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Title: Genetic introgression of ethylene-suppressed, long shelf-life transgenic tomatoes with higher-polyamines trait overcomes many unintended effects due to reduced ethylene on metabolome

Author
item SOBOLEV, ANATOLY - National Research Council - Italy
item Neelam, Anil
item FATIMA, TAHIRA - University Of Western Ontario
item SHUKLA, VIJAYA - Michigan State University
item HANDA, AVTAR - Purdue University
item Mattoo, Autar

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2014
Publication Date: 12/5/2014
Citation: Sobolev, A.P., Neelam, A., Fatima, T., Shukla, V., Handa, A.K., Mattoo, A.K. 2014. Genetic introgression of ethylene-suppressed, long shelf-life transgenic tomatoes with higher-polyamines trait overcomes many unintended effects due to reduced ethylene on metabolome. Frontiers in Plant Science. 5:632. DOI:10.3389/fpls.2014.00632.

Interpretive Summary: Post-harvest losses of fruit and vegetables are significant and therefore stemming such losses has been an on-going activity among horticulturalists and geneticists alike. Extending the postharvest life of fruits involved, in the past, chemical treatment, use of plastic films, and treatment with waxes and inhibitors of ethylene biosynthesis or action. Enhancing the quality attributes, particularly nutrients that potentially benefit human and animal health and flavor/aroma components that add to the produce value, has generated considerable research interest among nutraceutical and horticultural industries. Ethylene deficient fruit normally has a prolonged shelf life. We analyzed if this benefit occurs at the expense of a changed nutrient composition. Therefore, we developed an ethylene-deficient tomato line using a transgenic approach. A metabolomics approach was then applied to identify and quantify metabolites whose levels were affected in the transgenic tomato. This study shows that suppression of ethylene has a measurable impact on the metabolome of tomato fruits, the levels of many important constituents being drastically reduced. Thus, altering ethylene biosynthesis or signaling in plants by any approach to prolong shelf life of fruits penalizes the metabolic potential (nutrition) of such fruit. However, some of these unintended and unknown effects could be reversed by adding a new genetic event by developing a double transgenic plant with capacity to accumulate molecules such as polyamines. Therefore, it is essential that long shelf life produce be tested for any nutrient penalty. This information is important to horticulturists, geneticist, plant biologists and nutritionists.

Technical Abstract: Ethylene regulates a myriad physiological and biochemical processes in ripening fruits and is accepted as the ripening hormone for the climacteric fruits. However, its effects on metabolome and resulting fruit quality are not yet fully understood, particularly when some of the ripening-associated biochemical changes are independent of ethylene action. We have generated a homozygous transgenic tomato genotype (2AS-2HO) that exhibits reduced ethylene production as a result of impaired expression of the 1-aminocyclopropane-1-carboxylate synthase 2 gene by its antisense RNA. Double transgenic hybrid (2AS-2HO x SAM 579HO) developed through a genetic cross between 2AS-2HO and 579HO (Mehta et al., 2002) lines resulted in significantly higher ethylene production than either the WT or 2AS-2HO fruit. To determine the effects of reduced ethylene and introgression of higher polyamines, the metabolic profiles of ripening fruits from WT (556AZ), 2AS-2HO and 2AS-2HO x SAM 556HO lines were determined using 1H-NMR spectroscopy. The levels of Glu, Asp, AMP, Adenosine, Nucl1 and Nucl2 increased during ripening of the WT fruit. The increases in Glu, Asp, and AMP levels were attenuated in 2AS-2HO fruit but recovered in the double hybrid with higher ethylene and polyamine levels. The ripening-associated decreases in Ala, Tyr, Val, Ile, Phe, Malate and myo-Inositol levels in the 2AS-2HO line were not reversed in the double hybrid line suggesting a developmental/ripening regulated accumulation of these metabolites independent of ethylene. Significant increases in the levels of fumarate, formate, choline, Nucl1 and Nucl2 at most stages of ripening fruit were found in the double transgenic line due to introgression with higher-polyamines trait. Taken together these results show that the ripening-associated metabolic changes are both ethylene dependent and independent, and that the fruit metabolome is under the control of multiple regulators, including ethylene and polyamines.