EcoTILLING for the Identification of Allelic Variants of Melon EIF4E, a Factor That Controls Virus Susceptibility

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2007 Jun 23

PMID 17584936

Citations 47

Authors

Cristina Nieto

Florence Piron

Marion Dalmais

Cristina F Marco

Enrique Moriones

Ma Luisa Gomez-Guillamon

Veronica Truniger

Pedro Gomez

Jordi Garcia-Mas

Miguel A Aranda

Abdelhafid Bendahmane

Affiliations

Soon will be listed here.

Abstract

Background: Translation initiation factors of the 4E and 4G protein families mediate resistance to several RNA plant viruses in the natural diversity of crops. Particularly, a single point mutation in melon eukaryotic translation initiation factor 4E (eIF4E) controls resistance to Melon necrotic spot virus (MNSV) in melon. Identification of allelic variants within natural populations by EcoTILLING has become a rapid genotype discovery method.

Results: A collection of Cucumis spp. was characterised for susceptibility to MNSV and Cucumber vein yellowing virus (CVYV) and used for the implementation of EcoTILLING to identify new allelic variants of eIF4E. A high conservation of eIF4E exonic regions was found, with six polymorphic sites identified out of EcoTILLING 113 accessions. Sequencing of regions surrounding polymorphisms revealed that all of them corresponded to silent nucleotide changes and just one to a non-silent change correlating with MNSV resistance. Except for the MNSV case, no correlation was found between variation of eIF4E and virus resistance, suggesting the implication of different and/or additional genes in previously identified resistance phenotypes. We have also characterized a new allele of eIF4E from Cucumis zeyheri, a wild relative of melon. Functional analyses suggested that this new eIF4E allele might be responsible for resistance to MNSV.

Conclusion: This study shows the applicability of EcoTILLING in Cucumis spp., but given the conservation of eIF4E, new candidate genes should probably be considered to identify new sources of resistance to plant viruses. Part of the methodology described here could alternatively be used in TILLING experiments that serve to generate new eIF4E alleles.

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References

Carrington J, Whitham S . Viral invasion and host defense: strategies and counter-strategies. Curr Opin Plant Biol. 1999; 1(4):336-41. DOI: 10.1016/1369-5266(88)80056-6. View

Diaz J, Nieto C, Moriones E, Truniger V, Aranda M . Molecular characterization of a Melon necrotic spot virus strain that overcomes the resistance in melon and nonhost plants. Mol Plant Microbe Interact. 2004; 17(6):668-75. DOI: 10.1094/MPMI.2004.17.6.668. View

Gao Z, Johansen E, Eyers S, Thomas C, Ellis T, J Maule A . The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J. 2004; 40(3):376-85. DOI: 10.1111/j.1365-313X.2004.02215.x. View

Sato M, Nakahara K, Yoshii M, Ishikawa M, Uyeda I . Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett. 2005; 579(5):1167-71. DOI: 10.1016/j.febslet.2004.12.086. View

Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B . An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J. 2006; 48(3):452-62. DOI: 10.1111/j.1365-313X.2006.02885.x. View

Gilchrist E, Haughn G . TILLING without a plough: a new method with applications for reverse genetics. Curr Opin Plant Biol. 2005; 8(2):211-5. DOI: 10.1016/j.pbi.2005.01.004. View

Diaz-Pendon J, Fernandez-Munoz R, Gomez-Guillamon M, Moriones E . Inheritance of Resistance to Watermelon mosaic virus in Cucumis melo that Impairs Virus Accumulation, Symptom Expression, and Aphid Transmission. Phytopathology. 2008; 95(7):840-6. DOI: 10.1094/PHYTO-95-0840. View

Diaz-Pendon J, Truniger V, Nieto C, Garcia-Mas J, Bendahmane A, Aranda M . Advances in understanding recessive resistance to plant viruses. Mol Plant Pathol. 2010; 5(3):223-33. DOI: 10.1111/j.1364-3703.2004.00223.x. View

Ruffel S, Gallois J, Lesage M, Caranta C . The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics. 2005; 274(4):346-53. DOI: 10.1007/s00438-005-0003-x. View

10.

Comai L, Young K, Till B, Reynolds S, Greene E, Codomo C . Efficient discovery of DNA polymorphisms in natural populations by Ecotilling. Plant J. 2004; 37(5):778-86. DOI: 10.1111/j.0960-7412.2003.01999.x. View

11.

Ruffel S, Gallois J, Moury B, Robaglia C, Palloix A, Caranta C . Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. J Gen Virol. 2006; 87(Pt 7):2089-2098. DOI: 10.1099/vir.0.81817-0. View

12.

Nicaise V, German-Retana S, Sanjuan R, Dubrana M, Mazier M, Maisonneuve B . The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiol. 2003; 132(3):1272-82. PMC: 167067. DOI: 10.1104/pp.102.017855. View

13.

Tomoo K, Shen X, Okabe K, Nozoe Y, Fukuhara S, Morino S . Crystal structures of 7-methylguanosine 5'-triphosphate (m(7)GTP)- and P(1)-7-methylguanosine-P(3)-adenosine-5',5'-triphosphate (m(7)GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible.... Biochem J. 2002; 362(Pt 3):539-44. PMC: 1222416. DOI: 10.1042/0264-6021:3620539. View

14.

Pettit Kneller E, Rakotondrafara A, Miller W . Cap-independent translation of plant viral RNAs. Virus Res. 2005; 119(1):63-75. PMC: 1880899. DOI: 10.1016/j.virusres.2005.10.010. View

15.

Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S . The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J. 2005; 42(6):912-22. DOI: 10.1111/j.1365-313X.2005.02424.x. View

16.

Kushner D, Lindenbach B, Grdzelishvili V, Noueiry A, Paul S, Ahlquist P . Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci U S A. 2003; 100(26):15764-9. PMC: 307642. DOI: 10.1073/pnas.2536857100. View

17.

Robaglia C, Caranta C . Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci. 2005; 11(1):40-5. DOI: 10.1016/j.tplants.2005.11.004. View

18.

Kawaguchi R, Bailey-Serres J . Regulation of translational initiation in plants. Curr Opin Plant Biol. 2002; 5(5):460-5. DOI: 10.1016/s1369-5266(02)00290-x. View

19.

Kanyuka K, Druka A, Caldwell D, Tymon A, McCallum N, Waugh R . Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Mol Plant Pathol. 2010; 6(4):449-58. DOI: 10.1111/j.1364-3703.2005.00294.x. View

20.

Gilchrist E, Haughn G, Ying C, Otto S, Zhuang J, Cheung D . Use of Ecotilling as an efficient SNP discovery tool to survey genetic variation in wild populations of Populus trichocarpa. Mol Ecol. 2006; 15(5):1367-78. DOI: 10.1111/j.1365-294X.2006.02885.x. View