (formerly rsmX). Like the others rsm genes, its overexpression overrides the gacA mutation. We explored the expression and the stability of rsmX-1, rsmX-2, rsmY and rsmZ encoding genes under rich or nutrient-poor conditions, and showed that their amount is fine-tuned at the transcriptional and more interestingly at the post-transcriptional level. Unlike rsmY and rsmZ, we noticed that the expression of rsmX-1 and rsmX-2 genes was exclusively GacA-dependent. The highest expression level and longest half-life for each sRNA were correlated with the highest ppGpp and cyclic-di-GMP levels and were recorded under nutrient-poor conditions. Together, these data support the view that the Rsm system in P. brassicacearum is likely linked to the stringent response, and seems to be required for bacterial adaptation to nutritional stress.},
note = {2076-2607 (Print)
2076-2607 (Linking)
Journal Article},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
2020
Riley, L G; Rudinger-Thirion, J; Frugier, M; Wilson, M; Luig, M; Alahakoon, T I; Nixon, C Y; Kirk, E P; Roscioli, T; Lunke, S; Stark, Z; Wierenga, K J; Palle, S; Walsh, M; Higgs, E; Arbuckle, S; Thirukeswaran, S; Compton, A G; Thorburn, D R; Christodoulou, J
The expanding LARS2 phenotypic spectrum: HLASA, Perrault syndrome with leukodystrophy, and mitochondrial myopathy Article de journal
Dans: Hum Mutat, vol. 41, no. 8, p. 1425-1434, 2020, ISBN: 32442335, (1098-1004 (Electronic) 1059-7794 (Linking) Journal Article Research Support, Non-U.S. Gov't).
@article{nokey,
title = {The expanding LARS2 phenotypic spectrum: HLASA, Perrault syndrome with leukodystrophy, and mitochondrial myopathy},
author = {L G Riley and J Rudinger-Thirion and M Frugier and M Wilson and M Luig and T I Alahakoon and C Y Nixon and E P Kirk and T Roscioli and S Lunke and Z Stark and K J Wierenga and S Palle and M Walsh and E Higgs and S Arbuckle and S Thirukeswaran and A G Compton and D R Thorburn and J Christodoulou},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=32442335},
doi = {10.1002/humu.24050},
isbn = {32442335},
year = {2020},
date = {2020-01-01},
journal = {Hum Mutat},
volume = {41},
number = {8},
pages = {1425-1434},
abstract = {LARS2 variants are associated with Perrault syndrome, characterized by premature ovarian failure and hearing loss, and with an infantile lethal multisystem disorder: Hydrops, lactic acidosis, sideroblastic anemia (HLASA) in one individual. Recently we reported LARS2 deafness with (ovario) leukodystrophy. Here we describe five patients with a range of phenotypes, in whom we identified biallelic LARS2 variants: three patients with a HLASA-like phenotype, an individual with Perrault syndrome whose affected siblings also had leukodystrophy, and an individual with a reversible mitochondrial myopathy, lactic acidosis, and developmental delay. Three HLASA cases from two unrelated families were identified. All were males with genital anomalies. Two survived multisystem disease in the neonatal period; both have developmental delay and hearing loss. A 55-year old male with deafness has not displayed neurological symptoms while his female siblings with Perrault syndrome developed leukodystrophy and died in their 30s. Analysis of muscle from a child with a reversible myopathy showed reduced LARS2 and mitochondrial complex I levels, and an unusual form of degeneration. Analysis of recombinant LARS2 variant proteins showed they had reduced aminoacylation efficiency, with HLASA-associated variants having the most severe effect. A broad phenotypic spectrum should be considered in association with LARS2 variants.},
note = {1098-1004 (Electronic)
1059-7794 (Linking)
Journal Article
Research Support, Non-U.S. Gov't},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
2019
Knaap, M S; Bugiani, M; Mendes, M I; Riley, L G; Smith, D E C; Rudinger-Thirion, J; Frugier, M; Breur, M; Crawford, J; Gaalen, J; Schouten, M; Willems, M; Waisfisz, Q; Mau-Them, F T; Rodenburg, R J; Taft, R J; Keren, B; Christodoulou, J; Depienne, C; Simons, C; Salomons, G S; Mochel, F
Biallelic variants in LARS2 and KARS cause deafness and (ovario)leukodystrophy Article de journal
Dans: Neurology, vol. 92, no. 11, p. e1225-e1237, 2019, ISBN: 30737337, (1526-632X (Electronic) 0028-3878 (Linking) Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't).
@article{nokey,
title = {Biallelic variants in LARS2 and KARS cause deafness and (ovario)leukodystrophy},
author = {M S Knaap and M Bugiani and M I Mendes and L G Riley and D E C Smith and J Rudinger-Thirion and M Frugier and M Breur and J Crawford and J Gaalen and M Schouten and M Willems and Q Waisfisz and F T Mau-Them and R J Rodenburg and R J Taft and B Keren and J Christodoulou and C Depienne and C Simons and G S Salomons and F Mochel},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=30737337},
doi = {10.1212/WNL.0000000000007098},
isbn = {30737337},
year = {2019},
date = {2019-01-01},
journal = {Neurology},
volume = {92},
number = {11},
pages = {e1225-e1237},
abstract = {OBJECTIVE: To describe the leukodystrophy caused by pathogenic variants in LARS2 and KARS, encoding mitochondrial leucyl transfer RNA (tRNA) synthase and mitochondrial and cytoplasmic lysyl tRNA synthase, respectively. METHODS: We composed a group of 5 patients with leukodystrophy, in whom whole-genome or whole-exome sequencing revealed pathogenic variants in LARS2 or KARS. Clinical information, brain MRIs, and postmortem brain autopsy data were collected. We assessed aminoacylation activities of purified mutant recombinant mitochondrial leucyl tRNA synthase and performed aminoacylation assays on patients' lymphoblasts and fibroblasts. RESULTS: Patients had a combination of early-onset deafness and later-onset neurologic deterioration caused by progressive brain white matter abnormalities on MRI. Female patients with LARS2 pathogenic variants had premature ovarian failure. In 2 patients, MRI showed additional signs of early-onset vascular abnormalities. In 2 other patients with LARS2 and KARS pathogenic variants, magnetic resonance spectroscopy revealed elevated white matter lactate, suggesting mitochondrial disease. Pathology in one patient with LARS2 pathogenic variants displayed evidence of primary disease of oligodendrocytes and astrocytes with lack of myelin and deficient astrogliosis. Aminoacylation activities of purified recombinant mutant leucyl tRNA synthase showed a 3-fold loss of catalytic efficiency. Aminoacylation assays on patients' lymphoblasts and fibroblasts showed about 50% reduction of enzyme activity. CONCLUSION: This study adds LARS2 and KARS pathogenic variants as gene defects that may underlie deafness, ovarian failure, and leukodystrophy with mitochondrial signature. We discuss the specific MRI characteristics shared by leukodystrophies caused by mitochondrial tRNA synthase defects. We propose to add aminoacylation assays as biochemical diagnostic tools for leukodystrophies.},
note = {1526-632X (Electronic)
0028-3878 (Linking)
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
2018
Monsion, B; Incarbone, M; Hleibieh, K; Poignavent, V; Ghannam, A; Dunoyer, P; Daeffler, L; Tilsner, J; Ritzenthaler, C
Efficient Detection of Long dsRNA in Vitro and in Vivo Using the dsRNA Binding Domain from FHV B2 Protein Article de journal
Dans: Front Plant Sci, vol. 9, p. 70, 2018, ISBN: 29449856, (1664-462X (Print) 1664-462X (Linking) Journal Article).
@article{nokey,
title = {Efficient Detection of Long dsRNA in Vitro and in Vivo Using the dsRNA Binding Domain from FHV B2 Protein},
author = {B Monsion and M Incarbone and K Hleibieh and V Poignavent and A Ghannam and P Dunoyer and L Daeffler and J Tilsner and C Ritzenthaler},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=29449856},
doi = {10.3389/fpls.2018.00070},
isbn = {29449856},
year = {2018},
date = {2018-01-01},
journal = {Front Plant Sci},
volume = {9},
pages = {70},
abstract = {Double-stranded RNA (dsRNA) plays essential functions in many biological processes, including the activation of innate immune responses and RNA interference. dsRNA also represents the genetic entity of some viruses and is a hallmark of infections by positive-sense single-stranded RNA viruses. Methods for detecting dsRNA rely essentially on immunological approaches and their use is often limited to in vitro applications, although recent developments have allowed the visualization of dsRNA in vivo. Here, we report the sensitive and rapid detection of long dsRNA both in vitro and in vivo using the dsRNA binding domain of the B2 protein from Flock house virus. In vitro, we adapted the system for the detection of dsRNA either enzymatically by northwestern blotting or by direct fluorescence labeling on fixed samples. In vivo, we produced stable transgenic Nicotiana benthamiana lines allowing the visualization of dsRNA by fluorescence microscopy. Using these techniques, we were able to discriminate healthy and positive-sense single-stranded RNA virus-infected material in plants and insect cells. In N. benthamiana, our system proved to be very potent for the spatio-temporal visualization of replicative RNA intermediates of a broad range of positive-sense RNA viruses, including high- vs. low-copy number viruses.},
note = {1664-462X (Print)
1664-462X (Linking)
Journal Article},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Bastet, A; Lederer, B; Giovinazzo, N; Arnoux, X; German-Retana, S; Reinbold, C; Brault, V; Garcia, D; Djennane, S; Gersch, S; Lemaire, O; Robaglia, C; Gallois, J L
Trans-species synthetic gene design allows resistance pyramiding and broad-spectrum engineering of virus resistance in plants Article de journal
Dans: Plant Biotechnol J, 2018, ISBN: 29504210, (1467-7652 (Electronic) 1467-7644 (Linking) Journal Article).
@article{nokey,
title = {Trans-species synthetic gene design allows resistance pyramiding and broad-spectrum engineering of virus resistance in plants},
author = {A Bastet and B Lederer and N Giovinazzo and X Arnoux and S German-Retana and C Reinbold and V Brault and D Garcia and S Djennane and S Gersch and O Lemaire and C Robaglia and J L Gallois},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=29504210},
doi = {10.1111/pbi.12896},
isbn = {29504210},
year = {2018},
date = {2018-01-01},
journal = {Plant Biotechnol J},
abstract = {To infect plants, viruses rely heavily on their host's machinery. Plant genetic resistances based on host factor modifications can be found among existing natural variability and are widely used for some but not all crops. While biotechnology can supply for the lack of natural resistance alleles, new strategies need to be developed to increase resistance spectra and durability without impairing plant development. Here, we assess how the targeted allele modification of the Arabidopsis thaliana translation initiation factor eIF4E1 can lead to broad and efficient resistance to the major group of potyviruses. A synthetic Arabidopsis thaliana eIF4E1 allele was designed by introducing multiple amino acid changes associated with resistance to potyvirus in naturally occurring Pisum sativum alleles. This new allele encodes a functional protein while maintaining plant resistance to a potyvirus isolate that usually hijacks eIF4E1. Due to its biological functionality, this synthetic allele allows, at no developmental cost, the pyramiding of resistances to potyviruses that selectively use the two major translation initiation factors, eIF4E1 or its isoform eIFiso4E. Moreover, this combination extends the resistance spectrum to potyvirus isolates for which no efficient resistance has so far been found, including resistance-breaking isolates and an unrelated virus belonging to the Luteoviridae family. This study is a proof-of-concept for the efficiency of gene engineering combined with knowledge of natural variation to generate trans-species virus resistance at no developmental cost to the plant. This has implications for breeding of crops with broad-spectrum and high durability resistance using recent genome editing techniques.},
note = {1467-7652 (Electronic)
1467-7644 (Linking)
Journal Article},
keywords = {},
pubstate = {published},
tppubtype = {article}
}