Limits...
Multifunctional fructans and raffinose family oligosaccharides.

Van den Ende W - Front Plant Sci (2013)

Bottom Line: Here, two novel emerging roles are highlighted.Second, it is hypothesized that small fructans and RFOs act as phloem-mobile signaling compounds under stress.It is speculated that such underlying antioxidant and oligosaccharide signaling mechanisms contribute to disease prevention in plants as well as in animals and in humans.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Plant Biology, KU Leuven Leuven, Belgium.

ABSTRACT
Fructans and raffinose family oligosaccharides (RFOs) are the two most important classes of water-soluble carbohydrates in plants. Recent progress is summarized on their metabolism (and regulation) and on their functions in plants and in food (prebiotics, antioxidants). Interest has shifted from the classic inulin-type fructans to more complex fructans. Similarly, alternative RFOs were discovered next to the classic RFOs. Considerable progress has been made in the understanding of structure-function relationships among different kinds of plant fructan metabolizing enzymes. This helps to understand their evolution from (invertase) ancestors, and the evolution and role of so-called "defective invertases." Both fructans and RFOs can act as reserve carbohydrates, membrane stabilizers and stress tolerance mediators. Fructan metabolism can also play a role in osmoregulation (e.g., flower opening) and source-sink relationships. Here, two novel emerging roles are highlighted. First, fructans and RFOs may contribute to overall cellular reactive oxygen species (ROS) homeostasis by specific ROS scavenging processes in the vicinity of organellar membranes (e.g., vacuole, chloroplasts). Second, it is hypothesized that small fructans and RFOs act as phloem-mobile signaling compounds under stress. It is speculated that such underlying antioxidant and oligosaccharide signaling mechanisms contribute to disease prevention in plants as well as in animals and in humans.

No MeSH data available.


Fructan diversity and polyphyletic origin of fructan biosynthesis in higher plants. An unrooted phylogenetic tree of fructan initiator enzymes (1-SSTs and a pFT) derived from six well-known fructan accumulators (chicory, wheat, ryegrass, onion, Agave, and Pachysandra) is drawn to illustrate the polyphyletic origin of fructan biosynthesis in higher plants.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3713406&req=5

Figure 1: Fructan diversity and polyphyletic origin of fructan biosynthesis in higher plants. An unrooted phylogenetic tree of fructan initiator enzymes (1-SSTs and a pFT) derived from six well-known fructan accumulators (chicory, wheat, ryegrass, onion, Agave, and Pachysandra) is drawn to illustrate the polyphyletic origin of fructan biosynthesis in higher plants.

Mentions: Within GH32, it became clear that plant FTs evolved from VIs (Wei and Chatterton, 2001; Altenbach et al., 2009), contributing to the observed diversity in fructan accumulators in the plant kingdom (Figure 1). Two types of VIs (I and II, Van den Ende et al., 2002b) can be discerned in plants and for a long time it was assumed that all plant FTs evolved from (different forms of) type II VIs. This occurred at least three times: (i) in the Asterales (inulin-type of fructans; e.g., chicory, (ii) in the Poales with further distinction between cool-season grasses (mainly levan and neokestose-derived fructans, e.g., ryegrass) and cereals (predominantly graminan-type fructans, e.g., wheat and barley) in the Poaceae and (iii) in the Asparagales further splitting into the Allioideae (e.g., onion) and Agavoideae (e.g., Agave) subfamilies that also mainly accumulate neokestose-based fructans (Figure 1). However, this view was changed by the unexpected discovery of both levan- and graminan-type fructans in the basal eudicot Pachysandra terminalis species, containing a pFT that, surprisingly, evolved from a type I VI (Figure 2) and not from a type II VI as observed for all other FTs (Figure 2). This further confirmed the polyphyletic origin of fructan biosynthesis (Altenbach et al., 2009; Van den Ende et al., 2011a) and suggests that the capacity for fructan biosynthesis arose at least four times during the plant diversification process (Figure 1). Such polyphyletic origin did not likely occur within GH27 and GH36, although more sequences should be generated to reach this conclusion (Vanhaecke, 2010). By combining alignments, 3D structure information and phylogenetic analyses (Schroeven et al., 2008; Altenbach et al., 2009; Lasseur et al., 2011; Lammens et al., 2012), the current view within GH32 is that an ancestral VI duplicated in two VI types (I and II, Figure 2) before the separation of monocots and dicots (Wei and Chatterton, 2001). Most probably, monocot and dicot type II VIs were than recruited to create preliminary 1-SSTs and 6-SFTs that later specialized into genuine 1-SSTs and 6-SFTs (Figure 2). Mutations in the “WMNDPNG” and “W(A/G)W” motifs are believed to play a key role in such processes (Schroeven et al., 2008, 2009; Altenbach et al., 2009). In evolutionary terms, it seems reasonable to assume that, in monocots as well as in dicots, 1-FFTs and 6G-FFTs evolved later, likely from (premature) 1-SST precursors (Figure 2). For instance, in wheat the identity between Ta1-SST and Ta1-FFT is much higher (84%) than between Ta1-SST and TaVI (67%) and between Ta1-FFT and TaVI (66%), strongly suggesting that Ta1-FFT evolved from Ta1-SST (Figure 2; Schroeven et al., 2009). A similar reasoning led to the hypothesis that the Lolium perenne Lp6G-FFT evolved from a (premature) Lp1-SST (Figure 2; Lasseur et al., 2009). In the same way, it can be speculated that the chicory Ci1-FFT evolved from a (premature) Ci1-SST (Figure 2; Schroeven et al., 2009). Within the basal eudicots, a type I VI developed into a pFT in Pachysandra terminalis (Figure 2) and this is considered as a rather “recent” evolutionary event (Van den Ende et al., 2011a). On the contrary, defective invertases and FEHs evolved from CWIs within GH32 (Le Roy et al., 2007, 2013). It can be speculated that the loss or alteration of the above-mentioned “couple” is an early evolutionary event that led to the formation of defective invertases with cell wall localization and a high iso-electric point (pI) for interaction with the cell wall. To further develop genuine FEHs in fructan plants, it can be further hypothesized that precursor defective invertases retrieved (i) a vacuolar targeting signal for sorting to the central vacuole, (ii) a low pI typical for vacuolar proteins, (iii) amino acid alterations that helped stabilization of higher DP fructans as donor substrates (Le Roy et al., 2008).


Multifunctional fructans and raffinose family oligosaccharides.

Van den Ende W - Front Plant Sci (2013)

Fructan diversity and polyphyletic origin of fructan biosynthesis in higher plants. An unrooted phylogenetic tree of fructan initiator enzymes (1-SSTs and a pFT) derived from six well-known fructan accumulators (chicory, wheat, ryegrass, onion, Agave, and Pachysandra) is drawn to illustrate the polyphyletic origin of fructan biosynthesis in higher plants.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3713406&req=5

Figure 1: Fructan diversity and polyphyletic origin of fructan biosynthesis in higher plants. An unrooted phylogenetic tree of fructan initiator enzymes (1-SSTs and a pFT) derived from six well-known fructan accumulators (chicory, wheat, ryegrass, onion, Agave, and Pachysandra) is drawn to illustrate the polyphyletic origin of fructan biosynthesis in higher plants.
Mentions: Within GH32, it became clear that plant FTs evolved from VIs (Wei and Chatterton, 2001; Altenbach et al., 2009), contributing to the observed diversity in fructan accumulators in the plant kingdom (Figure 1). Two types of VIs (I and II, Van den Ende et al., 2002b) can be discerned in plants and for a long time it was assumed that all plant FTs evolved from (different forms of) type II VIs. This occurred at least three times: (i) in the Asterales (inulin-type of fructans; e.g., chicory, (ii) in the Poales with further distinction between cool-season grasses (mainly levan and neokestose-derived fructans, e.g., ryegrass) and cereals (predominantly graminan-type fructans, e.g., wheat and barley) in the Poaceae and (iii) in the Asparagales further splitting into the Allioideae (e.g., onion) and Agavoideae (e.g., Agave) subfamilies that also mainly accumulate neokestose-based fructans (Figure 1). However, this view was changed by the unexpected discovery of both levan- and graminan-type fructans in the basal eudicot Pachysandra terminalis species, containing a pFT that, surprisingly, evolved from a type I VI (Figure 2) and not from a type II VI as observed for all other FTs (Figure 2). This further confirmed the polyphyletic origin of fructan biosynthesis (Altenbach et al., 2009; Van den Ende et al., 2011a) and suggests that the capacity for fructan biosynthesis arose at least four times during the plant diversification process (Figure 1). Such polyphyletic origin did not likely occur within GH27 and GH36, although more sequences should be generated to reach this conclusion (Vanhaecke, 2010). By combining alignments, 3D structure information and phylogenetic analyses (Schroeven et al., 2008; Altenbach et al., 2009; Lasseur et al., 2011; Lammens et al., 2012), the current view within GH32 is that an ancestral VI duplicated in two VI types (I and II, Figure 2) before the separation of monocots and dicots (Wei and Chatterton, 2001). Most probably, monocot and dicot type II VIs were than recruited to create preliminary 1-SSTs and 6-SFTs that later specialized into genuine 1-SSTs and 6-SFTs (Figure 2). Mutations in the “WMNDPNG” and “W(A/G)W” motifs are believed to play a key role in such processes (Schroeven et al., 2008, 2009; Altenbach et al., 2009). In evolutionary terms, it seems reasonable to assume that, in monocots as well as in dicots, 1-FFTs and 6G-FFTs evolved later, likely from (premature) 1-SST precursors (Figure 2). For instance, in wheat the identity between Ta1-SST and Ta1-FFT is much higher (84%) than between Ta1-SST and TaVI (67%) and between Ta1-FFT and TaVI (66%), strongly suggesting that Ta1-FFT evolved from Ta1-SST (Figure 2; Schroeven et al., 2009). A similar reasoning led to the hypothesis that the Lolium perenne Lp6G-FFT evolved from a (premature) Lp1-SST (Figure 2; Lasseur et al., 2009). In the same way, it can be speculated that the chicory Ci1-FFT evolved from a (premature) Ci1-SST (Figure 2; Schroeven et al., 2009). Within the basal eudicots, a type I VI developed into a pFT in Pachysandra terminalis (Figure 2) and this is considered as a rather “recent” evolutionary event (Van den Ende et al., 2011a). On the contrary, defective invertases and FEHs evolved from CWIs within GH32 (Le Roy et al., 2007, 2013). It can be speculated that the loss or alteration of the above-mentioned “couple” is an early evolutionary event that led to the formation of defective invertases with cell wall localization and a high iso-electric point (pI) for interaction with the cell wall. To further develop genuine FEHs in fructan plants, it can be further hypothesized that precursor defective invertases retrieved (i) a vacuolar targeting signal for sorting to the central vacuole, (ii) a low pI typical for vacuolar proteins, (iii) amino acid alterations that helped stabilization of higher DP fructans as donor substrates (Le Roy et al., 2008).

Bottom Line: Here, two novel emerging roles are highlighted.Second, it is hypothesized that small fructans and RFOs act as phloem-mobile signaling compounds under stress.It is speculated that such underlying antioxidant and oligosaccharide signaling mechanisms contribute to disease prevention in plants as well as in animals and in humans.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Plant Biology, KU Leuven Leuven, Belgium.

ABSTRACT
Fructans and raffinose family oligosaccharides (RFOs) are the two most important classes of water-soluble carbohydrates in plants. Recent progress is summarized on their metabolism (and regulation) and on their functions in plants and in food (prebiotics, antioxidants). Interest has shifted from the classic inulin-type fructans to more complex fructans. Similarly, alternative RFOs were discovered next to the classic RFOs. Considerable progress has been made in the understanding of structure-function relationships among different kinds of plant fructan metabolizing enzymes. This helps to understand their evolution from (invertase) ancestors, and the evolution and role of so-called "defective invertases." Both fructans and RFOs can act as reserve carbohydrates, membrane stabilizers and stress tolerance mediators. Fructan metabolism can also play a role in osmoregulation (e.g., flower opening) and source-sink relationships. Here, two novel emerging roles are highlighted. First, fructans and RFOs may contribute to overall cellular reactive oxygen species (ROS) homeostasis by specific ROS scavenging processes in the vicinity of organellar membranes (e.g., vacuole, chloroplasts). Second, it is hypothesized that small fructans and RFOs act as phloem-mobile signaling compounds under stress. It is speculated that such underlying antioxidant and oligosaccharide signaling mechanisms contribute to disease prevention in plants as well as in animals and in humans.

No MeSH data available.