Figure 11.2 Peach growth is biphasic, showing a double sigmoidal pattern in terms of both fresh mass and dry mass. Pericarp cell division is especially active during early stages of phase 1, while enlargement of an existing population of cells is largely responsible for growth during phase 2. (Based on Chalmers and van den Ende (1975) Aust. J. Plant Physiol. 2, 623-634)
Fruit can increase in mass or volume by 100-fold or more from fertilisation to maturity, and such changes commonly follow a sigmoid curve (Figure 11.2). Interpretation of such growth curves is complex because a single variable (mass, length, volume) is commonly applied to an object that contains several organs and different tissue types, each developing at their own rate and in accordance with their own programme. Moreover, at a cellular level, comparative levels of division and expansion change with ontogeny, while shifts in airspace percentage also play a part in volume increases. Added to this, changes in storage products (oil, starch and sugar) and structural carbohydrate (endocarp thickening) influence dry matter content. Representative cases are covered later.
Despite complexities of fruit growth and development, there are some overall consistencies in patterns of cell division and enlargement, as well as tissue differentiation and fruit enlargement (Figure 11.3). During the first 1–4 weeks, flesh volume increases rapidly and embryo volume remains small. Growth at this time is mainly the result of cell division. In many commercial fruit (e.g. apple, kiwifruit, tomato and peach), cell division may cease a few weeks after anthesis, and fruit growth slows down, reflected as an inflection in the growth curve, and signalling an end to the first sigmoid phase.
Figure 11.3 A large number of complex processes are integrated in space and time during seed development and fruit growth and are shown here schematically. In broad terms, embryo differentiation and seed development are already well advanced as pericarp enlargement gets underway, and seed maturation usually precedes onset of ripening; consequently fruit ingested prematurely still represent vehicles for seed dispersal. A phase of carbohydrate accumulation during fruit maturation gives way to starch hydrolysis and sugar storage during maturation, accompanied by a peak in ethylene output and respiratory activity as fruit ripen. (Original diagram courtesy I.B. Ferguson)
During early growth, the fertilised embryo and endosperm develop and seeds start to form (Figure 11.3). A second phase begins where the pericarp resumes growth and continues to enlarge until slowing for a second time as fruit mature. This second phase in fruit growth is mainly accomplished by cell expansion in longitudinal, radial and tangential planes. Longitudinal growth, where cells enlarge parallel to the long axis of the fruit, will often be a big factor for development of elongated fruit such as cucumber and marrow. Radial growth increases diameter as in some pumpkins. Increases in cell volume during fruit growth can be considerable. Mature watermelons end up with some of the largest parenchyma cells in the Plant Kingdom, about 0.7 mm in diameter. In contrast to this general pattern where cell division ceases after a few weeks, pericarp cells of avocado fruit continue to divide over the whole growth period so that cells in mature fruit are still relatively small.
Cell enlargement is not a uniform process. Cells in various regions of a fruit often enlarge at different rates and in different planes, so that many mature fruit show strong gradients in cell size from their surface to the centre. In apple fruit, cells closest to the core are smallest, with cell size increasing towards the fruit surface. Conversely in many berries, such as cucumber, kiwifruit and grape, the smallest cells are found in outer regions of the pericarp, with size increasing progressively towards inner regions.
Figure 11.4. Physical characteristics of apple fruit change during growth and development with a notable increase in gas space to a maximum of around 0.1 mL gas mL-1 tissue at maturity, and a corresponding decrease in cell wall mass to around 15 mg g-1 fresh mass. Cell surface area shows an early rapid decrease from around 340 cm2 mL-1 tissue. (Based on Harker and Ferguson (1988) Physiol. Plant. 74, 695-700)
Patterns of cell growth and differentiation in cell layers can influence the quality of mature fruit. For example, pepino fruit with a compact exocarp composed of tightly packed cells are less likely to bruise during postharvest handling than cultivars having large intercellular airspaces. As cell size increases during development, other accompanying characteristics also change, such as cell wall thickness, differentiation of specific cell types (e.g. sclereids) and the formation of cell inclusions such as oil droplets or calcium oxalate crystals (raphides). In feijoa and pear, development of sclereids in the mesocarp provides the characteristic gritty texture. As another example, juiciness of orange depends on prior differentiation of juice sacs in the endocarp.
The extent and distribution of airspaces are particularly important, affecting both fruit texture and physiological properties. For instance, in apple, airspace relative to fruit volume can double during development, while cell wall thickness and relative cell surface area both decline (Figure 11.4). Such changes affect gas exchange and diffusion of solutes through pericarp tissues due to increased tortuosity.
Figure 11.5. Radial growth in kiwifruit is due mainly to enlargement of outer and inner pericarp. Vertical lines indicate cessation of cell division in each tissue. (Unpublished data courtesy K. Gould and I.B. Ferguson)
In kiwifruit all tissues of the mature fruit (exocarp, outer and inner pericarp and central core) are already discernable in the ovary before anthesis and pollination. Each layer grows to a different extent and at different rates, so that the relative contribution of each to the total fruit volume varies with time (Figure 11.5). Cell division ceases first in the exocarp and last in the innermost regions of the central core. The outer pericarp is first seen as a homogeneous population of cells but by c. 14 d after pollination two cell types become visible, namely small isodiametric parenchyma cells full of starch grains, and much larger heavily vacuolate ovoid cells in which the frequency of starch grains per unit volume is low.
Fruit anatomy affects our perception of fruit quality. In kiwifruit, hairs are developed as multicellular projections of the skin, giving a characteristic bristly appearance and rough feel in the case of the green flesh ‘Hayward’ or a silky, smooth appearance in the yellow flesh ‘Hort16A’ cultivar. Tough skin relative to soft flesh is another important character imparted by development of primary cell wall thickenings in the hypodermal collenchyma.
Figure 11.6. Fruit size in Braeburn apple depends closely on the number of viable seeds per fruit (up to a normal maximum of 10 per fruit), emphasising the strong influence that seed development has on fruit growth. (Figure based on data from E.D. Broome)
Fertilisation is generally crucial for fruit set and pericarp development (Figure 11.1). As fertilised ovules develop into seeds, this influence on pericarp growth continues where production of hormones by the endosperm and developing embryo promotes pericarp growth. Indeed, there is usually a positive correlation between the number of seeds in the fruit and final fruit size (de Jong et al. 2009). The importance of seeds as sources of hormones for initiation and stimulation of fruit growth is implied by fruit response to exogenous hormones in parthenocarpic systems (development of fruit without seeds).
Applying auxin and gibberellins to unfertilised embryos is one way of achieving parthenocarpy; another is to use auxin transport inhibitors such as chloroflurenol to prevent loss of auxin from embryos so that a threshold level for pericarp response is exceeded. Studies of parthenocarpy in tomato and cucumber indicate that high auxin levels enhance embryo cell division, and this cell division phase seems to be more critical than subsequent cell expansion in determining final fruit size.
Such results imply a cooperative mode of action where gibberellins combine with auxins to initiate cell division. Seed cytokinins and cell division are similarly related because tomato seeds accumulate cytokinins that subsequently influence cell division in surrounding pericarp tissue (Gillaspy et al. 1993).
Such interdependence between seed development and fruit growth shows up in final fruit size. Parthenocarpic fruit have reduced auxin content and are generally smaller than wild-type fruit. In apple fruit, seed numbers frequently correlate with fruit growth (Figure 11.6) or with shape and size of fruit. Inadequate pollination of kiwifruit (Figure 11.1) results in distortion, and a curvilinear relationship emerges between seed number and fruit weight. A similar response is obtained when young seeds are surgically removed from immature strawberry fruit, causing a corresponding distortion in flesh development.
Despite ample evidence that natural control of fruit shape is primarily exerted by plant hormones originating from seeds and stimulating growth to varying degrees, this is not true for all fruit. In banana, fertile seeds actually suppress development of the fleshy pulp. In this anomalous case, fertilisation failure allows an ovary to grow.
In marrow, tomato and kiwifruit, ovary shape dictates spatial distribution of seeds. They in turn influence pericarp growth, so that fruit size and shape then become a function of initial ovary shape plus subsequent fertilisation and seed development.