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

被引:151
作者
Martinez-Barajas, Eleazar [1 ]
Delatte, Thierry [2 ,3 ]
Schluepmann, Henriette [2 ]
de Jong, Gerhardus J. [3 ]
Somsen, Govert W. [3 ]
Nunes, Catia [1 ,4 ]
Primavesi, Lucia F. [1 ]
Coello, Patricia [1 ]
Mitchell, Rowan A. C. [1 ]
Paul, Matthew J. [1 ]
机构
[1] Rothamsted Res, Plant Sci, Harpenden AL5 2JQ, Herts, England
[2] Univ Utrecht, NL-3584 CH Utrecht, Netherlands
[3] Univ Utrecht, NL-3584 CG Utrecht, Netherlands
[4] Univ Nova Lisboa, Inst Tecnol Quim & Biol, Lab Biotecnol Celulas Vegetais, P-2781901 Oeiras, Portugal
基金
英国生物技术与生命科学研究理事会;
关键词
TREHALOSE-6-PHOSPHATE SYNTHASE-1; REDOX ACTIVATION; STARCH SYNTHESIS; GENE; STRESS; GROWTH; METABOLISM; EXPRESSION; EVOLUTION; NETWORKS;
D O I
10.1104/pp.111.174524
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
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 DAAT6P was 49 to 119 nmol g(-1) FW in filial and maternal tissues sufficient to inhibit SnRK1; at 17 DAAT6P 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.
引用
收藏
页码:373 / 381
页数:9
相关论文
共 40 条
[1]   COMPLEMENTATION OF SNF1, A MUTATION AFFECTING GLOBAL REGULATION OF CARBON METABOLISM IN YEAST, BY A PLANT PROTEIN-KINASE CDNA [J].
ALDERSON, A ;
SABELLI, PA ;
DICKINSON, JR ;
COLE, D ;
RICHARDSON, M ;
KREIS, M ;
SHEWRY, PR ;
HALFORD, NG .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1991, 88 (19) :8602-8605
[2]   Insights on the evolution of trehalose biosynthesis [J].
Avonce, Nelson ;
Mendoza-Vargas, Alfredo ;
Morett, Enrique ;
Iturriaga, Gabriel .
BMC EVOLUTIONARY BIOLOGY, 2006, 6 (1)
[3]   A central integrator of transcription networks in plant stress and energy signalling [J].
Baena-Gonzalez, Elena ;
Rolland, Filip ;
Thevelein, Johan M. ;
Sheen, Jen .
NATURE, 2007, 448 (7156) :938-U10
[4]   Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase [J].
Blázquez, MA ;
Santos, E ;
Flores, CL ;
Martínez-Zapater, JM ;
Salinas, J ;
Gancedo, C .
PLANT JOURNAL, 1998, 13 (05) :685-689
[5]   Determination of trehalose-6-phosphate in Arabidopsis seedlings by successive extractions followed by anion exchange chromatography-mass spectrometry [J].
Delatte, Thierry L. ;
Selman, Maurice H. J. ;
Schluepmann, Henriette ;
Somsen, Govert W. ;
Smeekens, Sjef C. M. ;
de Jong, Gerhardus J. .
ANALYTICAL BIOCHEMISTRY, 2009, 389 (01) :12-17
[6]   Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation [J].
Eastmond, PJ ;
van Dijken, AJH ;
Spielman, M ;
Kerr, A ;
Tissier, AF ;
Dickinson, HG ;
Jones, JDG ;
Smeekens, SC ;
Graham, IA .
PLANT JOURNAL, 2002, 29 (02) :225-235
[7]   Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions [J].
El-Bashiti, T ;
Hamamci, H ;
Öktem, HA ;
Yücel, M .
PLANT SCIENCE, 2005, 169 (01) :47-54
[8]   Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses [J].
Garg, AK ;
Kim, JK ;
Owens, TG ;
Ranwala, AP ;
Do Choi, Y ;
Kochian, LV ;
Wu, RJ .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (25) :15898-15903
[9]   Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes [J].
Ge, Liang-Fa ;
Chao, Dai-Yin ;
Shi, Min ;
Zhu, Mei-Zhen ;
Gao, Ji-Ping ;
Lin, Hong-Xuan .
PLANTA, 2008, 228 (01) :191-201
[10]   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 [J].
Gómez, LD ;
Baud, S ;
Gilday, A ;
Li, Y ;
Graham, IA .
PLANT JOURNAL, 2006, 46 (01) :69-84