Background: As an agricultural source of sugar that can be grown in temperate climate zones, sugar beet (Beta vulgaris) represents a crop of remarkable economic importance. Sugar beet taproots can accumulate up to 20% of their fresh weight as sucrose during vegetative growth, and can weigh up to 1 kg or more. Although extension of the sucrose storage phase would result in significantly increased yield, frost sensitivity of the taproot tissue prevents biennial, overwinter cultivation.

Questions: What is molecular basis of the cold response of sugar beet? What are the key factors critical for achieving frost tolerance? Findings: To answer these questions, we conducted proteomics, transcriptomics, photosynthetic and metabolic analyses of different sugar beet genotypes at different temperatures. We discovered that at a temperature of 4°C, sugars accumulated dramatically in shoots of sugar beets although photosynthetic capacity diminished nearly completely. Furthermore, we recorded a back-transport of taproot sugars towards the shoot in the cold.  

We were able to identify the sugar beet tap-root sugar loader TST2.1 on the molecular and functional level (Jung et al., 2015). Now we raised evidence that sugar back-transport may be due to downregulation of the taproot-specific vacuolar sucrose importer (TST2;1) accompanied by upregulation of the vacuolar exporter (SUT4), leading to a concerted remobilization of sugars previously stored in the taproot (Martins Rodrigues et al., 2020). Our results comparing leaves and taproots suggest that source and sink identities might be switched in the cold. To test this hypothesis, we used both radiolabeled sucrose and fluorescent sucrose analogues to trace sugar fluxes. Surprisingly, we found that a cold-induced reversal of the phloem stream direction occurs in sugar beet plants. Interestingly, this process might also be required for an adequate vernalization (cold-induced flowering) and therefore for floral competence.

Next steps: Integration of these findings with previous knowledge about the role of sugars during cold now allows us to identify candidate factors for functional gene editing. We anticipate that this will lead to decreased leakage of sugar from young sugar beet taproots, with the ultimate aim of improving sugar beet cold hardiness. In addition, our research will focus on an area in the upper part of the taproot, the so-called pith, which shows the most severe damages after freezing treatment. We try to answer questions about the function and role of this tissue, especially under freezing conditions. 

Figure:Cold-Induced Sink-to-Source Transition. Despite decreased photosynthesis (exemplified by RubisCO) and increased respiration, both, the biomass and the sugar content of sugar beet leaves increase in the cold. Concomitantly lower sucrose levels in tap roots, flanked by increased sugar synthesis (+ SPS), and lowered respiratory sugar consumption degradation (- SUSY) suggests a reversal of sugar flux allowing the tap root to provide sugars to leaves. The remobilization of the root-derived sugar is mediated by downregulation of the vacuolar loader (TST2;1) and upregulation of the sucrose unloader (SUT4). RubisCO: Ribulose-1,5-Bisphosphat-Carboxylase/-Oxygenase, SPS: Sucrose-Phosphate Synthase; SUSY: Sucrose Synthase; TST2;1: Tonoplast Sugar Transporter 2;1; SUT4: Sucrose Transporter 4. Created with BioRender.com 

Jung B, Ludewig F, Schulz A, Meißner G, Wöstefeld N, Flügge UI, Pommerrenig B, Wirsching P, Sauer N, Koch W, Sommer F, Mühlhaus T, Schroda M, Cuin TA, Graus D, Marten I, Hedrich R, Neuhaus HE (2015) Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nat.Plants. 1, 14001 doi:10.1038/nplants.2014.1 

Martins Rodrigues C, Müdsam C, Keller I, Zierer W, Czarnecki O, Corral JM, Reinhardt F, Nieberl P, Fiedler-Wiechers K, Sommer F, Schroda M, Mühlhaus T, Harms K, Flügge UI, Sonnewald U, Koch W, Ludewig F, Neuhaus HE, Pommerrenig B (2020) Vernalization alters sink and source identities and reverses phloem translocation from taproots to shoots in sugar beet (Beta vulgaris). Plant Cell. 32, 3206-3223 doi: 10.1105/tpc.20.00072