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

PLoS One. 2014 Mar 7;9(3):e90394. doi: 10.1371/journal.pone.0090394. eCollection 2014.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alleles
  • Eukaryotic Initiation Factor-4E / genetics
  • Eukaryotic Initiation Factor-4E / physiology*
  • Geography
  • Pisum sativum / genetics
  • Pisum sativum / metabolism*
  • Pisum sativum / virology*
  • Plant Diseases / virology*
  • Plant Proteins / genetics
  • Plant Proteins / physiology*
  • Potyvirus / pathogenicity*

Substances

  • Eukaryotic Initiation Factor-4E
  • Plant Proteins

Grants and funding

This work was supported by the Ministry of Agriculture IQ91A229 project. CC was supported by USDA (United States Department of Agriculture) project #5348-2100 = 017-00D. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.