Overexpression of a modified eIF4E regulates potato virus Y resistance at the transcriptional level in potato

Authors: GUTIERREZ SANCHEZ, PABLO - NATIONAL UNIVERSITY OF COLOMBIA AT MEDELLÍN; BABUJEE, LAVANYA - UNIVERSITY OF WISCONSIN; JARAMILLO MESA, HELENA - UNIVERSITY OF WISCONSIN; GANNON, MEGAN - UNIVERSITY OF WISCONSIN; Halterman, Dennis; JAHN, MOLLY - UNIVERSITY OF WISCONSIN; JIANG, JIMING - MICHIGAN STATE UNIVERSITY; RAKOTONDRAFARA, AURÉLIE - UNIVERSITY OF WISCONSIN

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/22/2019
Publication Date: 1/6/2020
Citation: Gutierrez Sanchez, P.A., Babujee, L., Jaramillo Mesa, H., Arcibal, E., Gannon, M., Halterman, D.A., Jahn, M., Jiang, J., Rakotondrafara, A.M. 2020. Overexpression of a modified eIF4E regulates potato virus Y resistance at the transcriptional level in potato. Biomed Central (BMC) Genomics. 21(1):18. https://doi.org/10.1186/s12864-019-6423-5.
DOI: https://doi.org/10.1186/s12864-019-6423-5

Interpretive Summary: Potato virus Y (PVY) is one of the most important pathogens affecting potato production worldwide. Infection by PVY requires certain factors within the host that are needed for infection and replication. One of these host factors is a translation initiation factor called eIF4e. Previously, it has been found that mutations within eIF4e confer resistance to PVY in potato, presumably because the virus is no longer able to use eIF4e for replication. In this work, we analyze plants that overexpress the mutated version of eIF4e for gene expression changes that are correlated with resistance. Our results indicate that, in addition to translation initiation, eIF4e may be involved in the regulation of a certain set of genes involved in defense responses. This work puts forward a new perspective on how the regulation of eIF4E may be part of a natural plant defense response against potyviruses and provides an additional layer of defense through potential re-programming of stress responses. Our results will impact the scientific community through new information related to plant defense responses and will also impact the deployment of eIF4e resistance deployment in potato and other crops affected by PVY.

Technical Abstract: Potato virus Y (PVY) is one of the most important pathogens affecting potato production worldwide. Resistance to PVY can be established through mutations within the eukaryotic translation initiation factor eIF4E that disrupt the interaction between viral proteins and host translation machinery, necessary for replication. Using potato overexpressing a modified potato eIF4E, we investigated transcriptome changes that determine the efficacy of engineered resistance against PVY. The data suggest that the failure of PVY to infect the modified plants not only resulted from the physical interference of the PVY-eIF4E interaction due to the combinatory effect of the overwhelming presence of the resistant eIF4E allele, which the virus cannot recruit, and the striking transcriptional suppression of the native susceptible allele, which was also targeted by viral infection; but also from a potential eIF4E-mediated regulation of some oxidative and stress response factors, that normally respond to viral infection. While it is clear that eIF4E recessive resistance is widely effective against potyviruses, our results suggest that the regulation of eIF4E may be part of a plant defense response that primes the modified lines to establish an additional layer of resistance, even in the absence of the virus.