Nonsymbiotic Hemoglobin-2 Leads to an Elevated Energy State and to a Combined Increase in Polyunsaturated Fatty Acids and Total Oil Content When Overexpressed in Developing Seeds of Transgenic Arabidopsis Plants

Nonsymbiotic hemoglobins are ubiquitously expressed in plants and divided into two different classes based on gene expression pattern and oxygen-binding properties. Most of the published research has been on the function of class 1 hemoglobins. To investigate the role of class 2 hemoglobins, transge...

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Bibliographic Details
Published in:Plant physiology (Bethesda) 2011-03, Vol.155 (3), p.1435-1444
Main Authors: Vigeolas, Helene, Hühn, Daniela, Geigenberger, Peter
Format: Article
Language:English
Subjects:
Agronomy. Soil science and plant productions
alpha-Linolenic Acid - metabolism
Arabidopsis - drug effects
Arabidopsis - embryology
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biological and medical sciences
Biosynthesis
Energy Metabolism - drug effects
ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS
Fatty acids
Fatty Acids, Unsaturated - metabolism
Fermentation - drug effects
Fundamental and applied biological sciences. Psychology
Genetic engineering applications
Genetics and breeding of economic plants
Hemoglobins
Hemoglobins - metabolism
Lead
Lipids
Organ Specificity - drug effects
Organ Specificity - genetics
Oxygen
Oxygen - pharmacology
Plant breeding: fundamental aspects and methodology
Plant Oils - metabolism
Plant physiology and development
Plants
Plants, Genetically Modified
Promoter Regions, Genetic - genetics
Seeds
Seeds - drug effects
Seeds - embryology
Seeds - genetics
Seeds - metabolism
Sucrose - metabolism
Symbiosis - drug effects
Transgenic plants
Triglycerides - metabolism
Unsaturated fatty acids
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Summary:Nonsymbiotic hemoglobins are ubiquitously expressed in plants and divided into two different classes based on gene expression pattern and oxygen-binding properties. Most of the published research has been on the function of class 1 hemoglobins. To investigate the role of class 2 hemoglobins, transgenic Arabidopsis (Arabidopsis thaliana) plants were generated overexpressing Arabidopsis hemoglobin-2 (AHb2) under the control of a seed-specific promoter. Overexpression of AHb2 led to a 40% increase in the total fatty acid content of developing and mature seeds in three subsequent generations. This was mainly due to an increase in the polyunsaturated C18:2 (ω-6) linoleic and C18:3 (ω-3) α-linolenic acids. Moreover, AHb2 overexpression led to an increase in the C18:2/C18:1 and C18:3/C18:2 ratios as well as in the C18:3 content in mol % of total fatty acids and in the unsaturation/saturation index of total seed lipids. The increase in fatty acid content was mainly due to a stimulation of the rate of triacylglycerol synthesis, which was attributable to a 3-fold higher energy state and a 2-fold higher sucrose content of the seeds. Under low external oxygen, AHb2 overexpression maintained an up to 5-fold higher energy state and prevented fermentation. This is consistent with AHb2 overexpression results in improved oxygen availability within developing seeds. In contrast to this, overexpression of class 1 hemoglobin did not lead to any significant increase in the metabolic performance of the seeds. These results provide evidence for a specific function of class 2 hemoglobin in seed oil production and in promoting the accumulation of polyunsaturated fatty acids by facilitating oxygen supply in developing seeds.
ISSN:0032-0889
1532-2548
DOI:10.1104/pp.110.166462