1. Introduction

In the plant kingdom, fruit ripening is a coordinated process that requires the change in expression of hundreds to thousands of genes to modify many biochemical and physiological signals including carbohydrate and organic acids metabolism, cell wall restructuring, ethylene production, stress response, and organoleptic compound formation. Several studies have tried to comprehend the main processes that take place during the transformation between a green fruit to ripe fruit, understanding horticultural maturity as the moment when the “plant or plant part possesses the prerequisites for utilization by consumers for a particular purpose” [1]. Ripening was also described by this author as “the composite of processes that occur from the later stages of growth and development through the early stages of senescence and that results in characteristic aesthetic and/or food quality, as evidenced by changes in composition, color, texture, or other sensory attributes” [1]. Ripening is a well-known step of fruit development and has been extensively studied because of the importance of accurately describing the exact point where the fruit expresses greater nutritional and economic value. Senescence is the process that follows fruit ripening and leads to the death of tissue. Though it is not lethal, senescence increases the susceptibility to disease, injury, dehydration, or microbial invasion. It is hard to discriminate between these stages since they sometimes overlap, but ripening includes processes like pigment accumulation and cell wall changes that are not usually involved in senescence processes [2].

Fruit ripening leads to the breakdown of complex carbohydrates into sugars, fruit firmness reductions (softening by cell wall degradation and cuticle properties alteration), color changes (loss of green color by chlorophylls degradation and increase in non-photosynthetic pigments like anthocyanins and carotenoids), acidity decreases, and aroma increases (production and release of organic volatile compounds) ^[3][4][3,4]. This process contributes to increased attractiveness and acceptance by consumers (Figure 1). Mainly, the composition of sugars, acids, color, and aroma depends on genetics; however, culture practices and environmental factors strongly influence fruit quality characters [5]. Understanding ripening mechanisms will make it feasible to implement agronomical strategies optimized to climatic conditions, enhance production, increase fruit quality, and facilitate the selection of new apricot varieties. Therefore, in this review, ripening was extensively studied because of the importance of defining exactly when a fruit displays the highest nutritional and economic value, thus rendering fruits more attractive and palatable due to the acquisition of fruit quality traits.

Figure 1.

Traditional and new Spanish apricot cultivars at consumer ripening state.

Additionally, fruit development is a regulated process unique to plants that involves three distinct steps: fruit set, fruit growth, and ripening. Fruit development finishes when the fruit is ripe and is defined as the optimum moment for harvest the fruit from the point of view of the consumer. Each step is controlled by genetic and environmental factors, influenced by culture practices. Each of these factors interacts in a multilevel process and triggers the coordinated action of master regulators, including hormone signaling, microRNAs, and epigenetic modifying genes [6]. On the other hand, the epigenetic regulation of gene expression has been recognized as remodeling gene expression during the ripening process ^[7][8][7,8], mainly by the DNA methylation of targeted loci involved in gene expression regulation. The presence of tissue-specific methylation patterns and the progressive demethylation of ripening-related gene promoters give tissue specificity and developmental stage-dependent gene expression that may be used as a strategy to monitoring ripening process ^[8][9][8,9].

In Prunus species including peaches, nectarines, (Prunus persica (L.) Batsch), prunes (Prunus domestica L.), Japanese plums (Prunus salicina Lindl), apricots (Prunus armeniaca L.) and sweet (Prunus avium L.) (2n = 2x = 16) and sour (Prunus cerasus L.) cherry fruits, four stages have been described during fruit development and ripening: S1: fruit growth; S2: green fruit; S3: changing color; and S4: physiological ripening (Figure 2). The beginning of S1 is characterized by fruit set and growth. A decrease in fruit growth at the S1/S2 transition is followed by endocarp lignification (stone hardening), from the middle of S2 to its end. The S3 phase begins with additional growth activation, mainly due to the increase in the number of cells, thus generating the second exponential growth phase. The maturation of the fruit is completed at the end of S3, and then the last ripening phase S4 occurs when the fruit fully develops its quality traits. The fruit developmental phases are determined using a mathematical model based on the first derivative of the growth cumulative curve, represented by a double sigmoid pattern. The identification and characterization of each phase of fruit growth are necessary for development studies and the precision harvesting of high quality fruits [10].

Figure 2. Stages of fruit development and ripening in apricot fruits. After flower bloom, pollination and fruit set, fruit growth begin with a fruit enlargement, stopping the size increase during stone hardening (S1). The reactivation of grown at green stage (S2) is followed by a color change in half-ripe fruit (S3). Maturation and ripening end at physiological ripening, when the fruit reaches the maximum sucrose accumulation and definitive color (S4).

On the other hand, fruits have been classified into two physiological groups with two distinct ripening fruit mechanisms—climacteric and non-climacteric—based on the presence or absence of a ripening-associated rise of ethylene and an increase of the respiration ratio. In climacteric fruits, such as Prunus species, the ripening process is marked by an increased respiration ratio induced by ethylene, while in non-climacteric fruits, it is controlled by an ethylene-independent process with little change in the respiration rate [11]. The attribute acquisition during the ripening process in climacteric fruit differs among species, varieties, nutritional feeds, and environments. The most significant changes during ripening are represented in Table 1 ^[2][3][2,3]. In the final phase of fruit ripening, oxidative processes with the accumulation of hydrogen peroxide and membrane lipid peroxidation occur. The identification of enzymes from the cell antioxidant systems including catalase (CAT), peroxidase (POX), and superoxide dismutase (SOD)involved in the scavenging of reactive oxygen species (ROS), is a symptom of the onset of the senescence ^[12][13][12,13].

Prunus species, as climacteric fruits, have a short ripening period and shelf-life after harvest, with a fast period of softening. The fruit firmness, soluble sugar content, and color changes are the parameters used to define the maturity stage, where a loss of firmness during ripening is the main limitation for apricot harvesting and commercialization. Hence, apricot fruit is often harvested unripe and still firm, stored at low temperature for some time and then moved to market to extend the supply period ^[5][14][5,14].

Fleshy fruits are enriched in flavor, mineral compounds, dietary fiber, vitamins, and antioxidants that make them an essential component of the human diet [15]. In this sense, fruit quality is a crucial factor for fruit consumption and acceptance by consumers, mainly due to the current situation of high competition in the markets with the presence of numerous new cultivars. In the case of Prunus, fruit quality is a complex human concept that includes sensory characteristics (including texture, taste, and aroma), aesthetic attributes (appearance, defect presence, sphericity, density, and firmness), and functional and nutritional values [16]. Consumers cherish the beauty and aromatic flavor of high-quality Prunus fruits, while other parameters, such as large fruit size, ease of handling, minimum processing, and long post-harvest shelf-life, are especially considered by the fruit industry. Therefore, the requirements by consumers and the priorities of Prunus breeding programs have led to the evolution of fruit quality parameters in the last few decades, increasing fruit taste with a good balance of sugars and acidity, improving attractiveness with orange flesh and reddish blush colors, and improving post-harvest behavior and shelf-lives ^[9][16][9,16]. From the point of view of the consumers, these traits increase the attractiveness and acceptance of new Prunus cultivars enriched in phenylpropanoids, carotenoids, and other nutraceutical compounds highly beneficial for human health ^{[17][18][19][20][21]}[17,18,19,20,21].

At this moment, the level of information on the molecular switch that occurs during the transition from unripe to ripe fruits is limited. Increasing this knowledge will have important consequences from a breeding point of view. During fruit development, fruit becomes ripe due to changes in physiological structure and biochemical composition, resulting in unique aesthetic and fruit quality traits. The regulation of this process is affected by various internal factors (epigenetic developmental signals, hormone signaling, microRNA regulation) and external factors (light, temperature, nutrition, humidity, and biotic and abiotic stress) involving exchanges between the fruit and its environment. Therefore, fruit should be examined as an integrated system of biological process network [22]. Most Prunus fruit quality traits, such as sugar content, acidity, fruit color, firmness, and enrichment in nutraceutical and antioxidant components are controlled by a polygenic expression, quantitatively inherited, and influenced by environment stimuli and internal signaling grow regulators. From the genomic point of view, the variation of these traits has been traditionally studied following quantitative genetics approaches such as the correlation of genetic marker–trait association analysis and transcriptomic analysis for differential gene expression in order to elucidate the implied molecular mechanism. Hence, integrated phenotypic, metabolomic, genomic, and transcriptomic analysis of this complex process must be addressed because of the many applications in breeding that are oriented towards the increase of fruit quality traits related to the handling, processing, marketing, and consumption phases [23].