175
MINI-REVIEW
THE ROLE OF ABSCISIC ACID DURING SEED
1
PRECOCIOUS GERMINATION
Renato Paiva 2 and Patrícia Duarte de Oliveira 3
Departamento de Biologia, Universidade Federal de Lavras, UFLA, CP
37, Lavras, MG, 37200-000, Brazil.
ABSTRACT- It is well established that the
phytohormone abscisic acid plays an important role
during different processes of plant development such
as seed maturation and germination. Advances in the
field of plant growth and development have shown the
involvement of abscisic acid at different signal
transduction pathways. Recent findings of the effects
of abscisic acid during processes of embryo
development that lead to inhibition of precocious
germination, a process also known as vivipary, are
summarized in this review.
Additional index terms: embryo, viviparous mutant
FUNÇÃO DO ÁCIDO ABSCÍSICO NO
PROCESSO DE GERMINAÇÃO PRECOCE
RESUMO- O fitohormônio ácido abscísico tem
importante função em diferentes processos do
desenvolvimento da planta como a maturação de
sementes e germinação. Avanços na área de
crescimento e desenvolvimento de plantas têm
mostrado o envolvimento do ácido abscísico em
diferentes rotas de transdução de sinal. Nesta revisão
são apresentadas as recentes descobertas sobre os
efeitos do ácido abscísico no desenvolvimento do
embrião inibindo o processo de germinação precoce,
processo este também denominado de viviparidade.
Termos adicionais de indexação: embrião, mutante
vivíparo.
ABA AND PRECOCIOUS GERMINATION
The phytohor mone abscisic acid (ABA) is be-
lieved to regulate many of the activities of late em-
br yogenesis that are associated with
developmental arrest (Robichaud & Sussex, 1986;
1 Received in 08/09/1994 and accepted in 10/02/1995.
2 PhD, Professor of Plant Physiology.
3 Graduate Student.
R.Bras.Fisiol.Veg., 7(2):175-179, 1995.
Bradford & Trewavas, 1994). High levels of ABA
present during embryo development possibly block
precocious ger mination, thus allowing seeds to
complete maturation (Quatrano, 1986; Lelu & La-
bel, 1994). In contrast to increased levels of endo-
genous ABA during late stages of seed
development, mature dry seeds contain reduced
ABA levels. Hetherington & Quatrano (1991) have
reported that in embryos of mature wheat seeds,
tissue sensitivity to ABA is reduced, and as a result
these seeds are able to germinate upon imbibition.
Accumulation of ABA during seed development
with high peaks preceding developmental arrest
has been reported in maize (Quatrano, 1986) and
cacao (Pence, 1991). In tomato seeds, ABA levels
increase during embryo growth and decrease as
the seeds mature and dehydrate. During the late
stages of tomato seed maturation, both embryo
and endosperm ABA levels decrease. The ABA de-
crease in the tomato seed appears necessary to
ensure germination, while simultaneous seed dehy-
dration prevents precocious germination (Hocher et
al., 1991). Groot & Karseen (1992) reported that in
tomato, endogenous ABA is able to induce dor-
mancy during seed development but precocious
ger mination in these seeds is supressed by os-
motic stress rather than by elevated levels of ABA.
Both ABA and sucrose are reported to be required
for the initiation of embr yo maturation in cacao
seeds. In these seeds, ABA mediates the uptake of
sugars which are required for normal cotyledon de-
velopment (Pence, 1992).
In many seeds, desiccation terminates the matu-
ration phase of development. Many studies suggest
that this drying plays an important role in changing
the developmental process to germination (Ker-
mode & Bewley, 1988; Black, 1991; Voesenek,
1994). Premature desiccation during seed develop-
ment leads to germination upon subsequent rehy-
dration and this germination is accompained by a
176
switch in the metabolism of the seed. The switch
from a developmental process to one of germina-
tion as result of premature drying induces the syn-
thesis of enzymes and proteins essential for
ger mination (Bewley et al., 1989; Chandler &
Robertson, 1994). Since most seeds undergo des-
iccation during the final stages of maturation, it is
logical to consider loss of water and increased ABA
levels as causative events leading to a change from
a seed developmental process to one of germina-
tion (Ker mode et al., 1986; Ker mode & Bewley,
1989).
Precocious germination can be induced in soy-
bean seeds after a slow dr ying treatment which
causes a decrease of its endogenous ABA (Acker-
son, 1984b). Conversely, if immature seeds are ex-
posed to high levels of ABA, desiccation tolerance
is induced. Meurs et al. (1992) were able to induce
desiccation tolerance in immature seeds of Arabi-
dopsis thaliana by treating them with elevated con-
centrations of ABA and sucrose. The authors
suggest that a possible action of ABA is to stimu-
late the release of sugars which may protect dehy-
dration sensitive str uctures from desiccation
damage. Crowe et al. (1989) have proposed that,
during dehydration, sugars are able to protect sen-
sitive structures such as membranes by replacing
bound water molecules. Blackman et al. (1995) re-
port that accumulation of the ABA-responsive late
embryogenesis abundant (LEA) proteins increases
desiccation tolerance in soybean seeds.
Accumulation of ABA preceding developmental
arrest strongly supports its role as an inhibitor of
seed growth (Quatrano, 1986). In soybean, when
endogenous ABA of immature embryos is reduced,
precocious ger mination is induced (Ackerson,
1984b). Studies in cotton led to the initial observa-
tions that ABA played a role in suppressing preco-
cious ger mination. Exogenously-supplied ABA
prevented germination of excised immature cotton
embryos and embryos placed on ABA-free medium
exhibited precocious ger mination (Ihle & Dure,
1970). Similar results were obtained when imma-
ture embryos of maize were cultured in the pres-
ence of ABA (Robichaud & Sussex, 1986) and
either ABA or sucrose (Kriz & Schwar tz, 1986).
ABA has also been reported to inhibit embryonic
germination in wheat (Walker-Simmons, 1987; Ried
& Walker-Simmons, 1990) and barley (Wang et al.,
1995).
The developmental stage of the embryo is also
important for the effect of ABA in preventing germi-
nation. Whereas mid-stage soybean embryos cul-
tured in the absence of ABA exhibit precocious
germination, young embryos undergo normal em-
br yogenesis in the presence of ABA (Ackerson,
R.Bras.Fisiol.Veg., 7(2):175-179, 1995.
1984a). In contrast, the suppression of germination
by ABA in rapeseeds seems to be more effective
dur ing ear ly stages of seed development. Low
water content, rather than ABA, prevents germina-
tion at the later stages of development. Exogenous
ABA is also able to suppress germination at later
stages, but higher concentrations are required.
Such exogenous treatment results in abnormal lev-
els of endogenous ABA and necrosis of embryos
(Finkelstein et al., 1985). High levels of ABA pre-
vents germination in rapesseds by inhibiting water
uptake (Finkelstein & Crouch, 1986)
The aleurone layer of cereal seeds contains hydro-
lytic enzymes that upon ger mination hydrolyze
seed reser ves that are conver ted to energy re-
quired at the initial stages of germination. The best
characterized hydrolytic enzyme of the aleurone
layer is α-amylase, a starch hydrolyzing enzyme
whose synthesis is induced by gibberellic acid
(Zeevart & Creelman, 1988; Karssen et al., 1989).
The phytohormone gibberellic acid produced at the
onset of germination induces the synthesis of en-
zymes whose function is to breakdown seed stor-
age products (Kuhlemeier et al., 1987; Folker,
1994). ABA has been repor ted to inhibit the gib-
berellic acid induction of α-amylase synthesis and,
consequently, prevent seeds from initiating germi-
nation (Garcia-Maya et al., 1990; Oishi & Bewley,
1990; Gallie, 1993). In respone to abscisic acid,
complementary α-amylase mRNA is expressed in
barley aleurone tissue causing the repression of α-
amylase gene expression and consequently, the
synthesis of the enzyme (Rogers, 1988). Gilroy &
Jones (1992) reported an increase in cytosolic free
calcium at the barley aleurone layers, preceeding
the gibberellic acid induction of α-amylase synthe-
sis. The effect of gibberellic acid on calcium con-
centration is reversed by treatment with ABA, which
has also been reported to inhibit ethylene action in
seeds of Townsville stylo ( Stylosanthes humilis ).
Stylosanthes germination is promoted by ethylene
and in these forage seeds, ABA prevents germina-
tion by inhibiting the conversion of 1-aminocyclo-
propane-1-carboxylic acid (ACC) to ethylene
(Vieira & Barros, 1994).
ABA AND VIVIPARY
Additional evidence supporting the suppression
of precocious ger mination by ABA comes from
studies of mutants defective in ABA metabolism
(Black, 1991; McCarty, 1995). During seed develop-
ment, embryos of monocot and dicot plants may
fail to complete maturation and germinate while the
immature seed is still attached to the maternal tis-
sue. This phenomenon is referred to as vivipary or

preharvest sprouting (Fong et al., 1983). Many vi-
viparous mutants of maize have been described in
the past (Robertson, 1955) and, for these mutants,
embr yos homozygous for the recessive allele at
any viviparous locus exhibit precocious germina-
tion between 20 and 30 days after pollination.
Maize viviparous ( vp ) mutants of the Class I type,
including vp1 , exhibit normal levels of carotenoids
but no production of anthocyanin pigments
(Dooner, 1985). Neill et al. (1987) repor ted that
ABA accumulation during development of wild type
and vp1 kernels were similar indicating that vivi-
pary in this mutant is caused in part by a lack of
response to growth inhibition by ABA. In addition,
when immature embryos of both vp1 and wild type
were cultured in the presence of ABA, the mutant
embryos exhibit a reduced sensitivity to the inhibi-
tory effects of applied ABA (Robichaud & Sussex,
1986).
Viviparous mutants of the Class II which includes
vp2 , vp5 , vp7 , and vp9 present carotenoids and
chlorophyll synthesis inhibition (Robertson, 1955;
Neil et al., 1986). A correlation between ABA levels
and carotenoid content for Class II mutants has
also been reported. Seedlings of carotenoid-defi-
cient mutants (Class II) rescued from viviparous
kernels exhibit reduced ABA levels compared to
wild type seedlings grown in the same way. Seed-
lings of the Class I vp1 mutant contain normal lev-
els of carotenoids and ABA but reduced amount of
chlorophylls (Neill et al., 1986). Apparently, the cor-
relation between carotenoid content and ABA lev-
els is due to the synthesis of ABA via the
carotenoid biosynthetic pathway and each of Class
II mutants is defective at some step of the carote-
noid biosynthesis pathway (Fong et al., 1983). It
has been proposed that because of the defective
ABA metabolism, viviparous kernels fail to become
dormant and, as a result, undergo precocious ger- ACKERSON, R. C. Regulation of soybean
mination on the ear. Class II mutant embryos sup-
plied with ABA undergo maturation rather than
precocious germination (Robichaud et al., 1980). ACKERSON, R. C. Abscisic acid and precocious
Apparently, the reduced ABA content observed in
seeds of Class II mutants is derived from maternal
tissues. Ober & Setter (1992) have reported that in BEWLEY, J.D.; KERMODE, A.R. & MISRA, S.
response to water stress, endosperm of maize vi-
viparous mutant seeds accumulate ABA synthe-
sized in vegetative tissues. Transport of ABA from
maternal tissues to developing maize embryos has
been reported by Hole et al. (1989).
Studies using inhibitors of carotenogenesis have BLACK, M. Involvement of ABA in the physiology of
shown their ability to induce precocious germina-
tion. Fong et al. (1983) were able to induce vivipary
in developing maize seeds after treatment with flu-
r idone, an inhibitor of carotenoid biosynthesis.
Their studies indicate that the action of this inhibi-
R.Bras.Fisiol.Veg., 7(2):175-179, 1995.
177
tor in maize tissues is developmentally related. In-
hibition of carotenoid and ABA accumulation in
seeds followed by induction of vivipary was only
obtained with fluridone treatment in seeds aged be-
tween 9 and 11 days after pollination. This result
indicates the presence of a developmental clock in
seeds which regulates the fate of seed develop-
ment. Between the age of 9 to 11 days after polli-
nation a decision is made in which seeds will
respond by either germinating precociously or fol-
lowing normal maturation processes.
ABA AND EMBRYO GENE EXPRESSION
Recent studies have established that, in re-
sponse to preventing precocious germination, ABA
induces the expression of embryo-specific genes.
Genes of the most abundant storage proteins of
maize embr yos (Globulin-1 and Globulin-2) are
positively regulated by ABA (Kriz et al., 1990; Paiva
& Kriz, 1994). In maize embryos, the expression of
these genes is under the control of different factors
which require specific endogenous ABA levels
(Paiva & Kriz, 1994; McCarty, 1995). Similarly Wil-
liamson & Scandalios (1994) have shown that dif-
ferent factors in combination with ABA levels
control the expression of Cat1 gene in germinated
maize embryos.
There is no doubt that ABA is involved on the ex-
pression of many genes during processes of plant
development. Many researchers are now directing
efforts in order to understand the role of ABA in sig-
nal transduction pathways related to plant develop-
ment. It is expected that the information obtained
with these studies will broad the understanding of
many molecular and physiological processes in
plants.
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