Interplay of pathogens, microRNAs, and regulation of resistance gene transcript abundance for rapid evolutionary responses in plants

RO 2491/6-1

Pathogens and hosts can differ by orders of magnitude in their generation time and population sizes. This difference presents a challenge for hosts to match and counter the rapid evolution and adaptation endowed by the shorter generation times (and larger population sizes) of pathogens. We seek to investigate by which means (i.e. which evolutionary genetic changes) plant species can match the rapid evolutionary potential of their microbial pathogen species. The focus of our work is the host-pathogen system involving wild tomato species and the oomycete pathogen, Phytophthora infestans. We will investigate the interplay of microRNA (miR) genes, NBS-LRR resistance genes, and pathogen resistance across multiple wild and domesticated tomato species. A small family of miR genes that negatively regulates transcript abundance of NBS-LRR genes has recently been discovered in tomato. The up-regulation of these miR genes leads to the downregulation of NBS-LRRs resistance genes, and vice-versa. Therefore, miRNA abundance is likely tied to levels of disease resistance in plants. Post-transcriptional control of R-genes may allow the plants to mount a more rapid defense response to pathogen attack and thus may be an adaptation deployed in plants to match the evolutionary potential of their pathogens. However, post-transcriptional control of R-genes can also be hijacked by pathogens to suppress defense responses. We predict that presence of pathogens in plants does affect the miR transcript abundance and subsequently the R-protein abundance. At the one extreme, pathogen up regulation of miR genes or secretion of miR molecular mimics would down regulate R-gene abundance. This would be viewed as an adaptation on the part of the pathogen. Alternatively, down-regulation by the pathogen of these miR genes would lead to up-regulation of R-genes. In this case, resistance would be activated and the plant would have the advantage. Either scenarios give us insight into the complex reciprocal evolutionary genetic changes that have taken place between these species. In this research initiative, we would like to investigate the post-transcriptional regulation of R-genes through members of a small miR gene family in the presence of pathogen infection. We will conduct controlled inoculations of eight different tomato species using four different pathogen genotypes. The level of pathogen spread and host resistance will be determined. Simultaneously we will assay the abundance of the primary and mature transcripts of seven miR genes during the infection. We will also assay the transcript abundance of eight putative P. infestans resistance genes, targeted by these miR transcripts. Through multivariate statistical analyses, we will be able to identify the which miR genes and which R-genes are up- or down-regulated during pathogen infection. These genes will be subjected to further investigation for functional, in planta, validation.

Publications
  • Sophie de Vries, Eva H. Stukenbrock and Laura E. Rose (2020) Rapid evolution in plant‐microbe interactions ‐ an evolutionary genomics perspective. New Phytologist. DOI: 10.1111/nph.16458

  • Frantzeskakis, L., von Dahlen, J.K., Panstruga, R., and Rose, L.E. (2018) Rapid evolution in the tug-of-war between microbes and plants. New Phytologist 219: 12-14. DOI: 10.1111/nph.15220

  • Sophie de Vries, Andreas Kukuk, Janina K. von Dahlen, Anika Schnake, Thorsten Kloesges, Laura E. Rose (2018) Expression profiling across wild and cultivated tomatoes supports the relevance of early miR482/2118 suppression for Phytophthora resistance. Proc. R. Soc. B 2018 285 20172560.

  • Sophie de Vries, Janina K von Dahlen, Anika Schnake, Sarah Ginschel, Barbara Schulz, Laura E Rose (2018) Broad-spectrum inhibition of Phytophthora infestans by fungal endophytes. FEMS Microbiology Ecology, Volume 94, Issue 4, 1 April 2018, fiy037. DOI: 10.1093/femsec/fiy037
  • Sophie de Vries, Janina K. von Dahlen, Constanze Uhlmann, Anika Schnake, Thorsten Kloesges and Laura E. Rose (2017) Signatures of selection and host-adapted gene expression of the Phytophthora infestans RNA silencing suppressor PSR2. Molecular Plant Pathology 18:110-124. DOI: 10.1111/mpp.12465
  • Sophie de Vries, Thorsten Kloesges and Laura E. Rose (2015) Evolutionarily Dynamic, but Robust, Targeting of Resistance Genes by the miR482/2118 Gene Family in the Solanaceae. Genome Biol Evol. 7:3307-3321. DOI: 10.1093/gbe/evv225