Spatiotemporal Dynamics of Oligofructan Metabolism and Suggested Functions in Developing Cereal Grains

Abstract

Oligofructans represent one of the most important groups of sucrose-derived water-soluble carbohydrates in the plant kingdom. In cereals, oligofructans accumulate in above ground parts of the plants (stems, leaves, seeds) and their biosynthesis leads to the formation of both types of glycosidic linkages [β(2,1); β(2,6)-fructans] or mixed patterns. In recent studies, tissue- and development- specific distribution patterns of the various oligofructan types in cereal grains have been shown, which are possibly related to the different phases of grain development, such as cellular differentiation of grain tissues and storage product accumulation. Here, we summarize the current knowledge about oligofructan biosynthesis and accumulation kinetics in cereal grains. We focus on the spatiotemporal dynamics and regulation of oligofructan biosynthesis and accumulation in developing barley grains (deduced from a combination of metabolite, transcript and proteome analyses). Finally, putative physiological functions of oligofructans in developing grains are discussed.

Keywords: antioxidant; cereals; grain development; oligofructan; spatial distribution; stress response.

FIGURE 1

Representation of the various fructan-types and suggested biosynthesis routes in developing barley grain tissues. A spatiotemporally specific coordinated biosynthesis of oligofructans has been observed for barley grains. The pathway in blue illustrates the major route of biosynthesis during the prestorage phase and red indicates the major route during the storage phase. During the prestorage phase a high transcript level for 1-SST and 6-SFT was observed for the endosperm leading to an accumulation of 6-kestose and bifurcose (indicated in blue). With transition to the storage phase a transcriptional switch was observed resulting in high transcript levels of 1-SST in the nucellar projection (NP). 1-FFT was found to be exclusively expressed in the NP during the storage phase. Induction of the inulin-type oligofructan biosynthesis pathway led to high amounts of 1-kestose and nystose accumulated in the endosperm cavity (indicated in red). Oligofructans of the neo-series were not detected in developing barley grains. Abbreviations are: 1-FFT, fructan:fructan 1-fructosyltransferase; 1-SST, sucrose:sucrose 1-fructosyl-transferase; 6-SFT, sucrose:fructan 6-fructosyltransferase; 6G-FFT, fructan:fructan 6G-fructosyltransferase.

FIGURE 2

Sugar contents in developing barley grains. (A) Accumulation patterns of oligosaccharides during barley grain development as observed by MALDI MSI. The top panel shows histological images illustrating the various developmental stages which were analyzed. The following panels show the ion intensity maps of the disaccharide (m/z of 381), the trisaccharide (m/z 543), the tetrasaccharides (m/z 705), the pentasaccharide (m/z 867), the hexasaccharide (m/z 1029), and the heptasaccharide (m/z 1191). Specific accumulation of the tri- and tetrasaccharides in and around the nascent endosperm cavity was observed from 10 DAP onwards. The penta-, hexa, and heptasaccharides, which accumulated in the pericarp during the prestorage phase (three DAP), moved to the endosperm at the beginning of the storage phase (from 10 DAP onwards). Bars = 1 mm. The images represent a reprint of Figure 2 and Supplemental Figure S2 from Peukert et al. (2014). (B) Quantities of sugars in total grains (μmol/g fresh weight). Hexoses (glucose and fructose) and sucrose decreased from 7 DAP until 20 DAP whereas maltose strongly increased (left diagram). For the oligofructans 6-kestose and bifurcose [both containing β(2,6)-linkages] a steep decline during the storage phase was observed. For the inulin-type oligofructans, 1-kestose and nystose, less pronounced changes were observed in the whole grain. Sugar quantities are graphically presented according to the data from Supplemental Table S1 of Peukert et al. (2014) (www.plantcell.org). Copyright American Society of Plant Biologists.

FIGURE 3

The proposed functions of oligofructans during barley grain development. Conversion of sucrose into oligofructans during the prestorage phase is supposed to maintain a high glucose to sucrose ratio in the developing endosperm and thus preventing premature differentiation into storage cells. During the storage phase inulin-type oligofructans accumulate in the transport tissues presumably protecting transport active cells from ROS-inflicted oxidative damage by sequestration into their plasma membranes. The black bars indicate the hypothesized insertion of oligofructans between the head groups of membrane phospholipids.