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Plant Physiology 144:3-5 (2007) © 2007 American Society of Plant Biologists The Role of Trehalose Biosynthesis in PlantsUniversity of Illinois, Urbana, IL 61801
The role of trehalose in plants is a curious one. Originally believed to serve as an osmoprotectant, its presence in plants at very low levels makes this role unlikely. This month's High Impact article by Avonce et al., titled "The Arabidopsis Trehalose-6-P Synthase AtTPS1 Gene Is a Regulator of Glucose, Abscisic Acid, and Stress Signaling," appeared in our November 2004 issue and adds to the growing body of evidence that it is not trehalose itself but more likely a synthesis pathway intermediate or perhaps an enzyme of the synthesis pathway that plays a key role in plants.
Trehalose (  -D-glucopyranosyl-1,1--D-glucopyranoside) is a nonreducing disaccharide formed through a 1-1 alpha bond linking two Glc moieties. A variety of organisms synthesize this compound, including plants, fungi, bacteria, and invertebrate animals. Trehalose is the main blood sugar in insects and serves as a major energy storage molecule enabling flight. In those plants that accumulate trehalose, it is most commonly believed to aid in their ability to survive extended periods of desiccation. However, with few exceptions, this is unlikely to stem from a direct role of trehalose itself since only trace amounts of trehalose are present in most (angiosperm) plants. Current studies are defining a role for the trehalose precursor, trehalose-6-P (T6P), as a regulatory molecule, especially in sugar influx and metabolism (for review, see Eastmond and Graham, 2003 ). Arabidopsis (Arabidopsis thaliana) plants with an insertion in AtTPS1 do not develop mature embryos, stressing the importance of the trehalose synthesis pathway in embryo maturation and development (for review, see Eastmond and Graham, 2003). Recently, T6P has been implicated in the redox activation of ADP-Glc phosphorylase, the enzyme that catalyzes the first committed step of starch synthesis (Kolbe et al., 2005). Also, T6P has been recognized as a key molecule enhancing photosynthetic capacity and thus offering a long-sought dream of agronomists: improvement of crop biomass (Pellny et al., 2004).
Multiple trehalose biosynthetic pathways have been identified in bacteria and archeae, but only one has been found in the eukaryotes examined to date (Avonce et al., 2006
In the study by Avonce et al. (2004) , AtTPS1, one of 11 TPS genes in Arabidopsis, was overexpressed in Arabidopsis under the control of the 35S promoter. Despite the accumulation of higher levels of AtTPS1 mRNA and protein than wild type, trehalose did not appreciably accumulate in these plants. This was similar to what was seen in earlier studies in tobacco (Nicotiana tabacum; Goddijn et al., 1997) and Arabidopsis (Schluepmann et al., 2003) expressing bacterial TPS1. T6P, the synthesis intermediate and product of TPS, was found at higher levels than wild type. Increased drought tolerance (relative to wild type) was also observed in the AtTPS1-overexpressing plants. The transgenic lines had higher relative water content than wild type and, unlike wild type, were able to recover from 2 weeks of water deprivation after a return to the normal watering regime. The authors noted that, since trehalose did not accumulate to high levels in these plants, the increase in drought tolerance was not likely due to a direct effect of trehalose but more likely due to other changes associated with AtTPS1 overexpression.
The overexpression of AtTPS1 caused no morphological changes other than delayed flowering, in contrast to previous studies where plants overexpressing bacterial or yeast TPS1 had altered morphology. One major difference between AtTPS1 and bacterial or yeast TPS1 is the presence of the N-terminal and/or C-terminal regions that could possibly account for the difference between these studies. Previous work from this lab had demonstrated that deletion of the N-terminal regions of AtTPS1 resulted in higher catalytic activity of the enzyme (Van Dijck et al., 2002
A Glc-insensitive phenotype was observed in AtTPS1-overexpressing plants, allowing seeds to germinate on Murashige and Skoog (MS) plates supplemented with 6% Glc, whereas wild-type seeds had poor germination rates under the same conditions. This group used this observation as a basis to develop a process to use AtTPS1 as a selectable marker for obtaining transgenic plants and thus avoid the use of antibiotics (Leyman et al., 2006
The product of TPS, T6P, is a known signaling molecule in yeast (Saccharomyces cerevisiae) and is believed to inhibit hexokinase, thus regulating the entry of Glc and Fru into glycolysis (Blázquez et al., 1998
Detection of trehalose and T6P in plants is a potential problem given that both are present at such low levels, potentially leading to inaccurate measurements. Lunn et al. (2006) developed a very sensitive assay to measure T6P in the femto-picomole range. They then used this assay to measure T6P levels in Suc-starved Arabidopsis plants after Suc addition and found that T6P levels increased with the sugar concentration. Additionally, they found that increasing levels of sugars and T6P led to a change in the redox status of ADP-Glc pyrophosphorylase and a stimulation of starch synthesis in vivo. This result lent further support to the notion that T6P acts as a regulatory molecule of the sugar status of a plant, defined by the Avonce et al. (2004) study, as well as the role of T6P in mediating Suc-induced changes in the rate of starch synthesis (Kolbe et al., 2005). The work by Avonce et al. (2004) was the first time that trehalose metabolism was linked to downstream changes in gene expression, further supporting its possible role as a second messenger.
Gómez et al. (2006)
It would be perplexing that Arabidopsis has 11 copies of TPS and 10 of TPP genes if a product of the biosynthesis pathway were not important to some aspect of the plant's life cycle or survival. Studies by Avonce et al. (2004) and others have demonstrated the importance of TPS to plant growth and survival, and more recent works have shown the importance of T6P. These studies, together with the low levels of trehalose present in the majority of plants, support the very important role of T6P for plant growth, development, and stress tolerance.
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900223
Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14: 2085–2096 Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136: 3649–3659 Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6: 109[CrossRef][Medline] Blázquez MA, Santos E, Flores CL, Martínez-Zapater JM, Salinas J, Gancedo C (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13: 685–689[CrossRef][ISI][Medline] Eastmond PJ, Graham IA (2003) Trehalose metabolism: a regulatory role for trehalose-6-phosphate? Curr Opin Plant Biol 6: 231–235[CrossRef][ISI][Medline] Goddijn OJM, van Dunn K (1999) Trehalose metabolism in plants. Trends Plant Sci 4: 315–319[CrossRef][ISI][Medline] Goddijn OJM, Verwoerd TC, Voogd E, Krutwagen RWHH, de Graaf PTHM, van Dun K, Poels J, Ponstein AS, Damm B, Pen J (1997) Inhibition of trehalose activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113: 181–190[Abstract] Gómez LD, Baud S, Gilday A, Li Y, Graham IA (2006) Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J 46: 69–84[CrossRef][ISI][Medline] Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118–11123 Leyman B, Avonce N, Ramon M, Van Dijck P, Iturriaga G, Thevelein JM (2006) Trehalose-6-phosphate synthase as an intrinsic selection marker for plant transformation. J Biotechnol 121: 309–317[CrossRef][ISI][Medline] Lunn JE, Feil R, Hendricks JHM, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajiresaei MR, Stitt M (2006) Sugar-induced increases in trehalose 6-phophate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397: 139–148[CrossRef][ISI][Medline] Pellny TK, Ghannoum O, Conroy JP, Schluepmann H, Smeekens S, Andralojc J, Krause KP, Goddijn O, Paul MJ (2004) Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol J 2: 71–82[CrossRef][Medline] Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16: 2128–2150 Schluepmann H, Pellny T, van Dijken A, Smeeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6849–6854 Van Dijck P, Mascorro-Gallardo JO, de Bus M, Royackers K, Iturriaga G, Thevelein JM (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase unlocks high catalytic activity and supports high trehalose levels on expression in yeast. Biochem J 366: 63–71[ISI][Medline] This article has been cited by other articles:
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