Geographical gradient of the eIF4E alleles conferring resistance to potyviruses in pea (Pisum) germplasm

. 2014 ; 9 (3) : e90394. [epub] 20140307

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid24609094

BACKGROUND: The eukaryotic translation initiation factor 4E was shown to be involved in resistance against several potyviruses in plants, including pea. We combined our knowledge of pea germplasm diversity with that of the eIF4E gene to identify novel genetic diversity. METHODOLOGY/PRINCIPAL FINDINGS: Germplasm of 2803 pea accessions was screened for eIF4E intron 3 length polymorphism, resulting in the detection of four eIF4E(A-B-C-S) variants, whose distribution was geographically structured. The eIF4E(A) variant conferring resistance to the P1 PSbMV pathotype was found in 53 accessions (1.9%), of which 15 were landraces from India, Afghanistan, Nepal, and 7 were from Ethiopia. A newly discovered variant, eIF4E(B), was present in 328 accessions (11.7%) from Ethiopia (29%), Afghanistan (23%), India (20%), Israel (25%) and China (39%). The eIF4E(C) variant was detected in 91 accessions (3.2% of total) from India (20%), Afghanistan (33%), the Iberian Peninsula (22%) and the Balkans (9.3%). The eIF4E(S) variant for susceptibility predominated as the wild type. Sequencing of 73 samples, identified 34 alleles at the whole gene, 26 at cDNA and 19 protein variants, respectively. Fifteen alleles were virologically tested and 9 alleles (eIF4E(A-1-2-3-4-5-6-7), eIF4E(B-1), eIF4E(C-2)) conferred resistance to the P1 PSbMV pathotype. CONCLUSIONS/SIGNIFICANCE: This work identified novel eIF4E alleles within geographically structured pea germplasm and indicated their independent evolution from the susceptible eIF4E(S1) allele. Despite high variation present in wild Pisum accessions, none of them possessed resistance alleles, supporting a hypothesis of distinct mode of evolution of resistance in wild as opposed to crop species. The Highlands of Central Asia, the northern regions of the Indian subcontinent, Eastern Africa and China were identified as important centers of pea diversity that correspond with the diversity of the pathogen. The series of alleles identified in this study provides the basis to study the co-evolution of potyviruses and the pea host.

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Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: Unlocking genetic potential from the wild. Science 277: 1063–1066. PubMed

Bhullar NK, Street K, Mackay M, Yahiaoui N, Keller B (2009) Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc Nat Academy of Sci USA 106: 9519–9524. PubMed PMC

Hofinger BJ, Russell JR, Bass CHG, Baldwin T, dos Reis M, et al. (2011) An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Mol Ecology 20: 3653–3668. PubMed

Nieto C, Piron F, Dalmais M, Marco CF, Moriones E, et al. (2007) EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biology 7: 34. PubMed PMC

Ibiza VP, Cañizares J, Nuez F (2010) EcoTILLING in Capsicum species: searching for new virus resistance. BMC Genomics 11: 631. PubMed PMC

Reeves PA, Panella LW, Richards CHM (2012) Retention of agronomically important variation in germplasm core collections: implications for allele mining. Theor Appl Genet 124: 1155–1171. PubMed

Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends in Plant Sci 11: 40–45. PubMed

Bhullar NK, Zhang Z, Wicker T, Keller B (2010) Wheat gene bank accessions as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project. BMC Plant Biol 10: 88. PubMed PMC

Chimwamurombe PM, Khulbe RK (2011) Domestication. In: Pratap A, Kumar J, editors. Biology and Breeding of Food Legumes. MA, USA: CABI, Cambridge. pp. 19–34.

Zohary D, Hopf M (1993) Domestication of Plants in the Old World—The Origin and Spread of Cultivated Plants in West Asia, Europe, and the Nile Valley. Oxford: Clarendon Press.

De Candolle A (1882) Origin of cultivated plants. Whitefish MT: Kesinger Publishing LCC.

Maxted N, Ambrose M (2001) Peas (Pisum L.). In: Maxted N, Bennett SJ, editors. Plant Genetic Resources of Legumes in the Mediterranean. Dordrecht: Kluwer Academic Publishers. pp. 181–190.

Smýkal P, Kenicer G, Flavell AJ, Corander J, Kosterin O, et al. (2011) Phylogeny, phylogeography and genetic diversity of the Pisum genus. Plant Gen Res 9: 4–18.

Smýkal P, Aubert G, Burstin J, Coyne C, Ellis N, et al. (2012) Pea (Pisum sativum L.) in the genomic era. MDPI Agronomy 2: 74–115.

Smýkal P, Coyne C, Redden R, Maxted N (2013) Peas. In: Singh M, Bisht IS, editors. Genetic and Genomic Resources for Grain Legume Improvement. London: Elsevier Insights. pp. 41–80.

Smýkal P, Hybl M, Corander J, JarkovskyJ, Flavell AJ, et al. (2008) Genetic diversity and population structure of pea (Pisum sativum L.) varieties derived from combined retrotransposon, microsatellite and morphological marker analysis. Theor Appl Genet 117: 413–424. PubMed

Jing R, Ambrose MA, Knox MR, Smykal P, Hybl M, et al. (2012) Genetic diversity in European Pisum germplasm collections. Theor Appl Genet 125: 367–380. PubMed PMC

Zong X, Redden R, Liu Q, Wang S, Guan J, et al. (2009) Analysis of a diverse global Pisum sp. collection and comparison to a Chinese local P. sativum collection with microsatellite markers. Theor Appl Gen 118: 193–204. PubMed

Kwon SJ, Brown AF, Hu J, McGee RJ, Watt CA, et al. (2012) Genetic diversity, population structure and genome-wide marker-trait association analysis emphasizing seed nutrients of the USDA pea (Pisum sativum L.) core collection. Genes & Genomics 34: 305–320.

Wang A, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pat 13: 795–803. PubMed PMC

Vavilov NI (1949-1950) The phytogeographic basis of plant breeding. In Chester KS trans. The origin, variation, immunity, and breeding of cultivated plants. Waltham MA: Chronica Botanica. pp. 13–54.

Abbo S, Lev-Yadun S, Gopher A (2012) Plant domestication and crop evolution in the Near East: on events and processes. Crit Rev in Plant Sci 31: 241–257.

Lovisolo O, Hull R, Rosler O (2003) Coevolution of viruses with hosts and vectors and possible paleontology. Adv Virus Res 62: 325–379. PubMed

Jones EI, Ferriere R, Bronstein JL (2009) Eco-evolutionary dynamics of mutualists and exploiters. American Naturalist 174: 780–794. PubMed

Le Gall O, Aranda MA, Caranta C (2011) Plant resistance to viruses mediated by translation initiation factors. In: Caranta C, Aranda MA, Tepfer M & López-Moya J, editors. Recent Advances in Plant Virology. Norfolk: Caister Academic Press. pp. 177–194.

Musil M (1966) Über das Vorkommen des Virus des Blattrollens der Erbse in der Slowakei (Vorlaufige Mitteilung). Biologia 21: 133–138.

Latham LJ, Jones RAC (2001) Alfalfa mosaic and pea seed-borne mosaic viruses in cool season crop, annual pasture, and forage legumes: susceptibility, sensitivity, and seed transmission. Austr J Agri Res 52: 771–790.

Hampton RO, Mink GI (1975) Pea seed-borne mosaic virus. CMI/AAB Descriptions of Plant Viruses. 146 n.

Alconero R, Weeden NF, Gonsalves D, Fox DT (1985) Loss of genetic diversity in pea germplasm by the elimination of individuals infected by pea seedborne mosaic virus. Ann of App Bio 106: 357–364.

Hjulsager CK, Olsen BS, Jensen DM, Cordea MI, Krath BN, et al. (2006) Multiple determinants in the coding region of pea seed-borne mosaic virus P3 are involved in virulence against sbm-2 resistance. Virology 355: 52–61. PubMed

Smýkal P, Šafářová D, Navrátil M, Dostálová R (2010) Marker assisted pea breeding: eIF4E allele specific markers to pea seed-borne mosaic virus (PSbMV) resistance Mol Breeding. 26: 425–438.

Bruun-Rasmussen M, Moller IS, Tulinius G, Hansen KR, Lund OS, et al. (2007) The same allele of translation initiation factor 4E mediates resistance against two Potyvirus spp. in Pisum sativum . Mol Plant Microbe Interact 20: 1075–1082. PubMed

Andrade M, Abe Y, Nakahara KS, Uyeda I (2009) The cyv-2 resistance to Clover yellow vein virus in pea is controlled by the eukaryotic initiation factor 4E. J Gen Plant Pathol 75: 241–249.

Johansen EI, Lund OS, Hjulsager CK, Laursen J (2001) Recessive resistance in Pisum sativum and Potyvirus Pathotype resolved in a gene-for-cistron correspondence between host and virus. J Virology 75: 6609–6614. PubMed PMC

Gao Z, Eyers S, Thomas C, Ellis N, Maule A (2004) Identification of markers tightly linked to sbm recessive genes for resistance to pea seed-borne mosaic virus. Theor Appl Genet 109: 488–494. PubMed

Olsen BS, Johansen IE (2001) Nucleotide sequence and infectious cDNA clone of the L1 isolate of Pea seed-borne mosaic potyvirus. Archives in Virology 146: 15–25. PubMed

Johansen IE, Rasmussen OF, Heide M, Borkhardt B (1991) The complete nucleotide sequence of pea seed-borne mosaic virus RNA. J Gen Virology 72: 2625–2632. PubMed

Johansen IE, Keller KE, Dougherty WG, Hampton RO (1996) Biological and molecular properties of a pathotype P-1 and a pathotype P-4 isolate of pea seed-borne mosaic virus. J Gen Virology 77: 1329–1333. PubMed

Ruffel S, Gallois J-L, Moury B, Robaglia C, Palloix A, et al. (2006) Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent Pepper veinal mottle virus infection of pepper. J GenVirol 87: 2089–2098. PubMed

Sato M, Nakaharaa K, Yoshii M, Ishikawa M, Uyeda I (2005) Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Letters 579: 1167–1171. PubMed

Fraile A, Garcia-Arenal F (2010) The coevolution of plants and viruses: resistance and pathogenicity. Adv Virus Res 76: 1–32. PubMed

Ashby AJ, Stevenson CEM, Jarvis GE, Lawson DM, Maule AJ (2011) Structure- Based Mutational Analysis of eIF4E in Relation to sbm1 Resistance to Pea Seed-Borne Mosaic virus in pea. PLoS ONE 6: e15873. PubMed PMC

Charron C, Nicolai M, Gallois JL, Robaglia C, Moury B, et al. (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54: 56–68. PubMed

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. PubMed

Rubio M, Nicolaï M, Caranta C, Palloix A (2009) Allele mining in the pepper gene pool provided new complementation effects between pvr2-eIF4E and pvr6-eIF(iso)4E alleles for resistance to pepper veinal mottle virus. J GenVirol 90: 2808–2814. PubMed

Jeong HJ, Kwon JK, Pandeya D, Hwang J, Hoang NH, et al. (2012) A survey of natural and ethyl methane sulfonate-induced variations of eIF4E using high-resolution melting analysis in Capsicum. Mol Breeding 29: 349–360.

Rigola DJ, van Oeveren J, Janssen A, Bonne A, Schneiders H, et al. (2009) High throughput detection of induced mutations and natural variation using KeyPoint technology. PLoS ONE 4: e4761. PubMed PMC

Gibbs AJ, Ohshima K, Phillips MJ, Gibbs MJ (2008) The Prehistory of Potyviruses: Their Initial Radiation Was during the Dawn of Agriculture. PLoS ONE 3: e2523. PubMed PMC

Cieslarová J, Hýbl M, Griga M, Smýkal P (2012) Molecular Analysis of Temporal Genetic Structuring in Pea (Pisum sativum L.) Cultivars Bred in the Czech Republic and in Former Czechoslovakia Since the Mid-20th Century. Czech J Gen and Plant Breeding 48: 61–73.

Werle E, Schneider C, Renner M, Völker M, Fiehn W (1994) Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research 22: 4354–4355. PubMed PMC

Hall TA (1999) BioEdit: a user-friendly biologicalsequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95–98.

Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48. PubMed

Šafářová D, Navrátil M, Petrusová J, Pokorný R, Piaková Z (2008) Genetic and biological diversity of the pea seed-borne mosaic virus isolates occurring in Czech Republic. Acta Virologica 52: 53–57. PubMed

Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, et al. (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive bymovirus resistance in Hordeum vulgare (L.). Plant J 42: 912–22. PubMed

Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, et al. (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 132: 1272–1282. PubMed PMC

Kang BC, Yeam I, Frantz DJ, Murphy JF, Jahn MM (2005) The pvr1 locus in pepper encodes a translation initiation factor eIF4E that interacts with tobacco etch virus VPg. Plant J 42: 392–405. PubMed

Hjulsager CK, Lund OS, Johansen E (2002) A new pathotype of pea seedborne mosaic virus explained by the properties of the p3-6k1 and viral genome-linked protein (VPg) coding regions. Mol Plant Microbe Interact 15: 169–171. PubMed

Wylie SJ, Coutts BA, Jones RAC (2011) Genetic variability of the coat protein sequence of pea seed-borne mosaic virus isolates and the current relationship between phylogenetic placement and resistance groups. Arch Virol 156: 1287–1290. PubMed

Hagedorn DJ, Gritton ET (1973) Inheritance of resistance to the pea seed-borne mosaic virus. Phytopathology 62: 1130–1133.

Hampton RO (1986) Geographic origin of pea seed-borne mosaic virus: a hypothesis. Pisum Newsletter 18: 22–26.

Ali A, Randles JW (2001) Genomic heterogeneity in Pea seed-borne mosaic virus isolates from Pakistan, the centre of diversity of the host species, Pisum sativum . Arch Virology 146: 1855–1870. PubMed

Ling Li, Redden RJ, Zong X, Berger JD, Bennett SJ (2013) Ecogeographic analysis of pea collection sites from China to determine potential sites with abiotic stresses. Genet Res Crop Evol 60: 1801–1815.

Jing R, Vershinin A, Grzebyta J, Shaw P, Smýkal P, et al. (2010) The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol Biol 10: 44. PubMed PMC

Roossinck MJ (2011) The big unknown: plant virus biodiversity. Current Opinions in Virology 1: 63–67. PubMed

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