Transcriptome profiling reveals molecular players in early soybean - Sclerotinia sclerotiorum interaction

Authors: WEI, WEI - University Of Illinois; WU, XING - University Of Illinois; BLAHUT-BEATTY, LAUREEN - Agriculture And Agri-Food Canada; SIMMONDS, DAINA - Agriculture And Agri-Food Canada; Clough, Steven

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/2/2022
Publication Date: 7/1/2022
Citation: Wei, W., Wu, X., Blahut-Beatty, L., Simmonds, D.H., Clough, S.J. 2022. Transcriptome profiling reveals molecular players in early soybean - Sclerotinia sclerotiorum interaction. Phytopathology. 112(8):1739-1752. https://doi.org/10.1094/PHYTO-08-21-0329-R.
DOI: https://doi.org/10.1094/PHYTO-08-21-0329-R

Interpretive Summary: Sclerotinia stem rot is an important disease of soybean that occurs throughout the world. One of the main virulence factors of the pathogen is the release of oxalic acid, and complete genetic resistance to Sclerotinia or oxalic acid does not exist in soybean. We analyzed gene expression of transgenic plants that are resistant due to the transgenic addition of an oxalate degrading gene, during the very early stages of infection- 4 and 8 hours post inoculation. We found that although the transgenic plants are resistant, the presence of the oxalate degrading gene made little difference on gene expression compared to the control plant, presumably due to the excessive amounts of oxalic acid during that period. However, genes that did show some differences were related to a stronger defense response. In addition to looking at gene expression in inoculated plants, we also examined the expression of genes in the pathogen during the infection. Analyses of the pathogen expression levels suggested that the pathogen might sense the gradual removal of oxalic acid as a major gene related to its production was slightly more expressed when infecting the transgenic plant than from the control. This work sheds more light on the basic biology of host resistance and pathogen behavior, and it supports the importance of oxalic acid as a virulence factor, as well as supports the production of additional virulence factor candidates such as botcinic acid.

Technical Abstract: Sclerotinia sclerotiorum causes Sclerotinia stem rot on soybean. Using RNA sequencing, this study investigated the transcriptomes of soybean and S. sclerotiorum simultaneously, during early infection, 4 and 8 hours post inoculation (hpi). Two soybean genotypes were involved, a resistant oxalate oxidase (OxO)-transgenic line and its susceptible parent, AC_Colibri (AC). The goal was to identify critical genes in both the hosts and pathogen that could affect the outcome of the interaction. Of the 424 genes that were significantly induced by S. sclerotiorum, both hosts expressed genes related to jasmonic acid, ethylene, oxidative burst, and phenylpropanoids. Thirty percent of the DEGs encoded signaling components and transcription factors, including receptor-like kinases, MAPK kinases and E3 ubiquitin ligases. The phenylpropanoid pathways and genes involved in cell redox were more expressed in the OxO genotype enabling a faster defense response as compared to AC. In contrast, AC expressed more abundantly several negative regulators of defense and contributors of programmed cell death, supporting the multifaceted role of oxalic acid (OA) as a major virulence factor. Looking at pathogen behavior, thousands of genes in S. sclerotiorum were induced at 8 hpi, compared to expression in culture. Genes involved in plant cell wall degradation, sugar transport and secondary metabolism were most up-regulated and could contribute to early pathogenesis. Higher expression of genes encoding OA, botcinic acid, PCWDEs, proteases and potential effectors were detected in S. sclerotiorum in the OxO genotype, showing the wealth of virulence factors available to this pathogen, and their expression behavior suggests that S. sclerotiorum could modulate their expression in response to levels of OA.