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Received: 16 February 2011 Returned for revision: 9 March 2011 Accepted: 7 April 2011 Published electronically: 28 June 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
and discusses possible insights that can be gained from other species. Although some informative phenological
studies have been carried out, nothing is as yet known about the genetic basis of sex determination in oil palm,
nor the mechanisms by which this process is regulated. Nevertheless new genomics-based techniques, when com-
bined with field studies and biochemical and molecular cytological-based approaches, should provide a new
understanding of the complex processes governing oil palm sex determination in the foreseeable future.
Current hypotheses and strategies for future research are discussed.
Key words: Sex determination, oil palm, Elaeis guineensis, inflorescence, monoecious, temporal dioecy,
flowering.
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1530 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.
palm inflorescences was studied by scanning electron In tropical humid climates with regular rainfall, inflores-
microscopy (SEM) by Van Heel et al. (1987) and in our cence and fruit production is spread evenly throughout the
group using SEM and light microscopy on stained tissue sec- year. From an experimental point of view, this allows the
tions (Adam et al., 2005). The earliest clear anatomical differ- possibility of dissecting mature palms so as to visualize a com-
ence between the two sexes is the greater number of ‘early plete series of inflorescence developmental stages within the
bracts’ arising at the base of ‘spikelet primordia’ in the male same individual. As a means of cross-referencing between
inflorescence compared with its female equivalent (Van Heel palms, inflorescences are usually numbered according to
et al., 1987). This reflects the larger number of flowers their subtending leaves. Thus, the youngest expanding leaf
borne on the male rachilla and confirms the earlier conclusions with separating leaflets (and its associated inflorescence) is
of Corley (1976a). A later key difference between the male and designated as +1, the immediately older leaves being +2,
female inflorescences concerns the arrangement of flowers on +3, etc., and younger leaves 0, – 1, etc. A summary of the
the rachillae, the staminate flowers being borne singly whereas key stages of inflorescence development in relation to leaf
pistillate flowers are flanked by a pair of abortive accompany- number is shown in Fig. 2.
ing staminate flowers. The female inflorescence thus produces
floral triads, a structural arrangement that is dominant I NS I G HT S I NTO T H E CH RO N OLO GY O F S E X
(although not universal) in the subfamily Arecoideae. The D E T E R M I N AT I O N F RO M F I E L D
OBS E RVAT I ON S
Typically, a mature palm will alternate between male and
A B female inflorescence production during its lifetime; however,
the proportion of time spent in each phase will vary consider-
ably depending on both environmental and genetic factors.
The sex ratio is normally defined as the ratio of female to
total inflorescences in a given group of palms. In regions
with high and regular rainfall (e.g. Malaysia and Indonesia),
oil palm sex ratios tend to vary little throughout the year, in
contrast to areas experiencing a marked dry season such as
in West Africa, where the sex ratio undergoes extensive fluctu-
ations. Corley (1976a) noted that in the latter case, the period
of lowest sex ratio (high male inflorescence production) occurs
during the rainy season and speculated that this character is an
adaptation against the reduction in airborne pollen density
caused by high atmospheric humidity. This illustrates the well-
established observation that oil palm sex determination is
strongly influenced by climatic factors, with male inflores-
cence production being promoted by water deficit.
F I G . 1. Macroscopic views of oil palm inflorescences: (A) mature female Male inflorescence production can also be induced artifi-
inflorescence, (B) mature male inflorescence. Scale bars ¼ 10 cm. cially by defoliating adult plants, a technique which has
Adam et al. — Environmental regulation of sex determination in oil palm 1531
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 +2
Initiation of floral bracts
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
1532 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
producing only male inflorescences in the crowded understorey changes that resulted in the monoecious and dioecious habits
whereas female expression was observed when they had grown are different for the most part in different evolutionary
and entered the energy-rich canopy. Reproductive cost measure- lineages (Ainsworth, 2000). Nevertheless, thanks to compara-
ments (estimated via dry weights of inflorescence and infructes- tive genomics and evo-devo approaches, it is clear that a wide
cence components) revealed the higher energetic demands of range of signalling elements that regulate reproductive devel-
mature female flowers and fruit compared with male flowers opment are conserved throughout flowering plants. An early
(1.6 and 13.2 versus 1.0 in relative units, respectively), with indication of this conservation was obtained by comparing
the production of an ‘initial female inflorescence’ requiring an the first two Angiosperms to have their genomes sequenced,
energy input estimated as over 10 times the annual budget of Arabidopsis thaliana and rice (Izawa et al., 2003). The latter
the youngest mature palms. A second species of Attalea, authors carried out a survey of the structural and functional
A. speciosa, was also studied in terms of its gender plasticity conservation of genes between the two model plants, using
(Barot et al., 2005). In this case, the onset of reproduction and flowering pathways as an example. This study revealed that a
sex allocation were compared in three contrasting environments: wide range of flowering-related genes are structurally con-
forest, partially invaded pasture and a pure stand (babassual). served between monocots and eudicots. Nevertheless, func-
Reproduction was found to start at a smaller size in the pasture tional divergence appears to have frequently occurred to give
and pure stand compared with forest. Male flowering started at novel regulatory mechanisms which distinguish the two
a lower height than female flowering in the pasture and pure model species, this degree of divergence providing a glimpse
stand; however, this was not the case in the forest environment. of the situation in flowering plants as a whole. As regards
Although several hypotheses were raised to explain these data, it sex determination, although it seems likely that a generalized
seems probable that the earlier flowering observed in more open signalling cascade for flower development has been partially
environments was made possible by the much greater light (and maintained during evolution, the genetic basis of sexual
therefore energy resources) available to palms in these habitats. dimorphism per se is likely to vary considerably. From a
As regards the earlier male flowering in pasture/babassual, it was developmental point of view, this hypothesis is supported by
postulated that the lower levels of stored energy in younger the great variety of ways in which unisexual flower develop-
palms (compared with larger mature palms in the forest) might ment is achieved. Examples of the latter, provided by the
be stretched beyond viability by the higher demands of female palm family, include non-initiation of the undesired organ
flowering and fruiting. Thus, the delayed female flowering of (e.g. the pistil of staminate flowers in certain Phytelephas
mature pasture/babassual palms might be considered as an adap- species), early developmental arrest of the undesired organ
tation conferring more efficient energy use and therefore (e.g. the androecium of pistillate flowers in Elaeis guineensis)
survival. or incomplete development of the gametophyte (e.g. the
At a more general level, although there is some scope for the androecium of pistillate flowers in Rhapidophyllum hystrix)
optimization of resource allocation to male and female repro- (Uhl and Moore, 1977; Adam et al., 2005; Dransfield et al.,
duction in hermaphrodite species by the modulation of pollen 2008). As discussed by Weiblen et al. (2000), dioecy and
and ovule development, the greatest flexibility is probably monoecy have probably arisen independently a number of
afforded by the monoecious and polygamous conditions, times since the palm family first originated; for this reason,
which allow the adjustment of the relative numbers of special- the Arecaceae provide an interesting microcosm for studying
ized male and female flowers both within the same plant and the evolution of sexual dimorphism in flowering plants as a
between individuals. Within the palm family it seems likely whole.
1534 Adam et al. — Environmental regulation of sex determination in oil palm
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
The fact that oil palm sex determination is a complex process process. It is interesting to note that a masculinizing effect of
is amply demonstrated by the complexity of phenological gibberellic acid treatment has also been observed in cucumber
information obtained from plants growing in the field. (Fuchs et al., 1977), whereas in maize, a feminizing effect is
Although the currently available data do not allow a precise observed with this type of treatment (Dellaporta and
model to be formulated to explain how oil palm sex determi- Calderon-Urrea, 1994). These opposing effects observed in
nation is regulated, we can nevertheless identify various different species no doubt reflect the diversity of sex-
factors of importance and propose a possible framework for determining mechanisms that have evolved in flowering
their interactions. At least four different types of factor can plants, even if some regulatory modules appear to be structurally
be identified that might participate in sex determination and conserved. Given the relatively distant phylogenetic relation-
differentiation: abiotic factors (e.g. water stress), metabolic ships between the Arecaceae and the various species for which
factors (e.g. carbon reserves), hormone status and genetic
factors. The masculinizing effects of drought conditions are
already well known; however, the physiological and genetic
Photosynthesis
bases of this induced developmental change remain to be elu-
cidated. In one of the earliest publications to mention the
subject of gender plasticity in oil palm, Beirnaert (1935) pos-
tulated that the ratio of carbon assimilation to nitrogen absorp-
tion was the key factor determining the sex ratio. This
hypothesis can be reconciled with the observed effects of Water
drought if the lowering of photosynthesis in conditions of availability
water stress is taken into account. Other factors affecting the Glucose Starch
metabolic status of palms, including the effects of high-density
planting, fruit pruning and the defoliation of neighbouring
palms, are all compatible with the notion that higher sex
ratios are associated with higher levels of carbon assimilates
(Sparnaaij, 1960). Compared with flowering plants as a
whole, oil palm exhibits relatively low phenotypic plasticity
in terms of its overall architecture; transitory carbon reserves Hormone status
therefore provide a more flexible means by which to buffer
source –sink imbalances associated with climate variability Genetic factors
in this species (Legros et al., 2009c). The latter authors per-
formed a comparative study between oil palms at two different
sites in Indonesia with or without a dry season; data were also Female
obtained on the effects of fruit pruning and photoperiod vari- inflorescence
ation (Legros et al., 2009a, b). One of the main elements Indeterminate
revealed by this work was that source – sink imbalances in inflorescence
Male
oil palm were buffered principally by fluctuations in non- inflorescence
structural carbohydrates in the stem, which consisted mostly
of glucose and starch. Of these two components, starch was F I G . 4. Possible modes of interaction of factors affecting inflorescence sex in
identified as a major physiological buffer of seasonal oil palm.
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