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

Abstract

Trehalose 6-phosphate (T6P) is a sugar signal that regulates metabolism, growth, and development and inhibits the central regulatory SNF1-related protein kinase1 (SnRK1; AKIN10/AKIN11). To better understand the mechanism in wheat (Triticum aestivum) grain, we analyze T6P content and SnRK1 activities. T6P levels changed 178-fold 1 to 45 d after anthesis (DAA), correlating with sucrose content. T6P ranged from 78 nmol g 21 fresh weight (FW) pregrain filling, around 100-fold higher than previously reported in plants, to 0.4 nmol g 21 FW during the desiccation stage. In contrast, maximum SnRK1 activity changed only 3-fold but was inhibited strongly by T6P in vitro. To assess SnRK1 activity in vivo, homologs of SnRK1 marker genes in the wheat transcriptome were identified using Wheat Estimated Transcript Server. SnRK1-induced and -repressed marker genes were expressed differently pregrain filling compared to grain filling consistent with changes in T6P. To investigate this further maternal and filial tissues were compared pre-(7 DAA) and during grain filling (17 DAA). Strikingly, in vitro SnRK1 activity was similar in all tissues in contrast to large changes in tissue distribution of T6P. At 7 DAA T6P was 49 to 119 nmol g 21 FW in filial and maternal tissues sufficient to inhibit SnRK1; at 17 DAA T6P accumulation was almost exclusively endospermal (43 nmol g 21 FW) with 0.6 to 0.8 nmol T6P g 21 FW in embryo and pericarp. The data show a correlation between T6P and sucrose overall that belies a marked effect of tissue type and developmental stage on T6P content, consistent with tissuespecific regulation of SnRK1 by T6P in wheat grain.

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

“…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 contents are related to those of Suc in plants (Lunn et al, 2006;Martínez-Barajas et al, 2011). Accordingly, a model has been developed where T6P elicits changes in gene expression through regulation of SnRK1 promoting growth in relation to Suc supply.…”

“…It could also represent a possible famine threshold level of Suc above which growth is induced. While a strong relationship is seen between Suc and T6P, other studies (Martínez-Barajas et al, 2011) in an analysis of wheat (Triticum aestivum) grain have shown a relationship with catabolites of Suc and T6P, including Glc. To test the specificity of the interrelationship between Suc and T6P, feeding of 0.5% (w/v) Glc was performed.…”

“…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).…”

Transitioning to the Next Phase: The Role of Sugar Signaling throughout the Plant Life Cycle

“…Spraying of wheat plants with compounds that release T6P upon exposure to sunlight led to increased grain yield due to the formation of larger grains with higher starch content (Griffiths et al, 2016b). Earlier work had shown that T6P naturally accumulates in wheat grains to previously unreported levels before grain filling (Martínez-Barajas et al, 2011). Interestingly, T6P content was low in the embryonic and maternal tissues and accumulated almost exclusively in the endosperm, although at later stages it may also be required in the embryo itself.…”

“…SnRK1 thus has a positive effect on seed maturation and storage protein synthesis, which is opposite to its characteristic role in starvation signaling and activation of catabolic pathways (Baena-González and Sheen, 2008). In developing wheat grains, in vitro SnRK1 activity was reported in the embryo and endosperm, which together with low T6P in the embryo may support high in vivo SnRK1 activity for embryo maturation (Martínez-Barajas et al, 2011). The C/S1 bZIP transcription factors, in particular, bZIP53, which is expressed late during seed development, have also been proposed to be involved in storage protein synthesis and seed maturation Alonso et al, 2009;Restovic et al, 2017).…”