Energy from the sun and carbon dioxide fuel photosynthesis in plants
and algae, making life on earth possible. Carbon that is fixed by
plants is converted to starch and sucrose, which are utilized by plants
for energy and to build biomass. Human evolution and society have been
intimately tied to our exploitation of plant biomass for food, fuel,
tools, and shelter.
However, to be usable, the starch carbohydrate stored in plants must
be broken down to component sugars. Some aspects of starch metabolism
have been known for many years, but regulation of the process and exact
physical mechanisms are still not well understood.
With new information emerging from genome sequencing and mutational
analyses, we are beginning to gain a better understanding of these
complex and finely tuned processes. Such knowledge is especially
critical as we struggle with issues of energy and food supply.
Some of the new molecular mechanisms and regulatory components in
starch metabolism have been identified by Dr. Samuel Zeeman and his
colleagues. Dr. Zeeman, of the Institute of Plant Sciences, ETH Zurich,
in Switzerland, who is the 2007 recipient of the Charles Albert Shull
Award, will be presenting this work at the opening Awards Symposium of
the annual meeting of the American Society of Plant Biologists in
Mérida, Mexico (June 27, 2:30 PM). Mutational and structural analyses
by Dr. Zeeman and his colleagues have revealed that starch degradation
in Arabidopsis leaves at night differs significantly from the versions
traditionally described in textbooks. Specifically, mutations at the
Starch Excess 4 (SEX4), Maltose Excess 1 (MEX1) and other loci produce
plants unable to metabolize starch to a usable form.
When we use starch in the lab or cook with it, we tend to think of
it as an amorphous mass, but it is really a complex, ordered substance.
Starch consists of two polysaccharides (polymers of the simple sugar
glucose)–amylopectin and amylose. Both are long chains of connected
glucose molecules, but amylopectin is also highly branched and forms a
tree-like structure. The branches are then packed so that double
helices can form between the chains, which are arranged into concentric
layers forming semi-crystalline starch granules. This exquisite
structure is extremely stable to enzyme activity and can thus be stored
by the plant for later use. However, when needed, starch must be broken
down to its component sugars for export to the rest of the plant. It
appears that a number of proteins are major players –debranching
enzymes, glucanotransferases and amylases, among others– and that in
leaves, their actions are finely tuned to the diurnal changes in
photosynthesis and the circadian rhythms of the plant.
Some of the new proteins that have been identified by Dr. Zeeman and
other researchers in the field act as glucan kinases and phosphatases,
that is, they place and remove phosphate groups on the starch
molecules. Among these proteins are glucan water dikinase (GWD),
phosphoglucan water dikinase (PWD) and SEX4. It is thought that GWD and
PWD act in concert to place phosphate groups on starch molecules. The
highly charged phosphate group may act as a wedge, disrupting the
semi-crystalline packing in the starch and allowing degradative enzymes
access to the glucose chains and branches. SEX4 then removes the
phosphate groups. Although the exact mechanisms of how these proteins
coordinate starch metabolism are still unknown, the importance of
phosphate groups in the process is now well established. Mutants of all
of these proteins result in plants with an excess of undigested starch.
Sequencing analyses have shown that GWD is conserved over many plant
taxa, and proteins similar to SEX4 have been found in other plant
species, including rice, maize, and tomato. The amylopectins of leaf
starches in different plant species have also been found to be
decorated with phosphate groups. Studies of Arabidopsis and potato
leaves suggest a common mechanism for starch breakdown, although
different pathways may operate in other plants. Further research is
needed to establish conservation of the process as well as the proteins
in the plant kingdom.
Elements of the newly-discovered mechanism of starch breakdown may
also be conserved across kingdoms. Amylopectin has similarities to
glycogen, the soluble storage carbohydrate accumulated in animals,
fungi, and bacteria. The SEX4 phosphatase is related to laforin, a
protein involved in animal glycogen metabolism. When laforin is
missing, insoluble starch-like polyglucosans (Lafora bodies)
accumulate, which results in neuronal dysfunction, severe epilepsy, and
death. The similarities between the animal and plant processes suggest
common regulatory mechanisms, which may be the result of evolutionary
convergence or conservation.
Understanding the molecular mechanisms of starch metabolism has
direct implications for genetic engineering of plants for biofuels such
as ethanol. It could also be important in adjusting the balance of
protein and carbohydrate in plants needed to feed a growing global
American Society of Plant Biologists. June 2008.