Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize

Authors: KIM, SAET-BYUL - North Carolina State University; KARRE, SHAILESH - North Carolina State University; CHOI, HOSEONG - Seoul National University; Christensen, Shawn; WANG, GUAN-FENG - North Carolina State University; JO, YEONHWA - Seoul National University; CHO, WON KYONG - Seoul National University; Balint-Kurti, Peter

Submitted to: Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/25/2021
Publication Date: 1/25/2021
Citation: Kim, S., Karre, S., Choi, H., Christensen, S.A., Wang, G., Jo, Y., Cho, W., Balint Kurti, P.J. 2021. Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize. Molecular Plant Pathology. https://doi.org/10.1111/mpp.13040.
DOI: https://doi.org/10.1111/mpp.13040

Interpretive Summary: In this study we have performed a detailed analysis of the response to infection by P. sorghi, causal agent of maize common rust, in two near-isogenic maize lines differing for the presence of a major resistance gene. We identified transcriptionally upregulated pathways and have then performed targeted metabolomics to characterize the effects on the levels of metabolites in several of these pathways. In doing so we have developed a rich dataset describing both the compatible and incompatible defense response in maize to one of its most common pathogens. This is, we believe, only the second such dataset available for the interaction between maize and a biotrophic pathogen and the first that describes the response mediated by a major resistance gene.

Technical Abstract: Common rust, caused by Puccinia sorghi, is a widespread and destructive disease of maize. The Rp1-D gene confers resistance to the P. sorghi IN2 isolate, mediating a hypersensitive cell death response (HR). To identify differentially expressed maize genes (DEGs) and metabolites associated with the compatible (susceptible) interaction and with Rp1-D-mediated resistance, we performed transcriptomic and targeted metabolomic analyses of P. sorghi IN2-infected leaves from the near-isogenic lines H95 and H95:Rp1-D which differed for the presence of Rp1-D. Microscopic analysis confirmed that H95:Rp1-D underwent a rapid HR upon infection and did not allow sporulation, whereas no HR and abundant sporulation was observed on H95. We sampled at four timepoints, 0, 12, 24 and 120 hours post-infection for transcriptomic analyses and at two time points, 24 and 48 hours, for targeted metabolomics. We observed up-regulation of genes involved in defense and secondary metabolism, including the phenylpropanoid, flavonoid and terpenoid pathways, and down regulation of genes involved in photosynthesis and primary metabolism in both lines. Metabolomic analyses confirmed that intermediates from several transcriptionally upregulated pathways accumulated during the defense response. The response of H95:Rp1-D was qualitatively similar to that of H95 but was generally faster and stronger as measured both transcriptionally and metabolomically.