Abstract
Controlled conversion of leaf starch to sucrose at night is essential for the normal growth of Arabidopsis. The conversion involves the cytosolic metabolism of maltose to hexose phosphates via an unusual, multidomain protein with 4-glucanotransferase activity, DPE2, believed to transfer glucosyl moieties to a complex heteroglycan prior to their conversion to hexose phosphate via a cytosolic phosphorylase. The significance of this complex pathway is unclear; conversion of maltose to hexose phosphate in bacteria proceeds via a more typical 4-glucanotransferase that does not require a heteroglycan acceptor. It has recently been suggested that DPE2 generates a heterogeneous series of terminal glucan chains on the heteroglycan that acts as a glucosyl buffer to ensure a constant rate of sucrose synthesis in the leaf at night. Alternatively, DPE2 and/or the heteroglycan may have specific properties important for their function in the plant. To distinguish between these ideas, we compared the properties of DPE2 with those of the Escherichia coli glucanotransferase MalQ. We found that MalQ cannot use the plant heteroglycan as an acceptor for glucosyl transfer. However, experimental and modeling approaches suggested that it can potentially generate a glucosyl buffer between maltose and hexose phosphate because, unlike DPE2, it can generate polydisperse malto-oligosaccharides from maltose. Consistent with this suggestion, MalQ is capable of restoring an essentially wild-type phenotype when expressed in mutant Arabidopsis plants lacking DPE2. In light of these findings, we discuss the possible evolutionary origins of the complex DPE2-heteroglycan pathway.
| Original language | English |
|---|---|
| Pages (from-to) | 28581-28598 |
| Number of pages | 18 |
| Journal | The Journal of Biological Chemistry |
| Volume | 288 |
| Issue number | 40 |
| Early online date | 15 Aug 2013 |
| DOIs | |
| Publication status | Published - 4 Oct 2013 |
Keywords
- carbohydrate metabolism
- computer modeling
- metabolic regulation
- oligosaccharide
- plant biochemistry
- glucanotransferase
- leaf cell
- maltose metabolism
- starch degradation
- PHO-2 phosphorylase isozyme
- Escherichia-coli
- cytosolic heteroglycans
- disproportionating enzyme
- subcellular-localization
- arabidopsis-thaliana
- plant
- amylomaltase
- degradation
- microarrays
Cite this
A bacterial glucanotransferase can replace the complex maltose metabolism required for starch to sucrose conversion in leaves at night. / Ruzanski, Christian; Smirnova, Julia; Rejzek, Martin; Cockburn, Darrell; Pedersen, Henriette L; Pike, Marilyn; Willats, William G T; Svensson, Birte; Steup, Martin; Ebenhoeh, Oliver; Smith, Alison M; Field, Robert A.
In: The Journal of Biological Chemistry, Vol. 288, No. 40, 04.10.2013, p. 28581-28598.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - A bacterial glucanotransferase can replace the complex maltose metabolism required for starch to sucrose conversion in leaves at night
AU - Ruzanski, Christian
AU - Smirnova, Julia
AU - Rejzek, Martin
AU - Cockburn, Darrell
AU - Pedersen, Henriette L
AU - Pike, Marilyn
AU - Willats, William G T
AU - Svensson, Birte
AU - Steup, Martin
AU - Ebenhoeh, Oliver
AU - Smith, Alison M
AU - Field, Robert A
PY - 2013/10/4
Y1 - 2013/10/4
N2 - Controlled conversion of leaf starch to sucrose at night is essential for the normal growth of Arabidopsis. The conversion involves the cytosolic metabolism of maltose to hexose phosphates via an unusual, multidomain protein with 4-glucanotransferase activity, DPE2, believed to transfer glucosyl moieties to a complex heteroglycan prior to their conversion to hexose phosphate via a cytosolic phosphorylase. The significance of this complex pathway is unclear; conversion of maltose to hexose phosphate in bacteria proceeds via a more typical 4-glucanotransferase that does not require a heteroglycan acceptor. It has recently been suggested that DPE2 generates a heterogeneous series of terminal glucan chains on the heteroglycan that acts as a glucosyl buffer to ensure a constant rate of sucrose synthesis in the leaf at night. Alternatively, DPE2 and/or the heteroglycan may have specific properties important for their function in the plant. To distinguish between these ideas, we compared the properties of DPE2 with those of the Escherichia coli glucanotransferase MalQ. We found that MalQ cannot use the plant heteroglycan as an acceptor for glucosyl transfer. However, experimental and modeling approaches suggested that it can potentially generate a glucosyl buffer between maltose and hexose phosphate because, unlike DPE2, it can generate polydisperse malto-oligosaccharides from maltose. Consistent with this suggestion, MalQ is capable of restoring an essentially wild-type phenotype when expressed in mutant Arabidopsis plants lacking DPE2. In light of these findings, we discuss the possible evolutionary origins of the complex DPE2-heteroglycan pathway.
AB - Controlled conversion of leaf starch to sucrose at night is essential for the normal growth of Arabidopsis. The conversion involves the cytosolic metabolism of maltose to hexose phosphates via an unusual, multidomain protein with 4-glucanotransferase activity, DPE2, believed to transfer glucosyl moieties to a complex heteroglycan prior to their conversion to hexose phosphate via a cytosolic phosphorylase. The significance of this complex pathway is unclear; conversion of maltose to hexose phosphate in bacteria proceeds via a more typical 4-glucanotransferase that does not require a heteroglycan acceptor. It has recently been suggested that DPE2 generates a heterogeneous series of terminal glucan chains on the heteroglycan that acts as a glucosyl buffer to ensure a constant rate of sucrose synthesis in the leaf at night. Alternatively, DPE2 and/or the heteroglycan may have specific properties important for their function in the plant. To distinguish between these ideas, we compared the properties of DPE2 with those of the Escherichia coli glucanotransferase MalQ. We found that MalQ cannot use the plant heteroglycan as an acceptor for glucosyl transfer. However, experimental and modeling approaches suggested that it can potentially generate a glucosyl buffer between maltose and hexose phosphate because, unlike DPE2, it can generate polydisperse malto-oligosaccharides from maltose. Consistent with this suggestion, MalQ is capable of restoring an essentially wild-type phenotype when expressed in mutant Arabidopsis plants lacking DPE2. In light of these findings, we discuss the possible evolutionary origins of the complex DPE2-heteroglycan pathway.
KW - carbohydrate metabolism
KW - computer modeling
KW - metabolic regulation
KW - oligosaccharide
KW - plant biochemistry
KW - glucanotransferase
KW - leaf cell
KW - maltose metabolism
KW - starch degradation
KW - PHO-2 phosphorylase isozyme
KW - Escherichia-coli
KW - cytosolic heteroglycans
KW - disproportionating enzyme
KW - subcellular-localization
KW - arabidopsis-thaliana
KW - plant
KW - amylomaltase
KW - degradation
KW - microarrays
U2 - 10.1074/jbc.M113.497867
DO - 10.1074/jbc.M113.497867
M3 - Article
VL - 288
SP - 28581
EP - 28598
JO - The Journal of Biological Chemistry
JF - The Journal of Biological Chemistry
SN - 0021-9258
IS - 40
ER -