Altering Trehalose-6-Phosphate Content in Transgenic Potato Tubers Affects Tuber Growth and Alters Responsiveness to Hormones during Sprouting    

Abstract

Trehalose-6-phosphate (T6P) is a signaling metabolite that regulates carbon metabolism, developmental processes, and growth in plants. In Arabidopsis (Arabidopsis thaliana), T6P signaling is, at least in part, mediated through inhibition of the SNF1-related protein kinase SnRK1. To investigate the role of T6P signaling in a heterotrophic, starch-accumulating storage organ, transgenic potato (Solanum tuberosum) plants with altered T6P levels specifically in their tubers were generated. Transgenic lines with elevated T6P levels (B33-TPS, expressing Escherichia coli osmoregulatory trehalose synthesis A [OtsA], which encodes a T6P synthase) displayed reduced starch content, decreased ATP contents, and increased respiration rate diagnostic for high metabolic activity. On the other hand, lines with significantly reduced T6P (B33-TPP, expressing E. coli OtsB, which encodes a T6P phosphatase) showed accumulation of soluble carbohydrates, hexose phosphates, and ATP, no change in starch when calculated on a fresh weight basis, and a strongly reduced tuber yield. [14 C]Glucose feeding to transgenic tubers indicated that carbon partitioning between starch and soluble carbohydrates was not altered. Transcriptional profiling of B33-TPP tubers revealed that target genes of SnRK1 were strongly up-regulated and that T6P inhibited potato tuber SnRK1 activity in vitro. Among the SnRK1 target genes in B33-TPP tubers, those involved in the promotion of cell proliferation and growth were down-regulated, while an inhibitor of cell cycle progression was up-regulated. T6P-accumulating tubers were strongly delayed in sprouting, while those with reduced T6P sprouted earlier than the wild type. Early sprouting of B33-TPP tubers correlated with a reduced abscisic acid content. Collectively, our data indicate that T6P plays an important role for potato tuber growth.

The Trehalose 6-Phosphate/SnRK1 Signaling Pathway Primes Growth Recovery following Relief of Sink Limitation

“…Some effects of T6P have been attributed to inhibition of SnRK1 by T6P (Zhang et al, 2009;Debast et al, 2011;Delatte et al, 2011). Inhibition of SnRK1 by T6P results in up-regulation of genes involved in biosynthetic processes and growth (Zhang et al, 2009;Paul et al, 2010;Debast et al, 2011;Martínez-Barajas et al, 2011;), whereas low T6P and active SnRK1 result in upregulation of plant stress responses and catabolism rather than anabolism (Baena-González et al, 2007;Zhang et al, 2009;Debast et al, 2011).…”

“…T6P is known to promote growth and to promote transcription of genes associated with biosynthetic processes and growth (Baena-González et al, 2007;Zhang et al, 2009;Debast et al, 2011). Given that T6P was related to Suc levels under all treatments with different growth rates, we wished to determine if transcript abundance of SnRK1 markers was related to T6P or to growth rate.…”

“…Recently, it was found that T6P inhibits the protein kinase SnRK1 in growing tissues of plants (Zhang et al, 2009;Debast et al, 2011;Delatte et al, 2011;Martínez-Barajas et al, 2011) through an intermediary factor. SnRK1 (AKIN10/AKIN11) is a member of the SNF1-related AMPK group of protein kinases that perform central functions in the regulation of responses of cells to endogenous energy and carbon status (Hardie, 2007).…”

The Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation

“…Phytohormone Signaling and Suc-Induced Hypocotyl Elongation under Light/Dark Cycles: Abscisic Acid ABA suppresses seedling development (Belin et al, 2009) and several studies have linked Tre6P and abscisic acid (ABA) signaling (Avonce et al, 2004;Ramon et al, 2007;Gómez et al, 2010;Debast et al, 2011). Therefore, we investigated whether ABA signaling contributes to Suc-induced hypocotyl elongation under light/dark cycles.…”

Regulation of potato tuber sprouting

“…Sucrose content correlates with the level of the signal metabolite trehalose-6-phosphate (T6P) which is supposed to decline with dormancy progression. Considering data of Debast et al (2011), a low T6P content may stimulate an increased reserve mobilisation and respiration by activation of the SnRK signalling pathway (dotted lines). Increased mobilisation of reserves such as starch during advanced stages of sprouting will fuel the energy demand of the growing sprout.…”