Update on the Roles of Polyamines in Fleshy Fruit Ripening, Senescence, and Quality

Abstract

Ripening of fleshy fruits involves complex physiological, biochemical, and molecular processes that coincide with various changes of the fruit, including texture, color, flavor, and aroma. The processes of ripening are controlled by ethylene in climacteric fruits and abscisic acid (ABA) in non-climacteric fruits. Increasing evidence is also uncovering an essential role for polyamines (PAs) in fruit ripening, especially in climacteric fruits. However, until recently breakthroughs have been made in understanding PA roles in the ripening of non-climacteric fruits. In this review, we compare the mechanisms underlying PA biosynthesis, metabolism, and action during ripening in climacteric and non-climacteric fruits at the physiological and molecular levels. The PA putrescine (Put) has a role opposite to that of spermidine/spermine (Spd/Spm) in cellular metabolism. Arginine decarboxylase (ADC) is crucial to Put biosynthesis in both climacteric and non-climacteric fruits. S-adenosylmethionine decarboxylase (SAMDC) catalyzes the conversion of Put to Spd/Spm, which marks a metabolic transition that is concomitant with the onset of fruit ripening, induced by Spd in climacteric fruits and by Spm in non-climacteric fruits. Once PA catabolism is activated by polyamine oxidase (PAO), fruit ripening and senescence are facilitated by the coordination of mechanisms that involve PAs, hydrogen peroxide (H₂O₂), ABA, ethylene, nitric oxide (NO), and calcium ions (Ca²⁺). Notably, a signal derived from PAO5-mediated PA metabolism has recently been identified in strawberry, a model system for non-climacteric fruits, providing a deeper understanding of the regulatory roles played by PAs in fleshy fruit ripening.

Keywords: ABA; Ca2+; NO; ethylene; fruit ripening; polyamines; review.

FIGURE 1

A proposed outline of the roles of polyamines during fruit ripening in climacteric and non-climacteric fruits. We propose a complex regulatory network, centered on the polyamine (PA) compounds Put, Spd, and Spm, metabolic enzymes (ADC, ODC, SAMDC, SPDS, and SPMS), and regulators (ethylene, ABA, NO, H₂O₂, and Ca²⁺) in tomato and strawberry, representing climacteric and non-climacteric fruits, respectively. PA biosynthesis begins mainly via Arg rather than Orn: ADC is crucial in both climacteric and non-climacteric fruits. SAM-derived dcSAM, catalyzed by SAMDC, is a key step in the biosynthesis of Spd and Spm. High Put levels inhibit fruit ripening, while high Spd and Spm contents promote fruit ripening. A synergetic regulation of SAMDC with SPDS for the production of Spd is critical for climacteric fruits, and of SAMDC with SPMS for the production of Spm for non-climacteric fruits. PAO-mediated PA metabolism of Spd/Spm produces H₂O₂ (rather than by CuAO/DAO), which together with ABA, ethylene, NO, and Ca²⁺ constitute a complex network. Put and ethylene form a negatively coordinated loop in climacteric fruit ripening. Spd/Spm and ABA comprise a positively coordinated loop for ripening, especially in non-climacteric fruit ripening. Solid lines represent core metabolic pathways. Dotted lines represent accessory metabolic pathways. The symbols represent promotion and inhibition, respectively. PA, polyamine; Put, putrescine; Spd, spermidine; Spm, spermine; Arg: arginine; Org, ornithine; SAM, S-adenosyl-L-methionine; dcSAM, decarboxylated SAM; ODC, ornithine decarboxylase; CuAO/DAO, copper amine oxidase/diamine oxidases; PAO, polyamine oxidases; ADC, arginine decarboxylase; SPDS, Spd synthase; SPMS, Spm synthase; SAMDC, SAM decarboxylase; Eth, ethylene; ABA, abscisic acid; NO, nitric oxide; H₂O₂, hydrogen peroxide.