Transcriptomic and metabolomic changes in postharvest sugarbeet roots reveal widespread metabolic changes in storage and identify genes potentially responsible for respiratory sucrose loss

Karen K Fugate; John D Eide; Abbas M Lafta; Muhammad Massub Tehseen; Chenggen Chu; Mohamed F R Khan; Fernando L Finger

doi:10.3389/fpls.2024.1320705

Transcriptomic and metabolomic changes in postharvest sugarbeet roots reveal widespread metabolic changes in storage and identify genes potentially responsible for respiratory sucrose loss

Front Plant Sci. 2024 Jan 30:15:1320705. doi: 10.3389/fpls.2024.1320705. eCollection 2024.

Authors

Karen K Fugate¹, John D Eide¹, Abbas M Lafta², Muhammad Massub Tehseen³, Chenggen Chu¹, Mohamed F R Khan^{2

4}, Fernando L Finger⁵

Affiliations

¹ Edward T. Schafer Agricultural Research Center, U.S. Department of Agriculture, Agricultural Research Service, Fargo, ND, United States.
² Department of Plant Pathology, North Dakota State University, Fargo, ND, United States.
³ Department of Plant Sciences, North Dakota State University, Fargo, ND, United States.
⁴ University of Minnesota Extension Service, St. Paul, MN, United States.
⁵ Departamento de Agronomia, Universidade Federal de Viçosa, Viçosa, Brazil.

Abstract

Endogenous metabolism is primarily responsible for losses in sucrose content and processing quality in postharvest sugarbeet roots. The genes responsible for this metabolism and the transcriptional changes that regulate it, however, are largely unknown. To identify genes and metabolic pathways that participate in postharvest sugarbeet root metabolism and the transcriptional changes that contribute to their regulation, transcriptomic and metabolomic profiles were generated for sugarbeet roots at harvest and after 12, 40 and 120 d storage at 5 and 12°C and gene expression and metabolite concentration changes related to storage duration or temperature were identified. During storage, 8656 genes, or 34% of all expressed genes, and 225 metabolites, equivalent to 59% of detected metabolites, were altered in expression or concentration, indicating extensive transcriptional and metabolic changes in stored roots. These genes and metabolites contributed to a wide range of cellular and molecular functions, with carbohydrate metabolism being the function to which the greatest number of genes and metabolites classified. Because respiration has a central role in postharvest metabolism and is largely responsible for sucrose loss in sugarbeet roots, genes and metabolites involved in and correlated to respiration were identified. Seventy-five genes participating in respiration were differentially expressed during storage, including two bidirectional sugar transporter SWEET17 genes that highly correlated with respiration rate. Weighted gene co-expression network analysis identified 1896 additional genes that positively correlated with respiration rate and predicted a pyruvate kinase gene to be a central regulator or biomarker for respiration rate. Overall, these results reveal the extensive and diverse physiological and metabolic changes that occur in stored sugarbeet roots and identify genes with potential roles as regulators or biomarkers for respiratory sucrose loss.

Keywords: Beta vulgaris; SWEET gene; bidirectional sugar transporter; glycolysis; pyruvate kinase; respiration.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Funding for this research was provided by the U.S. Department of Agriculture, Agricultural Research Service through Project 3060-21000-044-00D. Additional funding was provided by the Beet Sugar Development Foundation under Project 665. Funding for FF was through an appointment to the Agricultural Research Service Research Participation Program administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the U.S. Department of Energy and the U.S. Department of Agriculture.