A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of Potato virus Y Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in Capsicum annuum
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant and Viral Material
2.2. Virus Resistance Tests
2.3. Partial Sequencing of the PVY Genome
3. Results and Discussion
3.1. PM949 Exhibits Narrow Spectrum Resistance to Potyviruses of the PVY Clade
3.2. Genetic Inheritance of PM949 Resistance to PVY
3.3. Inoculations by Grafting Allowed Selection of PVY Variants Adapted to Pvr4 or PM949 Resistance
3.4. Substitution K472E in PVY NIb (RdRp) Determines Adaptation to PM949 Resistance
3.5. Additional Amino Acid Substitutions in PVY NIb Are Associated with Adaptation to PM949 Resistance
3.6. Insights into the Durability Potential of Pvr4 and PM949 Resistance
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Johnson, R. Durable resistance–Definition of, genetic control, and attainment in plant breeding. Phytopathology 1981, 71, 567–568. [Google Scholar] [CrossRef]
- Ayme, V.; Souche, S.; Caranta, C.; Jacquemond, M.; Chadoeuf, J.; Palloix, A.; Moury, B. Different mutations in the genome-linked protein VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Mol. Plant-Microbe Interact. 2006, 19, 557–563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moury, B.; Charron, C.; Janzac, B.; Simon, V.; Gallois, J.-L.; Palloix, A.; Caranta, C. Evolution of plant eukaryotic initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg): A game of mirrors impacting resistance spectrum and durability. Inf. Genet. Evol. 2014, 27, 472–480. [Google Scholar] [CrossRef] [PubMed]
- Avilla, C.; Collar, J.L.; Duque, M.; Fereres, A. Yield of bell pepper (Capsicum annuum) inoculated with CMV and/or PVY at different time intervals. J. Plant Dis. Prot. 1997, 104, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Gibbs, A.; Ohshima, K. Potyviruses and the digital revolution. Ann. Rev. Phytopath. 2010, 48, 205–223. [Google Scholar] [CrossRef]
- Moury, B.; Verdin, E. Viruses of pepper crops in the Mediterranean basin: A remarkable stasis. Adv. Virus Res. 2012, 84, 127–162. [Google Scholar] [CrossRef]
- Quenouille, J.; Vassilakos, N.; Moury, B. Potato virus Y: A major crop pathogen that has provided major insights into the evolution of viral pathogenicity. Mol. Plant Pathol. 2013, 14, 439–452. [Google Scholar] [CrossRef]
- Kyle, M.M.; Palloix, A. Proposed revision of nomenclature for potyvirus resistance genes in Capsicum. Euphytica 1997, 97, 183–188. [Google Scholar] [CrossRef]
- Caranta, C.; Lefebvre, V.; Palloix, A. Polygenic resistance of pepper to potyviruses consists of a combination of isolate-specific and broad-spectrum quantitative trait loci. Mol. Plant-Microbe Interact. 1997, 10, 872–878. [Google Scholar] [CrossRef] [Green Version]
- Grube, R.C.; Blauth, J.R.; Arnedo, M.S.; Caranta, C.; Jahn, M.K. Identification and comparative mapping of a dominant potyvirus resistance gene cluster in Capsicum. Theor. Appl. Genet. 2000, 101, 852–859. [Google Scholar] [CrossRef]
- Janzac, B.; Montarry, J.; Palloix, A.; Navaud, O.; Moury, B. A point mutation in the polymerase of Potato virus Y confers virulence toward the Pvr4 resistance of pepper and a high competitiveness cost in susceptible cultivar. Mol. Plant-Microbe Interact. 2010, 23, 823–830. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moury, B.; Janzac, B.; Ruellan, Y.; Simon, V.; Ben Khalifa, M.; Fakhfakh, H.; Fabre, F.; Palloix, A. Interaction pattern between Potato virus Y and eIF4E-mediated recessive resistance in the Solanaceae. J. Virol. 2014, 88, 9799–9807. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sage-Palloix, A.M.; Jourdan, F.; Phaly, T.; Nemouchi, G.; Lefebvre, V.; Palloix, A. Analysis of diversity in pepper genetic resources: Distribution of horticultural and resistance traits in the INRA pepper germplasm. In Progress in Research on Capsicum & Eggplant; Niemirowicz-Szczytt, K., Ed.; Warsaw University of Life Sciences Press: Warsaw, Poland, 2007; pp. 33–42. [Google Scholar]
- Janzac, B.; Fabre, M.-F.; Palloix, A.; Moury, B. Phenotype and spectrum of action of the Pvr4 resistance in pepper against potyviruses, and selection for virulent variants. Plant Pathol. 2009, 58, 443–449. [Google Scholar] [CrossRef]
- Salinier, J.; Lefebvre, V.; Besombes, D.; Burck, H.; Causse, M.; Daunay, M.C.; Dogimont, C.; Goussopoulos, J.; Gros, C.; Maisonneuve, B.; et al. The INRAE Centre for Vegetable Germplasm: Geographically and Phenotypically Diverse Collections and Their Use in Genetics and Plant Breeding. Plants 2022, 11, 347. [Google Scholar] [CrossRef]
- Moury, B.; Morel, C.; Johansen, E.; Guilbaud, L.; Souche, S.; Ayme, V.; Caranta, C.; Palloix, A.; Jacquemond, M. Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol. Plant-Microbe Interact. 2004, 17, 322–329. [Google Scholar] [CrossRef] [Green Version]
- Moury, B. A new lineage sheds light on the evolutionary history of Potato virus Y. Mol. Plant Pathol. 2010, 11, 161–168. [Google Scholar] [CrossRef]
- Dogimont, C.; Palloix, A.; Daubèze, A.M.; Marchoux, G.; Gebre Selassie, K.; Pochard, E. Genetic analysis of broad spectrum resistance to potyviruses using doubled haploid lines of pepper (Capsicum annuum L.). Euphytica 1996, 88, 231–239. [Google Scholar] [CrossRef]
- Charron, C.; Nicolai, M.; Gallois, J.L.; Robaglia, C.; Moury, B.; Palloix, A.; Caranta, C. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J. 2008, 54, 56–68. [Google Scholar] [CrossRef]
- Ben Khalifa, M.; Simon, V.; Marrakchi, M.; Fakhfakh, H.; Moury, B. Contribution of host plant resistance and geographic distance to the structure of Potato virus Y (PVY) populations in pepper in northern Tunisia. Plant Pathol. 2009, 58, 763–772. [Google Scholar] [CrossRef]
- Sacristán, S.; Garcia-Arenal, F. The evolution of virulence and pathogenicity in plant pathogen populations. Mol. Plant Pathol. 2008, 9, 369–384. [Google Scholar] [CrossRef]
- Lee, J.M.; Jahn, M.M.; Yeam, I. Allelic relationships at the pvr1 locus in Capsicum annuum. Euphytica 2013, 194, 417–424. [Google Scholar] [CrossRef]
- Gauffier, C.; Lebaron, C.; Moretti, A.; Constant, C.; Moquet, F.; Bonnet, G.; Caranta, C.; Gallois, J.L. A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy. Plant J. 2016, 85, 717–729. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Der Biezen, E.; Jones, J.D.G. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 1998, 23, 454–456. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Ullah, Z.; Grumet, R. Interaction between zucchini yellow mosaic potyvirus RNA-dependent RNA polymerase and host poly-(A) binding protein. Virology 2000, 275, 433–443. [Google Scholar] [CrossRef] [Green Version]
- Dufresne, P.J.; Thivierge, K.; Cotton, S.; Beauchemin, C.; Ide, C.; Ubalijoro, E.; Laliberté, J.F.; Fortin, M.G. Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles. Virology 2008, 374, 217–227. [Google Scholar] [CrossRef] [Green Version]
- Kelley, L.A.; Mezulis, S.; Yates, C.M.; Wass, M.N.; Sternberg, M.J.E. The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols 2015, 10, 845–858. [Google Scholar] [CrossRef] [Green Version]
- Ng, K.K.; Cherney, M.M.; Vazquez, A.L.; Machin, A.; Alonso, J.M.; Parra, F.; James, M.N. Crystal structures of active and inactive conformations of a caliciviral RNA-dependent RNA polymerase. J. Biol. Chem. 2002, 277, 1381–1387. [Google Scholar] [CrossRef] [Green Version]
- Steitz, T.A. DNA polymerases: Structural diversity and common mechanisms. J. Biol. Chem. 1999, 274, 17395–17398. [Google Scholar] [CrossRef] [Green Version]
Virus Species and/or Isolate a | Accession Number | Phylogenetic Cluster | Infectivity and Symptoms in PM949 b | Infectivity and Symptoms in W4 b,c |
---|---|---|---|---|
PVY-SON41p | AJ439544 | PVY | Ø/Ø d | Ø/Ø |
PVY-LYE72 | EU334782 | PVY | Ø/Ø | NEC/Ø |
PVY-Chile1 | FJ951646, FJ951645 | PVY | NEC/Ø | NEC/Ø |
PepSMV | X66027 | PVY | NEC/Ø | NEC/Ø |
PepYMV | AB541985 | PVY | MO/MO | NEC/Ø |
PTV-Quito | - | PVY | NEC/NEC | NEC/Ø |
PTV-Cuzqueño2 | EU495235 | PVY | NEC/NEC | NEC/Ø |
PepMoV-Texas | - | PVY | MO/MO | NEC/Ø |
EcRV | EU495234 | PVY | NEC/Ø | NEC/Ø |
PVMV-Ivory Coast | DQ009807, MG334358 | PVMV | MO/MO | MO/MO |
ChiVMV-Taiwan | - | PVMV | MO/MO | MO/MO |
TEV-HAT | M11458 | TEV | MO/MO | MO/MO |
Pepper Genotype | Test Conditions a | Resistance Test (Infected/ Inoculated) b | Nonsynonymous Substitutions in the NIb Cistron |
---|---|---|---|
YW | Mechanical, 1 mpi | 20/20 | no |
W4 | Mechanical, 1 mpi | 0/1500 c | - |
PM949 | Mechanical, 1 mpi | 0/20 | - |
W4 | Grafting, 5 mpi | 6/25 | SON41p-G1: D88N + L234H + K472E d SON41p-G2: E390G + K472E d SON41p-G3 and SON41p-G4: K472E d SON41p-G5: I94T + V416A + A504V SON41p-G6: M365I + G471E + S478N |
PM949 | Grafting, 5 mpi | 10/10 | E47K (2 plants) I94T (1 plant) K108E (1 plant) R488G (1 plant) M502I (3 plants) E508G (1 plant) E508K (1 plant) |
PVY cDNA Clone or Isolate | Location and Impact of Mutation on NIb | Plant Genotype | Resistance Test (Infected/Inoculated) a | Mutations in the NIb of PVY Progeny b |
---|---|---|---|---|
SON41p-G1 to -SON41p-G4 c | W4 | 20/20 each isolate | no | |
PM949 | 20/20 each isolate | no | ||
SON41p-G5 d | W4 | 20/20 | no | |
PM949 | 0/20 | |||
SON41p-G6 d | W4 | 20/20 | no | |
PM949 | 0/20 | |||
SON41p-K472E (cDNA clone) | Thumb domain; change of surface charge | W4 | 50/50 | no |
PM949 | 40/40 | no | ||
SON41p-E47K (2 isolates) | Bridge between thumb and finger domains; change of surface charge | W4 | 0/20 and 1/20 for the two isolates | Y271C e |
PM949 | 20/20 each isolate | no | ||
SON41p-I94T | Finger domain; change of local structure and more polar | W4 | 0/20 | |
PM949 | 20/20 | no | ||
SON41p-K108E | Finger domain; change of surface charge and local structure | W4 | 0/20 | |
PM949 | 20/20 | no | ||
SON41p-R488G | Thumb domain; change of surface charge and local structure | W4 | 1/20 | not determined |
PM949 | 20/20 | no | ||
SON41p-M502I (3 isolates) | Structure not modelled | W4 | 0/20 each isolate | |
PM949 | 20/20 each isolate | no | ||
SON41p-E508G | Change of charge; structure not modelled | W4 | 0/20 | |
PM949 | 20/20 | no | ||
SON41p-E508K | Change of charge; structure not modelled | W4 | 0/20 | |
PM949 | 20/20 | no |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Moury, B.; Michon, T.; Simon, V.; Palloix, A. A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of Potato virus Y Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in Capsicum annuum. Viruses 2023, 15, 1081. https://doi.org/10.3390/v15051081
Moury B, Michon T, Simon V, Palloix A. A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of Potato virus Y Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in Capsicum annuum. Viruses. 2023; 15(5):1081. https://doi.org/10.3390/v15051081
Chicago/Turabian StyleMoury, Benoît, Thierry Michon, Vincent Simon, and Alain Palloix. 2023. "A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of Potato virus Y Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in Capsicum annuum" Viruses 15, no. 5: 1081. https://doi.org/10.3390/v15051081