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Received: 16 February 2011 Returned for revision: 9 March 2011 Accepted: 7 April 2011
† Background The African oil palm (Elaeis guineensis) is a monoecious species of the palm subfamily
Arecoideae. It may be qualified as ‘temporally dioecious’ in that it produces functionally unisexual male and
female inflorescences in an alternating cycle on the same plant, resulting in an allogamous mode of reproduction.
The ‘sex ratio’ of an oil palm stand is influenced by both genetic and environmental factors. In particular, the
enhancement of male inflorescence production in response to water stress has been well documented.
† Scope This paper presents a review of our current understanding of the sex determination process in oil palm
Key words: Sex determination, oil palm, Elaeis guineensis, inflorescence, monoecious, temporal dioecy,
flowering.
# The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
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Page 2 of 9 Adam et al. — Environmental regulation of sex determination in oil palm
‘sex ratio’ of an oil palm stand is affected by both environ- accompanying staminate flowers develop pollen sacs with pro-
mental and genetic factors. In this paper, we first discuss liferating microsporocytic cells; however, the latter display
current knowledge of the mode of action of environmental incomplete development and the flower is shed soon after,
factors on oil palm inflorescence development, and then before the pistillate flower of the triad has reached maturity
discuss how they might act upon the plant’s reproductive (Adam et al., 2005). Both types of inflorescence are protected
development to regulate sex determination. during their development by the prophyll and first penduncular
bract, which are ruptured just before flower maturity is
reached. Other peduncular bracts are small, triangular struc-
I NF LO R E S C E N C E D E VE LO P M E N T IN OI L PA L M tures which do not envelope the developing inflorescence
As mentioned earlier, the oil palm normally produces func- (Dransfield et al., 2008).
tionally unisexual male and female inflorescences in an alter-
nating cycle, thereby minimizing the chances of I N F LO R E S C E N C E D E V E LO P M E N T I N
self-pollination. Macroscopic views of the normal male and RE LATI ON TO VE GETATIV E GROW TH
female inflorescences are shown in Fig. 1. Male and female
inflorescences are branched and easily distinguishable from In favourable growing conditions, an inflorescence is initiated
their overall structure, the male inflorescence bearing a in the axil of each leaf of the palm. The rate of leaf emission
larger number of rachillae (branches) inserted into the rachis varies with age, with typically three leaves produced per
(central axis). Another easily recognizable difference month in young palms and two per month in the case of
between the two sexes is in the form of the rachillae them- older individuals. The development of an oil palm inflores-
selves; in the case of the female inflorescence they bear a cence between the stages of initiation and flower maturity
distal sterile region that develops into a characteristic spine lasts 2 – 3 years for both sexes, the process being initiated
not seen in the male rachilla. The early differentiation of oil soon after seedling establishment.
Leaf +15
Floral development
Leaf +18
Flower maturity
Sex Leaf +6
determination
Individualization of
Leaf –26 floral meristem ( )
Initiation of prophyll and first
peduncular bract Leaf –27
Individualization of
rachis meristem
Leaf –6
Initiation of rachilla
meristem (•) Leaf –2
Individualization of rachilla
meristem ( )
proved invaluable for increasing pollen production from pisi- as to remove the entire lamina, the unopened leaves in the
fera palms (Durand-Gasselin et al., 1999). The latter are spear being cut around 1 m from their base (Durand-Gasselin
used as the male parent in most breeding programmes as et al., 1999). Field observations of sex ratio changes in response
they are homozygous for the Sh– thin shell thickness allele to defoliation have provided clear indications of the chronology
and give rise to high oil-yielding tenera palms (Sh– /Sh + ) of sex determination and differentiation. The timeline of oil
when crossed with a thick-shelled dura (Sh + Sh + ) female palm inflorescence development, as inferred from the effects
parent. It is interesting to note that pisifera palms produce of defoliation, are summarized in Fig. 3, as reproduced from
abortive fruit, which place lower demands on the plant’s Hartley (1988) by Durand-Gasselin et al. (1999). It can be
resources. As a result, pisifera palms usually remain female seen that the time intervals between the different stages of inflor-
when grown in conditions of high and regular water avail- escence development vary according to the age of the palm, in
ability, thus creating the problem of limited pollen production accordance with the lower rate of leaf emission seen in mature
for breeding, which can be overcome by defoliation as men- palms compared with young individuals. One important point
tioned earlier. The exact nature of the stress response under- to note is that sex determination is not the only effect of leaf
lying the induction of male inflorescence production by pruning; the latter treatment also induces inflorescence abortion.
defoliation is not yet clear, but current hypotheses will be dis- However, the two effects occur at different phases of develop-
cussed in more detail below. ment: whereas abortion is mostly observed for inflorescences
Beyond the obvious agronomic interest in using defoliation as at stages +4 to +10 (4 – 6 months prior to flower maturity),
a means of controlling pollen production, the same approach can sex determination changes are typically seen in the region of
also provide a useful experimental system by which to investi- stage –20, approx. 22 months before flower maturity in adult
gate the process of sex determination in oil palm. In the palms (summarized in Durand-Gasselin et al., 1999). As with
context of the studies described here, defoliation can be most aspects of flowering, the exact chronology of these
defined as the pruning of all expanded leaves at their bases so effects varies according to palm age. Although it can be
Page 4 of 9 Adam et al. — Environmental regulation of sex determination in oil palm
LEAF POSITION
–40 –30 –20 –10 0 +10 +20
LEAF
OPENING
F I G . 3. Development and sex determination of the oil palm inflorescence in relation to palm age [after Hartley (1988), as reproduced by Durand-Gasselin et al.
(1999)].
coexist with female and male individuals, only the former that the gender plasticity of at least some of the other five ‘tem-
were found to display a variable sex ratio, with different porally dioecious’ genera producing unisexual inflorescences
clones of the same genotype varying in the percentage of (see above) might be subject to environmental regulation.
male flowers produced (Glawe and de Jong, 2005). One intriguing case is that of the Madagascan Marojejya
Subsequent studies revealed that the maternal parent strongly darianii: a number of specimens of this species were success-
contributes to sex ratios, the exact genetic mechanism involved fully grown to maturity on the island of Hawaii, but as yet,
remaining as yet unresolved (Glawe and de Jong, 2007, 2009). after several years of flowering, only male inflorescence pro-
Although relatively few data are available for the palm family, duction has been observed (Marcus, 2010). Although environ-
sexual expression has been shown to be influenced by environ- mental factors may play a causal role in cases such as this, it
mental factors not only in oil palm but also in two different can also be speculated that endogenous factors within the
species of the monoecious Arecoid genus Attalea. In plant that change during its life-cycle progression (e.g.
A. funifera, a study was carried out in Brazil by Voeks (1988) hormone composition), or indeed a combination of the two
on the relative abundance of the three different inflorescence elements, may be involved.
types produced: male with staminate flowers, bisexual with a
few pistillate and many staminate flowers, and female with
M O L E C U L A R D E T E R M I N A N T S O F F LOW E R
pistillate and sterile staminate flowers. Although bagging exper-
A N D IN F LO R E S C E NCE S E X: CA N W E L E A R N
iments had revealed that autogamy was possible in the bisexual
F RO M OT H E R S P E C I E S ?
inflorescences, the latter contribute only very weakly to fruit-set,
given their low abundance at the population level (5 % compared Dioecy and monoecy appear to have arisen on a large number
with 80 % male and 15 % female inflorescences). The data of occasions during the evolution of flowering plants, as
obtained in this study suggested that sexual expression in witnessed by their wide and fragmented distribution within
A. funifera is related to energetic factors, with palms apparently the Angiosperm tree of life. This suggests that the genetic
led to the abolition of pistil abortion and the appearance of the source – sink imbalances, but glucose was not (Legros et al.,
tasselseed phenotype. 2009c). Interestingly, however, glucose levels were found to
As regards the question of sex determination in oil palm, the decrease progressively in response to fruit pruning over the
lack of a widely conserved pathway for this key developmental 22-month period of study (Legros et al., 2009b).
process amongst flowering plants suggests that at best only As regards the possible involvement of hormones in oil palm
part of the knowledge gained in model plants can be transposed sex determination, some indications were obtained by using the
directly to the Arecaceae. In terms of phylogenetic relationships, experimental strategy of applying growth regulators to young
the Poaceae are clearly the closest family for which in-depth palms grown in large polythene bags (Corley, 1976b). In the
knowledge has been obtained, through studies on maize. The latter study, the auxin NAA (a-naphthyleneacetic acid) was
latter species is therefore a useful starting point from which to found to promote female inflorescence production; however,
initiate searches for palm orthologues of key genes previously this effect was not observed until 24 months after the end of treat-
shown to be involved in sex differentiation, notably those ident- ment, whereas sex differentiation was expected to take place
ified via the tasselseed mutants. The increasing body of genomic 16– 22 months before anthesis. For this reason, the feminizing
sequence data now becoming available for palms, including the effect was assumed to be indirect. In the case of ethephon, the
date palm draft sequence (Al-Dous et al., 2011), will prove very predominant effect was to delay flowering, albeit with a statisti-
useful in this connection. cally insignificant lowering of the sex ratio. Treatment with gib-
berellic acid, however, was shown to significantly increase the
production of male inflorescences and reduce production of
TOWA RDS A M OD E L TO E XP L A IN SE X
female inflorescences within the expected time frame; gibberel-
DE T E R M I NAT IO N IN OI L PA L M
lins are thus likely to play a role in the oil palm sex determination
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is amply demonstrated by the complexity of phenological gibberellic acid treatment has also been observed in cucumber
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