Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity.

Eleazar Martínez-Barajas,Cátia Nunes,Henriette Schluepmann,Lucia F Primavesi,Rowan A C Mitchell,Govert W Somsen,Thierry Delatte,Gerhardus J De Jong,Patricia Coello,Matthew J Paul

doi:10.1104/pp.111.174524

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(-1) fresh weight (FW) pregrain filling, around 100-fold higher than previously reported in plants, to 0.4 nmol g(-1) 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(-1) FW in filial and maternal tissues sufficient to inhibit SnRK1; at 17 DAA T6P accumulation was almost exclusively endospermal (43 nmol g(-1) FW) with 0.6 to 0.8 nmol T6P g(-1) 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 tissue-specific regulation of SnRK1 by T6P in wheat grain.

Highlights

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)
We showed that a signaling partner of T6P in growing tissues is the SNF1-related protein kinase1, SnRK1, of the SNF1/AMPK group of protein kinases (Zhang et al, 2009; Paul et al, 2010)
As evidence that regulation of SnRK1 by T6P could operate in vivo, homologs of SnRK1 marker genes designated in Arabidopsis (Baena-Gonzalez et al, 2007) were identified in wheat using Wheat Estimated Transcript Server (WhETS; Mitchell et al, 2007)

Summary

Introduction

Trehalose 6-phosphate (T6P) is a sugar signal that regulates metabolism, growth, and development and inhibits the central regulatory SNF1-related protein kinase (SnRK1; AKIN10/AKIN11). In growing tissues inhibition of SnRK1 by T6P is a mechanism of switching from catabolism to anabolism by activation of biosynthetic processes by T6P in response to Suc supply (Zhang et al, 2009; Paul et al, 2010) Metabolic pathways such as those involved in cell wall and protein metabolism were up-regulated through T6P inhibition of SnRK1 in Arabidopsis seedlings (Zhang et al, 2009; Paul et al, 2010). The data show a relationship between T6P and Suc overall that belies a marked effect of tissue type and developmental stage on T6P content, consistent with tissue-specific regulation of SnRK1 by T6P in wheat grain

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Conclusion