Genetic introgression of ethylene-suppressed transgenic tomatoes with higher-polyamines trait overcomes many unintended effects due to reduced ethylene on the primary metabolome

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages

  Sobolev, Anatoly P ^a   Neelam, Anil ^b   Fatima, Tahira ^b   Shukla, Vijaya ^b   Handa, Avtar K ^c   Mattoo, Autar K ^b  

^a CNR Consiglio Nazionale delle Ricerche   (Italy)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

ACC synthase; Fruit ripening; LeACS2; Metabolome; Polyamines; Spermidine; Spermine; Transgenics

Indexed keywords

LYCOPERSICON ESCULENTUM;

EID: 84937543200     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00632     Document Type: Article

References (40)

1. Abeles, F. B., Morgan, P. W., and Saltveit, M. E. (1992). Ethylene in Plant Biology. San Diego: Academic Press.
2. Bauchot, A. D., Mottram, D. S., Dodson, A. T., and John, P. (1998). Effect of aminocyclopropane-1-carboxylic acid oxidase antisense gene on the formation of volatile esters in Cantaloupe Charentais melon (cv. Vedrantais). J. Agric. Food Chem. 46,4787-4792. doi: 10.1021/jf980692z
3. Braun, S., Kalinowski, H. O., and Berger, S. (1998). 150 and More Basic NMR Experiments, 2nd Edn. Weinheim: Wiley-VCH.
4. Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M. I., Nunes- Nesi, A., etal. (2006). Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatoryaspects of metabolic network behavior. PlantPhysiol. 142,1380-1396. doi: 10.1104/pp.106.088534
5. Davies, C., and Böttcher, C. (2014). “Other hormonal signals during ripen­ing" in Fruit Ripening, Physiology, Signalling and Genomics, eds P. Nath, M. Bouzayen, A. K. Mattoo, and J. C. Pech (Oxfordshire: CAB International), 202-216.
6. Defilippi, B. G., Dandekar, A. M., and Kader, A. A. (2004). Impact of suppression of ethylene action or biosynthesis on flavor metabolites in apple (Malus x domestica Borkh) fruits. J. Agric. Food Chem. 52, 5694-5701. doi: 10.1021/jf049504x
7. Defilippi, B. G., Dandekar, A. M., and Kader, A. A. (2005). Relationship of ethylene biosynthesis to volatile production, related enzymes, and precursor availabil­ity in apple peel and flesh tissues. J. Agric. Food Chem. 53, 3133-3141. doi: 10.1021/jf047892x
8. Fan, T. W. M. (1996). Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog. Nucl. Magn. Reson. Spectrosc. 28, 161-219. doi: 10.1016/0079-6565(95)01017-3
9. Flores, F., Yahyaoui, F. E., de Billerbeck, G., Romojaro, F., Latche, A., Bouzayen, M., et al. (2002). Role of ethylene in the biosynthetic pathway of aliphatic ester aroma volatiles in Charentais Cantaloupe melons. J. Exp. Bot. 53, 201-206. doi: 10.1093/jexbot/53.367.201
10. Fluhr, R., and Mattoo, A. K. (1996). Ethylene - biosynthesis and perception. CRC Crit. Rev. PlantSci. 15,479-523.
11. Gapper, N. E., Giovannoni, J. J., and Watkins, C. B. (2014). Understanding devel­opment and ripening of fruit crops in an ‘omics’ era. Hortic. Res. 1, 14034. doi: 10.1038/hortres.2014.34
12. Grierson, D. (2014). “Ethylene biosynthesis" in Fruit Ripening, Physiology, Sig­nalling and Genomics, eds P. Nath, M. Bouzayen, A. K. Mattoo, and J. C. Pech (Oxfordshire: CAB International), 178-192.
13. Hamilton, A., Lycett, G. W., and Grierson, D. (1990). Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346,284-287. doi: 10.1038/346284a0
14. Handa, A. K., and Mattoo, A. K. (2010). Differential and functional interactions emphasize the multiple roles of polyamines in plants. PlantPhysiol. Biochem. 48, 540-546. doi: 10.1016/j.plaphy.2010.02.009
15. Harpaz-Saad, S., Yoon, G. M., Mattoo, A., and Kieber, J. J. (2012). The formation of ACC and competition between polyamines and ethylene for SAM. Ann. Plant Rev. 44, 53-81. doi: 10.1002/9781118223086.ch3
16. Heldt, H.-W. (2005). PlantBiochemisty. Burlington: Elsevier.
17. Hiwasa-Tanase, K., and Ezura, H. (2014). “Climacteric and non-climacteric ripen­ing," in Fruit Ripening Physiology, Signalling and Genomics, eds P. Nath, M. Bouzayen, A. K. Mattoo, and J. C. Pech (Oxfordshire: CAB International), 1-14.
18. Kausch, K. D., Sobolev, A. P., Goyal, R. K., Fatima, T., Laila-Beevi, R., Saftner, R. A., et al. (2012). Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicumL.) fruit. AminoAcids 42,843-856. doi: 10.1007/s00726-011-1000-5
19. Klee, H. (1993). Ripening physiology of fruit from transgenic tomato (Lycopersicon esculentum) plants with reduced ethylene synthesis. PlantPhysiol. 102, 911-916.
20. Klie, S., Osorio, S., Tohge, T., Fabiana, M., Fait, A., Giovannoni, J. J., etal. (2013). Conserved changes in the dynamics of metabolic processes during fruit development and ripening across species. Plant Physiol. 164, 55-68. doi: 10.1104/pp.113.226142
21. Lasanajak, Y., Minocha, R., Minocha, S. C., Goyal, R., Fatima, T., Handa, A. K., et al. (2013). Enhanced flux of substrates into polyamine biosynthesis but not ethylene in tomato fruit engineered with yeast S-adenosylmethionine decarboxylase gene. Amino Acids 46, 729-742. doi: 10.1007/s00726-013-1624-8
22. Martens, H., and Martens, M. (2001). Multivariate Analysis of Quality. Chichester: JohnWiley and Sons.
23. Mattoo, A. K., Chung, S. H., Goyal, R. K., Fatima, T., Solomos, T., Srivastava, A., et al. (2007). Overaccumulation of higher polyamines in ripening transgenic tomato fruit revives metabolic memory, upregulates anabolism-related genes, and positively impacts nutritional quality. J. AOACInt. 90, 1456-1464.
24. Mattoo, A. K., and Handa, A. K. (2008). Higher polyamines restore and enhance metabolic memory in ripening fruit. Plant Sci. 174, 386-393. doi: 10.1016/j.plantsci.2008.01.011
25. Mattoo, A. K., Minocha, S. C., Minocha, R., and Handa, A. K. (2010). Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38, 405-413. doi: 10.1007/s00726-009-0399-4
26. Mattoo, A. K., and Suttle, J. C. (1991). The PlantHormone Ethylene. BocaRaton, FL: CRC Press.
27. Mattoo, A. K., Sobolev, A. P., Neelam, A., Goyal, R. K., Handa, A. K., and Segre, A. L. (2006). Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen-carbon interactions. PlantPhysiol. 142, 1759-1770. doi: 10.1104/pp.106.084400
28. Mehta, R. A., Cassol, T., Li, N., Ali, N., Handa, A. K., and Mattoo, A. K. (2002). Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality and vine life. Nat. Biotechnol. 20, 613-618. doi: 10.1038/nbt0602-613
29. Merchante, C., Vallarino, J. G., Osorio, S., Aragüez, I., Villarreal, N., Ariza, M. T., et al. (2013). Ethylene is involved in strawberryfruit ripening in an organ-specific manner. J. Exp. Bot. 64, 4421-4439. doi: 10.1093/jxb/ert257
30. Nath, P., Bouzayen, M., Mattoo, A. K., and Pech, J. C. (2014). Preface to Fruit Ripening, Physiology, Signalling and Genomics (Oxfordshire: CAB International). doi: 10.1079/9781845939625.0000
31. Oeller, P. W., Min-Wong, L., Taylor, L. P., Pike, D. A., and Theologis, A. (1991). Reversible inhibition of tomato fruit senescence byantisense RNA. Science 254, 437-439. doi: 10.1126/science.1925603
32. Osorio, S., Alba, R., Damasceno, C. M. B., Lopez-Casado, G., Lohse, M., Zanor, M. I., etal. (2011). Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. PlantPhysiol. 157, 405-425. doi: 10.1104/pp.111.175463
33. Osorio, S., Scossa, F., and Fernie, A. R. (2013). Molecular regulation of fruit ripening. Front. PlantSci. 4:198. doi: 10.3389/fpls.2013.00198
34. Paliyath, G., Murr, D. P., Handa, A. K., and Lurie, S. (2008). Postharvest Biology and Technology of Fruits, Vegetable, and Flowers. New Delhi: Wiley-Blackwell Publishing.
35. Perez-Fons, L., Wells, T., Corol, D. I., Ward, J. L., Gerrish, C., Beale, M. H., etal. (2013). A genome-wide metabolomic resource for tomato fruit from Solanum pennellii. Sci. Rep. 4, 3859. doi: 10.1038/srep03859
36. Pfitzner, A. J. P. (1998). “Transformation of tomato. Plant virology protocols: from virus isolation to transgenic resistance" in Methods in Molecular Biology, eds G. D. Foster and S. C. Taylor (Totowa, NJ: Humana Press Inc.), 359-363. doi: 10.1385/0-89603-385-6:359
37. Saltveit, M. E. (1999). Effect of ethylene on quality of fresh fruits and veg­etables. Postharvest Biol. Technol. 15, 279-292. doi: 10.1016/S0925-5214(98) 00091-X
38. Sobolev, A. P., Segre, A. L., and Lamanna, R. (2003). Proton high-field NMR study of tomato juice. Magn. Reson. Chem. 41, 237-245. doi: 10.1002/mrc.1176
39. Srivastava, A., Chung, S. H., Fatima, T., Datsenka, T., Handa, A. K., and Mattoo, A. K. (2007). Polyamines as anabolic growth regulators revealed by transcriptome analysis and metabolite profiles of tomato fruits engineered to accumulate spermi­dine and spermine. PlantBiotechnol. 24, 57-70. doi: 10.5511/plantbiotechnology.24.57
40. Wilkinson, J. Q., Lanahan, M. B., Clark, D. G., Bleecker, A. B., Chang, C., Meyerowitz, E. M., etal. (1997). A dominant mutant receptor from Arabidopsis confers ethy­lene insensitivity in heterologous plants. Nat. Biotechnol. 15, 444-447. doi: 10.1038/nbt0597-444