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

Authors: Fugate, Karen; Eide, John; LAFTA, ABBAS - North Dakota State University; TEHSEEN, MASSUB - North Dakota State University; Chu, Chenggen; KHAN, MOHAMED - North Dakota State University; FINGER, FERNANDO - Universidade Federal De Vicosa

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/15/2024
Publication Date: 1/30/2024
Citation: Fugate, K.K., Eide, J.D., Lafta, A., Tehseen, M., Chu, C.N., Khan, M., Finger, F. 2024. Transcriptomic and metabolomic changes in postharvest sugarbeet roots reveal widespread metabolic changes in storage and identify genes potentially responsible for respiratory sucrose loss. Frontiers in Plant Science. 15. Article 1320705. https://doi.org/10.3389/fpls.2024.1320705.
DOI: https://doi.org/10.3389/fpls.2024.1320705

Interpretive Summary: Harvested sugarbeet roots remain alive and metabolically active until they are frozen for long-term storage or processed into sugar. The metabolism that occurs between harvest and processing is largely responsible for the loss of sucrose and processing quality that occurs during storage, yet information of the internal factors in roots that cause and regulate this metabolism is limited. Research was carried out to identify the genetic elements and metabolic pathways that contribute to and regulate sugarbeet root metabolism by analyzing changes in the genetic elements and molecular compounds present in roots during 120 days of storage under favorable and unfavorable temperature conditions. In total, 8656 genetic elements and 225 molecular compounds changed during storage. A number of these genetic elements and molecular compounds participated in or correlated to root respiration rate. Genetic elements and compounds that associate with root respiration were of particular interest since root respiration is the primary cause of sucrose loss during storage. Quantitative changes in three genetic elements that participate in respiration were found to be closely correlated to changes in root respiration rate, suggesting their possible role in regulating storage respiration rate. Overall, the results of this study reveal the extensive and diverse metabolic changes that occur in stored sugarbeet roots and identify genetic elements with potential roles as regulators or biomarkers for respiration-related sucrose loss during storage.

Technical 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 cellular 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 root 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.