Abstract
Rice yellow mottle virus (RYMV) is the most damaging rice-infecting virus in Africa. However, few sources of high resistance and only a single major resistance gene, RYMV1, are known to date. We screened a large representative collection of African cultivated rice (Oryza glaberrima) for RYMV resistance. Whereas high resistance is known to be very rare in Asian cultivated rice (Oryza sativa), we identified 29 (8%) highly resistant accessions in O. glaberrima. The MIF4G domain of RYMV1 was sequenced in these accessions. Some accessions possessed the rymv1-3 or rymv1-4 recessive resistance alleles previously described in O. glaberrima Tog5681 and Tog5672, respectively, and a new allele, rymv1-5, was identified, thereby increasing the number of resistance alleles in O. glaberrima to three. In contrast, only a single allele has been reported in O. sativa. Markers specific to the different alleles of the RYMV1 gene were developed for marker-assisted selection of resistant genotypes for disease management. In addition, the presence of the dominant susceptibility allele (Rymv1-1) in 15 resistant accessions suggests that their resistance is under different genetic control. An allelism test involving one of those accessions revealed a second major resistance gene, i.e., RYMV2. The diversity of resistance genes against RYMV in O. glaberrima species is discussed in relation to the diversification of the virus in Africa.
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References
Albar L, Lorieux M, Ahmadi N, Rimbault I, Pinel A, Sy A, Fargette D, Ghesquière A (1998) Genetic basis and mapping of the resistance to Rice yellow mottle virus. I. QTLs identification and relationship between resistance and plant morphology. Theor Appl Genet 97:1145–1154
Albar L, Ndjiondjop M-N, Esshak Z, Berger A, Pinel A, Jones M, Fargette D, Ghesquière A (2003) Fine genetic mapping of a gene required for Rice yellow mottle virus cell-to-cell movement. Theor Appl Genet 107:371–378
Albar L, Bangratz-Reyser M, Hébrard E, Ndjiondjop MN, Jones M, Ghesquière A (2006) Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J 47:417–426
Bakker W (1974) Characterisation and ecological aspects of Rice yellow mottle virus in Kenya. PhD thesis, Wageningen University, p 151
Boisnard A, Albar L, Thiémélé D, Rondeau M, Ghesquière A (2007) Evaluation of genes from eIF4E and eIF4G multigenic families as potential candidates for partial resistance QTLs to Rice yellow mottle virus in rice. Theor Appl Genet 116:53–62
Braasch DA, Corey DR (2001) Locked nucleic acid (LNA): fine-tuning the recognition of DNA and RNA. Chem Biol 8:1–7
Cavatorta JR, Savage AE, Yeam I, Gray SM, Jahn MM (2008) Positive Darwinian selection at single amino acid sites conferring plant virus resistance. J Mol Evol 67:551–559
Charron C, Nicolai M, Gallois JL, Robaglia C, Moury BT, Palloix A, Caranta C (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54:56–68
Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349
Fargette D, Pinel-Galzi A, Sérémé D, Lacombe S, Hébrard E, Traoré O, Konaté G (2008) Diversification of Rice yellow mottle virus and related viruses spans the history of agriculture from the Neolithic to the present. PLoS Pathog 4:e1000125. doi:10.1371/journal.ppat.1000125
Fauquet C, Thouvenel JC (1977) Isolation of the Rice yellow mottle virus in Ivory Coast. Plant Dis Rep 61:443–446
Hébrard E, Pinel-Galzi A, Bersoult A, Siré C, Fargette D (2006) Emergence of a resistance-breaking isolate of Rice yellow mottle virus during serial inoculations is due to a single substitution in the genome-linked viral protein VPg. J Gen Virol 87:1369–1373
Hébrard E, Pinel-Galzi A, Fargette D (2008) Virulence domain of the RYMV genome-linked viral protein VPg towards rice rymv1-2-mediated resistance. Arch Virol 153:1161–1164
Kouassi NK, N’Guessan P, Albar L, Fauquet CM, Brugidou C (2005) Distribution and characterization of Rice yellow mottle virus: a threat to African farmers. Plant Dis 89:124–133
McCouch SR, Committee on Gene Symbolization, Nomenclature, Linkage, Rice Genetics Cooperative (2008) Gene nomenclature system for rice. Rice 1:72–84
N’Guessan P, Pinel A, Caruana ML, Frutos R, Sy A, Ghesquière A, Fargette D (2000) Evidence of the presence of two serotypes of Rice yellow mottle sobemovirus in Côte D’Ivoire. Eur J Plant Pathol 106:489–491
Ndjiondjop MN, Albar L, Fargette D, Fauquet C, Ghesquière A (1999) The genetic basis of high resistance to Rice yellow mottle virus (RYMV) in cultivars of two cultivated rice species. Plant Dis 83:931–935
Pinel-Galzi A, Rakotomalala M, Sangu E, Sorho F, Kanyeka Z, Traoré O, Sérémé D, Poulicard N, Rabenantoandro Y, Séré Y, Konaté G, Ghesquière A, Hébrard E, Fargette D (2007) Theme and variations in the evolutionary pathways to virulence of an RNA plant virus species. PloS Pathog 3:1761–1770
Portères R (1950) Vieille agriculture de l’Afrique intertropicale. Agron Afr 9:489–507
Rakotomalala M, Pinel-Galzi A, Albar L, Ghesquière A, Rabenantoandro Y, Ramavovololona P, Fargette D (2008) Resistance to Rice yellow mottle virus in rice germplasm in Madagascar. Eur J Plant Pathol 122:277–286
Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45
Sarla N, Swamy BPM (2005) Oryza glaberrima: a source for the improvement of Oryza sativa. Curr Sci 89:955–963
Second G (1982) Origin of the genic diversity of cultivated rice (Oryza spp). Study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57:25–57
Semon M, Nielsen R, Jones M, McCouch S (2005) The population structure of African cultivated rice Oryza Glaberrima Steud.: evidence for elevated levels of LD caused by admixture with O. sativa and ecological adaptation. Genetics 169:1639–1647
Sérémé D, Lacombe S, Konate M, Pinel-Galzi A, Traoré VSE, Hébrard E, Traoré O, Brugidou C, Fargette D, Konaté G (2008) Biological and molecular characterization of a putative new sobemovirus infecting Imperata cylindrica and maize in Africa. Arch Virol 153:1813–1820
Thottappilly G, Rossel HW (1993) Evaluation of resistance to Rice yellow mottle virus in Oryza species. Indian J Virol 9:65–73
Thottappilly G, Vanlent JWM, Rossel HW, Sehgal OP (1992) Rottboellia Yellow Mottle Virus, a New Sobemovirus affecting Rottboellia cochinchinensis (Itch Grass) in Nigeria. An Appl Biol 120:405–415
Traoré O, Sorho F, Pinel-Galzi A, Abubakar Z, Banwo O, Maley J, Hébrard E, Winter S, Séré Y, Konaté G, Fargette D (2005) Processes of diversification and dispersion of Rice yellow mottle virus inferred from large-scale and high-resolution phylogeographical studies. Mol Ecol 14:2097–2110
Traoré O, Pinel-Galzi A, Hébrard E, Gumedzoe MYD, Fargette D, Traoré AS, Konaté G (2006) Occurrence of resistance-breaking isolates of Rice yellow mottle virus in West and Central Africa. Plant Dis 90:259–263
Acknowledgments
This work was supported by a PhD grant to D. Thiémélé through the French-speaking University Network (AUF), and by Generation Challenge Program (GCP) (Project No. G3007.01: iBridges). A GCP Fellowships & Travel Grant (Project No. G4007.14) supported D. Thiémélé’s stay at the Africa Rice Center (WARDA) for RYMV resistance evaluation. We thank WARDA and the International Rice Research Institute (IRRI) for providing most of the O. glaberrima accessions. We gratefully acknowledge Agnès Pinel-Galzi for help in VPg sequencing, and Denis Fargette and Thomas Roscoe for critical reviews of the manuscript.
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Communicated by T. Sasaki.
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Thiémélé, D., Boisnard, A., Ndjiondjop, MN. et al. Identification of a second major resistance gene to Rice yellow mottle virus, RYMV2, in the African cultivated rice species, O. glaberrima . Theor Appl Genet 121, 169–179 (2010). https://doi.org/10.1007/s00122-010-1300-2
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DOI: https://doi.org/10.1007/s00122-010-1300-2