Targeted Systems Biology Profiling of Tomato Fruit Reveals Coordination of the Yang Cycle and a Distinct Regulation of Ethylene Biosynthesis during Postclimacteric Ripening

• Published in: Plant physiology (Bethesda) 2012-11, Vol.160 (3), p.1498-1514
• Main Authors: Van de Poel, Bram, Bulens, Inge, Markoula, Aikaterina, Hertog, Maarten L.A.T.M., Dreesen, Rozemarijn, Wirtz, Markus, Vandoninck, Sandy, Oppermann, Yasmin, Keulemans, Johan, Hell, Ruediger, Waelkens, Etienne, De Proft, Maurice P., Sauter, Margret, Nicolai, Bart M., Geeraerd, Annemie H.
• Format: Article
• Language: English
• Subjects: Amino Acid Oxidoreductases - metabolism; Amino Acids, Cyclic - metabolism; Biocatalysis; Biosynthesis; Blotting, Western; Cell Respiration; Climacteric; Enzymes; Ethylene production; Ethylenes - biosynthesis; Fruit - cytology; Fruit - enzymology; Fruit - genetics; Fruit - growth & development; Fruiting; Fruits; Gene Expression Profiling; Gene expression regulation; Gene Expression Regulation, Plant; Genes; Genes, Plant - genetics; Lyases - metabolism; Lycopersicon esculentum - cytology; Lycopersicon esculentum - enzymology; Lycopersicon esculentum - genetics; Lycopersicon esculentum - growth & development; Lycopersicon esculentum - physiology; Metabolic Networks and Pathways; Metabolomics - methods; Models, Biological; Plant Proteins - genetics; Plant Proteins - metabolism; Postharvest handling; Principal Component Analysis; Reproducibility of Results; Ripening; Systems Biology - methods; SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.112.206086

The concept of system 1 and system 2 ethylene biosynthesis during climacteric fruit ripening was initially described four decades ago. Although much is known about fruit development and climacteric ripening, little information is available about how ethylene biosynthesis is regulated during the postclimacteric phase. A targeted systems biology approach revealed a novel regulatory mechanism of ethylene biosynthesis of tomato (Solatium lycopersicum) when fruit have reached their maximal ethylene production level and which is characterized by a decline in ethylene biosynthesis. Ethylene production is shut down at the level of 1-aminocyclopropane-1-carboxylic acid oxidase. At the same time, 1-aminocyclopropane-1-carboxylic acid synthase activity increases. Analysis of the Yang cycle showed that the Yang cycle genes are regulated in a coordinated way and are highly expressed during postclimacteric ripening. Postclimacteric red tomatoes on the plant showed only a moderate regulation of 1-aminocyclopropane-1-carboxylic acid synthase and Yang cycle genes compared with the regulation in detached fruit. Treatment of red fruit with 1-methylcyclopropane and ethephon revealed that the shut-down mechanism in ethylene biosynthesis is developmentally programmed and only moderately ethylene sensitive. We propose that the termination of autocatalytic ethylene biosynthesis of system 2 in ripe fruit delays senescence and preserves the fruit until seed dispersal.