Divergent molecular pathways govern temperature-dependent wheat stem rust resistance genes

Authors: HEWITT, TIM - Commonwealth Scientific And Industrial Research Organisation (CSIRO); Sharma, Keshav; ZHANG, JIANPING - University Of Sydney; CHUNHONG, CHEN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); BAJGAIN, PRABIN - University Of Minnesota; BHATT, DHARA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); YANG, JUN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); Olivera Firpo, Pablo; SINGH, SMRITI - University Of Sydney; WANG, QIAOLI - Henan Agricultural University; UPADHYAYA, NARAYANA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); POZNIAK, CURTIS - University Of Saskatchewan; MCINTOSH, ROBERT - University Of Sydney; LAGUDAH, EVANS - Commonwealth Scientific And Industrial Research Organisation (CSIRO); ZHANG, PENG - University Of Sydney; Rouse, Matthew

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/13/2025
Publication Date: 5/28/2025
Citation: Hewitt, T.C., Sharma, K.N., Zhang, J., Chunhong, C., Bajgain, P., Bhatt, D., Yang, J., Olivera Firpo, P.D., Singh, S., Wang, Q., Upadhyaya, N., Pozniak, C., Mcintosh, R., Lagudah, E., Zhang, P., Rouse, M.N. 2025. Divergent molecular pathways govern temperature-dependent wheat stem rust resistance genes. Nature Communications. 16.Article 4905. https://doi.org/10.1038/s41467-025-60030-x.
DOI: https://doi.org/10.1038/s41467-025-60030-x

Interpretive Summary: Stem rust is historically a major disease of wheat in the United States and around the world. Newly emerged strains of this pathogen, such as Ug99, have developed virulence to most deployed stem rust resistance (Sr) genes. Several Sr genes display a resistance that is effective at specific temperatures including Sr6, Sr13, and Sr21. Sr6-mediated resistance is enhanced at lower temperatures whereas Sr13 and Sr21 resistances are enhanced at higher temperatures. In this study we identified the DNA sequence responsible for Sr6-mediated resistance. The DNA sequences of Sr13 and Sr21 were previously identified. With the DNA sequences of these three temperature-sensitive resistance genes identified, we studied gene expression of wheat lines with and without these three genes to characterize the molecular pathways associated with temperature-sensitive disease resistance. We found divergent molecular pathways responsible for low- and high-temperature-sensitive resistance. This study informed future strategies for deployment and engineering of genetic resistance in response to seasonal variation and changing climates in order to protect United States crops such as wheat from emerging diseases.

Technical Abstract: The wheat stem rust pathogen, Puccinia graminis f. sp. tritici (Pgt), has caused devastating crop losses worldwide. Newly emerged strains of this pathogen, such as Ug99, have developed virulence to most deployed stem rust resistance (Sr) genes. Several Sr genes display a temperature-dependent immune response, including Sr6, Sr13, and Sr21. Sr6-mediated resistance is enhanced at lower temperatures whereas Sr13 and Sr21 resistances are enhanced at higher temperatures. Whereas Sr13 and Sr21 encoding genes were previously identified, here we report the cloning of Sr6 by mutagenesis and resistance gene enrichment and sequencing (MutRenSeq), showing it to be a nucleotide-binding leucine-rich repeat protein (NB-LRR) with an integrated BED domain. We also demonstrate that in addition to resistance, Sr6 temperature sensitivity is also transferred to wheat plants transformed with the Sr6 transgene. To characterize the molecular basis of temperature sensitivity in these three Sr genes, differential gene expression analysis was performed using near-isogenic wheat lines inoculated with Pgt at varying temperatures, revealing that genes upregulated in the low-temperature-effective Sr6 response differed significantly from those of the high-temperature-effective responses associated with Sr13 and Sr21. Understanding the molecular mechanisms and pathways involved in temperature sensitivity can inform future strategies for deployment and engineering of genetic resistance in response to seasonal variation and changing climates.