FRUIT DEVELOPMENTAND SENESCENCE
CHARLES W. COGGINS, JR.
Introduction
The mature citrus fruit represents the end of a complex set of events starting
with the formation of reproductive structures we call flowers. Likewise. the forma-
tion of flowers is preceded by complex and incompletely understood physiological
processes and morphological changes. The purpose of this lecture is to briefly
describe (not explain) some of the .orphological and horticultural changes between the
time citrus flowers open and fruits mature. This lecture draws heavily on the 4 papers
cited. on the author's experience and knowledge of appropriate literature. and on the
author's research.
Morphological Changes
Between full-bloom and aaturation, cell division, cell differentiation, and cell
growth convert a small citrus ovary into a fruit of considerable economic value. Gen-
erally, large-fruited citrus varieties start ou~ with relatively large flowers which
have relatively large ovaries. In the case of Valencia orange, the transition from an
ovary at full-bloom to a aature fruit represents something on the order of a 4,000-
fold increase in size. That is, an ovary of approximately 0.04 ml with 8 to 12
carpels develops int9 a aature fruit of 160 ml containing 4,000 or 80 juice sacs in 8
to 12 segments.
Excellent fruit development studies have been done by Bain (1958) and Holtzhausen
(1969) on Valencia and navel orange, respectively. Also, in 1981, Holtzhausen referred
to a useful unpublished (M.Sc. thesis) study made by Button on grapefruit. ~ecause
these studies are in close agreement, I have assumed that their findings are generally
applicable to citrus.
Figure 1 is a diagram8atic representation of a citrus ovary at full-bloom. A
brief review of the location of various tissues will make the following discussion
1DOre Maningful.
Stone fruits, fig, raspberry, blueberry, grape, and olive have a double sigmoid
growth curve. Apple, pear, date, pineapple, banana, avocado, strawberry, tomato,
melon, and citrus fruits have a single sig80id curve as shown in Figure 2 for grape-
fruit.
Whether the growth pattern of a fruit fits a single or a double sigmoid curve
cannot be used to decide whether the fruit is of the climacteric or nonclimacteric
type. For example, a sharp rise in respiration is associated with the ripening of an
avocado. No such rise is seen at any Iftaturation stage of citrus fruits. Avocado and
citrus have a single sigmoid growth curve. Avocado is a climacteric fruit and citrus
fruits are nonclimacteric.
Stage I.--Bain described 3 stages of development for the Valencia orange. Stage
I is a period of slow volume growth but of intense cell division throughout all
tissues. This period requires approximately 9 weeks. Subsequently, cell division is
found only in the outer layers of the peel and in juice sacs. Roltzhausen found
essentially the same for the navel orange, including a time span of 9 weeks. Because
the navel orange matures in considerably less time than the Valencia orange, it is
obvioua that the navel orange spends lesa tilE at Stages II and III than does the
Valencia. However, apart from time differences, the developmental events are similar
for these cultivars.
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In Stage I. fruit growth is due to cell divi8ion and cell enlargement. Oil
glands present at full-bloom enlarge and new ones appear. Juice sacs are present at
full-bloom and continue to be formed throughout Stage I. Growth of juice sacs during
Stage I is primarily by cell division. which occurs mainly at the head of developing
sacs. However. most of the volume growth that occurs in Stage I is due to the peel.
For example. Bain found that the peel made up 95% of the fruit volume at the end of
Stage I.
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1. (left panel). Diagrammatic cr08s-section of a citrus fruit (adapted from
Holtzhausen, 1969).
2. (right panel). Development of the grapefruit (adapted from Button as
reported by Holtzhausen, 1981).
Stage II.--The demarcation between stages is not abrupt, but Stage II is charac-
terized by very rapid fruit growth. During this period, cell enlargement and cell
differentiation predo8inate. Except for the epider8is, the outer layers of the
flavedo, and the tips of juice sacs, cell division has concluded by the beginning of
Stage II.
During the early parts of Stage II, the peel grows in thickness, mainly by
en~arge~nt of albedo cells. Subseqtlently. the peel beco~s thinner in concert with
rapid growth of the pulp seg18ents. During the ti~ the peel beco~s thinner, the
albedo cells continue to enlarge. The peel becomes thinne~ because the albedo cells
enlarge primarily in the tangential direction via growth of arms (Fig. 3). At this
stage of develop..nt, albedo cells have the general shape of spiders positioned such
that they join one another at the tips of their legs. This forms a spongy tissue. Due
to further growth of the arms of these cells, considerable increase in circu8ference
along with a decrease in rind thickness occurs. This growth pattern results in fewer
cell layers than existed in the peel at the end of Stage I.
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The same kind of spongy tissue that develops in the albedo also develops in the
central axis and in septua tissue. In absolute terms, there is considerable growth
in all these tissues during Stage II. Rowever, in absolute as well as relative terms,
the increase in size during Stage II is due mainly to growth of the pulp segments. For
example, at the end of Stage I, Bain reported that the central axis and pulp accounted
for 5% of the volume of the developing Valencia orange. At the end of Stage II, she
found that the central axis and pulp accounted for 58% of the volume and 67% of the
fresh weight of the fruit. Most of this is due to pulp segments--juice sacs become
larger and juice content increases in the enlarging cells of the juice sacs.
The relative contribution of the central axis, endocarp (pulp segments.) and peel
to the cross-sectional area of the navel orange throughout development is shown in
Figure 4. Even though cross-sectional area figures are less dramatic than volume
changes, it is clear that the endocarp is a minor constituent at full-bloom and
becomes the major constituent as fruit growth proceeds.
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Flg. 3. (left panel). Development of albedo cells - Stage II (adapted from
1958).
Pig. 4. (right panel). Development of the navel orange fruit (adapted
Holtzhausen, 1969).
Stage III.--Tbis is the maturation period. Although volu8e growth continues for
essentially as long as the fruit remains on the tree, the rate of growth is consider-
ably lower than in Stage II. Fissures develop in the central axis and in the albedo
of many cultivars. In so~ cultivars, the albedo becomes a minor constituent, and in
these cultivars, the peel can be removed with great ease.
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In subtropical climates, chlorophyll pigments disappear from the flavedo and
carotenoid pigments are revealed. In many cultivars, carotenoids increase substan-
tially and/or are converted into highly colored pigments during and after the loss of
chlorophyll from the flavedo. Depending on the type of citrus fruit being considered,
regreening occurs during Stage III.
Sugars and water continue to accumulate in juice sacs and the concentration of
organic acids decreases.
Sumaary.--Now that you have a general idea of morphological changes that occur
during development, let's briefly look at the summation of changes that occur in the
variOU8 parts of the fruit. We will start with the outer-most part and proceed
inward.
The cuticle is very thin at full-blooa and becomes SO8ewhat thicker during growth
and development. Wax components of the cuticle increase substantially in quantity
and complexity. Stomata appear several weeks after full-bloom and become somewhat
plugged during saturation and senescence. The epldera1s is one cell layer deep and
cell size increases little, if any, during fruit growth. The tremendous increase in
circumference is brought about primarily by continued cell division.
Cell division and cell enlargement occur in the outer layers of the flavedo up
to maturity. Growth of the inner layer of the flavedo and growth of the albedo is
due to cell division and enlargement through Stage I, and to cell enlargement there-
after. Oil glands are present at full-bloom and new ones develop continuously. Oil
glands enlarge throughout fruit Jrowth and develop~nt.
Some juice sac primordia are present at full-bloom on dorsal and lateral walls of
the locules. During Stage It the number and size of primordia increase. Cell division
occurs in the tips of juice sacs into the early part of Stage II. Subsequent growth
is due to cell enlargement. The bulk of the tissue between the segments and in the
central axis consists of cells that follow a developmental pattern similar to those
of the albedo. That ist cell division and enlargement occur during Stage I and subse-
quent growth is due to the development of multi-armed cells which form a spongy tissue.
Vascular bundles increase in length and cross-sectional area during fruit develop-
ment. The dorsal bundle, which probably transports the photosynthate stored in juice
sacs, has a larger cross-sectional area than the ventral and lateral bundles.
Final fruit size is a product of cell division and cell enlargement. Cell divi-
sion predominates in Stage I, cell enlargement Is the main feature of Stag~ II, and
..turation events characterize Stage III.
Horticultural Changes
Brix and Acid. Juice sacs are the primary site for the accumulation of soluble
solids. The absolute quantity of soluble solids (primarily sugars and organic acids)
increases trenendously during growth and development, but toward the end of Stage .II,
the aaount of acid relative to the remainder of the soluble solids decreases. Once
the soluble solids-to-acid ratio reaches specific levels in oranges, grapefruit,
tangerines, and mandarins, the fruit are said to be mature and of edible quality.
Subsequently, the concentration of acid continues to decrease. This causes the ratio
to increase. Eventually the solids-to-acid ratio beCO8eS so high that the juice is
insipid and the fruit is judged to be overaature, or senescent.
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Pigments .--Chlorophyll and somecarotenoid pigments are present in flavedo tissue
at full-bloom and throughout Stage II in all cultivars. In many cultivars, especially
in subtropical climates, essentially all of the chlorophyll disappears from the
flavedo sometime during Stage III. In many cultivars, such as white grapefruit, the
loss of chlorophyll simply reveals the carotenoid pigments. In other cultivars,
additional and different carotenoids accumulate in the flavedo, giving the fruit its
characteristic mature color. Carotenoids also accumulate in juice sacs. These
pigments are not water soluble. In some cultivars, for example the blood orange,
water-soluble pigments, called anthocyanins, also accumulate in juice sacs and in
cells of the flavedo. As mentioned earlier, regreening can occur in the flavedo.
Regreening is favored by high nitrogen and high potassium nutrition and by warm
weather.
Rind Integrity.--At the end of Stage II. the rind is physically strong. During
Stage III, the rind softens rapidly and then continues to soften at a slower rate for
essentially as long as the fruit is kept on the tree. Whether rapid softening occurs
early or somewhat later in Stage III varies with cultivars. Softening seems to be
related to fissures which develop in the albedo, and to the development of weaker
connections between cells, possibly due to changes in pectic constituents. Also,
flavedo and albedo cell membranes become more permeable during this stage of develop-
ment. It is at this stage of development that citrus fruits become quite susceptible
to physical damage and to decay organisms.
Susceptibility to Decay Organism8.--Toward the end of Stage II and early in Stage
III. most citrus fruits are reasonably resistant to decay organisms. For example.
if spores of Penicillium digitatua or Geotrichum candidua are placed into lemon rind
tissue at this stage of development. decay will not result. At a later stage. these
organisms are aajor proble.s in the storage of lemons. Geotrichua in particular is
of no consequence until fruit become more susceptible due to age.
In nature, susceptibility to decay organisms depends on entry and subsequent
growth of the organism. Both seem to be more likely as the fruit matures and
approaches senescence. This seems to be due to the organism having less trouble
entering the rind, either by its own action or through injuries, and on the rind
tissue providing a better growth mediua for the organism as maturity and senescence
progress.
Exogenous Growth Regulators
~.--Thi8 growth regulator is widely used in citrus to reduce the incidence
of mature fruit drop. Alsot it is widely used postharvest on lemons to delay aging
of the fruit and to delay absci8sion of the button. Whether used preharvest or post-
harvestt its primary action is to delay the development of the abscission layer.
When used preharvest, the delayed development of the abscission layer peraits a
longer harvest season with only modest losses from fruit drop. Also, the delayed
development of the abscission layer keeps the phloem and xylem connnections in better
condition for a longer period of time. This results in a slight delay in fruit senes-
cence. When used postharvest, the delayed abscission and the resulting delayed senes-
cence of the button, keeps the port of entry for the Alternaria fungus closed. Decay
from this fungus is thereby controlled without the use of a fungicide or a fungistat.
The advantage of such an approach is that the fungus is not exposed to a fungicide or
fungistat to which it can become resistant.
~.--Under certain conditions, this growth regulator is applied preharvest
during Stage II or Stage III to delay fruit maturation or senescence. For example,
it is used on grapefruit in South Africa and Florida, on Valencia orange in Israel
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and California, on Minneola tangelo in Australia and California, and on navel orange
in South Africa and California. GAJ is used routinely on most of the California navel
orange acreage scheduled for late harvest. Typically, GAJ is applied two weeks before
color break and 2,4-0 is applied approximately 2 8Onths later. The objective is to
minimize fruit drop with 2,4-0 and to delay senescence with GAJ. Such a combination
permits California to continue harvest of navel orange into early July when production
and marketing factors make this desirable.
The primary benefit from GAJ is delayed rind senescence. This reduces the
severity of a number of preharvest and postharvest rind disorders, reduces suscepti-
bility to decay, and prolongs storage, shipping, and shelf life. It also causes a
modest delay in the decline of acid level in the juice and delays the development of
"over-ripe" flavors- On the other hand, once GAJ is applied, any subsequent plan to
harvest early in the season is doomed due to the substantial delay in rind color
development caused by GAJ- Obviously, the primary value of GAJ is for fresh-fruit
market situations.
By design. this lecture has placed emphasis on 8Orphological changes during
growth and development of citrus fruits and less emphasis on horticultural changes
and on the impact of exogenous growth regulators on development and senescence. I
hope the emphasis on morphological changes provides the background information you
need for the subsequent lectures in this series.
REFERENCE
S
1. Bain, J.M. 1958. Morphological, anatomical, and physiological changes in the
developing
Bot. 6:1-24. fruit of the Valencia orange, .'Citrus sinensis (L.) Osbeck. Austr. J.
2. Cooabe, B.G. 1976. The development of fleshy fruits. Ann. Rev. Plant Physiol
27:507-528.
3. Holtzhausen, L.C. 1969. Ob8ervations on the developing fruit of Citrus sinensis
cv. Washington navel from anthesis to ripeness. Tech. COIIDD.91 (15 pp), Depart-
ment of Agricultural Technical Services, Univ. of Stellenbosch, South Africa.
4. Holtzhauseu. L.C. 1981. Creasing: Formulating a hypothesis. Proc. Int. Soc.
Citriculture. Vol. 1:201-204.
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