Morpho-physiological and transcriptomic responses of field pennycress to waterlogging

Rachel Combs-Giroir; Manesh B Shah; Hari B Chhetri; Mallory Morgan; Erica Teixeira Prates; Alice Townsend; Mary E Phippen; Winthrop B Phippen; Daniel A Jacobson; Andrea R Gschwend

doi:10.3389/fpls.2024.1478507

Morpho-physiological and transcriptomic responses of field pennycress to waterlogging

Front Plant Sci. 2024 Dec 18:15:1478507. doi: 10.3389/fpls.2024.1478507. eCollection 2024.

Authors

Affiliations

¹ Center for Applied Plant Sciences, The Ohio State University, Columbus, OH, United States.
² Department of Horticulture and Crop Science, The Ohio State University, Columbus, OH, United States.
³ Biosciences, Oak Ridge National Laboratory, Oak Ridge, TN, United States.
⁴ Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee-Knoxville, Knoxville, TN, United States.
⁵ School of Agriculture, Western Illinois University, Macomb, IL, United States.

Abstract

Field pennycress (Thlaspi arvense) is a new biofuel winter annual crop with extreme cold hardiness and a short life cycle, enabling off-season integration into corn and soybean rotations across the U.S. Midwest. Pennycress fields are susceptible to winter snow melt and spring rainfall, leading to waterlogged soils. The objective of this research was to determine the extent to which waterlogging during the reproductive stage affected gene expression, morphology, physiology, recovery, and yield between two pennycress lines (SP32-10 and MN106). In a controlled environment, total pod number, shoot/root dry weight, and total seed count/weight were significantly reduced in SP32-10 in response to waterlogging, whereas primary branch number, shoot dry weight, and single seed weight were significantly reduced in MN106. This indicated waterlogging had a greater negative impact on seed yield in SP32-10 than MN106. We compared the transcriptomic response of SP32-10 and MN106 to determine the gene expression patterns underlying these different responses to seven days of waterlogging. The number of differentially expressed genes (DEGs) between waterlogged and control roots were doubled in MN106 (3,424) compared to SP32-10 (1,767). Functional enrichment analysis of upregulated DEGs revealed Gene Ontology (GO) terms associated with hypoxia and decreased oxygen, with genes in these categories encoding proteins involved in alcoholic fermentation and glycolysis. Additionally, downregulated DEGs revealed GO terms associated with cell wall biogenesis and suberin biosynthesis, indicating suppressed growth and energy conservation. Interestingly, MN106 waterlogged roots exhibited significant stronger regulation of these genes than SP32-10, displaying a more robust transcriptomic response overall. Together, these results reveal the reconfiguration of cellular and metabolic processes in response to the severe energy crisis invoked by waterlogging in pennycress.

Keywords: ERF-VII; RNA-seq; Thlaspi arvense; hypoxia; recovery; root stress; transcriptomics; waterlogging.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program (DE-SC0021286). This research used resources of the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory, which is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC05-00OR22725. Combs-Giroir was also financially supported in part by the National Science Foundation Graduate Research Fellowship Program.