Trehalose‐6‐phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation

Abstract

SummaryDespite the recent discovery that trehalose synthesis is widespread in higher plants very little is known about its physiological signi®cance. Here we report on an Arabidopsis mutant (tps1), disrupted in a gene encoding the ®rst enzyme of trehalose biosynthesis (trehalose-6-phosphate synthase). The tps1 mutant is a recessive embryo lethal. Embryo morphogenesis is normal but development is retarded and stalls early in the phase of cell expansion and storage reserve accumulation. TPS1 is transiently up-regulated at this same developmental stage and is required for the full expression of seed maturation marker genes (2S2 and OLEOSN2). Sucrose levels also increase rapidly in seeds during the onset of cell expansion. In Saccharomyces cerevisiae trehalose-6-phosphate (T-6-P) is required to regulate sugar in¯ux into glycolysis via the inhibition of hexokinase and a de®ciency in TPS1 prevents growth on sugars (Thevelein and Hohmann, 1995). The growth of Arabidopsis tps1±1 embryos can be partially rescued in vitro by reducing the sucrose level. However, T-6-P is not an inhibitor of AtHXK1 or AtHXK2. Nor does reducing hexokinase activity rescue tps1±1 embryo growth. Our data establish for the ®rst time that an enzyme of trehalose metabolism is essential in plants and is implicated in the regulation of sugar metabolism/embryo development via a different mechanism to that reported in S. cerevisiae.

A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis

“…It has been shown that T6P has a regulatory role in carbohydrate utilization during plant growth and development (Eastmond et al 2002;Schluepmann et al 2003Schluepmann et al , 2004van Dijken et al 2004). We have reported before that overexpression in Arabidopsis of its AtTPS1 homolog leads to a glucose and abscisic-acid insensitive phenotype and to stress tolerance, suggesting that trehalose metabolism plays an important role in signaling gene regulation to integrate environmental and metabolic cues during vegetative development (Avonce et al 2004).…”

“…Overexpression of the Arabidopsis AtTPS1 gene in its homologous background does not produce such drastic eVects but still there is a delay in Xowering (Avonce et al 2004). The accumulation of higher levels of T6P are probably causing these defects since T6P has turned out to be a Wne-tuned signaling molecule that has a regulatory role in carbohydrate utilization during plant growth, embryo development and Xowering (Eastmond et al 2002;Schluepmann et al 2003Schluepmann et al , 2004van Dijken et al 2004). Therefore, it was decided to construct a bifunctional TPS-TPP enzyme, which while maintaining trehalose biosynthesis capacity would not lead to excess accumulation of free T6P in the cytosol avoiding undesired secondary eVects in the transgenic plants.…”

Wheat Grain Development Is Characterized by Remarkable Trehalose 6-Phosphate Accumulation Pregrain Filling: Tissue Distribution and Relationship to SNF1-Related Protein Kinase1 Activity

“…T6P is an important regulatory molecule in plants with a large impact on metabolism, growth, and development (Eastmond et al, 2002;Schluepmann et al, 2003;Paul et al, 2008;Smeekens et al, 2010). We recently established a mechanistic basis for the signaling function of T6P in growing tissues through inhibition of SnRK1 of the SNF1/AMPK group of protein kinases (Zhang et al, 2009;Paul et al, 2010).…”

“…The expression profile of SnRK1 marker genes at 7 and 17 DAA can be explained by differences in T6P concentrations at these times. Active SnRK1 is clearly important for embryo development (Radchuk et al, 2010) as is T6P in Arabidopsis embryos (Eastmond et al, 2002). However, T6P may not be sufficiently high to inhibit SnRK1 in embryos and regulation of SnRK1 by T6P may not be a primary function of T6P in this tissue.…”

“…In Arabidopsis there are 21 genes that encode putative trehalose phosphate synthase (TPS) and trehalose phosphate phosphatase (TPP) genes (Avonce et al, 2006;Lunn, 2007). The trehalose pathway is ubiquitous in plants and it has been known that it is an indispensable component of plant development in seeds (Eastmond et al, 2002) and for vegetative development and transition to flowering (van Dijken et al, 2004) with trehalose 6-P (T6P) shown as the critical factor (Schluepmann et al, 2003). Significantly, when T6P levels are increased by genetic means, growth in response to Suc and expression of genes encoding enzymes for growth and biosynthetic pathways are increased (Zhang et al, 2009;Paul et al, 2010).…”