Submitted to: Plant Science
Publication Type: Peer reviewed journal
Publication Acceptance Date: 1/20/2008
Publication Date: 2/2/2008
Citation: Mattoo, A.K., Handa, A.K. 2008. Higher polyamines restore and invigorate metabolic memory in ripening fruit. Plant Science. 174: 386–393. Interpretive Summary: Tomato fruit and its processed products are dietary source of antioxidants, vitamins and minerals. It is a model fruit crop whose genetic manipulation has become a routine and is used to address important questions in functional genetics related to nutritional quality improvements. Until recently, fruit ripening was considered a senescence program that had reached a point of no return because of enhanced degradation of cell integrity. Ripening is delayed in tomato mutants that accumulate biogenic amines, such as putrescine, spermidine and spermine, which are ubiquitous in living organisms and collectively called polyamines. In an effort to gain insight into the role of polyamines in fruit biology, we genetically altered the levels of spermidine and spermine at the cost of putrescine by over-expressing a gene of polyamine biosynthesis. We are using these fruit as an important resource akin to a ‘gain-of-function’ mutant, providing a model system to define effects of higher polyamines on the nutrient content and genetic constituents. Our data show that a ripening fruit can be activated by spermidine/spermine to resuscitate the developmental program involving metabolic memory linked to nitrogen and carbon interactions. The nature of the genes identified and their function suggests that higher polyamines act as anabolic growth regulators. The active response of tomato fruit to engineered high levels of polyamines till late into ripening predicates that it will be possible to modulate ripening and influence nutrient levels of the fruit by rational design of genes with precision-based and ripening stage-specific promoters. These findings are of use to horticulturists, biotechnologists and molecular biologists interested in understanding how plant cells function and in manipulating nutritional content in fruits and vegetables.
Technical Abstract: Polyamines (PAs) are ubiquitous, biogenic amines that have been implicated in diverse cellular functions in most living organisms. Ever since spermine (Spm) phosphate crystals were isolated over three centuries ago, scientists have kept busy in unraveling the mystery behind biological roles of Spm and other known PAs, viz., putrescine (Put) and spermidine (Spd). Although the biosynthetic pathway of polyamines has been elucidated, the, molecular basis of their in vivo function is far from being understood. Molecular biology tools have provided a promising avenue in this direction, with success achieved in altering endogenous PAs in animals and plants by over-expression and knock-out of genes of PA biosynthesis. Transcriptome analysis and metablolite profiling of such transgenic material have yielded new information of fundamental nature about the effects of PA and their interaction with other signaling molecules. Interestingly, engineering accumulation of higher PAs, Spd and Spm, in a fruit-specific manner was found to revive metabolic activity even at late developmental stages of fruit ripening, resuscitating cellular programs underlying N:C signaling, energy and glucose metabolism. Along with these, a wide array of genes regulating transcription, translation, signal transduction, chaperone activity, stress protein, amino acid biosynthesis, ethylene biosynthesis and action, polyamine biosynthesis, isoprenoid pathway and flavonoid biosynthesis was resuscitated. Based on various reports and our results, we suggest that PAs, among other things, act as ‘surrogate messengers’ and nudge other signaling molecules, such as plant hormones and NO, to activate a vast genetic network to regulate growth, development and senescence.