Regulation of starch metabolism: the age of enlightenment?

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Starch and sucrose are the primary products of photosynthesis in the leaves of most plants. Starch represents the major plant storage carbohydrate providing energy during the times of heterotrophic growth. Starch metabolism has been studied extensively, leading to a good knowledge of the numerous enzymes involved. In contrast, understanding of the regulation of starch metabolism is fragmentary. This review summarises briefly the known steps in starch metabolism, highlighting recent discoveries. We also focus on evidence for potential regulatory mechanisms of the enzymes involved. These mechanisms include allosteric regulation by metabolites, redox regulation, protein–protein interactions and reversible protein phosphorylation. Modern systems biology and bioinformatic approaches are uncovering evidence for extensive post-translational protein modifications that may underlie enzyme regulation and identify novel proteins which may be involved in starch metabolism.

Introduction

Starch is the major higher plant storage carbohydrate and is made up of the glucose polymers amylose and amylopectin. Plants use starch as an energy store when they cannot generate enough energy through photosynthesis, such as in leaves during the dark period. Moreover, starch represents a cornerstone for human and animal nutrition and a feedstock for many industrial applications, including bioethanol production. Despite its simple composition, starch forms complex semi-crystalline structures, starch granules, which accumulate in plastids.

Starch metabolism in higher plants involves the concerted and controlled actions of many enzymes including soluble and granule-bound starch synthases (STS and GBS, respectively), branching enzymes (SBE), the debranching enzymes isoamylase and limit dextrinase (ISA and LDA, respectively), α-glucan phosphorylases (PHS), disproportionating enzymes (DPE), α-amylases (AMY) and β-amylases (BAM). In most cases, multiple genes encode different isoforms of each enzyme, which may have slightly different roles depending on plant species and tissue. We illustrated this complex interplay in our model (Figure 1) which summarises previously published concepts (for review see [1, 2, 3, 4, 5, 6]) and includes the concepts discussed in the present review. Despite our present knowledge of the core enzymatic reactions, our understanding of the regulation of the biosynthetic and degradative pathways is far from complete.

Here we focus on recent discoveries of the regulation of starch synthesis and breakdown. We will summarise current evidence for the control of starch metabolism and then discuss mechanisms that were recently suggested to be involved in the regulation of the pathway including reversible starch phosphorylation, redox regulation and protein complex formation initiated by protein phosphorylation.

Section snippets

Evidence for the control of starch metabolism

In plant storage organs, starch synthesis and degradation can be developmentally separated (e.g. in the developing and germinating cereal grain). In other tissues, such as leaves, or in unicellular algae, these processes happen on a diurnal basis and in a regulated manner. The amount of photoassimilate partitioned into leaf starch varies between plant species. Whilst in some plants, like Arabidopsis, it is the major storage form [7, 8, 9], others accumulate sucrose [7, 10], raffinose-family

Reversible glucan phosphorylation

It has recently been shown that reversible phosphorylation of the starch granule is essential for its subsequent degradation ([21, 22, 23, 24••], reviewed in [2, 3, 5, 6]). Within starch granules, glucan chains of the amylopectin fraction form double helices which pack to form crystalline lamellae. It is thought that during starch degradation, the lamellae and the double helices at the granule surface become disrupted by the addition of phosphate groups at the C6-position and C3-position of

Redox regulation

The activities of several enzymes involved in starch metabolism have been demonstrated to be affected by reducing or oxidising conditions, indicating that they may be regulated by the redox potential of the plastid stroma [35, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50•]. A summary of the knowledge gained from these studies is shown in Table 1. Much research in this area has focused on the control of ADP-glucose pyrophosphorylase (AGPase), because this is the first enzyme on the committed pathway

Protein complex formation and protein phosphorylation

The roles of the many proteins known to be involved in synthesising and degrading starch have often been considered in isolation. A recent paper, however, has demonstrated that two STS isoforms in Arabidopsis are probably responsible for initiating starch granule synthesis as when both are mutated starch synthesis is eliminated [55••], when a double mutant lacking two SBE isoforms was produced starch accumulation was also eliminated [56]. To understand starch metabolism fully, therefore, the

Conclusions

In this review we have examined recent advances in our understanding of the regulation of starch metabolism. These data are beginning to enlighten us, but much still needs to be understood. For example, it is unclear for many of the mechanisms discussed whether they play a role in vivo, so more work is needed to confirm their significance. If these mechanisms do play a role, then they have to be integrated with variables known to influence starch metabolism, such as sugar supply.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors would like to acknowledge the funding from the Swiss-South African Joint Research Programme 08 IZ LS Z3122916 and the ETH Zurich. We also thank Martin Umhang (ETH Zurich) for providing unpublished data.

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