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This review dis-
cusses what is
known and is not
known about how
temperature and
light affect seed
germination.
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
TEMPERATURE AND LIGHT EFFECTS
ON SEED GERMINATION
John
Erwin
University
of
Minnesota
How can we increase the percent germi-
nation
of
difficult
to
germinate species?
Two environmental stimuli which have
the greatest potential for increasing seed
5ermination are temperature and light.
I’his review discusses what is known and
is
not
known
about how temperature and
light affect
seed
germination.
Although it is somewhat technical, the
review below lets you know the ‘state
of
the art’ of the environmental physiology
3f
seed germination. Most studies have
been done on weed species. However, the
zoncepts which we have learned from
them may have application on many
bedding plant and perennial species
of
Lommercial significance.
Introduction
The breaking
of
seed
dormancy involves
a
complex sequence
of
events which may
or may not interact to influence germi-
nation. The potential for germination
arises from both environmental and
hormonal stimuli.
Two
of
the most
important environmental stimuli which
effect seed germination are tempera-
ture and light. Although the effects
of
temperature and light on seed germina-
tion have been researched extensively,
a full understanding
of
how these
2
stimuli influence seed germination and
dormancy is only now being under-
stood.
What is the ecological significance
of
developing
a
system whereby tempera-
ture and light influence seed dor-
mancy? The basis for seed dormancy is
presumably an environmental adapta-
tion to allow
the
survival
of
a
species
through adverse environmental condi-
tions. Seed dormancy allows
the
seed
to conserve its reserves until environ-
mental conditions are favorable for
survival
of
the seedling. Temperature
is perhaps the most limiting factor
of
the physical environment with respect
to species distribution. Competition
for light can also limit seedling sur-
vival when temperature is not limiting.
Temperature
Limiting
Light
Limiting
Temperature
Li initing
Figure
1.
World map showing temperature limitations
on
species indigenous to
temperate regions and light limitations on species indigenoir
r
to tropical regions.
16
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
The
greater importance
of
either tem-
perature or light in the breaking
of
dormancy
is
dependent on the most
limiting factor for seedling survival in
the
indigenous environment of the spe-
cies (Went,
1953).
For instance,
the
ger-
mination
of
a number
of
temperate spe-
cies, where cold winters may be the
most limiting environmental factor,
often require a chilling treatment for
successful germination to occur (Toole,
1973)
(Figure
1).
In contrast,
the
germi-
nation
of
tropical species, where com-
petition for light may
be the
most
limiting environmental factor, often
require an exposure to red light for
successful germination (Smith,
1975).
It
is
important
to
realize, however, that
temperature and light often
both
influ-
ence seed dormancy regardless
of
the
place
of
origin
of
a species (Smith,
1975).
In addition, breaking
of
seed
dormancy and/or germination
of
all
plant species can be inhibited by non-
optimal temperature or light condi-
tions regardless
of
the
primary stimula-
tory mechanism for germination.
I.
Effect
of
Temperature and Light on
Seed
Germination: Seed
of
many tem-
perate species require a chilling treat-
ment, after seed are imbibed, before
germination can occur (VanDeWoude
and Toole,
1980).
The effectiveness
of
a chilling treatment increases linearly
as temperature decreases from
18
to
4OC.
Stratification is the process
of
de-
livering a cool moist treatment
to
seed
to encourage germination (Hartmann
and Kester,
1959).
The
effectiveness
of
a chilling treat-
ment in potentiating germination can
be greatly modified by light (Toole,
1%2; 1973).
For instance, the length
of
a chilling treatment can
be
greatly re-
duced in some species by a red light
exposure prior to chilling (Brevington
and Hoyle,
1981;
Toole
et al,
1962;
Duke et
al,
1977).
Irradiation
of
seed
immediately after a
chilling treatment can increase the per-
cent germination
of
some species.
Seed
of
Pinus
strobus
typically require
30
to
90
days
of
chilling prior to germination.
Red light irradiation
of
seed after only
2
days
of
chilling increased germination
from
9
to
32%
(Toole et al,
1955; 1962).
The promotive role
of
red light prior
to
or during chilling is reversible with far
red light if the far red exposure is given
shortly after the exposure
to
red light
(Taylorson and Hendricks,
1969;
Cone
and Kendrick,
1986).
This reversibility
of
the
red light stimulation
of
germina-
tion by far red light suggests phyto-
chrome involvement (Smith,
1975)
(Figure
2)
*
Phytochrome is a pigment in the plant
which enables a plant to detect whether
it is being shaded
by
other plants.
Phyto-
chrome also allows the plant
to
deter-
mine the length
of
the photoperiod (and/
or nyctoperiod) (Smith,
1975).
Phytochrome has
2
forms,
P,
and
P,.
P,
absorbs red light
(660
nm) and then con-
verts to P,. Conversely, P, absorbs far
red light
(720
nm) and converts to P, P,
is continually being synthesized and P,,
is continually being degraded (Figure
3).
The
effect
of
red and far red light on
seed dormancy prior to and during chilling
suggests that high endogenous P, levels
favor germination (Mancinelli et al,
1967;
Takaki et al,
1981).
There are a number
of
theories as to how
red light and temperature may interact
to
stimulate seed germination. VanDe-
Woude and Toole
(1980)
found that
temperatures below
18OC
greatly increase
the sensitivity
of
Lactuca
sativa
seed
to
the P, form of phytochrome.
A
chilling
treatment
is
associated with the
preservation
of
P, within the seed through
low reversion rate
from
P,
to
P,
(Breving-
ton and Hoyle,
1981).
As
stated above,
high P, levels are believed to encourage
germination.
Hendricks and Taylorson
(1976)
defined
a temperature sensitivity
of
membrane
leakage with probe fluorescence at tem-
peratures above
17OC
in
seed
of
Avena,
Lactuca,
Barbarea,
Autilon, Lychnis, Dau-
cua,
and
Datura.
They
suggested that
temperatures above
17OC
after imbibi-
tion result in membrane lipid dissocia-
The greater impor-
tance
of
either tem-
perature or light In
the breaking
ofdor-
mancy is depend-
ent on the most
limiting factor for
seedling
sunrival
in
the Indigenous en-
vironment of the
species.
Seed of many tem-
perate species re-
quire a chilling
treatment before
germination can
occur.
The effectiveness
of a chilllng treat-
ment increases
linearly
as
tempera=
ture decreases
from
18
to 4OC.
The effectiveness
of a chilling treat-
ment In potenti-
ating germination
can be greatly
modified by light.
The promotive role
of red light prior to
or during chilling
is
reversible with far
red light
if
the far
red exposure is
given shortly after
the exposure to red
light.
17
FhxtWhsIntem-
perature stimulate
germination in
some species.
The effect of tem-
perature fluctua-
tions on germina-
tion
can
be
negated
by
exposure of
seedtofarredlight.
Short
term tem-
perature pulses
can also stimulate
seed germination
in some
species.
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
Red
Then
Far
Red Light
Far
Red
Light
Far
Red
Light
Then
Red
Light
Figure
2.
germination.
The effects of red
and
far red light on lettuce seed
tion and both ion and amino acid leak-
age which ultimately results in a
loss
of
seed germination potential.
11.
Temperature Fluctuation:
Fluctua-
tions in temperature stimulate germina-
tion in some species (Aragino,
1981).
Rumex retroflexus
is skotoblastic (germi-
nation
is
inhibited by dark);
Rumex
seed
will
not germinate at either
20
(@OF)
or
3OOC
(%OF)
in the dark. However, ger-
mination can be
as
great as
100%
when
the temperature is fluctuated, in
the
dark, between
20
and
3OOC
diurnally,
i.e.
in a
24
hour cycle (Toole et al,
1955).
Cucumis anguria
is photoblastic (inhib-
ited by light) but will germinate in the
light if temperatures are fluctuated
between
15
and
35OC
(Felippe,
1980).
Seed of
Rumex obtusifolius
which is
skotoblastic will germinate in the dark
if
temperatures fluctuate between
15
(590F)
and
35OC
(95OF).
The effect
of
temperature fluctuations
on germination can be negated by expo-
sure
of
seed to far red light (Felippe,
1980).
When temperatures are alternated
between
5
and
25OC,
far red light
will inhibit ger-
mination
of
both
Rumex
and
Cu-
cumis
(Felippe,
1980).
Presuma-
bly, this
is
an
ecological adapta-
tion to allow ger-
mination
of
Ru-
mex
during peri-
ods
of
the year
when fluctuations
in day and night
temperature are
great
and
when
seedling survival
would not be lim-
ited by competi-
tion from adjacent
plants. Shading
by adjacent plants
increases the pro-
portion
of
far red
light versus red
light which
shaded plants are
exposed to.
A
high far red:red light
ratio allows the plant
to
perceive that
it
is
being shaded by adjacent plants.
Short term temperature pulses can also
stimulate seed germination in some
species (Takaki et al,
1981).
Cucumis
seed imbibed at
25OC
can be stimulated
to germinate by a
2
hour
O°C
tempera-
ture pulse (Felippe,
1980).
Low tem-
perature treatment
of
Rumex obtusifo-
lius
also stimulates germination (Takaki
et
al,
1981).
Seed
of
Rumex, Nicotiana
and
Nigella
can be stimulated to germi-
nate by a short term high temperature
pulse (Aragino,
1981).
Similarly,
Lac-
tuca
seed was stimulated to germinate
by
exposure to
33OC
for
30
minutes
(Hendricks and Taylorson,
1976).
Stimu-
lation
of
germination by a high tem-
perature pulse in
Cucumis
is reversible
by an exposure
of
seed
to far
red
light
(Felippe,
1980;
Takaki et
al,
1981).
High temperature pulse stimulation
of
germination is not reversible by far
red
light in
Rumex obtusifolius
unless seed
is exposed to red light prior to the
far
red exposure. Presumably, the red light
18
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
Far
Red
Light
Exposure
(720
nm)
---
Biosynt
hesis
Deg
radati
o
n
Figure
3.
Effect
of
red and far red light
exposure is necessary to completely
cycle the phytochrome pool (Takaki et
al, 1981). Takaki et a1 (1981) suggested
that high temperature pulses may in-
crease the available
P,,
to above a
threshold level in the
seed
through an
increase in phytochrome synthesis.
The effectiveness of a high tempera-
ture pulse in stimulating
seed
germina-
tion
of
some species is greatly enhanced
by an exposure to red light (Toole,
1973; Taylorson and Hendricks, 1972).
However, red light enhancement of a
high temperature pulse is only effec-
tive in stimulating enhancement of
seed germination if
the
red light expo-
sure occurs after or during an exposure
of
the
seed
to temperatures below 32OC
(Taylorson and Hendricks, 1979). For
example, exposure
of
Amaranthus
retroflexus
seed to red light while
seed
maintained at
40%
(104OF) resulted in
only 2% germination (Taylorson ahd
Hendricks, 1969). However, germina-
tion at 4OoC was greatly enhanced if
the exposure to red light at
4OOC
was
followed by a 10 minute exposure to
32OC
(WF)
then returned to
40%.
In
fact, a 64 minute exposure to 15OC
(59OF)
before moving seed back to 40%
increased
Amaranthus
germination to
80%.
Based on these results Taylorson
and Hendricks (1979) suggested that
phytochrome must interact with a reac-
tion center
which
is
stable
at temperatures
at or below 32OC
in order to elicit
a
response,
i.e.
germination.
111.
Interaction
Between Lipht,
TemDerature
and Hormones:
The hormonal
content
of
seed
changes
as
the
length
of
time
which seed are
stratified in-
creases. Absci-
on phytochrome
(P)
form.
sic
acid
(ABA)
content de-
creases as the length of a chilling period
increases in
Fraxinus americana, Juglans
regia
and
Cotylus avellana
(Wareing and
Saunders, 1971). Higher concentrations
of
abscissic acid are associated with an
inhibition of germination.
In contrast to
ABA,
gibberellin content
increases
as
the length of the stratifica-
tion time increases in
Cotylus.
Gibber-
ellins are associated
with
the
promotion
of
germination. In fact, application of
gibberellic acid (GA4+,) has been shown
to overcome the stratification require-
ment of a number of species (Taylorson
and Hedricks, 1976; Felippe, 1980). Gib-
berellins can also overcome inhibition
of
germination of
Cucumis,
skotoblastic, in
light (Felippe, 1980).
Light also influences seed hormone
content. Felippe
et
a1 (1980) showed that
seed gibberellin content increased after
an exposure to red light and/or high
temperatures. Cytokinin content
of
seed
has also been shown to increase in seed
following an exposure of seed to light
(Wareing and Saunders, 1971). Exogenous
applications of cytokinin stimulate ger-
mination of a number
of
light sensitive
species (Felippe, 1980).
Interestingly, The effectiveness
of
cy-
tokinins and gibberellins on stimulating
Cucumis
germination
is
greatly enhanced
The effecthreness
of
a high tempera-
ture pulse in stimu-
lating seed germl-
nationofsomespe
cies
Is
greatly en-
hanced
by
an ex-
posure to red light.
The hormonal con-
tent
of
seed
changes
as
the
length
of
time
which seed are
stratified ln-
creases.
Light
also
influ-
ences seed
hormone
content.
19
Perceptlon
of
light quality (or
achieved
through altera-
tionsinthephyb
chrome chromo-
phore between
the
P,,
state and
the
P,
state.
color)
Is
Minnesota Flower Growers Bulletin
-
May,
by
an exposure of
seeds
to red light (Fe-
lippe, 1980). Such a synergism was not
observed in
Chenopodium
album
(Karssen,
1968).
IV.
Perception
of
Light
and Temperature:
Perception of light quality (or color) is
achieved through alterations in the phyto-
chrome chromophore between the P,,
state and the
P,
state (Smith, 1975). This
alteration in the chromophore is be-
lieved to result in an interaction
with
the
plasma membrane within a cell to elicit
a response (Mackenzie et al., 1975; Marme,
1977). More recent studies have sug-
gested that phytochrome is not associ-
ated with the plasma membrane, but
instead suggest that phytochrome is dis-
tributed throughout the cytosol (Saun-
ders
et
al., 1983). After irradiation (ex-
1991
Volume
40,
Number
3
posure) with red light, phytochrome is
sequestered into dense structures within
the cytosol (Speth et al., 1986). Interest-
ingly, these structures disappear within
1-4 hours after
they
are formed. Speth
et
al. (1986) have suggested that
P,
induces aggregation
of
some unknown
protein receptor which ultimately leads
to a germination response.
How
is
temperature perceived? This is
a difficult question since
it
inherently
suggests
the
presence
of
a receptor. In
one respect, the entire seed responds to
temperature since the rate of every
metabolic reaction is affected. There
is, however, some evidence to suggest
that there may be temperature recep-
tors. The effects
of
temperature on
phytochrome reversion and degrada-
Factors Which Can Affect Germination
Imbibed Seed
Growth
Rea
u
lators
Gibberellin Promotes
Anesthetic Promotes
Cytokinin Promotes
Environmental
Light Environment
Temperature Environment
Fluctuating Temperatures
Temperature Pulse
Germination
Figure
4.
-
tion are well
known (Smith,
1975). Therefore,
one may suggest
that phytochrome
is a temperature
receptor as total
phytochrome and
the ratio of P, to
P,
are altered by
temperature. In
addition, the
p
hy t ochr ome-re-
ceptor complex or
the receptor itself
may play a role in
temperature sens-
ing in plants.
Most
seed
can not
germinate at tem-
peratures above
3OOC
(%OF)
(Hen-
dricks and Tay-
lorson, 1979). This
loss
of
germina-
tion potential at
high temperatures
has been attrib-
uted to membrane
leakage and al-
terations in mem-
brane organiza-
tion within
the
seed (Hendricks
20
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
Membrane Effects On Seed
Germination
V.
Potential
Ways
Which
Temperature
Effects Seed
Red Lightat
104~~
Germination:
Then
64
Minutes At
Either tem-
68
OF
>90
OF
Anesthetic
590F
Then
perature or
Returned To
1040F
light
can
of-
@
Figure
5.
and Taylorson, 1979). Many seed leak
endogenous sugars and amino acids at
temperatures above
30%
(Aragino, 1981;
Hendricks and Taylorson, 1976; Hen-
dricks and Taylorson, 1979). Seed which
do not show membrane leakage at tem-
peratures above
30%
such as
Amaran-
thus
albus
and
Amaranthus theophrasti
germinate successfully at temperatures
above
3OoC
(Hendricks and Taylorson,
1978). The dramatic increase in seed
germination at temperatures below
30%
suggest that membrane lipids may have
to be intact for successful germination
to occur (Aragino, 1981). Temperatures
above 32OC (90OF) disrupt membrane
organization and may limit germina-
tion (Taylorson and Hendricks, 1979).
Therefore, temperatures may also be
sensed
by
a gradient in membrane
organization (Figure
5).
The importance
of
the plasma mem-
brane in potentiating seed germination
is unequivocal. Disruption of the plasma
membrane with high concentrations
of
anesthetic virtually eliminates stimula-
tion of germination by chilling or red
light (Hendricks and Taylorson, 1979).
Interestingly, low concentrations of
anesthetic can stimulate dark germina-
tion
of
Panicum dichotomiflorum
seed,
which normally require light for ger-
mination (Taylorson and Hendricks,
1979).
ten stimulate
seed germina-
tion. This sug-
gests that tem-
perature and
light affect
seed
germina-
tion through
2
different par-
allel mecha-
nisms, rather
than in se-
quence, which
interact to potentiate germination.
However, the numerous interactions
between temperature and light suggest
that although the initial perception
of
temperature and light
by
a seed may be
different, the transduction pathway,
which ultimately results in germination,
is similar.
The
question arises then as to
where the interaction between tempera-
ture and light occurs and where do the
transduction pathways coincide.
The initial effects
of
either light or shorl
term temperature pulses on seed germi-
nation does not require protein synthesis
(Taylorson and Hendricks, 1972). There-
fore, the initial response
of
a seed tc
either temperature or light is physical
and not metabolic in nature. In
othei
words, the primary effect
of
tempera-
ture or light does not involve the transduc-
tion pathway in itself but rather some
physical phenomenon which initiates
a
biochemical response.
Perhaps a receptor
is
associated with the
cellular membrane. Initiation
of
a re.
sponse may require dissociation
of
thc
receptor from the membrane surface
High temperatures may limit the effec.
tiveness of the receptor by not allowini
membrane dissociation. In contrast, shori
term temperature pulses may encouragc
receptor separation from the membrant
surface.
Wost seed cannot
aerminate
at
tem-
peratures above
3OoC
(86OF).
The effects
of
tem-
perature and light
on seed germina-
tion are often syn-
ergistic.
The effects
of
ei-
ther light or short
term temperature
pulses
on
seed
ger-
mination does
not
require protein
synthesis.
21
There
are synergis-
tic
relationships
be-
tween
growth regu-
lators and either
temperature or
light.
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
Alternatively, a receptor may be present
in the cytosol at all times. Stimulation
of
germination may require an intact
membrane in which the receptor-phyto-
chrome complex must bind with stimu-
late a biochemical response. In contrast,
phytochrome could modify the receptor
to allow binding
to
the membrane.
How could temperature alterations and/
or pulses alter the receptor? Perhaps
the
receptor is also temperature sensitive in
the same way as the membrane. Short
term pulses may alter the receptor
to
allow an interaction with the membrane.
There are synergistic relationships
be-
tween growth regulators and either tem-
perature or light. The synergism of
ei-
ther cytokinin or gibberellin and light in
stimulating germination indicates that
light and plant growth regulators are not
acting sequentially
to
stimulate germi-
nation. Instead, the effect
of
growth
regulators and light or temperature on
germination are initially independent.
Presumably this is due
to
a separation
of
processes involved in hormone synthesis
versus physical temperature and/or light
perception. Therefore, the effects
of
light, temperature and hormones on the
breaking
of
seed
dormancy and germina-
tion must result from a variety
of
paral-
lel but mutually interacting mechanisms.
It is probable that some physical mecha-
nism is involved which may combined
with hormonal responses to induce a syn-
ergism.
We are currently experimenting with
some
of
the before mentioned interac-
tions
to
increase
the
percent germination
and decrease the time for germination
on difficult
to
germinate perennial spe-
cies.
I
encourage all
of
you to experi-
ment with any ideas you may get from
this review.
If
you have any successes,
be sure to let me know!
LITERATURE CITED
Aragino, M.
1981.
Response
of
macro-
phytes to temperature. Encyl.
of
plant physiology, Vol
12a,
Ed.
A.
Pirson and M.H. Zimmerman. pp.
339-371.
Brevington, J.M. and M.C. Hoyle.
1981.
Phytochrome action during pre-
chilling induced germination
of
Betula
paMera
Marsh. Plant Phvs-
-
iol.
67:705-710.
Cone, J.W. and
R.E.
Kendrick.
1986.
Photocontrol
of
seed germination.
In: Photomorphogenesis in plants.
Ed. R.E. Kendrick and G.H.M.
Kronenberg. Marinus Nijoff Pub.,
Dordecht, The Netherlands. pp.
443-465.
Duke,
S.O.,
G.H. Egley and B.J. Reger.
1977.
Model for variable light sen-
sitivity in imbibed dark-dormant
seeds.
Plant Phvsiol.
59:244-249.
Felippe,
G.M.
1980.
Germination
of
light-sensitive seeds of
Cucumis an-
guria
and
Rumex
obtusifolius:
Effects
of
temperature. New Phvtol.
84:439-448.
Hartmann,
H.T
and
D.E.
Kester
1959.
Plant Propagation: Principles and
Practices. Prentice-Hall, Inc. Engle-
wood Cliffs, New Jersey.
Hendricks, S.B. and R.B. Taylorson.
1976.
Variation in germination and
amino acid leakage
of
seeds with
temperature related
to
membrane
phase change. Plant Phvsiol.
58:7-
11.
Hendricks,
S.B.
and
R.B.
Taylorson.
1979.
Dependence
of
thermal re-
sponses
of
seeds on membrane tran-
sitions. Proc. Natl. Acad.
&i.
USA
76~778-781.
Karssen,
C.M.
1968.
The
light pro-
moted germination
of
seeds
of
Ch-
enopodium album
L.
(11).
Effects
of
(RS)-abscisic acid,
m.
m.
17:293-306.
22
Minnesota Flower Growers Bulletin
-
May,
1991
Volume
40,
Number
3
Mackenzie, J.M., R.A Coleman, W.R.
Briggs and L.H. Pratt.
1975.
Revers-
ible redistribution
of
phytochrome
within the cell upon conversion
to
its physiologically active form.
&.
--
Natl. Acad.
&i.
USA
72:799-803.
Mancenelli,
A.L.,
Z.
Yaniv and P. Smith.
1967.
Phytochrome and seed germi-
nation I. Temperature dependence
and relative P, levels in the germi-
nation
of
dark-germinating tomato
seed. Plant Phvsiol.
42:333-337.
Marme, D.
1977.
Phytochrome: mem-
branes as possible sites
of
primary
action. Ann. Rev. Plant Phvsiol.
28: 173- 198.
McLemore, B.F.
1964.
Light during
stratification hastens dark-germi-
nation
of
loblolly pine seed.
-
Sci.
10:348-349.
Forest
Saunders, M.J., M.M. Cordonnier, B.A.
Palevitz and L.H. Pratt.
1983.
Im-
munofluorescence visualization
of
phytochrome in
Pisum sativum
L.
epicotyls using monoclonal anti-
bodies. Planta
159545553.
Smith,
H.
1975.
Phytochrome and
Phytomorphogenesis. McGraw-Hill.
New York. pp.
121-128.
Speth, V., V. Otto and
E.
Schafer.
1986.
Intracellular localization
of
phyto-
chrome in oat coleoptiles by elec-
tron microscopy. Planta
168:299-
304.
Takaki, M., R.E. Kendrick and S.M.C.
Dietrich.
1981.
Interaction
of
light
and temperature on the germina-
tion
of
Rumex obtusifolium
L.
Planta
152~209-214.
Taylorson, R.B. and S.B. Hendricks.
1%9.
Action
of
Phytochrome dur-
ing prechilling
of
Amaranthus
retroflexus
L.
seeds.
Plant Physiol.
44~821-825.
Taylorson, R.B. and S.B. Hendricks.
1972.
Interaction
of
light and a tempera-
ture shift on seed germination.
Plant Phvsiol.
49:127-130.
Taylorson, R.B. and
S.B.
Hendricks.
1973.
Phytochrome transformation and
action in seeds
of
Rumex crispus
L.
during secondary dormancy. Plant
Phvsiol.
52:475-479.
Taylorson, R.B. and S.B. Hendricks.
1976.
Interactions
of
phytochrome and ex-
ogenous gibberellic acid
on
germina-
tion
of
Lamium amplexicaule
L.
seeds.
Planta
132:65-70.
Taylorson, R.B. and S.B. Hendricks.
1979.
Overcoming dormancy in seeds with
ethanol and other anesthetics. Planta
145:507-510.
Went,
F.
1953.
Temperature effects on
plant growth. Ann. Rev.
of
Plant
phvs.
4:347-362.
Toole, E.H., V.K. Toole,
H.A.
Brothwick
and S.B. Hendricks.
1955.
Interac-
tion
of
temperature and light on ger-
mination
of
seeds.
Plant Physiol.
30~473-478.
Toole,
V.K,
E.H.
Toole,
H.A.
Brothwick
and
AG.
Snow.
1962.
Responses
of
seeds
of
Pinus taeda
and
Pinus
strobus
to light. Plant Phvsiol.
37:228-233.
Toole, V.K.
1973.
Effects
of
light, tem-
perature and their interactions on
the
germination
of
seed.
&i.
-
and Technol.
1:339-396.
VanDeWoude, W.J. and V.K.
Toole.
1980.
Studies of the mechanism of
enhancement of phytochrome de-
pendent lettuce seed germination
by prechilling. Plant Phvsiol.
66:220-
224.
Wareing, P.F. and P.F. Saunders.
1971.
Hormones and dormancy. Ann. Rev.
Plant Phvsiol.
22:261.
23