Abstract
Horticultural industries are increasingly crucial in providing livelihoods, food quality, profits, and economic growth. In many horticultural plants, extensive studies were conducted to study the roles of hormones, epigenetics, and genes in regulating the development of cell number, cell size, fruit size, fruit weight, and endo-reduplication primarily via a gene-mapping technique known as quantitative trait loci (QTL). In general, these plants encompassed those with full-genomes sequenced, such as the apple, tomato, strawberry, and bananas. However, apart from fully sequenced apple genomes, the genome sequences of many other plants, particularly highly profitable tropical fruits, such as mangoes, pineapples, durians, and coconuts are yet available. This chapter will describe the interplay of plant hormones in determining fruit cell number and cell size, which, in turn, affects the final fruit size in horticultural plants.
Keywords
- fruit development
- plant hormones
- cross-talk
- fruit size
- hormonal control
1. Introduction
1.1 Origin of apple fruit cultivars
Apple (
2. Fruit development
2.1 Stages of fruit development
Fruiting bodies of the Angiosperms range from a completely dry fruit, such as
Fruit development involves fruit set, cell division, cell expansion, and ripening. In accessory fruits, like apples, fruit set is the initiation phase of fruit development, encompassing development of the ovaries and its accessory organs into a rapidly growing young fruit. This happens during and soon after fertilisation has been completed [13]. If fertilisation does not happen, the fruit will be abscised or be small, resulting in very few or no seeds [12]. A successful fertilisation process is influenced by several factors, including adequate pollination, nutrition, and optimum temperature [12]. Fruit produced without fertilisation could be an advantage for improvement of many crops as seedless fruits are easy to consume. Therefore, tomato mutants that exhibit parthenocarpic (seedless) fruit growth in the absence of fertilisation have been extensively studied [14].
For fruit set to take place, pollination and fertilisation must be accomplished or the flowers will be abscised [13, 15, 16]. Pollination is the crucial starting point in fruit development as it is required for fertilisation. During fruit set, rapid cell division occurs and then stops when the fruit reaches its mature size [16, 17, 18]. Levels of plant hormones, such as auxins, CKs (CKs), and gibberellic acids (GAs), increase to promote fruit set [13, 16]. In tomato, after successful fertilisation, ovary development into a fruit starts with cell division until roughly 10–14 days, and during the following six to seven weeks, the fruit grows by cell expansion [14]. During cell division, which starts during fruit setting and continues until three to four weeks after pollination, the concentrations of auxin, CK and GA increase to stimulate and support the process [14, 19, 20].
Cell division ceases to allow cell expansion to then take place. Auxin, gibberellin (GA), brassinosteroid (BR) and abscisic acid (ABA) levels rise during cell expansion [13], which continues until the end of ripening, reaches its peak at 40–60 days after anthesis and becomes constant during ripening [1]. Fruit ripening is a developmental process involving physiological and metabolic changes of colour, texture, aroma, and nutritional status [21]. These changes are helpful in promoting seed dispersal by making it attractive to birds and animals. With the onset of ripening, auxin stimulates ethylene production until reaching its optimum concentration, but it can also delay ripening [22, 23]. ABA and ethylene are produced during ripening to regulate ripening [22].
2.2 Cell differentiation
At the cellular level, fruit cells undergo a differentiation process in order to change into mature cells. The term differentiation is sometimes used in two different manners: 1) it may be used to describe the development of different specialised types of mature cells within an organ or tissue; 2) it can refer to the changes that occur during the development of a meristematic cell into a mature cell, which usually involves cell division and cell expansion [24]. For the purposes of this study, cell differentiation was defined as changes of undifferentiated meristematic cells into differentiated cells that divide, expand, and ripen. The early phase of apple fruit development involves rapid cell division where the cell number is greatly amplified prior to exit from cell division at approximately 24 days after full bloom (DAFB) [25]. Final fruit size is determined by the extent of cell division and cell expansion during growth and development. Therefore, understanding cell cycle regulation and cell expansion is important to the study of fruit development in plants [26].
Once cell proliferation has ceased, cells generally undergo an expansion process that results in water uptake into the central vacuole [24]. Plant cells are large, pressurised, and have a large central vacuole that allows accumulation of water and solutes, along with a strong cell wall [27]. The cell wall is made up of a mixture of carbohydrates and a small amount of proteins, making it rigid yet extensible [28]. During cell division, cells are divided from one cell into two cells while cell expansion occurs because of the expanded vacuole, ensuing in volume growth beyond the size of the mother cell before mitosis [29]. Water uptake and cell turgor are the main factors behind the expansion process. Though the cell size increased, it was generally assumed that little to no increase in cytoplasmic mass occur [30]. Rather, it is the vacuole that grows considerably in volume and the cell wall become thinner as it is stretched and new cell wall material is added to maintain wall thickness. To allow the cell wall to grow, transcripts encoding wall-loosening enzymes, such as polygalacturonase (PG), are up-regulated and newly deposited cell wall materials are hydrated resulting in relaxation and extensive thinning of the wall [31]. Other classes of cell wall-modifying enzymes/proteins are also involved in this process, such as pectin methylesterase (PME), β-galactosidase (β-gal), endo-1,4-β-glucanase (EGAe), xyloglucan endotransglucosylase/hydrolase (XTH), and expansins [32]. These enzymes also interact synergistically by promoting ripening through disassembling the pectin of the cell wall that results in fruit softening. The secondary wall is deposited after expansion has ceased, becoming impermeable and providing strength to cells and tissues [33].
3. Hormonal control during early fruit development
After fruit set, fruit undergo cell division and subsequently cell expansion stage. It is difficult to separate fruit set from subsequent stages of fruit development, though auxin and GA are indeed key in the sustained growth of fruit. Plant hormones such as CK and auxins are involved mostly in cell division and cell expansion during fruit development [34]. These hormones have been well-documented in stimulating cell cycle activity [13]. Auxin and GA co-regulate fruit set via auxin activation of GA synthesis [35]. Therefore, auxin and GA have been widely used to increase fruit set by inducing parthenocarpic growth in many crops [36]. For example, GA or auxin treatments to tomatoes can lead to parthenocarpic fruit development [17, 37, 38, 39, 40, 41]. Silencing of
In normal fruit development, successful pollination and fertilisation induces an increase in both auxin and GA concentrations within the ovary [14, 45, 46, 47]. Japanese pears produced larger fruits as a result of hand pollination, indicating that an increased number of fertilised stigma leads to higher levels of GA being produced by the pollen, therefore enhancing cell division and development of larger fruit [48]. This suggests that GA is critical in pollination and fertilisation [43]. Treatment of tomato ovaries with auxin causes the formation of fruits with a higher number of pericarp cells from cell division stimulation by auxin compared to GA-induced fruits that consist of fewer cell numbers but larger cells because of GA cell’s enlargement role during fruit growth [13]. Normal-sized fruits undergo a balance cell division and cell expansion processes as a result of stable concentrations of both auxin and GA [49]. In addition, GA is also involved in the growth of certain fruits without the help of auxin and the outcome are fruit sizes that are twice as large, as shown in a transgenic tomato (
Another important function of GA in fruit development is to stimulate organ growth [51]. GA also features in germination, flowering, and fruit set in many plant species [40, 52, 53]. GA concentrations during fruit development increase twice; once during early fruit growth in order to trigger cell division and a second time during cell expansion [18]. During early development, GA is produced by pollen to facilitate pollen tube growth and germination [14]. As the pollen will transfer some GA into the ovary to trigger fruit growth [14, 38], an elevated GA concentration in the ovaries following pollination (which later cause auxin levels to increase [18]) suggests that both are involved together in fruit set and growth of tomato [40]. Studies on GA during cell division have been reported in hypocotyls of cucumber and tomato [48, 54]. GA is also reported to induce and maintain cell expansion [18, 48, 55] when auxin concentrations have decreased [18]. The function of GA in cell expansion is supported by the findings of larger cells in GA3-induced fruit (parthenocarpic) compared to seeded fruit even though the fruit size was smaller than the seeded [14]. Application of 2,4-D and GA3 together results in same size and shape of cells of parthenocarpic fruit as seeded fruit [14]. GA maintains cell expansion when it is used during the early stage of cell expansion in Japanese pears, resulting in larger fruits compared with untreated fruits [48, 56, 57, 58]. Meanwhile, in tracheid element differentiation, application of GA3 in conjunction with auxin results in substantial tracheid expansion as GA causes the cell to expand while application of auxin only results in short tracheid growth [59]. This shows that both auxin and GA play a coordinated role in controlling cell division and cell expansion, probably based on a common response pathway. Early hypotheses speculated that GA may cause an increase in auxin biosynthesis or transport [60].
Meanwhile, the function of auxin during fruit set is demonstrated by its presence in pollen, its production in the stalk (style), and during fertilisation [14]. Its role in tomato fruit set regulation has been described by De Jong et al. [42] through the loss-of-function of
Besides fruit set, auxin is also known for promoting cell division and cell expansion [24]. While CKs control cyclin activity during the transition phase between G1 to S during the cell cycle (which will be discussed further later), auxin’s involvement in the cell cycle occurs much earlier than that by acting as a permissive signal for cell division to start [64]. However, this process is not yet fully understood [64, 65, 66]. Much research has been carried out focusing on identifying auxins` role in regulating cell differentiation in plants. For example, an auxin gene, auxin response factor (
Along with auxin and GA, CK and ABA are also believed to be involved in fruit set. However, the cross-talk between them during fruit development is only partly understood. ABA is also involved in long-term developmental plant growth processes. While auxins, CKs, and BR are involved in early development, ABA is mainly present in the later stage of development where cell maturation transpires. During pollination of tomato fruit, where auxin and GA are present, ABA concentrations decrease while those of CK increase [69]. ABA concentrations continue to decrease shortly after pollination [69], and validated by a decrease in the mRNA levels of ABA biosynthesis genes after pollination [49] and the diminution of ABA concentrations in tomato pistils after pollination [70]. However, higher concentrations of ABA were observed in pollinated fruits compared to that in parthenocarpic fruits [71]. Despite being suppressed during and shortly after pollination in tomato fruit, ABA levels rose afterwards to support fruit set where they were detected about 5 days after pollination, enhanced in seed and pericarp until 30–50 days after pollination, with concentrations also increasing during cell expansion [20]. In rice (
Auxin role in regulating cell division by stimulating cell cycle progression has been discussed earlier. As for CKs, reducing CKs concentrations by overexpression of an inactivating enzyme [74, 75] and insensitivity to the hormone cause dwarfism because of reduced cell numbers in
BRs play an important role in early fruit development by promoting cell division, cell expansion in the stem, inhibiting root growth, promote xylem differentiation, ripening, and abscission [85, 86, 87, 88] such as in tomato [89, 90], grape berry [91], and cucumber [36, 92]. In tomato fruit, treatment with BR restores the dry mass content, sugar, and amino acid levels in dwarf tomato mutants, showing that BR is required for tomato fruit development [89, 92]. In cucumber, the application of exogenous BR to a cultivar without parthenocarpic capacity induces parthenocarpic growth and increases cell division via cell cycle-related gene expression [36]. In contrast, application of a BR biosynthesis inhibitor (brassinazole (Brz)) to a cucumber cultivar with parthenocarpic growth blocks fruit set, whereas this inhibitory effect was subsequently reversed by applying exogenous BR [36].
4. Fruit ripening, ethylene biosynthesis, and other related hormones
In general, there are two types of fruits based on the rate of respiration. Non-climacteric fruits do not increase ethylene production when they ripen [93]. Climacteric fruits require synthesis, perception, and signal transduction of the plant hormone ethylene in order to fully ripen [94]. In climacteric fruits, when ethylene is detected, they undergo autocatalytic ethylene biosynthesis and increased cell respiration, denoted by increased CO2 production, which leads to fruit ripening [93]. Non-climacteric fruit, such as strawberries, grapes and citrus, require ethylene for certain ripening processes, such as skin de-greening, and do not undergo the autocatalytic response observed in climacteric fruit [94].
The inability of transgenic tomato plants to ripen where ethylene biosynthesis has been disrupted shows that the autocatalytic burst of ethylene biosynthesis is essential for climacteric fruit ripening [95]. Nevertheless, the distinction between climacteric and non-climacteric is not clearly delimited; closely related species of melon can be either climacteric, such as the cantaloupes, or non-climacteric like the ‘honey dew’ melon [94]. Climacteric fruit spans an evolutionarily wide range of angiosperm taxa, from eudicotyledons, such as tomato and apple, to monocotyledons like the banana [96]. Climacteric fruits are advantageous from an economic perspective as they are able to continue ripening even when removed from the plant [97]. This allows the fruit to be harvested and transported before they are fully ripe, resulting in reduced loss through fruit spoilage in transit [97]. Many non-climacteric fruit lack this ability and must ripen on the plant [97].
In the ethylene biosynthetic pathway, L-methionine is the main precursor which is then transformed into ethylene by the enzymes 1-aminocyclopropane-1-carboxylate (ACC) synthase (ACS) and ACC oxidase (ACO). ACS and ACO are encoded by multigene families in various plant species [98]. In addition, ethylene production can be brought about by using propylene with climacteric fruit (but not in non-climacteric type fruit). In apple fruit, the level of
A number of investigations have been carried out on the ripening process at both the biochemical and genetic levels in many fruits, with tomato being the classical model of choice for fleshy fruit ripening [94, 96]. As tomato ripens, it undergoes a colour change from green to red through the transformation of chloroplasts to chromoplasts [104]. Then, the fruit softens and its texture changes as the fruit cell wall is modified and partially disassembled by enzymes [104]. Alteration of specific volatiles concentrations and the sugar-acid balance will lead to the development of flavours associated with a ripened tomato [104]. Similar changes occur during ethylene-induced ripening in apples and a number of other fruits [104]. When fruits ripen, cellular turgor pressure is decreased, the cell wall is dissembled, and cell adhesion is reduced, resulting in fruit softening; a process which is facilitated by many classes of cell wall-modifying enzymes such as PG, PME, β-gal, XTH, and expansin [32, 99].
ABA concentrations are very low in unripe fruit but increase when the fruit ripens [105]. This happens in both climacteric fruits, such as mango [93], pear, avocado, and apple [106], and non-climacteric fruits like citrus [107], cherry [108], and grapes [109]. In climacteric fruits like apples, ABA concentrations increase from maturation to harvest, while in non-climacteric sweet cherries, ABA concentrations increase before maturation and decrease until harvest [105, 110]. ABA appears to have a similar function to ethylene in regulating the changes of fruit during ripening by supporting the colour changes, cell wall metabolism, fruit softening, and sugar and acid metabolism [105].
In climacteric tomato fruit, BR has been reported to promote the ripening process through increasing ethylene production and lowering chlorophyll levels [90, 92, 93]. However, in mango, low concentrations of castasterone and brassinolide are present throughout the ripening period indicating that BR is unlikely to modulate ripening [93]. Chai et al. [92] demonstrated that BRs are involved in strawberry fruit ripening through downregulating the BR receptor gene (
5. Conclusions
The molecular mechanisms controlling fruit growth and fruit size in apples have yet to be fully understood [26]. The recent publication of the genome sequence of apple provides a powerful tool to reveal the underlying mechanisms during fruit development [5].
Acknowledgments
I would like to express appreciation to the University of Auckland, New Zealand, for my doctorate studies opportunity. An appreciation also goes to Malaysia Ministry of Education and Universiti Teknologi MARA (UiTM) for my doctorate financial support.
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