High overexpression of CERES, a plant regulator of translation, induces different phenotypical defence responses during TuMV infection

• Published in: The Plant journal : for cell and molecular biology 2021-07, Vol.107 (1), p.256-267
• Main Authors: Toribio, René, Muñoz, Alfonso, Sánchez, Flora, Ponz, Fernando, Castellano, M. Mar
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - virology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; CERES; Defence; Ectopic expression; Eukaryotic Initiation Factor-4E - genetics; Eukaryotic Initiation Factor-4E - metabolism; Eukaryotic Initiation Factors - genetics; Eukaryotic Initiation Factors - metabolism; eukaryotic translation initiation factor 4E; Gene Expression Regulation, Plant; Host plants; Host-Pathogen Interactions - genetics; Host-Pathogen Interactions - physiology; Hypersensitive response; Infections; Initiation factor eIF-4E; Initiation factors; Isoforms; Leucine; Leucine‐rich repeat protein; Mutation; Necrosis; Nicotiana - genetics; Nicotiana - virology; Nicotiana benthamiana; Phenotype; Phenotypes; Plant Diseases - virology; Plant Leaves - virology; Plant virus diseases; Plant viruses; Plants, Genetically Modified; Potyvirus - pathogenicity; Potyvirus - physiology; Protein Isoforms - metabolism; Proteins; translation regulation; turnip mosaic virus; Virus Replication; Viruses
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15290

SUMMARY Mutations in the eukaryotic translation initiation factors eIF4E and eIF(iso)4E confer potyvirus resistance in a range of plant hosts. This supports the notion that, in addition to their role in translation of cellular mRNAs, eIF4E isoforms are also essential for the potyvirus cycle. CERES is a plant eIF4E‐ and eIF(iso)4E‐binding protein that, through its binding to the eIF4Es, modulates translation initiation; however, its possible role in potyvirus resistance is unknown. In this article, we analyse if the ectopic expression of AtCERES is able to interfere with turnip mosaic virus replication in plants. Our results demonstrate that, during infection, the ectopic expression of CERES in Nicotiana benthamiana promotes the development of a mosaic phenotype when it is accumulated to moderate levels, but induces veinal necrosis when it is accumulated to higher levels. This necrotic process resembles a hypersensitive response (HR)‐like response that occurs with different HR hallmarks. Remarkably, Arabidopsis plants inoculated with a virus clone that promotes high expression of CERES do not show signs of infection. These final phenotypical outcomes are independent of the capacity of CERES to bind to eIF4E. All these data suggest that CERES, most likely due to its leucine‐rich repeat nature, could act as a resistance protein, able to promote a range of different defence responses when it is highly overexpressed from viral constructs. Significance Statement CERES was recently described as a novel eIF4E‐interacting protein that acts as a translational regulator during specific stages of the light cycle in plants. In this work, we unravel that, when overexpressed from viral constructs, AtCERES is able to promote a range of phenotypical defence responses during TuMV infection. Interestingly, these defence responses do not seem intrinsically linked to CERES´ capacity to bind eIF4E isoforms, but seem associated with its leucine‐rich repeat nature.