Metabolic Balance and its Outcome: Deficiency of Vitamin B9 and Sucrose Supply Ectopically Induces Starch Synthesis in Etioplasts

Plastids play a central role in plant metabolism, especially in carbon metabolism. Immature plastids display plasticity in that undifferentiated proplastids can differentiate into multiple different forms, such as chloroplasts, etioplasts and amyloplasts, carrying out different functions. This process is determined by developmental and environmental cues. For instance, plastids differentiate into etioplasts in the dark. Etioplasts do not accumulate starch; rather the latter accumulates in other plastid forms, including chloroplasts and amyloplasts. Despite their plasticity, the functionality of plastids and the metabolism occurring within plastids is heavily restricted under a given environment. For example, photosynthesis occurs in chloroplasts where carbon dioxide is converted into glucose. Glucose is utilized for energy production and serves as the starting material for downstream metabolism in the source organ or is converted to storage forms, such as starch, in the sink organ. In this issue, Hayashi et al. (2017) investigated the mechanisms underlying sucrose metabolism in non-photosynthetic cells. They set up a genetic screen to isolate Arabidopsis mutants defective in the interconversion between sucrose and starch. One mutant, fpgs1, showed a shortened hypocotyl only when grown in darkness in media containing sucrose, and not in media without sucrose. The fpgs1 mutant grown in the presence of sucrose contained significantly larger plastids than the wild type and accumulated starch, which was not observed in wild-type etioplasts (Fig. 1). The causal gene, FPGS1, encodes a plastidial folypolyglutamate synthetase that catalyzes the addition of a polyglutamate tail to tetrahydrofolate (THF) (Ravanel et al. 2001). The THF derivatives, collectively known as folates or vitamin B9, are essential cofactors for various methyltransferase reactions including the formation of nucleotides and amino acid metabolism (Rebeille et al. 2006). Application of 5-formyl-THF to the fpgs1 mutant efficiently rescued the mutant phenotypes, while application of methotrexate, an antifolate, to the wild type mimicked the fpgs1 mutant phenotypes. An important finding from this work is that the fpgs1 mutant accumulates adenine >10 times more than that the wild type. More importantly, the application of adenine induced both sucrose-dependent starch accumulation and the inhibition of hypocotyl growth in etiolated wild-type seedlings, phenocopying the fpgs1 mutant. The authors discussed that the application of adenine in the presence of exogenous sucrose possibly increases the ATP levels, which in turn increases ADP-glucose (the ADP-glucose level is 2-fold higher in the fpgs1 mutant than in the wild type). It would be of interest to see if ectopic starch accumulation in wild-type etioplasts could be induced simply by the application of ADP-glucose. The metabolic imbalance caused by both a vitamin B9 deficiency and an exogenous sucrose supply leads to a surprising outcome—the ectopic accumulation of starch in etioplasts and enlargement of this organelle. The plasticity of plastids relies on both the sophisticated molecular switch of plastid differentiation and the rigid control of individual differentiated forms. Further studies could help elucidate how this metabolic imbalance disturbs the rigid functionality of etioplasts and identify a molecular switch to control sink–source metabolism. Accumulation of starch in etioplasts. The wild-type etioplast is not able to accumulate starch when sucrose is supplied (Suc →), but the fpgs1 mutant is able to accumulate starch in the etioplasts in plants treated with exogenous sucrose (fpgs1 →, Suc + fpgs1 → starch). The phenotype of the fpgs mutant is chemically complemented by the application of folate (Suc + fpgs1 + folate →) and is mimicked in the wild type by the application of an antifolate agent (Suc + antifolate → starch). The starch accumulation in the etioplast is also induced by adding adenine together with sucrose (Suc + adenine → starch). Hayashi et al. (2017) also showed that starch accumulation in etioplasts is tightly coupled with growth inhibition. Indeed, in all organisms, carbon metabolism is associated with growth as it determines metabolic flow to either the storage form or for energy consumption. Despite its importance, the mechanism of how carbon metabolism is linked to growth is poorly understood. Studies using the Arabidopsis hypocotyl elongation system have identified numerous mutations and chemicals that alter hypocotyl growth through forward genetic and chemical genetic screening to explore the molecular mechanisms regulating plant development and signaling. Although the metabolic processes related to storage lipid mobilization in Arabidopsis hypocotyls have been extensively studied (Penfield et al. 2004, Andre and Benning 2007, Eastmond et al. 2015), most of the developmental and signaling mutants have not been explored in a metabolic context. The rich collection of such resources would be useful for identifying the mutations/chemicals decoupling growth and carbon metabolism, and thus require further exploration. The shortened hypocotyl of the fpgs1 mutant is conditional, observed only in the presence of exogenous sucrose. Media containing exogenous sucrose may visualize a totally different outcome for well-characterized mutations/chemicals altering hypocotyl growth. The starch accumulation in etioplasts of the fpgs1 mutant with exogenous sucrose is observed only in the shoot, but not in the root. This indicates that starch synthesis is differentially regulated between the shoot and the root. It was reported that in the amyloplasts of rice endosperm, ADP-glucose synthesis is a rate-limiting step in starch synthesis under normal growth conditions, but not under elevated CO2 conditions (Sakulsingharoj et al. 2004, Nagai et al. 2009). This indicates that, even in the same tissue, starch accumulation is regulated by distinct mechanisms under different growth conditions. It seems that the regulatory mechanisms of starch synthesis vary among experimental settings and cannot be summarized by a single model. Nonetheless, collecting snapshots at various time points, in different tissues and under every given condition, is a promising way to piece together such dynamic regulations.

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