MIMEOGRAPH SERms #1631
DORMANCY IN APPLE TREE BUDS
B. C. Allen and H. Wann
Biomathematics Series No. 13
Institute of Statistics Mimeo Series No. 1631
North Carolina State University
Raleigh, North Carolina
September
1983
i
ACKNOWLEDGMENTS
This work was supported in part by USDA grant (Apple CIMP National
Project No. 71-59-2481-1-2-039-1).
efficiency and dispatch.
Ann Ethridge typed this manuscript with
it
TABLE OF CONTENTS
Page
................................
LIST OF FIGURES ...............................................
I. Introduction ...............................................
A. General Remarks •••••••• .
.
B. A Note on Nomenclature .
.
II. Factors Controlling Dormancy .
.
ACKNOWLEDGMENTS ••••••••••••••••
III.
IV.
V.
VI.
i
iii
1
1
2
2
A.
Environmental Factors: Photoperiod and Temperature
3
B.
Interaction of Environmental and Endogenous Factors
5
Phases of Dormancy •••••.••••••
...........................
.
.
6
A.
Induction of Dormant States
B.
Effects of Temperature on Various Phases of Dormancy
7
C.
Growth and Development in Dormant Period
9
D.
Physiological Changes •••••••••..••.•••.•••••••••••••••
10
Hormonal Control of Dormancy •••••••.••••••••••••••••••••••
13
A.
Origin of Endogenous Factors •...••••.••••••.•••.••••••
13
B.
Growth Inhibitors
C.
Growth Promotors
.
.
17
D.
Balance and Interaction of Inhibitors and Promotors •..
19
E.
Mechanism of Control and Nature of Dormant States
20
Conclusions
.
Bibliography
.
6
.
.
.............................................
15
24
32
iii
LIST OF FIGURES
Fig. 1.
Diagrammatic representation of changes in temperature range for
bud break at times of change in growth activity.
A.
Narrowing and widening of the temperature range due to
changes in the maximum temperature at which bud break can
occur. (Adapted from Vegis (122».
B.
Narrowing and widening of the temperature range due to
changes in the minimum temperature at which bud break can
occur.
Fig. 2.
A schematic representation of seed dormancy and germination
involving three classes of phytohormones, gibberellins,
cytokinin and inhibitors. n+n (or "-") indicates effective
(or ineffective) levels of the hormone. (Adapted from
Khan (70».
Fig. 3.
Possible pathway of action leading to bud break.
Chandhry, Broyer and Young (30».
Fig. 4.
A postulated scheme for the action of GA.
Frankland and Cherry (67».
Fig. 5.
Possible biochemical pathways in the termination of seed
dormancy. (Adapted from Amen (5».
(Adapted from
(Adapted from Jarvis,
I.
Introduction
This report summarizes the results of a part of coordinated efforts
led by Dr. H. J. Gold to develop apple orchard ecosystem models (144).
One essential component of the system is apple tree buds.
To integrate
this component to the overall system, we must quantify the effects of
environmental
factors on bud growth and development.
The difficulties
in construction of such a model are mainly due to the complexity of
the underlying biological mechanism and lack of detailed data.
preliminary step of model development, we made a
As a
survey of current
literatures on bud physiology emphasizing environmental effects.
A.
General Remarks
In the summer, apple tree buds enter dormant period during which
growth (dry matter accumulation) is sharply reduced.
not resume until the next spring.
Normal growth will
It is known that changes in
structure and internal function of the bud in dormant period can have
profound effects not only on timing of bud break but also on bud
growth (111).
The initiation, maintenance and release of dormancy may be viewed
as a continuous process consisting of a sequence of stages (111).
The
morphological, physiological and molecular changes that occur during
dormant period are thought to be under genetic control but may be
modified by exogenous factors (57).
From this point of view, the basic
mechanism responsible for dormancy can only be revealed by simultaneous
studies of changes in internal function of the bud and its relation to
environmental conditions.
2
We report here
a survey of literature on apple bud dormancy and,
to a certain extent, some general aspects of dormancy in other fruit
trees.
Its purpose is only to draw together some basic knowledge in
such a fashion that fundamental parts of this knowledge can be used to
develop a framework for quantitative experimental studies into the bud
development in relation to temperature and other environmental factors.
B.
A Note on Nomenclature
In this survey, we will generally follow the nomenclature of
Romberger (104)..
Thus, "dormancy" will refer to a period of time, or
the state of the bud, during which that bud will show no extensive
growth, for whatever reason.
By "innate dormancy" or "rest" we mean
that portion of the dormant period in which the cause of the lack of
growth is due to endogenous factors; i.e.,
environment.
it is not imposed by the
The reduction or stoppage of growth due to environmental
factors is called "quiescence" or "imposed dormancy".
It must be
remembered that the state of dormancy, its imposition and release, is a
continuous process and that these terms are used only because they
are sometimes useful.
However, the distinctions are not
comp~etely
adequate because they separate the internal and external influences in
an artificial manner.
II.
Factors Controlling Dormancy
It has long been noted that environmental factors influence the
development, maintenance, and break of dormancy.
Factors most studied
are temperature and photoperiod (or light intensity) and to a lesser
extent nutrient and water stress.
Early theories of dormancy suggested
that the resting state in buds results from a lack of nutrients in the
3
buds themselves.
Now it is generally believed that dormancy is under
the control of plant-produced chemicals, i.e., growth promoters and
inhibitors (90).
This does not imply that nutrient stress is not a
factor in the induction of rest; it means merely that this stress acts,
as do the other factors mentioned above, through the actions of hormones.
A.
Environmental Factors: Photoperiod and Temperature
Changes in photoperiod have long been seen as a naturally occurring
cyclic process that could account for the alternation between dormant
and growth states (90, 122, 131).
For the most part, short days are
thought to induce dormancy; long days to end it.
We will not comment
upon this extensively since it has been shown (89, 128) that photoperiod
changes do not induce dormancy in apples.
Suffice it to say that, as
in peaches (55), the intensity of apple bud break may be sensitive to
light (56).
Temperature (i.e., air temperature) is another matter however.
Cool temperatures (12.5°C) were found to be sufficient to halt growth
of apple trees (89).
Of course, the well-documented "chilling
requirement" of many species is shown to be present in apples as
well (44).
There are indications, nonetheless, that the effect of
temperature may be more complicated than simply a cool temperature
induction and a chilling temperature break of dormancy.
Weinberger (134) suggests and Erez and his colleagues (51, 52) attempt
to show that
~cling
temperatures (alternately high and low) affect the
progression of dormancy in peaches.
cycle length and maximum temperature.
The important variables seem to be
The longer the cycle (six or
•
4
nine days), the less the negative effect on rest progression.
More
interesting is the effect of maximum temperature: in a daily cycle
(eight hours high, sixteen hours low) a high temperature of 21°C or
higher completely negated the prior chilling.
between 6° and 15°C
~nd
However, an alternation
to a lesser extent between 6°C and 18°)
•
enhanced the chilling process; i.e., bud break was advanced.
Thompson, et al. (115) noted the same trends in apple.
Borkowska (22)
showed that although chilling may be insufficient for bud burst it may
be enough to promote bud elongation.
Generally, he suggests that there
may be two processes at work within the bud, one controlling burst and
the other controlling cell elongation, and that each has its own
environmentally optimum requirements.
Sparks (112) demonstrates that in pecan, subfreezing temperatures
may also advance bud break.
He attributes this to tissue injury or to
prevention of the attainment of the deepest resting state.
Indeed,
it is generally believed that the optimum chilling temperatures are
somewhat above freezing, roughly 2°C to 7°C (54, 100, 115), and that
freezing retards bud development and dormancy break (25).
A number of
studies have suggested that the time of chilling, early or late in the
winter, will affect both the number of buds which break and their
subsequent growth (1, 72, 115).
The rate of bud development in the
spring was found to depend most heavily on the cold conditions of the
preceding autumn or'early winter (1).
That is, warmer autumn conditions
promote further bud development (delayed onset of quiescence), which
facilitates renewal and completion of growth once dormancy has ended
(1, 72).
On the other hand, Abbott (1) suggests that warm temperatures
in late winter or spring may allow for earlier bud break (i.e.,
earlier
)
5
removal of imposed dormancy).
Abbott also hypothesizes that the
temperature above which bud growth can resume in spring (i.e., above
which dormancy is no longer imposed) is not constant; it depends upon
the extent to which dormancy has been broken by cold treatment.
Thus,
those buds which receive more chilling can leave the quiescent state
at lower temperatures than those which get less chilling.
Eggert (44)
suggests that there is a correlation, within the apple species, between
the date of bloom and the chilling requirement: those varieties which
bloom late need more chilling during winter.
The general effect of temperature on dormancy may be summarized
as follows.
Cooling air temperature promotes dormancy, which perhaps
begins as quiescence and may therefore be reversed by subsequent
warmer temperatures.
Once the cooling has induced rest, that state is
maintained until chilling brings it to an end.
That the process is more
complicated than this cursory summation allows is indicated by the
facts noted above for temperature cycling and times of cold imposition.
We later attempt to tie these observations to theories about the
action of growth hormones.
B.
Interaction of Environmental and Endogenous Factors
As mentioned above, there is some difficulty in a notion of
dormancy which divides the dormant state into a rest (endogenous control)
phase and a quiescent (environmental control) phase.
For one thing, we
have seen above that, even during rest, the environment (e.g.,
temperature) exerts an influence, shortening or prolonging rest.
Furthermore, with a hormonal mechanism postulated for the control of
6
growth, and knowing that the environment can affect hormone levels in
many ways, it is misleading to try to separate in time environmental
and endogenous effects.
Rather, we would think, as does Tyurina (119),
of these effects as a dual control.
This complements his notion that
growth and dormancy are just parts of a continuous process and that
in the course of one, the other is prepared for, actively.
Thus there
is an endogenous rhythm upon which environmental stimuli can operate.
He states that if for some reason (e.g. because of a late growth start
or under unfavorable grOWing conditions) the endogenous rhythm is not
conducive to the imposition of rest, the environmental signals that
the plant receives can compensate and initiate rest itself.
This
could also account for the fact that buds in a resting state will
eventually leave that state, even if they do not receive their
chilling "requirement."
If they do get chilling, though, the endogenous
and environmental factors work in harmony and vegetative growth can
recommence much sooner.
III. Phases of Dormancy
A.
Induction of Dormant States
There remains a question about the ability of plants to enter
dormancy.
Specifically, will the bud enter dormancy whenever a
prolonged environmental stress is encountered, or does the bud have to
be at a certain stage of development before dormancy is induced?
There appears to be no resolution of this question as yet.
reports that cells which do not contain significant amount
are not able to enter dormancy.
In particular,
o.
Romberger (104)
of lipids
Abbott (2) cites
7
Simon (1919), stating that buds will not enter a resting state until a
certain degree of development has been attained.
On the other hand,
D. L. Abbott (1) supports the idea that mild autumns promote further
growth and development, harsher falls inhibit this, but buds at any
stage of development can enter a normal dormant state.
confirms this.
Landsberg (72)
Brown and Abi-Fadel (26) state that buds at earlier
developmental stages do not require more chilling to end rest, i.e.,
the bud developmental state seems to be no index of the chilling
requirement.
These reports are not conclusive; the requisite degree of
development may be attained early in autumn
or even in summer.
The
various stages of morphogenesis reported by these authors may
correspond to development beyond the required minimum.
More to the
point is an investigation by Chandler et. ale (29) who state that apple
leaf buds are quick to enter rest in summer if ever their shoots stop
growing.
Moreover, these authors found that a water stress of a few
weeks duration, even in early summer, was enough to cause a resting
state so deep that no growth was possible for the remainder of that
summer.
B.
Effects of Temperature on Various Phases of Dormancy
The realization that the onset of rest is not an instantaneous, but
rather a gradual process probably led Vegis (122) to propose a classification scheme for dormancy consisting of three phases: predormancy,
innate dormancy, and post-dormancy.
During the predormant period, the
temperatures at which the plant can grow become more restricted, until
the plant can no longer grow at any temperature, the point which marks
8
the passage to innate dormancy.
After some period of innate dormancy
the plant becomes capable of growing in some small temperature range;
as post-dormancy progresses this range becomes increasingly wider until
it reaches the widest limits for vegetative growth.
Vegis states that
for fruit trees in the Rosaceae group the diagram would look like that
shown in Fig. lAo
However, Tyurina (119) mentions a lowering of the
growth temperature minimum as dormancy comes to an end (for apples)
(Fig. 18).
Vegis further states that a high temperature early in post-
dormancy can actually induce a secondary dormancy.
Thus he visualizes
the widening of the range not as a monotonic process, but as one that
can be reversed.
His view of this widening phenomenum is supported by
Rom and Arrington (103) who report that a stepwise increase in
temperature produces a better bud break than a sudden jump to the final
warm temperature.
This approach is more satisfactory for it does not try to separate
endogenous and environmental factors.
The new characterization of the
process of dormancy uses forcing experiments to determine a depth of
the dormant state.
This generally results in a bell-shaped curve
(49, 60) with the mode coinciding with innate dormancy.
Such
observations are consistent with the division of the dormancy period
proposed by Samish (107).
quiescence
-+
It consists of the following sequence:
preliminary rest
-+
mid rest
-+
after rest
-+
quiescence.
Here quiescence is a state of growth stoppage reversable by favorable
conditions.
Preliminary rest and after rest are characterized by a lack
of growth, but an ability to be forced.
innate dormancy,
Midrest corresponds roughly to
the state in which forcing is difficult or impossible.
9
This scheme, it seems, can be made to correspond to that of Vegis.
The
two characterizations may merely divide the continuous process of dormancy
into different discrete portions.
illustrated in Fig. lA.
A probable correspondence is
We will see later if any such scheme is
compatible with the internal mechanisms at work during dormancy.
c.
Growth and Development in Dormant Period
It should not be thought that growth and development
during the dormant period.
do not occur
Tyurina (119) and Romberger (104) state that
the apical meristem cells remain active; the subapical cells are
inhibited in their gorwth.
Both growth and development in dormant buds
proceed at slow but continuous rates (13, 27, 28, 134, 141).
Flower
buds not only increase in weight (33), they show an increase in flower
clusters within the bud (27).
increase in the number
Similarly, leaf buds demonstate an
of primordia as dormancy progresses (104, 141).
Even though Brown and Kotob (27) state that Zeller reports slow
development of apple flower buds even during the coldest part of winter,
it is generally believed that subfreezing temperatures may retard bud
development (25, 119).
Both Young(14l) and Romberger (104) state that
the bud parts developed during dormancy have_a morphology different from
those in vegetatively growing buds.
Moreover, Young (141) has shown
that the increase in size and in number of leaf primordia is more
marked in March through June in buds with prolonged dormancy (given
insufficient chilling, i.e., no temperatures below 15°C).
This
corresponds to the time when bud burst and rapid growth would occur had
dormancy ended as usual.
Perhaps there are two mechanisms, i.e.,
10
internal systems, one controlling growth and development within the bud,
the other controlling the processes associated with bud burst.
Indeed,
Hewitt and Wareing (64) suggest that development of the bud during
dormancy is mediated by regulators and that subsequent growth in spring
results from a "well-defined metabolic pathway."
The growth and
development of apple leaf and flower buds during dormancy has been
reported by Zlobina (143), Tyurina (119), Brown and Kotob (27).
Since growth and development do occur during dormancy, albeit
slowly, how is dormancy different from vegetative growth?
As mentioned
above, Tyurina (119) and Romberger (104) state that growth inhibition
occurs in the subapical meristem cells, and the former author stresses
that it is the transition to dormancy that initiates apical meristem
cell activity.
Thus, there is no shoot elongation.
But there are more
fundamental and important distinctions between dormant and non-dormant
states.
Tyurina (120) hypothesizes that the advantage to temperate-
climate plants of a dormant phase is that such a phase allows the plant
to separate the
energy-requiring processes of growLh and of
preparation for cold hardiness.
This indeed appears to be the major
function of dormancy: reducing susceptability to environmental stresses.
D.
Physiological Changes
Whatever is responsible for the maintenance of dormancy, the
external differences that are seen must reflect cellular changes
occurring in the buds.
These changes not only result in the dormant
state but also prepare the cells for the subsequent phases of their
development (120).
The internal changes are a direct result of the
11
mechanisms of dormancy control.
Thus an examination of the changes may
reveal the nature of those mechanisms.
During the latter part of summer, perhaps after the onset of
quiescence, photosynthesis builds up a reserve of carbohydrates and
other compounds (2, 119, 120).
Also noted is the synthesis of high-
molecular-weight, acid-insoluble phosphorus compounds.
As dormancy
progresses, this ceases as acid-soluble phosphorus compounds
(apparently for storage) are manufactured (119).
Phosphorus uptake
(109), and, correspondingly, phosphorus metabolism (119) cease almost
entirely during the deepest part of rest.
The DNA-RNA-protein system
has been working actively in autumn (119) and by the time rest passes to
imposed dormancy the metabolic activity is completed through DNA
transcription.
The fact that RNA and protein synthesis occurs during
dormancy is confirmed by many investigators (13, 37).
Eke1und (46) notes
the slow pace of RNA and protein synthesis, rRNA being the primary
nucleic acid produced.
However, Yeh Feng et. a1. (140) note that later
in dormancy (January to March) changes in the nucleus occur and more
protein and RNA are produced.
Although transcription may be complete
by end of rest, the mRNA cannot enter the cytoplasm because of a double
membrane around the nucleus and the absence of nuc1eopores (140).
Other changes associated with the onset of dormancy include a decrease
in amino acids (48), perhaps due to active protein synthesis and increase
in the protein content of the ribosomal and mitochondrial fractions (119).
Also reported is a rapid hydor1ysis of polysaccharides and the appearance
of large quantities of oligosaccharides (118).
Samish (107) reports
that the protop1asts in the cell contract and assume a convex shape;
12
they withdraw from the cell wall, rupturing the plasmodesmata, and
become covered with a lipoid layer.
and pear.
This is most evident in apple
Tyurina (119) states that upon entry into dormancy there is
a coincident increase in nuclear dimensions and protoplasmic content.
During the course of the dormant period, various changes in cell
activity occur.
There is an increased metabolic activity of cell wall
formation and lipid droplets are at a maximum in early December; these
comprise the source for membranes of new organelles formed later (140).
Ekelund (46) notes the increase of ribonuclease activity from autumn
to spring, with much greater increase in March and April.
An early
article by Abbott (2) reports that hydrogen ion concentration decreases
through winter in apple bud cells, a fact that he claims affects the
activity of certain plant enzymes.
that
~
Bachelard and Wightman (10) note
absorption increases through dormancy; however Hatch and
Walker (60) saw no significant difference in respiration rates until
late in the dormant period, February or March.
As dormancy is coming to a close, many of the changes seen at the
inception of dormancy are reversed.
Amino acid content increases, due
to the rapid breakdown of the protein found in large quantities up to
this time (10, 48).
cytoplasm (140).
Nucleopores reappear, allowing mRNA to enter the
Carbohydrates are markedly decreased (10), especially
starch content in apples (65).
prior to break (48).
Organic acid content increases just
There is a net loss of nitrogenous material (10)
and phosphorus uptake is resumed (109).
Bachelard and Wightman (10)
report that the respiratory quotient decreases from about 3 (indicating
anaerobiosis) to between 1 and 1.5.
They state that metabolic activity
13
changes from catabolism to anabolism about two weeks prior to renewed
growth.
Before this occurs, the carpel size of the Golgi bodies
increases, an important event because of the extra cell surface area
provided.
At about the same time, the number of mitochondria increases,
indicating that more energy is needed for cell reactions.
Also smooth
endoplasmic reticulum (ER) is transformed into rough ER in preparation
for synthesis of proteins to be transported (140).
Samish (107) reports
that the protoplasts swell and reestablish plasmodesmatic connections.
Total sugars increase significantly about two weeks after the completion
of rest (48), particularly the monosaccharides glucose and fructose (10).
A number of investigators (10, 114, 128) report the increased water
content of cells as they end dormancy.
Taylor and Dumbroff (114) cite
a change from a low of 3810 of total fresh weight to 7110 at burst in
sugar maple buds.
IV.
Hormonal Control of Dormancy
A.
Origin of Endogenous Factors
We have seen that environment is one influence on the dormancy
status of woody plants.
It remains to be considered by what internal
mechanisms the changes in this status are affected.
As mentioned
previously, a hormonal control system is generally accepted (see
Wareing and Sanders (131) for a review).
In particular, a balance
between inhibitor(s) and promoter(s) is hypothesized (131).
An early
work (41) showed that dormancy is a property of the buds alone, i.e.,
no other tissues are dormant.
In fact Corgan and Martin (33) suggest
that in peach flower buds rest is localized within the floral cup.
14
Semin and Madis (109) confirmed that the roots do not become dormant by
measuring uptake of labeled phosphorus.
It is not at all clear however
that the place of origin of the inhibitors or promoters is within the
bud.
Mielke and Dennis (86, 87) suggest that the senescing leaves may
be responsible for abscisic acid accumulation in the bud in autumn.
Mauget's work (84) would support such a conclusion.
Davison and Young
(38) report a quick rise of abscisic acid (ABA) concentration in xylem
sap after leaf fall.
Along the same lines, Corgan and Peyton (34) and
Chandler and Tufts (28) state that later leaf retention corresponds to
later bloom.
On the other hand, Hodgson (65) reports no relationship
between leaf retention and rest.
Promoters too have been associated
with the leaves: Eady and Eaton (43) note that in cranberry, gibberellic
acid is transported from leaves to terminal buds prior to elongation.
Luckwill and Whyte (80) suppose that cytokinins, another group of
promoters, may be translocated from the roots to the buds in spring since
the authors could detect none of these substances in the xylem sap from
September to January.
However, Borokowska (21) found that in apples,
the distal buds had consistently high cytokinin activity throughtout
dormancy.
Hewitt and Wareing (64) claim that the increase is
independent of the roots, but dependent on the sap.
Romberger (104)
considers any root influence on growth hormone levels unlikely, an
opinion based primarily on the fact that break of buds can occur
normally in excised shoots.
The possibility of influences on the buds by other tissues seems to
be supported by a number of investigators who note that the dormant
state of buds can vary depending on their position on a shoot.
In
15
peaches, a difference was found in the optimal chilling temperatures (54);
terminal buds had the highest optimum (were easiest to break), lateral
buds on lateral shoots had the lowest.
Eggert (44) suggests that
lateral buds lag behind terminal buds and spur buds because of a
resumption of apical dominance.
Weinberger (132) notes one result of
prolonged dormancy in peaches to be bloom only near the tips of shoots,
perhaps followed sometime later by basal bud bloom.
This would seem to
corroborate Borkowska and Powell's hypothesis (21, 22) of a "rest
influence" that moves from base to apex as dormancy commences; thus
distal buds tend to be less dormant.
In a somewhat related experiment,
Robitaille (102) reports that on shoots placed in a horizontal position,
the buds on the lower side exhibited dormant characteristics longer.
He attributes this to an auxin effect.
In contrast, a group of French
authors report strikingly different results.
Mauget (84), working
with almond trees, found that the basal ends of shoots are normally
least dormant.
Arias and Crabbe (8) and
Barnola et al. (12) confirm
this and go on to speak of a dormancy resisting (growth stimulating)
factor at the basal end, an "inertia" (growth inhibiting) factor at the
distal end.
Mauget (84) also describes the effect of mechanical
defoliation, i.e., reduction of the dormant state as being strongest on
the distal buds.
B.
Growth Inhibitors
Repeated reference has been made to the importance of inhibitors
and/or promoters in the control of dormancy.
Many investigators have
reported correlations between endogenous levels of these substances and
the onset or lift of dormancy.
For instance, El-Mansy and Walker (49)
·
,
16
have investigated the inhibitor naringenin in peach flower buds; they
found its levels to coincide with the bell-shaped rest intensity curve.
A substance of particular interest has been abscisic acid (ABA) found to
be a constituent of the a-inhibitor complex, very active in inhibiting
growth.
Reports of its accumulation in late summer/early fall
(63, 87, 119), presence during dormancy (21, 33, 63, 69, 72, 77, 82, 98,
99) and diminution in spring (4, 63, 87, 88, 119) are plentiful.
Some
researchers have found, however, that its levels do not correspond to
rest intensity (40, 86, 114).
In particular, Dennis and Edgerton (40)
state that ABA levels correspond not to rest but to dormancy, a view
that appears to fit with the schemes of Vegis or Samish noted above,
i.e., the gradual development of rest, which perhaps then corresponds
to ABA above some threshold of irreversability.
However, Mielke and
Dennis (87) report that in mechanically defoliated trees with low ABA
levels, the resting state is as intense as in buds with high ABA levels.
It has been suggested that the relative concentrations of a bound and a
free form of ABA are
important in determining dormancy status: free ABA,
causing dormancy, decreases through winter with a concommitant increase
in bound ABA, an inactive form which allows bud burst (15, 77, 86).
Specifically, Lesham et a1. (77) working with almonds report that one
stereoisomeric form, trans-trans-ABA, is of overriding importance in the
inactivation, and that the binding is glycosidic in nature.
Bardle and
Bulard (15) propose that the change from a free to a bound form is due
to chilling, but Mielke and Dennis (87) claim that chilling is not
necessary for a decrease in ABA activity in cherry tree buds.
Corgan
and Martin (33) suggest that ABA breakdown is a secondary result due to
enzymatic changes brought about by chilling.
A somehwat different finding
17
is reported by Kawase (69) for peach and Malus sy1vestris:
dormancy
lasted as long as the inhibitor activity increased; as soon as it
started to decrease, the bud breaking process commensed, even though
activity was as high as levels which earlier maintained dormancy.
It
appears (40, 82) that the inhibitor resides for the most part in the
bud scales, one report (40) stating that it did not enter the primordia
until after they have expanded.
Mielke and Dennis (86) point out that
the concentration of ABA is highest in the primordia, especially in
November and early December, coincident with the deepest rest in some
years.
This is consistent with the theory that ABA is transported from
leaves to scales (where it is
store~,
then to primordia.
It is also
consistent with the thoughts of Corgan and Martin (33) that rest is a
property of the floral cup.
C.
Growth Promotors
Growth promoters have also received a great deal of attention.
But
since vegetative growth was thought to be the normal state for plants,
promoters were at first studied only in relation to inhibitors or to
an inhibitor/promoter balance.
Nevertheless, Taylor and Dumbroff (114)
now claim that it is variation in cytokinins, not ABA, that is
responsible for dormancy break in sugar maple.
Gibbere11ins have been
studied extensively and high levels of their activity (perhaps with
simultaneous decrease in inhibitor) have often been found to promote
resumption of vegetative growth (4, 66, 111, 119, 138).
In relation to
the dormancy period, Jarvis et a1. (67) propose that chilling
"potentiates" gibberellic acid (GA) synthesis, which then proceeds when
18
higher temperatures occur.
Hull and Lewis (66) and Walker and
Donoho (125) claim that GA has no effect on apple tree growth or
dormancy.
Auxins have been implicated in dormancy control less
frequently (4, 20).
Blommaert (20) postulates that increase in auxin
levels by cold treatment functions to inactivate the inhibitor.
Eggert (45) has proposed a model for auxin
growth.
control of apple spur bud
As long as cells enlarge, auxin does not build up; it is present
in medium concentrations and so promotes growth.
However, when
environmental factors slow or stop growth, auxin concentration increases
to inhibitory levels.
This continues and buds enter "fore-rest".
Auxin accumulates further, unless there is some feedback or diminution
of
produc~ion
due to the senescence of the leaves.
Cytokinins are generally recognized as being important in dormancy
control (14, 21, 64, 98, 119), and are known to be active in apple
fruitlets and shoots (78).
In fact, Khan (70) states that Piendazek
(1970) found cytokinins capable of reversing ABA inhibition in apple
explants, but not so for GA or auxins.
Hewitt and Wareing (64)
emphasize the enhancement of cytokinin activity is dependent upon cold
treatment.
The dynamics claimed by Borkowska (21), who proposed ABA
and cytokinins as the inhibitor/promoter pair in apples, are as follows:
in the period from December to February, cytokinin activity is low
(but detectable) with an increase in March and subsequent disappearance
just before burst.
Hewitt and Wareing (64) corroborate this and add
that cytokinin activity again increases with shoot elongation.
Barthe (14), working with apple seed embryos, maintains that cytokinins
exist in free or bound form, similar to ABA, and that free-form
cytokinin increases during afterripening leading to germination.
19
D.
Balance and Interaction of Inhibitors and Promotors
Corgan and Martin (33), noting the fluctuating levels of ABA during
dormancy, conclude that rest is a more complex phenomenon than a simple
accumulation and maintenance of an inhibitor at a concentration high
enough to stop growth.
This view is supported by the findings of
Kawase (69), as stated above, and Ramsey and Martin (99), who show that
both the promoter and the inhibitor levels increase during dormancy.
They found however that the increase in promoter just prior to break was
much greater than that of inhibitor, so that the ratio of promoter to
inhibitor increased.
These and other findings support the hypothesis
that the relative amounts (or concentrations) of promoter and inhibitor
are important in determining the dormancy status: a promoter-inhibitor
balance.
The manner in which the effects of these substances are
balanced will be discussed later.
In an investigation on apple buds, Borkowska and Powell (22)
suggest that the processes of bud burst and shoot elongation are under
the control of different hormones, probably cytokinins and gibberellins
respectively.
Khan (70) too, suggests different roles for these hormones,
as specified in his model,for see dormancy.
Noting that ABA levels
increase and cytokinin levels decrease during stress, and that cytokinins
can modify the effects of other hormones without having a marked effect
by themselves (49), he proposes that gibberellin, cytokinin, and ABA
play primary, permissive, and preventive roles respectively.
That is,
gibberellins generally promote seed germination whereas cytokinins and
ABA act, and interact with each other, to either allow or prevent
gibberelin from carrying out its role.
A schematic representation is
20
shown in Fig. 2.
Khan also proposed a similar scheme for bud dormancy,
but allowing for auxins to playa role, perhaps even prior to or in
conjunction with gibberellin.
This later suggestion is consistent with
the enhancing capabilities of IAA on GA found by Ahmed and Mathew (4).
If it is allowed that varying concentrations of all four hormones have
effects more subtle than an effective-ineffective dichotomy, the picture
of bud doemancy becomes quite complicated.
Moreover, Corgan and
Peyton (34) suggest possible interactions with inhibitors other than ABA.
Some such model may be appropriate.
explaining certain anomolous results.
It can go a long way toward
For example, Mielke and Dennis
(85, 87) note that temperature had no effect on ABA levels.
The model
might then propose that the chilling treatment affected the cytokinin
levels in this species (cherry), negating ABA, and producing normal
break of dormancy.
E.
Mechanism of Control and Nature of Dormant States
The most important question still remaining concerns the mode of
operation of the inhibitors and the promoters.
It is still a largely
unanswered question, various investigators proposing various mechanisms.
It is now generally accepted that dormancy does not represent a total
inhibition of cellular activity, but rather a "change in direction" of the
growth process (19).
Young et. al. (41) speak of "certain morphological
manifestations inherently induced by the environment."
Thus, strictly
speaking, the terms "inhibitor" and "promoter" are inaccurate.
They
derive from the earlier belief that the inhibitor acts as a hormone
which stops all growth and development.
cells still respire, grow, and develop.
We have seen though that the
21
Further evidence that dormancy is not a simple shutdown of cellular
activity is provided by Esashi and Leiopold (57).
In fact, they show
that dormancy is a programmed part of the plant's life cycle.
total gene repressor is applied before dormancy,
not attained.
When a
a dormant state is
This result is not to be expected if dormancy is due to a
lack of essential elements in the metabolic activity of the cell.
It
suggests that active transcription of genetic material is necessary for
the initiation of rest.
Given that the onset of dormancy is an active process, how is it
accomplished?
fall.
There are two general categories into which auggestions
First, the inhibitor/promoter pair affects the availability of
substances necessary for growth.
Alternately, the pair is hypothesized
to interact with substances already present.
Note, however, that if we
assume ABA to be the inhibitor, then, as Wareing et al. (130) suggest,
its simple structure may enable it to act in more than one enzyme
system.
No single mechanism need be hypothesized, even for a single
inhibitor.
The inhibitor/promoter pair may act as hormones or as participants
in intermediate metabolic reactions (104).
Such theories suggest that
ABA, as the inhibitor, interferes with the metabolic reactions of growth
or that promoter is necessary for such reactions to continue.
On the
other hand the promoter may interfere with dormant metabolism, ABA may
enhance it.
(a)
Specific suggestions include
allosteric binding of inhibitor and promoter on a key growth
enzyme (91, 130).
22
(b)
enzyme activation roles of the inhibitor and promoter
(65, 75) and
(c)
interaction with cell membranes, controlling the availability
of enzymes, substrates, etc. (75).
Any of these means alone does not seem capable of explaining the "change
in direction" of metabolic activity seen upon entry to dormancy.
Zelniker (142) proposed that the lack of growth is due to a
deficiency in high energy phosphate bonds.
speculated effect of the
e complex
Whether this is due to a
(i.e., the uncoupling of phosphorylation
and the electron transport system) (81) or due to the utilization of
the tyrosinase pathway rather than the cytochrome oxidase system
(Todd, 1953, in (30», the result is less ATP production.
Chaudhry
et. al. (30) suggest that high temperature variation in spring causes
renewed production of the high energy bonds.
Lack of energy may be
sufficient to explain the cessation of visible growth and may thus occur
in the subapical meristem cells, but it cannot account for the active
metabolism of the apical meristem cells.
Some other mechanism(s) must
be involved.
For the reasons mentioned above, many authors have focused
attention on promoter/inhibitor control of protein synthesis.
Control
of protein synthesis can arise from action at the transcription or
translation stages or after translation into polypeptides.
Some
investigations (3, 31, 126) indicate that control may occur after
transcription, probably at the translation stage.
Most, however,
concentrate on the block to transcription hypothesized as a function of
the inhibitor.
Some possibilities include:
23
(a)
action of the inhibitor/promoter as an inactivator/activator
pair for DNA or RNA polymerase (91, 128), or
(b)
effect of the inhibitor on the availability of ribonucleoside
triphosphates (117).
But again, to reflect the selective change in metabolic activity, most
investigators have hypothesized that ABA and the promoter function only
on specific genes or RNA's (3, 31, 67, 119, 121, 123, 128).
Chaudhry
et al. (30) have reviewed a number of proposals, specifically for
Pyrus Communis, and have concluded that the primary factor in dormancy
control is that identified by Tuan and Bonner (117), repression of DNA
and consequent lack of protein synthesis.
Such repression may be due
to histones (67) or to other phosphoproteins (30) (see Fig. 3).
neither of these cases is it clear how an inhibitor fits in.
In
On the other
hand, Jarvis (67) postulates an operon system (Fig. 4).
Indeed, the manner in which the inhibitor-promoter pair interact is
a matter of some speculation.
Apart from the opposing effects of
allosteric binding mentioned above, there have been a number of
suggestions.
We have already touched upon the ideas of Khan (70).
He
states that studies indicate that ABA and cytokinins act at the same
level (RNA transcription, for example) but that this is not known for
certain.
It has been suggested (130) that ABA and a promoter (perhaps
cytokinins in the case of apples) affect the biosynthesis of one
another.
It
precursor (3).
has even been proposed that GA and ABA arise from the same
A fact about cytokinins that may be important is that
many tRNA's actually have cytokinins incorporated into them (58).
Any
interaction between ABA and cytokinins would then manifest itself in
24
blockage of tRNA formation and subsequent lack of protein synthesis.
The observation (114) that cytokinin levels, not ABA levels, are crucial
to break of dormancy is perhaps tied to this point.
Other observations about inhibitor-promoter interactions are
numerous.
Chrispeels and Varner (31) suggest that GA and ABA act
antagonistically (but neither competitively nor noncompetitively).
They postulate the promotive effect of GA on the transcription of
specific mRNA's and the inhibitory effect of ABA to stop that synthesis.
Kawase (69) notes that application of GA decreases inhibitor levels
in vivo in Malus sylvestris.
This may be accomplished via hydrolytic
and proteolytic enzymes (which are affected by GA (138», increasing
the permeability of cell membranes.
the ABA.
Increased water content dilutes
Zelniker (142) noted that for rapid synthesis of nucleic
acids, the cell must reach certain levels of hydration: at 65%
hydration RNA content increases (coinciding with initiation of growth),
at 71% DNA content increases (coinciding with growth maximum).
In a note of caution,
Lan~
(75) and Chrispeels and Varner (31)
state that all the results indicating action by inhibitors or promoters
on the protein-synthesizing system are open to reinterpretation.
These
authors recognize the fact that the most that can safely be said now is
that nucleic acid and protein synthesis must proceed at certain rates
for the hormones to exert an influence.
v.
Conclusions
Given our present knowledge, and the lack of conclusive evidence for
any particular theory of dormancy regulation, it is certainly not
25
possible to propose a general correspondence between the phases of
dormancy as espoused by Vegis (122) or Samish (107) and the endogenous
mechanisms of control.
It is possible that observations of empirical
behavior will allow one to decide between likely proposals.
That is,
any promising candidate among models of internal, biochemical action
must at least be amenable to such tests.
Little work has been done to try to reconcile environmental
influences and endogenous controls.
Those that have are
For
sketchy~
instance, Moustafa (88), working with peach seeds, states that cold
(stratification) inactivates auxin oxidase, causing an increasee in
auxin concentration, more RNA synthesis and consequent de
of lipase.
~
synthesis
Also hypothesized is a rather more vague effect of cold on
the removal of an inhibitor of a-oxidation of fatty acids.
As cited
above Jarvis (67) suggests that chilling "potentiates" GA synthesis,
which proceeds later with increased temperatures.
More generally,
El-Mansy and Walker (48) state that cold inactivates some inhibitors
and stimulates synthesis and release of enzymes necessary for the
degradation of metabolites.
area.
Much more work needs to be done in this
Any modeling attempt will necessarily be quite speculative on the
point of environmental-endogenous control interaction.
Several empirical models have been proposed (72, 100, 101).
They
deal with the action of chilling in the break of dormancy and subsequent
growth.
Amen (5) has proposed a model of seed dormancy; it deals only
superficially with external influences.
If his ideas can be fleshed
out, a useful basis for a model of bud dormancy may be available.
basic scheme is as pictured in Fig. 5.
His
26
In closing, we would like to point out those areas or ideas that
we believe to be most worth further investigation.
The modeling attempt
by Amen (5) should be expanded and experimental results obtained to
corroborate his ideas.
The work of Khan (70) on the interaction of
three or more hormones all involved in dormancy control appears to have
much promise.
A point that does not seem to be adequately emphasized is
the distinction between apical and subapical meristem cells.
It may
turn out that these two areas have distinct hormonal control mechanisms.
The major weak point of course is the absence of a link between
environment and biochemical workings.
Work here is needed.
27
A
TEMPERATURE
MAX
MIN
..
.......
',J'"
QUIESCENCE
....,.
PRELIMINARY
'INNATE AFTER
REST
TIME
QUIE ENCE
REST
REST
B
TEMPERATURE
MIN
TIME
Fig. 1.
28
GIBBERELLIN
CYTOKININ
INHIBITOR
+
+
+
+
+
+
+
+
+
+
+
Fig. 2
+
GERMINATION
29
DNA.PHOSPHOPROTEIN
Pi' SUGAR, AMINO ACIDS, ETC.
COMPLEX
TEMPERATURE
. -a4
....- - (CRITICAL
VARIATION)
r
ATP
DNA
+ Protein
ATP
ATP -
ATP_
RENE.WED
PLANT GROWTH &
DEVElOPMENT
Fig. 3
-
-
e
..
mRNA's
REGULATOR
I
REPRESSIO~
DEREPRESSION
PROK>TER
--:lTOR
U
!TRulL
GENts
OPERON
Fig. 4
Co.)
o
e
·
e
I
-L
Phy to chrome
(trigger agent)
~
e
inhibitor inactivation ~
~
gibberell in
pro teolytic enzymes\
(germination ag~ (releasing enzymes) ~.--iir-------rlr.,_~_~~~,r..~_~~~,r._~_~\\""""-------------'i
I
germina tion -../ ., /
inhibitor
cellulase
wall hydrolysis
~
-<
Germina tion
~
(activation)
~
proteinases
1~
a-amylase
releasing
enzyme
/
~
1 i
id h d 1 i
nuc e c at
y ro ya a
a-amylas~
(synthesis stimulation)1
Fig. 5
glutenin bound
polymerase
structural protein hydrolysis
starch hydrolysis
,
proteinase activation
(trypsin)
~
/
germination
inhibitor
,
~
I
ribonuclease
~
derepressing
enzyme
Jrepressed
DNA~DNA
mRNA
histone
actinomycin-D
....w
.'
32
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