Evolution of plant eukaryotic initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg): a game of mirrors impacting resistance spectrum and durability.

Polymorphism in the plant eukaryotic translation initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg) determine, in many cases, the outcome of the confrontation between these two organisms: compatibility (i.e. infection of the plant by the virus) or incompatibility (i.e. resistance of the plant to the virus). The two interacting proteins eIF4E and VPg show strikingly similar evolution patterns. Most codon positions in their coding sequences are highly constrained for nonsynonymous substitutions but a small number shows evidence for positive selection. Several of these latter positions were shown to be functionally important, conferring resistance to the host or pathogenicity to the virus. Determining the mutational pathways involved in pepper eIF4E diversification revealed a link between an increase of the pepper resistance spectrum towards a panel of potyvirus species and an increase of durability of the resistance towards Potato virus Y. This relationship questions the interest of using more generally the spectrum of action of a plant resistance gene as a predictor of its durability potential.

The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene.

The translation initiation factor 4E (eIF4E) has been implicated in naturally occurring resistance to Potato virus Y (PVY) determined by the pvr2 locus in pepper (Capsicum annuum). Here, the molecular basis of the recessive resistance to PVY and Tobacco etch virus (TEV) controlled by the pot-1 locus in tomato (Lycopersicon esculentum; now Solanum lycopersicum) was investigated. On the basis of genetic mapping data that indicated that pot-1 and pvr2 are located in syntenic regions of the tomato and pepper genomes, the possible involvement of eIF4E in pot-1-mediated resistance was assessed. Genetic mapping of members of the eIF4E multigenic family in tomato introgression lines revealed that an eIF4E locus indeed maps in the same genomic region as pot-1. By comparing eIF4E coding sequences between resistant and susceptible Lycopersicon genotypes, a small number of polymorphisms that co-segregate with the pot-1 locus were identified, suggesting that this gene could be involved in resistance to potyviruses. Functional complementation experiments using Potato virus X-mediated transient expression of eIF4E from a susceptible genotype in a resistant pepper genotype confirmed that a small number of amino acid substitutions in the eIF4E protein indeed account for resistance/susceptibility to both the PVY and TEV, and consequently that pot-1 and pvr2 are orthologues. Taken together, these results support the role of this eIF4E gene as a key component of recessive resistance to potyviruses, and validate the comparative genomic approach for the molecular characterization of recessive resistance genes.

The Arabidopsis chloroplast ribosomal protein L21 is encoded by a nuclear gene of mitochondrial origin.

Many chloroplast genes of cyanobacterial origin have been transferred to the nucleus during evolution and their products are re-addressed to chloroplasts. The RPL21 gene encoding the plastid r-protein L21 has been lost in higher plant chloroplast genomes after the divergence from bryophytes. Based on phylogenetic analysis and intron conservation, we now provide evidence that in Arabidopsis a nuclear RPL21c gene of mitochondrial origin has replaced the chloroplast gene. The control of expression of this gene has been adapted to the needs of chloroplast development by the acquisition of plastid-specific regulatory promoter cis-elements.