Is There an Alternative Pathway for Starch Synthesis?'

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Is There an Alternative Pathway for Starch Synthesis?' Plant Physiol. (1992) 100, 560-564 Received for publication February 18, 1992 0032-0889/92/1 00/0560/05/$01 .00/0 Accepted May 15, 1992 Is There an Alternative Pathway for Starch Synthesis?' Thomas W. Okita Institute of Biological Chemistry, Washington State University, Pullman, Washington ABSTRACT 15, 17), indicating that the basic enzymology of starch syn- In leaf tissue, carbon enters starch via the gluconeogenesis thesis is the same in amyloplasts as in chloroplasts. The flow pathway where D-glycerate 3-phosphate formed from CO2 fixation of carbon and the exchange of metabolites between the is converted into hexose monophosphates within the chloroplast amyloplast and cytosol in developing sink organs, however, stroma. In starch-containing sink organs, evidence has been ob- are not identical to the processes established for leaves (1, 6, tained indicating that the flow of carbon into starch follows a 7, 9, 17, 19). different pathway whereby hexose monophosphates formed from An alternative pathway of starch synthesis recently has sucrose are transported into the amyloplast, a plastid specialized been proposed based on the capacity of both chloroplasts in starch accumulation. In both chloroplasts and amyloplasts, the and amyloplasts to transport ADPGlc (16 and refs. cited formation of ADPglucose, the substrate for starch synthase, is therein). In this review, I first summarize the latest develop- controlled by the activity of ADPglucose pyrophosphorylase, a key ments regulatory enzyme of starch synthesis localized in the plastid. in starch biosynthesis and then discuss whether the Recently, an alternative pathway of starch synthesis has been operation of this proposed alternative pathway of starch proposed in which ADPglucose is synthesized from sucrose and synthesis is compatible with our present knowledge of the transported directly into the plastid compartment, where it is used biochemistry and genetics of starch biosynthesis. for starch synthesis. On the basis of the biochemical phenotypes exhibited by various plant mutants with defined genetic lesions, it STARCH FORMATION OCCURS VIA ADPGIc is concluded that ADPglucose pyrophosphorylase is essential for PYROPHOSPHORYLASE starch synthesis, whereas the alternative pathway has only a minor role in this process. Extensive evidence indicates that the biochemical events leading to the formation of ADPGlc and its subsequent utilization for starch synthesis are restricted to the chloro- plasts (reviewed in refs. 15 and 17). The more recent isolation and study of mutants defective in carbon metabolism also The events that lead to the flow of carbon into starch and support this view. Caspar et al. (4) obtained a null mutant of their regulation have been well established for chloroplasts Arabidopsis thaliana for the chloroplastic PGM that was (reviewed in ref. 17). In contrast, less is known about the highly defective in starch synthesis, accumulating less than biochemical events that lead to starch synthesis in the amy- 2% of the normal levels. The starchless phenotype of this loplasts of developing sink organs (1). This organelle, con- null plastidic PGM mutant supports the prevailing view that taining one or more starch granules, is delimited by a double the bulk of, if not all, carbon flow into starch occurs via the envelope and is usually devoid of intracellular membranes. gluconeogenesis pathway within the plastid compartment. Because the amyloplast is dependent on the cytoplasm for Kruckeberg et al. (11) examined mutant plants of Clarkia both energy and carbon, the biochemistry of this organelle is xantiana containing reduced activities of the cytosolic PGI likely to be distinct from that exhibited by the autotrophic (64%, 36%, and 18% of wild-type levels) or chloroplastic PGI (ATP-generating, C02-fixing) chloroplasts of leaf tissue. Re- (75% and 50% of wild type) to assess the effect of enzyme cent studies have shown that the allosterically regulated levels on carbon fluxes toward starch and sucrose synthesis ADPGlc2 pyrophosphorylase, as well other enzymes involved under saturating and limiting light conditions. Decreased in starch synthesis, are localized in the amyloplasts (1, 10, levels of the plastid enzyme had very little influence on starch and sucrose synthesis in low light. In saturating light, however, starch synthesis was suppressed, whereas little l Supported in part by Department of Energy grant DE-FG06- effect on sucrose synthesis was observed. Conversely, reduc- 87ER13699, The Rockefeller and Foundation, Project 0590, College tion in the levels of the caused an of Agriculture and Home Economics, Washington State University, cytosolic enzyme increase Pullman, WA 99164. in starch synthesis with a corresponding decrease in sucrose 2 Abbreviations: ADPGlc, ADPglucose; 3-PGA, D-glycerate 3- synthesis; this response was more evident under low light phosphate; PGI, phosphoglucoisomerase; PGM, phosphoglucomu- intensity than under saturating conditions. These observa- tase; SS-ADPGlc, sucrose synthase-dependent synthesis of ADPGlc; tions with the plastid mutant lines reinforce the view that UDPGlc, UDPglucose; Glc 1-P, glucose 1-phosphate; Glc 6-P, glu- the events leading to carbon flow into starch are restricted to cose 6-phosphate. the plastid. Moreover, when sucrose synthesis is depressed 560 THE FLOW OF CARBON INTO STARCH 561 in the cytosolic mutants, more of the carbon is directed away metabolism. Muller-Rober et al. (13) transformed potato with from the cytosol and rerouted toward the synthesis of starch 'antisense' constructs for the small subunit of the heterotet- in the chloroplast. rameric tuber ADPGlc pyrophosphorylase (14). These work- Direct evidence has been obtained showing that most, if ers observed the almost complete absence of starch formation not all, of the ADPGlc formed is controlled by the action of in the developing tubers of these transgenic plants and ADPGlc pyrophosphorylase. Lin et al. (12) isolated two Ar- thereby clearly demonstrated an essential role for ADPGlc abidopsis lines mutated at the Adgl and Adg2 loci that were pyrophosphorylase in starch synthesis. defective in starch synthesis and ADPGlc pyrophosphorylase activity. Plants of the adgl line, which accumulated very little THE FLOW OF CARBON INTO STARCH leaf starch, were devoid of both the large and small subunits of the ADPGlc pyrophosphorylase as viewed by immunoblot In actively photosynthesizing leaves, the events leading to analysis, whereas plants of the line adg2, which accumulated carbon flow into starch are restricted to the chloroplasts 40% as much starch, were deficient in the large subunit of (reviewed in ref. 17). The 3-PGA formed during CO2 fixation ADPGlc pyrophosphorylase. Therefore, the absence or is readily transformed into hexose monophosphates via glu- depression in the levels of starch synthesis can be attributed coneogenesis within the stroma where they can serve as to a direct causal relationship between defects in the expres- substrates for ADPGlc formation (Fig. 1). In young develop- sion of the structural genes for ADPGlc pyrophosphorylase ing leaves that serve as sinks, sucrose is first broken down and the concomitant lower amounts of enzyme activity. by an alkaline invertase or by the successive action of sucrose The rate of CO2 incorporation into starch by isolated chlo- synthase and UDPGlc pyrophosphorylase in the cytoplasm roplasts is directly correlated with 3-PGA levels and inversely correlated with Pi levels (17). This is consistent with the in vitro evidence that ADPGlc synthesis is controlled by the Hexose pathway activation and inhibition of ADPGlc pyrophosphorylase via these metabolites. Recently, a starch-deficient mutant of Glc 6-P do . Gic 6-P Chlamydomonas reinhardtii contained a defective ADPGlc py- that was less to allosteric acti- rophosphorylase responsive Gic 1-P - IT Gic 1-P vation by 3-PGA and inhibition by Pi. This provides direct ATP in vivo evidence that the allosteric activation by 3-PGA of chloroplastic ADPGlc pyrophosphorylase is essential for PP UDPG fructose maximum starch synthesis (2). A direct role for the allosteric ADPG regulation of the amyloplast enzyme in starch synthesis has yet to be resolved. However, Hnilo and Okita (8) have shown that when tuber slices were incubated in the presence of mannose, an effective sequestration agent of intracellular Pi, starch sucrose UDP the incorporation of "4C-sucrose into starch was enhanced by 50%. These results suggest that the activity of the amyloplast amyloplast cytosol enzyme is also modulated by intracellular Pi levels. Genetic studies also indicate a major role for ADPGlc SS-ADPG pathway pyrophosphorylase in starch synthesis of nonphotosynthetic developing sink organs. Maize mutations at two unlinked loci, Shrunken-2 (Sh2) and Brittle-2 (Bt2), result in a 60% reduction in starch levels in the endosperm with correspond- ADPG - -ADPG fructose ing decreases in ADPGlc pyrophosphorylase activities of 66% and 63%, respectively (17). Recent biochemical and molecular studies (3, 15, 17) have shown that Sh2 and Bt2 encode starch ADPGlc pyrophosphorylase subunits of 54 kD and 51 kD, sucrose ADP respectively, and that both subunits are required for maxi- mum enzyme activity and starch synthesis. ADPGlc pyrophosphorylase also seems to have a major role in starch synthesis in pea embryos. Mature seeds reces- sive at the Rb locus have reduced levels of starch and elevated Figure 1. The flow of carbon into starch: two hypotheses. The lipid and sucrose levels and contained less than
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