Cold-Triggered Induction of ROS- and Raffinose Metabolism in Freezing-Sensitive Taproot Tissue of Sugar Beet

Abstract

Sugar beet (Beta vulgaris subsp. vulgaris) is the exclusive source of sugar in the form of sucrose in temperate climate zones. Sugar beet is grown there as an annual crop from spring to autumn because of the damaging effect of freezing temperatures to taproot tissue. A collection of hybrid and non-hybrid sugar beet cultivars was tested for winter survival rates and freezing tolerance. Three genotypes with either low or high winter survival rates were selected for detailed study of their response to frost. These genotypes differed in the severity of frost injury in a defined inner region in the upper part of the taproot, the so-called pith. We aimed to elucidate genotype- and tissue-dependent molecular processes during freezing and combined analyses of sugar beet anatomy and physiology with transcriptomic and metabolite profiles of leaf and taproot tissues at low temperatures. Freezing temperatures induced strong downregulation of photosynthesis in leaves, generation of reactive oxygen species (ROS), and ROS-related gene expression in taproots. Simultaneously, expression of genes involved in raffinose metabolism, as well as concentrations of raffinose and its intermediates, increased markedly in both leaf and taproot tissue at low temperatures. The accumulation of raffinose in the pith tissue correlated with freezing tolerance of the three genotypes. We discuss a protective role for raffinose and its precursors against freezing damage of sugar beet taproot tissue.

An Insight into the Abiotic Stress Responses of Cultivated Beets (Beta vulgaris L.)

“…Alkaline stress WRKY transcription factor family (WRKY10 and 16) [35] Alkaline stress Metal Tolerance Protein 11 (MTP11) [36] Alkaline stress Ethylene-insensitive protein 2 (EIN2) [36] Alkaline stress Polyphenol Oxidase (PPO) [36] Cold stress Integral membrane protein (IMP) [37] Cold stress A novel ER-located aquaporin gene (COLD1) [38] Cold stress Raffinose synthase 1 and 2 (RS1 and RS2) [39] Freezing Galactinol synthase 2 and 3 (GOLS2 and GOLS3) Raffinose synthase 2 and 5 (RS2 and RS5) [40] Heavy metal Metal tolerance protein (BmMTP10 and BmMTP11) [41] Heavy metal Toxic nickel concentration (NIC3, NIC6 and NIC8) [42] Heavy metal Natural resistance-associated macrophage protein 3 (NRAMP3) [43] 2.1. Alkaline Stress Alkaline stress (high pH) is one of the abiotic constraints of plants, which co-exists with salt stress and elicits severe detrimental damages to global agricultural production [44].…”

“…Nevertheless, prolonged exposure of sugar beets at the young seedling stage to extreme cold temperatures seriously limits the yield [ 75 ]. Cold-treated sugar beet plants displayed a decrease in photosynthetic efficiency, quantum yield of PSII, leaf CO 2 concentration, CO 2 assimilation rate, and leaf transpiration rate [ 40 , 80 ]. Moreover, compatible solutes such as glucose, fructose, and raffinose in leaves were increased by 0 °C and 4 °C cold treatments [ 40 , 80 ], but decreased in taproots in response to freezing temperature [ 40 ].…”

“…Cold-treated sugar beet plants displayed a decrease in photosynthetic efficiency, quantum yield of PSII, leaf CO 2 concentration, CO 2 assimilation rate, and leaf transpiration rate [ 40 , 80 ]. Moreover, compatible solutes such as glucose, fructose, and raffinose in leaves were increased by 0 °C and 4 °C cold treatments [ 40 , 80 ], but decreased in taproots in response to freezing temperature [ 40 ]. Consistently, under freezing conditions, the sucrose content decreased in roots, followed by leakage of the root sap due to cell alteration in membrane permeability and infection with microbes.…”

“…In a very recent work, three sugar beet genotypes (GT1, GT2, and GT3) were evaluated for freezing tolerance. Freezing temperatures caused the production of ROS, raffinose accumulation, and transcription of genes involved in raffinose metabolism in leaves and taproots [ 40 ]. These results suggest that raffinose metabolism has a protective role against freezing injury in sugar beet.…”

“…These results suggest that raffinose metabolism has a protective role against freezing injury in sugar beet. Moreover, ROS-scavenging enzymes including SOD and CAT significantly enhanced in response to 4 °C [ 40 ]. Consistently, the maximum expression levels of genes encoding antioxidant enzymes such as CAT, APX, ascorbate reductase, and glutathione peroxidase (GPX) were seen at 4 °C, but the expression was reduced at 0 °C.…”