Modifications in Organic Acid Profiles During Fruit Development and Ripening: Correlation or Causation?

Abstract

The pivotal role of phytohormones during fruit development and ripening is considered established knowledge in plant biology. Perhaps less well-known is the growing body of evidence suggesting that organic acids play a key function in plant development and, in particular, in fruit development, maturation and ripening. Here, we critically review the connection between organic acids and the development of both climacteric and non-climacteric fruits. By analyzing the metabolic content of different fruits during their ontogenetic trajectory, we noticed that the content of organic acids in the early stages of fruit development is directly related to the supply of substrates for respiratory processes. Although different organic acid species can be found during fruit development in general, it appears that citrate and malate play major roles in this process, as they accumulate on a broad range of climacteric and non-climacteric fruits. We further highlight the functional significance of changes in organic acid profile in fruits due to either the manipulation of fruit-specific genes or the use of fruit-specific promoters. Despite the complexity behind the fluctuation in organic acid content during fruit development and ripening, we extend our understanding on the importance of organic acids on fruit metabolism and the need to further boost future research. We suggest that engineering organic acid metabolism could improve both qualitative and quantitative traits of crop fruits.

Keywords: carbon metabolism; development; fruit; metabolism; organic acids; primary metabolism; ripening.

FIGURE 1

Comparative metabolite accumulation during fruit growth in two significant examples of climacteric (tomato, Solanum lycopersicum) and non-climacteric (pepper, Capsicum spp.) species. (A) Organic acids and sugars changes that occur in climacteric fruits during different stages of development and ripening using tomato fruit as a model of climacteric fruit. The concentration of each metabolite is dependent on the metabolic intensity and the time of development of the fruit with major changes during the climacteric peak phase (approximately 35 days after anthesis). (B) Organic acids and sugar changes that occur in non-climacteric fruit during different stages of development and ripening using pepper as a model. Although lacking a climacteric peak, fruits considered non-climacteric present metabolite profile alterations during maturation, but with lower intensities than in climacteric fruits.

FIGURE 2

Hormonal pattern changes of two significant examples of climacteric (Solanum lycopersicum) or non-climacteric (Capsicum spp.) during fruit development and ripening. (A) Differential hormones concentrations in tomato fruit during development: increases in auxin, cytokinin, gibberellin, and brassinosteroids at fruit set, followed by increases in auxin, cytokinin and gibberellin at fruit growth until maturation, which have their levels drastically reduced, with increases in ethylene and abscisic acid (ABA). (B) Differential hormonal patterns in non-climacteric fruit during development show increases in auxin, cytokinin and gibberellin during fruit set and growth, followed by reductions along the maturation phase, with increases in ABA and brassinosteroids, and few changes in ethylene.