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Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds

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Abstract

Two genes encoding sucrose synthase (SUS), namely SUS2 (At5g49190) and SUS3 (At4g02280), are strongly and differentially expressed in Arabidopsis seed. Detailed biochemical analysis was carried out in developing seeds 9–21 days after flowering (DAF) of wild type and two knockouts. SUS2 and SUS3 are not redundant genes since single knockouts show a phenotype in developing seeds. The mutants had 30–50% less SUS activity and therefore accumulated 40% more sucrose and 50% less fructose at 15 DAF. This did not affect the hexose-P pool, but led to 30–70% less starch in embryo and seed coat. Lipids were 55% higher in both mutants at 9–15 DAF. It seems that sucrolysis via SUS is not required for oil or protein synthesis but rather for channeling carbon toward ADP-glucose and starch in seeds. Metabolite profiling with GC–TOF revealed specific downstream changes in primary metabolism as a consequence of signaling or regulatory fine-tuning. While sucrose increased, hexoses and specific amino acids decreased reciprocally. There was a developmental shift regarding an earlier timing of dry weight accumulation, germinative maturity, oil deposition, sugar levels, transient starch buildup, and protein storage. Nevertheless, final seed size and composition were unaltered due to an earlier cessation of growth, thus giving rise to an apparent silent phenotype of mature mutant seeds. We conclude that SUS is important for metabolite homeostasis and timing of seed development, and propose that an altered sucrose/hexose ratio can modify carbon partitioning and the pattern of storage compounds in Arabidopsis.

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Abbreviations

SUS:

Sucrose synthase

INV:

Invertase

DAF:

Days after flowering

ADP:

Adenosine diphosphate

Hexose-P:

Hexose phosphate

GC/TOF-MS:

Gas chromatography coupled to time of flight mass spectrometry

FA:

Fatty acid

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Acknowledgments

We thank J. P. Delano, J. P. Boutin and several INRA colleagues and scientists for critical reading of the manuscript. We thank Samuel Gómez Vargas for the help with Arabidopsis cultures. This study was supported by fellowships from the Consejo Nacional de Ciencia y Tecnología (CONACYT México) to J. G. Angeles-Núñez. A. Tiessen also acknowledges project funding by Deutsche Forschungs Gemeinschaft (DFG), CONACYT and SAGARPA.

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  1. Departamento de Ingeniería Genética, CINVESTAV Unidad Irapuato, Km 9.8 Libramiento Norte, CP 36821, Irapuato, Guanajuato, México

    Juan Gabriel Angeles-Núñez & Axel Tiessen

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  1. Juan Gabriel Angeles-Núñez
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  2. Axel Tiessen
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Correspondence to Axel Tiessen.

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This article is dedicated to the memory of the late Christine Rochat.

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Angeles-Núñez, J.G., Tiessen, A. Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 232, 701–718 (2010). https://doi.org/10.1007/s00425-010-1207-9

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