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Plant Physiology I

Section II: Embryo and seed development:


Lecture VIII: Seed and fruit development:
Seed development:
Our knowledge of the commencement of seed development (embryogeny and storage tissue
formation) has been discussed by Dr. Perry over the course of the last few lectures. I will continue
this discussion on the latter stages of development focussed on the synthesis and deposition of
reserves to fill the cells of the storage tissues and the phases of seed maturation.
Basic anatomy: Deposition of reserves in the storage tissue of seeds is the hallmark of every
seed known, providing material for energy and early growth. The assimilate for storage reserve
synthesis is translocated from the mother plant into the sink cells of the seed. The nature of the
reserves laid down as well as the tissue in which they are laid down delimits major seed
characteristics as well as morphologically distinguishing features used to classify plants. One of
the most fundamental differences is related to whether the embryo develops one or two
cotyledons (or many cotyledons as in the Pinaceaea). This trait has permitted a sharp
differentiation between two classes of Angiosperm, the monocotyledones (one cotyledon) and
dicotyledones (two cotyledons) plants. The single cotyledon of the monocots (the scutellum
Fig. 1, 3A) is usually of a secretory and absorptive nature, never exiting the seed proper, even
after germination is complete. It abscises from the seedling and is shed along with the exhausted
endosperm and testa upon the completion of seedling establishment. It rarely contains
substantial amounts of stored reserves being associated with endospermic seeds (seeds in
which the major storage organ is an endosperm). Dicotyledonous embryos can be found in
endospermic and non-endospermic seeds. Many dicots remain endospermic but some (e.g. Pea)
absorb the endosperm during development redistributing the reserves within the cotyledons (Fig.
1). Endospermic seeds may retain live endosperm cells while in other endospermic seeds the
endosperm is dead at maturity. In the latter instance, a thin layer of live, non-storage, secretory
cells often surrounds the endosperm along the periphery of the seed, inside the testa. This is
known as the aleurone layer and aids in digesting the endosperm to provide the embryo with the
nutrients stored in this now dead tissue (Fig. 1).
Reserve deposition in storage tissue: There are usually only two major storage reserves
deposited in seeds and several minor reserves. Storage protein is found ubiquitously in seeds as
a major storage reserve of nitrogen and carbon along with either polysaccharides (usually starch)
or lipid, never both in major quantities, as the second major reserve. These major reserves are
extensively hydrolysed only after the completion of germination and the seed depends initially on
a minor reserve of soluble carbohydrate (sucrose, and often the raffinose series
oligosaccharides) for initial metabolism and structural molecules prior to radicle protrusion.
Additionally, essential macro- and micro-nutrients are sequestered in the seed, usually in a
complex with myo-inositol named phytin located in the protein storage vacuole. How are these
reserves deposited in the seed?
Storage protein deposition: During seed development, massive (relatively speaking) amounts of
specialized proteins are synthesized for use as a source of nitrogen, amino acids, and energy
during seed germination and subsequent seedling establishment. There are many families of
storage proteins that can be synthesized and stored in the same seed. They are often
oligomers of several different polypeptides and frequently exhibit different physical
characteristics most notably regarding solubility. Hence, seeds can have storage proteins that
freely dissolve in water (albumins), those that dissolve in buffers of high ionic strength but not
water (globulins), those dissolving in aqueous alcohol (70-90% v/v prolamins) and those requiring
dilute buffers of either high or low pH to solubilize (glutelins).

Crease
Cereal
seed

Aleurone layer
Seed coat

Endosperm

Vascular bundle
Funiculus-chalazal region

Embryo
Maize
seed

Aleurone
layer

Starchy
(Floury)
endosperm

Funiculus
Scutellum

Horny
endosperm

Pea
seed

Cotyledons
Radicle
Residual
endosperm

Funiculus

Pea pod vasculature


Redrawn from Bewley and Black 1985.
Seeds: Physiology of Development and Germination

Figure 1: Some anatomical features of mono- and di-cot seeds.


The storage proteins are all synthesized on the rough endoplasmic reticulum (ER) and
are deposited in the lumen of the rough ER. The storage proteins are placed in the lumen by
virtue of an amino-terminal signal peptide that directs the nascent protein through the ER
membrane while the protein is still being translated from the storage protein mRNA in the
cytoplasm. The signal peptide binds with a special docking protein in the ER membrane and is
cleaved off the nascent protein co-translationally. Upon deposition of the full-length protein into
the ER lumen, the ribosomal complex that has orchestrated the translation disassemble from the

mRNA and disassociate from the ER (Fig. 2). The storage protein aggregates within the ER
lumen and is moved to a peripheral terminus that then has various fates depending on the class
of plant (Monocotyledones vs Dicotyledones).

Storage Protein Synthesis and Deposition


Monocots
Blebed ER
membrane bounded
protein body
(maize)

Endoplasmic
Reticulum

Burst ER
unbounded
protein body
(wheat)

Endoplasmic
Reticulum
Dicots

3 end

Ribosome
receptor

Vacuole

Ribosomal
complex

Signal
peptidase
removes
signal
cotranslationally

AU

mRNA

5 end

Signal
peptide
on elongating
protein
Start
codon

Signal
receptor

Golgi
Stacks

Endoplasmic
Reticulum

Figure 2: Synthesis and deposition of storage proteins in mono- and di-cots.


Monocotyledonous storage protein deposition: In monocots, the protein body may be simply an
aggregate of the storage proteins that have stretched the ER until it ruptured, releasing the
aggregate into the cytoplasm unbounded by any membrane (e.g. wheat, Fig. 2). Alternatively, the

storage proteins can accumulate until the ER terminus eventually blebs off and forms a lipid
bilayer surrounding the protein in the protein body (a unit membrane) (Fig. 2).

A.

coleoptile
leaves

Scutellum
the single cotyledon

radicle
coleorhiza
Details of the monocot embryo.

Lipid deposition in oleosomes


B.
Lipid accumulation
between the ER
ER
membranes

Oleosomes

Figure 3: A) Details of the embryo of many monocots (maize is featured). B) A schematic of the
deposition of lipid in oleosomes.
Dicotyledonous storage protein deposition: The storage protein aggregated in a terminus of the
ER in dicots accumulates until the ER terminus blebs off from the ER. However, the ER vesicle

containing the storage protein is then transported to the Golgi apparatus where it fuses,
releasing the storage protein into the Golgi. Considerable processing of the storage protein can
occur in the ER and the Golgi usually in the form of glycosylation, partial or complete assembly of
oligomeric polypeptides, the formation of disulfide bonds, and/or the cleavage of cotranslated
subunits. The protein is passed from the proximal stacks to the distal in the cisternae until it is
packaged in a Golgi vesicle and transported to the vacuole. The vacuole of the dicots during seed
development can either remain as a single, central vacuole or, more commonly, become highly
convoluted, pinching off small vacuoles that are filled with storage protein and phytin. Regardless,
they are referred to as protein storage vacuoles to reflect their origin and not as protein bodies
(Fig. 2).
Storage lipid formation and deposition: Many, but not all, seeds deposit lipid for use as an energy
and carbon source during germination and seedling establishment. Lipid is synthesized in the
seed from assimilate sucrose delivered to the seed from the mother plant. It is converted via the
pentose phosphate pathway-, glycolytic-, and the triglyceride biosynthetic pathway-enzymes
located in the cytosol and proplastids into three primary free fatty acid precursors of the large
diversity of lipids stored in seeds (Palmitate (16:0), Stearate (18:0), and Oleate (18:1)). From the
proplastids, these precursors are transferred to the endoplasmic reticulum where they undergo a
myriad of alterations (elongation, addition of double bonds, hydroxylation, addition to glycerol to
form triglycerides, and temporary phosphorylation) before being bulked and packaged in
membrane vesicles formed from the ER, the oleosomes (lipid bodies). There is a variety of
oleosome forms, all arising from deposition of lipid in the ER but in different manners. The
oleosome can remain attached to the ER though thin membrane channels, or bud off forming an
oleosome bounded by a single layer of ER membrane (a half unit membrane) that either does or
does not have an extension of ER membrane attached to it (Fig. 3B).
Storage polysaccharide formation and deposition: Polysaccharides constitute a third form of
major storage compound. Usually, seeds storing carbohydrate do not also store major amounts of
lipid. By far the most common form of polysaccharide used by seeds as a storage reserve is
starch. Starch is formed in proplastids by the daily deposition of amylose (unbranched chains of
-1-4 linked glucose) or amylopectin (chains of -1-4 linked glucose with branches of -1-4 linked
glucose chains attached through -1-6 links). The proplastid, termed the amyloplast, is filled with
a single grain or numerous grains of starch.
In other seeds, the major polysaccharide deposited is fructan, galactomannan, or
xyloglucan. These reserves, except for fructan, are deposited outside the cell as a secondarily
thickened cell wall. In some seeds such as tomato, the secondarily thickened cell wall of the
endosperm does not affect the cells themselves while in other species, e.g. fenugreek, the
secondary thickened cell wall eventually occludes the cytoplasm and kills the cell.
Phytin synthesis and deposition: Little is known about phytin synthesis or deposition. Phytin is a
water-insoluble accumulation of a mixed salt of magnesium, calcium, and potassium ionically
bound to myo-inositol hexaphosphoric acid (phytic acid). It can also contain iron, manganese, and
copper, and sodium salts. Current evidence suggests that phytin is synthesized in the ER and,
upon sufficient accumulation, an ER vesicle buds from the ER and fuses with the protein body or
protein storage vacuole and deposits the phytin in the globoid (the aggregate of phytin
embedded in the storage protein).
Soluble carbohydrate (oligosaccharide) synthesis and deposition: The non-reducing sugar
sucrose is usually found in considerable quantities in mature seeds. The non-reducing nature of
sucrose along with its versatility, being quickly converted into energy and/or carbon skeletons for
use in germination and/or seedling establishment, enables those seeds that do desiccate to
maintain a quick energy source and do so without incurring non-enzymatic reactions of cellular
contents with the reducing end of a sugar. These so-called Maillard reactions (non-enzymatic
reactions between proteins and carbohydrates) result in deleterious denaturing of essential
cellular components that would severely damage if not destroy the seed should they occur (they

are responsible for the browning of food during cooking). Sucrose, when present in large
quantities, during the removal of water tends to crystallize out of solution which constitutes a
quandary for seeds undergoing maturation drying. How to keep the sucrose from crystallizing as
it becomes more concentrated due to water loss? Typically, the inclusion of some of the raffinose
series oligosaccharides (sucrose with one or more galactose moieties added to them) provides
sufficient disruption of the sucrose crystalline structure to prevent crystallization and instead leads
to an amorphous, highly viscose solution or glass. It is thought that those seeds that have the
ability of losing most of their water and yet maintain life (anhydrobiosis) do so by substituting
sucrose and raffinose for water in providing a shell of hydrogen bonding substances around
membranes and proteins. This serves to preserve most of the intracellular structural organization
until such time as water is reintroduced by imbibition.
Maturation desiccation: A fundamental difference between the seeds of two classes of plants is
exhibited at this stage of seed maturation. Those species whose seeds naturally undergo drastic
water loss upon maturing are referred to as orthodox seeds and represent the vast majority of
the angiosperms. Those species whose seeds do not undergo desiccation upon reaching
maturity are designated as recalcitrant. Recalcitrant seeds that are dried do not survive. There
have been further classifications based also on the ability of the seeds to survive cold
temperatures but these are less clear cut than the orthodox and recalcitrant designations.
For orthodox seeds maturation desiccation is necessary for the seed to subsequently
complete germination normally. Seeds that do not undergo maturation drying typically stay in the
maturation phase of reserve synthesis and deposition and fail to complete germination. Hence,
desiccation is considered as a physiological and genetic switch from maturation to germination
phases of a seed's development. Recalcitrant seeds do not undergo maturation desiccation and
are capable of making the switch from the maturation to the germination programs in the absence
of the desiccation switch.
Fruit development:
Upon fertilization in many angiosperms, the carpel(s) of the gynoecium develop into a fruit
enclosing the fertilized zygotes in an environment conducive to their development into mature
seeds and embryos. The fruit can also aid seed dispersal and, in some plants, need not develop
from the gynoecium. In so called pseudocarpic fruit, receptacle bracts, the floral tube, or
enlarged inflorescence axes can contribute to the fruit.
Esau (1977) classifies fruit into many different types based on whether the fruit is dry or
fleshy, dehiscent or indehiscent, true or false. This classification was tabulated by Mauseth
th
(1988) in 12 groups to which I have added a 13 (number 8 in the table) and excerpted below as
Table 1.
When the ovary of the gynoecium develops into a fruit the ovary wall is termed a
pericarp. The ovary of tomato is such a fruit with two, three or four carpels (depending on the
species and variety of tomato) fusing to form it. The number of cells recruited from the L3 layer in
the shoot apical meristem into the inflorescence meristem determines the size of the floral
meristem and the number of carpels it is to produce. It is the L3 layer that gives rise to the
preponderance of the pericarp tissue and this may be the reason why the L3 layer dictates the
final carpel number in tomato. The argument runs that, genetically, the cells of the L3 layer will
control how great a sink the developing fruit is and therefore, how much assimilate will be
potentially available to the fruit and enclosed seeds.
The fruit of tomato consists of two to four carpels that fuse and develop into a pericarp.
Developmentally, the carpel can be compared to a leaf that has curled around upon itself and
houses the ovules. The cells of the carpel of tomato most resemble those of the palisade layer of
the leaf and maintain their chloroplasts; functional chlorophyll, and photosynthetic capacity well
into fruit development. Although it is not substantial, the fruit photosynthesis does contribute to

photoassimilate required for fruit development. The carpel expresses many of the genes that are
typically associated with leaves, albeit, only a sub-set of so-called leaf specific genes and often
at stages of development divergent from that of the leaf.
Table 1: A classification of fruit types from
Mauseth (1988) Plant Anatomy.The
Benjamin/Cummings Publishing Co., Inc.
Menlo Park, California, USA.
Dry Fruits
Indehiscent Fruits
Developing from a single carpel
1. An achene is simple and small, contains
only one seed. Fruit wall thin, papery with
seed loose inside (sunflower).
2. A caryopsis has attributes of an achene but
the pericarp and testa of the single seed
become fused (wheat, corn).
3. A samera is a one-seeded fruit with a winglike extension (maple).
Developing from a compound gynoecium with
several carpels.
4. A nut commences from an ovary with
several carpels, all but one of which
degenerate leaving one carpel and one seed.
The pericarp is sclerenchymatous (walnut).

Developing from a compound gynoecium with


several carpels
7. A capsule may open in one of many ways:
spitting along the fusion lines or sutures (Iris,
lily, poppy).
8. A silique develops from two carpels that
enclose a false partition that holds the seeds
following dehiscence (arabidopsis).
Fleshy Fruits
9. A berry (bacca) is a fleshy fruit in which the
endocarp, mesocarp, and epicarp are easily
distinguishable and are soft (grape, tomato).
10. A drupe has the endocarp especially thick
and hard (peach, cherry, almond).
11. A pome has a papery, not a stony
endocarp (apple, pear).
12. A pepo has a hard exocarp forming a rind
(pumpkin, squash).
False Fruits

Dehiscent Fruits

13. A cypsela is similar to an achene except


that it develops from an inferior ovary and
therefore contains extra tissues around the true
pericarp (dandelion).

Developing from a single carpel

Schizocarpic Fruits

5. A follicle is a podlike fruit that splits open on


the ventral side (columbine).
6. A legume breaks open on both the ventral
and the dorsal sides (beans, peas).

Fruits that develop from a compound ovary but


then break up into individual mericarps
(achenes) when mature (parsley).

There are usually three periods or phases of fruit growth; 1) fruit set; 2) cell division and,
3) cell elongation.
Phase I: Fruit set: Although little is known about the control of ovary development, it is known to
be dependent on the successful pollination and fertilization of ovules within the ovary. Some
signal is released between the time of pollination to the time of fertilization, perhaps throughout,
that avoids ovary abortion and sets the stage for the second phase of fruit development, cell
division. This positive signal may be gibberellin which is released by the pollen, the pollen tube
and, the fertilized ovule. Exogenously supplied GA can promote parthenocarpic fruit production
in tomato. However, the GAs produced by parthenocarpic fruit are not the same set as those
produced by normally fertilized fruit. Additionally, applied GA stimulates auxin production by the
ovary, and auxin too could participate in signaling the ovary to avoid abortion. It is possible that
parthenocarpy is a direct result of improper synthesis of auxin both temporally and spatially within
the ovary. This suggests that the synthesis of GA and auxin during ovary development must be
highly regulated in order to coordinate both fruit set and the commencement of cell divisionthe
next phase of fruit development.
Phase II: Cell Division: In normal fruit development it is the developing seed that controls the
rate of cell division in the surrounding tissue. Phase II lasts between 7 to 10 days during which
cell division occurs throughout the fruit. Mitotic activity is high initially in the whole pericarp, but
more so in the outer relative to the inner pericarp. Additionally, cell division is initially higher in the
integumentary layers of the developing seeds than in the embryo. The developing vascular trace

in the placenta also exhibits high cell division activity early during phase II. At the middle of phase
II, mitotic activity is restricted to the outer pericarp, developing seeds, vascular tissue, and
placenta proximal to the developing seeds. At the end of Phase II, cell division remains the same
in the pericarp as it was in the middle portion of Phase II, Cell division in the placenta is also
restricted to the outer layer of cells from which the locular tissue arises. The vascular tissue and
the developing embryo also exhibit high mitotic activity.
There is a general observation that the number of fertilized ovules within a fruit controls
the initial rate of cell division in the ovary. This is exemplified by the observation that if seeds
develop on one side of a fruit but not on the other, lop-sided fruit develop with the larger lobe
containing the developing seeds. An additional correlation perhaps explaining the first is that the
amounts of cytokinin present in the fruit tissue surrounding the developing seeds is correlated
with the amount of cytokinin present in the seeds. It appears as though the fruit acquires cytokinin
from the developing seeds. Yet, the seeds themselves do not produce cytokinin but transport it in.
Hence, the more seeds, the more cytokinin present in them which may leach out into the
surrounding tissue leading to more cell division and larger potential fruit. Alternatively, high
cytokinin concentrations in the seeds drives the production of a positive regulator of cell division
in the tissues surrounding the seed which is released into the tissue. Additionally, prolonged fruit
development in the next phase, cell enlargement, is also dependent to a certain extent on the
presence of seeds in the ovary. However, this is not the complete story since part of the control of
final fruit size is the number of cells recruited to the ovary prior to fertilization. Additionally, the
extent of cell enlargement also affects final fruit size. The latter parameter is largely controlled by
phytohormonal levels present in the fruit during Phase III. It is important to attempt to differentiate
between factors that control fruit size genetically versus those that do so hormonally.
Phase III: Cell Division: Cell expansion and early embryo maturation: This stage increases
the fruit far beyond its size during the previous two stages through the controlled expansion of the
cells formed in the previous stage. The primary hormonal stimulant driving fruit cell expansion is
auxin and the hormone peaks twice during Phase III. The first peak indicates the onset of phase
III and auxin is most prominent in the developing seeds. However, in parthenocarpic fruit,
exogenously supplied auxin is not sufficient to replace developing seeds as a stimulant of cell
expansion. This has lead to the belief that it is the seeds ability to act as intense sinks that permit
access to photoassimilate which is also used for fruit development. Alternatively, it is possible
that high seed auxin concentrations promote the production of another stimulatory molecule
within the seed that diffuses or is transported into the surrounding tissue and stimulates cell
expansion. Since seeds are not present in parthenocarpic fruit, applied auxin would not stimulate
the production of the second compound and would therefore be insufficient to stimulate fruit
expansion. This scenario is further supported by the observation that the tomato mutant
diageotripica (dgt) which exhibits attributes of auxin-deficiencies in its growth produces normal
fruit.
The second peak of auxin coincides with the end of the fruit expansion phase occurring
at the period of maximum embryo expansive growth. Again, auxin levels are high in the seed but
low in the fruit and is absent in parthenocarpic fruit. This peak is associated with the cell
expansion occurring in the embryo since the fruit cells are at their final size.
A second plant hormone that may play a role in fruit development is gibberellic acid (GA).
As with auxin there are two peaks of GA occurring during fruit development one during Phase II
the second during Phase III. In Phase II, GA peaks at the onset of cell division. In Phase III GA
peaks, possibly due to auxin stimulation of GA production, during cell expansion, at maximal fruit
growth. However, parthenocarpic fruit exhibit an exaggerated first GA peak in the absence of
seeds that are the main sites of auxin concentration in the fruit (see above).
Both the rate of fruit development and final fruit size are controlled by cell number and the
sink strength of the cells comprising the fruit. The affect of cell number may be a function of a
greater cumulative sink produced by many versus few cells. This is apparent when the timing of
fruit set on a truss is altered. Normally fruit set occurs basipetally and the first fruit to set are those
proximal to the main axis of the plant and these fruit contain more cells than do fruit that set more
distally along the truss. If fruit are prevented from setting proximally until after more distal fruit

have set, the more distal fruit have a greater rate of development despite having fewer cells. In
addition to metabolic control of fruit development, there are indications that phytosterols are also
responsible for early events in fruit development. Injection of an inhibitor of hydroxy-methyl CoA
reductase (HMGR) results in arrested fruit development. However, whether phytosterols
themselves are responsible for the observed effects or whether it is a lack of the cytokinin and
gibberellic acid produced from the mevalonic acid common to both pathways is unknown.

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