Trans-species synthetic gene design allows resistance pyramiding and broad-spectrum engineering of virus resistance in plants

Anna Bastet (1) , Baptiste Lederer (1) , Nathalie Giovinazzo (1) , Xavier Arnoux (2) , Sylvie German-Retana (2) , Catherine Reinbold (3) , Véronique Brault (3) , Damien Garcia (4) , Samia Djennane (3) , Sophie Gersch (3) , Olivier Lemaire (3) , Christophe Robaglia (5, 6) , Jean-Luc Gallois (1)

1 GAFL - Génétique et Amélioration des Fruits et Légumes
2 BFP - Biologie du fruit et pathologie
3 SVQV - Santé de la vigne et qualité du vin
4 IBMP - Institut de Biologie Moléculaire des Plantes
5 BIAM - Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB)
6 LGBP - Luminy Génétique et Biophysique des Plantes

To infect plants, viruses rely heavily on their host's machinery. Plant genetic resistances based on host factor modifications can be found among existing natural variability and are widely used for some but not all crops. While biotechnology can supply for the lack of natural resistance alleles, new strategies need to be developed to increase resistance spectra and durability without impairing plant development. Here, we assess how the targeted allele modification of the Arabidopsis thaliana translation initiation factor eIF4E1 can lead to broad and efficient resistance to the major group of potyviruses. A synthetic Arabidopsis thaliana eIF4E1 allele was designed by introducing multiple amino acid changes associated with resistance to potyvirus in naturally occurring Pisum sativum alleles. This new allele encodes a functional protein while maintaining plant resistance to a potyvirus isolate that usually hijacks eIF4E1. Due to its biological functionality, this synthetic allele allows, at no developmental cost, the pyramiding of resistances to potyviruses that selectively use the two major translation initiation factors, eIF4E1 or its isoform eIFiso4E. Moreover, this combination extends the resistance spectrum to potyvirus isolates for which no efficient resistance has so far been found, including resistance‐breaking isolates and an unrelated virus belonging to the Luteoviridae family. This study is a proof‐of‐concept for the efficiency of gene engineering combined with knowledge of natural variation to generate trans‐species virus resistance at no developmental cost to the plant. This has implications for breeding of crops with broad‐spectrum and high durability resistance using recent genome editing techniques.

Mots clés: Arabidopsis thaliana; synthetic allele; translational research; eIF4E; potyvirus; resistance

Domaines: Amélioration des plantes; Biologie moléculaire

Anna Bastet, Baptiste Lederer, Nathalie Giovinazzo, Xavier Arnoux, Sylvie German-Retana, et al.. Trans-species synthetic gene design allows resistance pyramiding and broad-spectrum engineering of virus resistance in plants. Plant Biotechnology Journal, In press, 16 (9), pp.1569-1581. ⟨10.1111/pbi.12896⟩. ⟨hal-01852177⟩