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Pollination in conifers John N. Owens, Tokushiro Takaso

and C. John Runions
Our understanding of pollination in conifers has advanced rapidly in recent years, but it still lags
behind our knowledge of this process in angiosperms. In part this is because conifers are not
considered to be high priority crops and, unlike many cultivated flowers, conifer seed cones are
generally neither large nor colorful. The use of genetics to improve tree growth has primarily been
through selection and asexual propagation rather than breeding, and because incompatibility is
not thought to occur in conifer pollination systems, concern about pollination has primarily been
with regard to seed production. Here we examine the ancestral wind-pollination mechanism
in conifers and discuss how the process may have evolved to improve pollination success.

he seeds of gymnosperms are naked, meaning that they

are not completely enclosed within another structure, but
are borne at the tip of a shoot, or on the surface of a bract or
scale. The seeds often appear enclosed because in conifers (such
as pine) they are contained in a seed cone. Unlike angiosperms,
most of which are insect pollinated (entomophily), the majority of
gymnosperms are wind pollinated (anemophily).
Conifers are a small group of gymnosperms that dominate
north temperate forests. All are wind pollinated, but an array of
mechanisms have evolved to increase pollination success. For
example, the integument tip of the ovule
may be modified for pollen collection; pollination drops secreted from the ovule may
aid in scavenging pollen; pollen may have
wings (sacci); and seed cones at receptivity may have shapes and orientations that
direct pollen to the receptive surfaces.

Pinaceae; and Cephalotaxaceae. Some taxonomists combine the

Cupressaceae and Taxodiaceae or place the Taxaceae in a separate
order. There are approximately 550 conifer species in 53 genera2.
Most are north temperate, such as the Pinaceae, but others are
tropical or found primarily in the southern hemisphere, such as the
Podocarpaceae and Araucariaceae.
One might expect an essential feature like pollination to show
little diversity in such a small taxon. However, conifers are a very
ancient group and there have been repeated climatic changes that
probably restricted and isolated species for long periods of time3.

Conifer origin and reproductive diversity

Conifers evolved from the progymnosperms

in the Late Devonian and were at their most
diverse and abundant during the Mesozoic
Era1. Early pollen cones (microsporangiate
strobili) were simple structures consisting
of an axis with modified leaves (microsporophylls) that bore microsporangia. Seed
cones (megasporangiate strobili or megastrobili) were compound, consisting of an
axis bearing modified leaves (bracts) in the
axil of which developed a shoot that bore
one to many erect ovules. The ovules, after
pollination and fertilization, formed seeds.
The axillary fertile shoots varied in different taxa. Early forms such as the Voltziales
had radially symmetrical fertile shoots bearing several scales and erect ovules. Subsequent taxa showed a flattening of the fertile
shoot, fusion of the scales, shortening of
the ovule and cone axes and inversion of
the ovules. The fossil record is fairly complete but there is disagreement about affinities among taxa. Most modern families
are recognizable by the Late Triassic, and
familiar genera such as Pinus date from
approximately 130 million years ago.
Modern conifers are commonly placed
in seven families listed here according to
their time of origin from the earliest to
most recent: Podocarpaceae; Araucariaceae;
Cupressaceae; Taxodiaceae; Taxaceae;

Fig. 1. Scanning electron micrographs of conifer pollen. (a) Chamaecyparis pollen with
orbicules (arrow) on the surface and indentations due to natural dehydration. (b) Pinus
pollen showing body (arrow) and two sacci (wings). (c) Pseudotsuga pollen with indentation
due to natural drying. (ac) Scale bar 5 10 mm. (d) Tsuga heterophylla pollen showing
sculptured surface and spines (arrow). Indentation due to natural drying. Scale bar 5 20 mm.

1360 - 1385/98/$ see front matter 1998 Elsevier Science. All rights reserved. PII: S1360-1385(98)01337-5

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This has led to diversity in certain traits,
such as pollen, megastrobili and pollination
mechanisms, not only among genera within
a family, but occasionally between species
within a genus.
Megastrobilus and pollen morphology

Fig. 2. Light micrographs of three types of seed cones (megastrobili) representing three
pollination mechanisms. (a) Juniperus with fused bract-scales (Bs), one central ovule and a
pollination drop (arrow). Scale bar 5 1 mm. (b) Picea with broad flat scales (S) and separate, small pointed bracts (B, arrow). Scale bar 5 5 mm. (c) Tsuga with broad flat scales (S)
and broad serrate bracts (B) covered with pollen (arrow). Scale bar 5 1 mm.

Cupressaceae,
Taxodiaceae, Taxaceae,
Cephalotaxaceae and
some Podocarpaceae

Some Pinaceae
(Pinus, Picea,
Cedrus and some Tsuga),
Podocarpaceae

Some Pinaceae
(Abies)

Megastrobilus orientation and morphology

are important features for wind pollination.
In a series of classic experiments, Niklas4,5
studied the aerodynamics of pollen-grain
deposition based on models of fossil seed
plants and living megastrobili of conifers
and cycads (non-coniferous gymnosperms).
In most conifer megastrobili at pollination
there are a complex system of air eddies
generated by the cones geometry and that
of the individual bract and scale complexes6. The megastrobilus channels pollen
around the cone, and pollen settles on to
bracts or scales or passes down around the
cone axis. Minute surface features may
affect where the pollen comes to rest.
The morphology of the pollen plays an
important part in the pollination mechanism. Conifer pollen varies in diameter from
approximately 20 mm to more than 100 mm,
and has a low water content, usually 510%.
The grains may be smooth or sculptured,
bear minute orbicules and be saccate or nonsaccate (Fig. 1)7. Although conifer pollen
is generally larger than pollen from most
angiosperm species, it is light for its size
and can be carried long distances. Maximum dispersal distances in the Pinaceae are
3001300 km in strong air currents8. The airfilled sacci present in about 50% of conifer
species reduce the density of the pollen,
but their primary function is flotation.

Some Pinaceae
(Pseudotsuga, Larix)

Some Pinaceae
(some Tsuga) and
Araucariaceae

Fig. 3. Three traits are correlated in conifer pollination mechanisms: ovule orientation at the time of pollination (upright, variable or inverted);
pollination drop exuded from the micropyle (present or absent); and, pollen buoyant or sinking (saccate or non-saccate). (a) Non-saccate pollen
sink into the pollination drop which is exuded from upright or variably oriented ovules. (b) Pollen with sacci float upwards into the pollination
drop exuded from inverted ovules. (c) The pollination drop is absent or not exuded from the micropyle in some genera of Pinaceae and pollen
float into the ovule in rainwater. (d) Pollen have lost the ability to float and are taken into the inverted ovule by engulfment. (e) Pollen grains
germinate extra-ovularly and pollen tubes grow into the ovule.

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Megastrobilus and pollen morphology
and pollination mechanisms are, of course,
linked, often in intriguing ways. Here we
discuss five pollination mechanisms, some
of which show considerable variation. Similar mechanisms have evolved independently
in unrelated taxa.
Pollination mechanisms
Pollination drop, non-saccate pollen and
ovules without preferred orientation

The least specialized pollination mechanism

is found in four of the seven conifer families: Cupressaceae, Taxodiaceae, Cephalotaxaceae and Taxaceae. All four families
have small, non-saccate pollen (Fig. 1).
The first three families have megastrobili,
whereas Taxaceae have separate ovules
that are commonly erect at pollination or
without preferred orientation (variable),
but not pendant. Megastrobili have fused
bract-scale complexes (Fig. 2) and the
ovules are flask shaped, variable in number
and attached in the axil of the bract-scale.
Ovules lie at an angle to the axis and may
adopt a vertical or horizontal orientation
depending on cone orientation. The integument tip has a narrow neck and a small,
unspecialized micropyle.
A pollination drop has been observed in
many species in these families (Fig. 3)9.
Fig. 4. Scanning electron micrographs of portions of fresh megastrobili at pollination.
Light and scanning electron microscopy
(a) Chamaecyparis showing all ovules, some with pollination drops (Pd) exuded from the
have been used for these studies (Fig. 4),
micropyle (arrow) of the ovule. Scale bar 5 200 mm. (b) Chamaecyparis integument tip
but the destructive sampling required has
showing pollination drop after pollen has entered the drop leaving marks on the surface
made it difficult to determine the sequence
(arrow). Scale bar 5 35 mm. (c) Pinus integument tip showing the micropyle (M) and
micropylar arms (Ma) that secrete microdroplets (arrow) to which pollen (P) adheres. Scale
of pollination drop emergence and recession.
bar 5 20 mm. (d) Picea integument tip with a large pollination drop emerging from the
Time-lapse cinematography of Chamaemicropyle and filling the space between the micropylar arms. Scale bar 5 20 mm.
cyparis nootkatensis trees revealed one example of the sequence10. Megastrobili open
and ovules become fully exposed for about
2 days; then in the early morning a pollination drop is exuded The action of water droplets in scavenging pollen and transferfrom the micropyle of some ovules (Fig. 4). If no pollen is ap- ing it to the ovules suggests that an internally produced pollination
plied, the drops remain until mid-day and then slowly recede into drop was not essential in early conifers in the warm and humid
the micropyle. If pollen is dusted onto the receptive cone the drops habitats that existed during much of their early evolution3.
recede within 20 min. Pollen dusted onto the cone enters the drops
We presume that this simple pollination mechanism existed in
immediately, signalling an end to active secretion and allowing the Mesozoic conifers, and is the ancestral mechanism from which
rapid evaporation (Fig. 4). There is no evidence of active reab- other forms evolved. A prerequisite for this process appears to be
sorption of the drops by ovular tissue. If cones are not pollinated the existence of non-saccate pollen that would sink into the pollithe drops repeatedly emerge then recede each day for several nation or water drops. The driving force for evolutionary change
days, then the bract scales thicken and cover the ovules sealing the may have been the occurrence of dry periods and subsequent
cone. Pollinated ovules no longer secrete drops. In field-grown lower pollen to ovule ratios that would favor large pollination
Thuja plicata, unpollinated cones enclosed in isolation bags con- drops and more efficient mechanisms for scavenging pollen from
tinued to secrete drops diurnally for 1520 days, until the cones cone surfaces.
were completely closed, whereas naturally pollinated cones secrete
drops for only 45 days11. Anatomical studies in Chamaecyparis Pollination drops, saccate pollen and inverted ovules
and Thuja show that the drop is secreted from the nucellar tip. Sur- A mechanism that combines pollination drops, saccate pollen and
face cells become vacuolate, release the clear vacuolar contents inverted ovules is found in the Pinaceae and Podocarpaceae (Fig. 3).
and then collapse, creating a cavity, the pollen chamber, in the In some Mesozoic conifers, ovules became inverted, the ovule stalk
nucellar tip. After pollen is taken in, cells lining the micropylar shortened bringing the inverted ovule close to the megastrobilus
canal enlarge to form a collar that seals the ovule.
axis, and ovules fused with the ovuliferous scale1. With few excepWater in the form of rain or dew may assist in pollination. In tions, megastrobili in the Pinaceae are upright at pollination (Fig. 2).
Thuja, an epicuticular wax layer on the bract scale causes water to The two ovules per ovuliferous scale are inverted, and fused to the
bead; beads roll down the surface, picking up pollen, and then con- adaxial surface of the scale close to the axis. Receptive megastrobili
tact the ovules where the water fuses with the pollination drops11. of most Pinaceae are shaped so that they channel pollen towards
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Fig. 5. (a) Megastrobili of Picea glauca are erect at pollination

and ovules are inverted. Saccate pollen floats up into the pollination drop and into the micropyle. (b) Picea orientalis megastrobili are pendant at pollination and ovules are nearly erect. The
pollen is saccate but porous and it floats only briefly before sinking into the pollination drop and into the micropyle. Adapted, with
permission, from Ref. 15.

the cone axis and micropyles5. In many genera, as ovules develop

the integument tip elongates and forms two prongs (micropylar
arms), between which is a small micropyle. The micropyle faces
downwards (Figs 3 and 4) so pollen cannot simply fall in12.
This pollination mechanism is best described in Picea1214. Megastrobili become erect and burst from their bud scales, the bracts and
scales reflex and become receptive for pollination. Megastrobili
appear receptive (Fig. 2) for 2 weeks, but take in pollen for approximately only 1 week. At receptivity the epidermal cells of the
micropylar arms secrete microdroplets to which pollen adheres
(Fig. 4). Pollen also comes to rest on other cone surfaces, most of
which are covered with minute hairs or wax rodlets such that any
water entering the megastrobilus beads on these surfaces. Rainwater can move down the surfaces carrying pollen towards the
micropyle. A large pollination drop is then exuded from the micropyle, filling the space between the arms (Figs 3 and 4), often contacting the cone axis or adjacent scales. The saccate pollen (similar
to that in Fig. 1b) enters the pollination drop and floats up into the
micropyle to the surface of the nucellus (Fig. 5). The arms then
wither and the scales thicken, closing the megastrobilus which
then becomes pendant. Experiments using pipettes filled with sugar
solutions to simulate pollination drops have shown that saccate
pollen is scavenged from surfaces and floats upwards, whereas
non-saccate pollen remains on the surface12,14. This demonstrates
that the sacci function as flotation devices for inverted ovules.
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The function of sacci in flotation was recently demonstrated in a

species of spruce (Picea orientalis) in which megastrobili are pendant at pollination; thus the ovules are upright, in contrast to other
spruces (Fig. 5). In this species, the pollen is saccate, but does not
float up into a simulated pollination drop; instead it sinks into the
drop on an erect ovule. Upon close examination using confocal
and transmission electron microscopy, it was found that the sacci,
although normal in appearance, are more porous than sacci on
pollen from other spruce species. Upon wetting, swelling of the
pollen body displaces the air within the sacci and the pollen functions as non-saccate pollen15. Most species of Picea freely hybridize, but oriental spruce does not. One reason for this is now clear
saccate pollen of other spruces would not sink into the erect
ovules of oriental spruce, and the functionally non-saccate oriental spruce pollen would not float up into the pollination drop of
inverted ovules (Fig. 5). Saccate pollen and inverted ovules in the
Pinaceae are considered to be the ancestral form from which the
upright ovules of oriental spruce have evolved. Oriental spruce is
native to the Caucasus Mountains and has been isolated from
other spruces. This isolation has allowed evolutionary change in
both the pollination mechanism and in vegetative characters. In
this species, as in many other conifers, the key innovation16 necessary for the origin of the new taxon seems to be a change in the
pollination mechanism.
Most members of the Podocarpaceae studied to date have a pollination mechanism similar in function, but not structure, to Pinaceae17. In the Podocarpaceae, all megastrobili morphologies are
based on a consistent unit, involving a uniovulate complex in the
axil of a fertile bract. The ovule is inverted in all but two genera.
Cone position is closely correlated with leaf type in most Podocarpaceae: terminal cones are associated with scale-like leaves,
and lateral cones with bifacially-flattened, linear leaves. Highly
derived genera within the Podocarpaceae have a reduced number
of ovules per megastrobilus, and fusion of ovulate structures, such
as the integument and epimatium, occurs. There is some debate
over whether the epimatium is homologous to the ovuliferous
scale, or a sterile part of the seed-scale complex. Most genera associate a fleshy structure (axil, epimatium or peduncle) with the
mature ovule. There are usually two inverted ovules per unit, each
producing a pollination drop, and pollen is saccate. Where ovules
are erect, the ovule axis bends downward soon after pollination so
that the micropyle faces downward18. In members of the Podocarpaceae with inverted ovules, the pollination drop extends beyond
the micropyle and makes contact with megastrobilus surfaces in a
variety of configurations depending on the shape of the wettable
cone surface. Saccate pollen is scavenged from these surfaces by
the pollination drop, and the floating pollen then passes into the
micropyle towards the nucellus17,19.
No pollination drops, saccate pollen and inverted ovules

There are several reports of rainwater supplementing the pollination

drop in the Pinaceae14,20, the Cupressaceae11 and the Podocarpaceae18. Current studies indicate that Abies species (Pinaceae)
lack a pollination drop, but they have saccate, buoyant pollen (L.
Chandler, pers. commun.): they represent an interesting evolutionary step in which rainwater appears to serve the function of a
pollination drop. The integument tip forms a short funnel, often
with fluted edges, around a large micropyle21. Microdrops form on
the inner surface of the funnel and the saccate pollen adheres to
this surface. In Abies amabilis the wettable internal surfaces of the
cone are directly below the funnel-shaped tip of the inverted
ovule. Rainwater forms beads on many surfaces and moves down
towards the axis near the wettable surfaces. Here the water accumulates to form a large drop or column joining the funnel and the

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subjacent scale (Fig. 3). Buoyant pollen
floats into the micropyle in the accumulated drop. In this mechanism the integument tip has been simplified and the
pollination drop appears to have been lost,
with rainwater taking over its function.
Remnants of a pollination drop may be secreted from the nucellar apex to stimulate
pollen germination.
Engulfment of non-saccate pollen and
reduction of the pollination drop

In Pseudotsuga and Larix (Pinaceae) the

ovule is inverted and the integument tip
forms two unequal lobes; the adaxial lobe
is larger and both lobes develop unicellular
papillae. The micropyle is a narrow slit
between the two lobes and no pollination
drop is exuded from the micropyle (Fig. 3).
The structure is called a stigmatic area17, or
tip22. The cones are upright at pollination
and pollen passes down the smooth, adaxial surface of the bract and is funneled to
the stigmatic tip, where they become entangled in or adhere to the papillae (Fig. 6).
The cones are open and collect pollen for
several days, then the cells on the outer surface of the stigmatic tip elongate and cells
around the micropyle collapse. As a result
the papillae and attached pollen are drawn
Fig. 6. Scanning electron micrographs of portions of megastrobili at pollination. (a) Pseudointo the micropyle, in much the same way
tsuga stigmatic tip at receptivity showing the two lobes with unicellular papillae and slit-like
as a sea anemone engulfs its prey (Fig. 6).
micropyle between (arrow). Pollen (P) has begun to adhere to papillae on the abaxial lobe.
Once pollen is within the micropylar
22
Scale bar 5 75 mm. (b) Pseudotsuga stigmatic tip after engulfment of the pollen. Some
canal the processes in Pseudotsuga and
pollen (arrow) has been left outside the micropyle. Scale bar 5 100 mm. (c) Tsuga heteroLarix23 differ. In Pseudotsuga, pollen may
phylla bract surface (right) with cobweb-like epicuticular wax threads to which spines of
remain entangled in the papillae just inside
pollen attach (arrow). Scale bar 5 10 mm. (d) Ovule tip of Agathis showing large U-shaped
the sealed micropyle or be released into the
micropyle (arrow) with tongue-like nucellus (N) protruding with a distal nucellar flap (Nf) to
micropylar canal. Within a day the pollen
which pollen attaches. Scale bar 5 100 mm.
hydrates and the exine bursts. Then over
several weeks, the intine elongates several
hundred micrometres down the micropylar
canal and makes contact with the nucellar apex where a narrow pollen tube enters the large, open micropyle and penetrates the nupollen tube forms and penetrates the nucellus. Recently, secretions cellus25. In early studies of Agathis australis, the mechanism aphave been shown to arise from the inner wall of the integument, peared to be similar to that of Araucaria26; it differed in that the
the nucellar apex and the megagametophyte. These secretions pollen tubes appeared to grow under the bract-scale surface and
may stimulate pollen elongation and tube formation24. In Larix, permeate cortical and vascular tissues until they reached the ovule
engulfed pollen hydrates and sheds its exine within days, but does where they emerged to enter the micropyle. A recent study of
not elongate. Instead, it remains at the distal end of the micropylar A. australis from the same location in New Zealand has not borne
canal for 56 weeks; then a fluid secretion fills the micropylar this out27. This later study indicates that the non-saccate pollen
canal and the pollen is carried to the nucellar apex, where a pollen comes to rest near the cone axis, the ovule tip elongates and presses
tube forms and penetrates the nucellus23.
the exposed nucellus apex (Fig. 6) against the cone axis. Pollen
pressed between the nucellus and cone axis germinates and then
Extra-ovular pollen germination, non-saccate pollen and no
branches before penetrating the nucellus. Another study of tropical
pollination drop
A. borneensis indicates that pollen tubes penetrate the ovule in many
In three quite unrelated taxa all of the Araucariaceae, most locations and not just through the exposed nucellus. In Saxegothaea
Tsuga species within the Pinaceae, and Saxegothaea in the Podo- the nucellus is extruded through the micropyle28, as observed in
carpaceae the loss of the pollination drop coupled with extreme A. australis.
siphonogamy, has evolved in a parallel fashion. Pollen lands on a
In Tsuga (Pinaceae) there are two pollination mechanisms. The
surface of the megastrobilus (integument bract, scale or axis) where genus is divided into two sections, Micropeuce, which contains at
it germinates and, usually after some delay, the long pollen tube least ten extant species and Hesperopeuce, which contains one or
grows into the ovule (Fig. 3). In Araucaria, pollen has been reported two remnant extant species and many recently extinct species.
to land and germinate on the fused bract-scale, penetrate the epi- Pollination in T. heterophylla has been studied extensively29, and
dermis, and grow under the surface before emerging and proceeding is considered to be typical of the Micropeuce. The mechanism shows
to the single proximal adaxial ovule. Upon reaching the ovule the remarkable co-evolution of megastrobilate and pollen structures.
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Pollen is non-saccate, although rudimentary sacci are present as
frills on the exine. The pollen is unique for conifers in that it is
covered with short spines (Fig. 1). At pollination, the bract is exposed beyond the scale (Fig. 2) and its exposed abaxial surface is
covered by a web-like epicuticular wax. This allows pollen to adhere to the bract surface (Fig. 6), but few enter the megastrobilus
or adhere to the scale. The bracts collect pollen for 12 weeks,
then the scales overgrow the bracts and encase the pollen. The
pollen remains in this position for about 6 weeks while the megastrobilate cone enlarges considerably. The pollen then germinates
and each grain forms a long pollen tube that grows over the bract
surface towards the ovules on a subjacent scale. The ovules have
a simple, funnel-shaped integument tip, large micropyle and short
micropylar canal. Several pollen tubes may grow into each micropyle and penetrate the nucellus. It is not known what attracts
pollen tubes to the nucellus, here or in the Araucariaceae. The pollination mechanism of T. heterophylla is the most efficient known in
conifers and ensures a high rate of pollination success and seed set29.
The Hesperopeuce, represented by T. mertensiana, have saccate pollen and a pollination mechanism that is more similar to
Picea12 or Cedrus20 than other hemlocks. The integument tip has
two flaps on which pollen lands. Secretion of a pollination drop is
suspected, but has not been convincingly recorded because the
species grows at high altitudes and fresh specimens are difficult to
obtain. The integument flaps appear to fold over to trap the pollen.
Upon germination, the pollen tube has only a short distance to
grow to reach the nucellus30. Two such different pollination mechanisms in one genus is unique within the conifers, and may be the
result of prolonged isolation over time. It also suggests that the
loss of the ancestral pollination drop may have occurred several
times in unrelated taxa.
The nature of the pollination drop

The pollination drop, which in different taxa may be prominent,

reduced or absent, was first observed in the mid-1800s. Chemical
analysis has shown it to be a weak sugar solution, consisting of
sucrose, glucose and fructose at a total concentration of between
110% (Refs 31,32) or glucose and fructose at a total concentration of about 8% (Ref. 12). The solution also contains various
amino acids, peptides and organic acids32,33. Early studies did not
consider secretion of the pollination drop to be an active secretory
process31,32 and it was likened to gluttation in Pinus31. More recent
studies have shown it to be an active secretory process12,23, similar
to nectar production in angiosperms. However, the volume of the
pollination drop is too great to be produced by the nucellar tip
alone; suggested secretory sources include other tissues such as
the megagametophyte and integument. In addition, a small pollination drop may be augmented by rainwater or dew.
Conclusions

The conifers are a small group of primitive seed plants that appear
at first glance to be conservative in their morphological and reproductive traits. However, close inspection reveals five major types
of pollination mechanism that vary in structure and function (Fig.
3) while achieving the same result the capture of airborne pollen
and its transport into the megastrobilus or ovule. The most primitive
and widespread of these mechanisms makes use of a pollination
drop. Here, there has been co-evolution of pollen and ovules nonsaccate pollen occurs in species that have erect ovules, whereas
saccate pollen occurs in species with inverted ovules. Reduction
in size or loss of the pollination drop has been accompanied by
adaptive changes in the integument tip that allow it to engulf pollen; such adaptations include making use of rainwater or allowing
pollen tubes to grow into the ovule. Subtle changes in the pollination
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mechanism lead to reproductive isolation and resulting divergence

in other traits. The changes seen among the conifers probably arose
as a result of the frequent isolation of genera or species brought
about by geoclimatic changes, especially in north temperate regions
over millions of years a conclusion supported by the abundance
of endemic and monotypic conifer genera and species.
Few conifer pollination mechanisms include incompatibility
mechanisms as seen in angiosperms. Pollen discrimination may
be limited to saccate or non-saccate traits and the resulting ability
to float or sink in pollination drops, or to restrictions imposed by
pollen size or wall morphology. The incompatibility mechanisms
that exist are late acting and occur within the ovule. Such late-acting
incompatibility mechanisms are also common in woody perennial
angiosperms some are late prezygotic, others postzygotic. The
classical view that conifers have only postzygotic incompatibility
mechanisms (inviability), may have to be rethought. Recent research has demonstrated that primitive prezygotic incompatibility
mechanisms exist in conifers34. Future experiments and molecular
studies on these different pollination mechanisms may reveal the
full nature of incompatibility in conifers.
Acknowledgements

We thank the research assistants and graduate students who over

many years have contributed to our understanding of pollination
in conifer species. These include Marje Molder, Anna Colangeli,
Margaret Blake, Vivienne Wilson, Erika Anderson, Tajudin Komar
and Luke Chandler. Most of the research has been supported by
a Natural Sciences and Engineering Research Council of Canada
grant (A1982) to J.N. Owens.
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8 Potter, L.D. and Rowley, J. (1960) Pollen rain and vegetation, San Augustin
Plains, New Mexico, Bot. Gaz. 112, 125
9 Takaso, T. (1990) Pollination drop time at the Arnold Arboretum, Arnoldia
50, 27
10 Owens, J.N., Simpson, S. and Molder, M. (1980) The pollination mechanism
in yellow cypress (Chamaecyparis nootkatensis), Can. J. For. Res. 10,
564572
11 Colangeli, A.M. and Owens, J.N. (1990) The relationship between time of
pollination, pollination efficiency and cone size in western redcedar (Thuja
plicata), Can. J. For. Res. 69, 439443
12 Owens, J.N., Simpson, S.J. and Caron, G. (1987) The pollination mechanism
of Engelmann spruce (Picea engelmannii Parry), Can. J. Bot. 65, 14391450
13 Runions, C.J., Catalano, G.L. and Owens, J.N. (1995) Pollination mechanism
of seed orchard interior spruce, Can. J. For. Res. 25, 14341444
14 Runions, C.J. and Owens, J.N. (1996) Pollen scavenging and rain involvement
in the pollination mechanism of interior spruce, Can. J. Bot. 74, 115124
15 Runions, C.J. et al. Pollination of Picea orientalis (Pinaceae): saccus
morphology governs pollen buoyancy, Am. J. Bot. (in press)

trends in plant science

perspectives
16 Hunter, J.P. (1998) Key innovations and the ecology of macroevolution,
Trends Ecol. Evol. 13, 3136
17 Tomlinson, P.B. (1994) Functional morphology of saccate pollen in
conifers with special reference to Podocarpaceae, Int. J. Plant Sci. 155,
699715
18 Wilson, V. and Owens, J.N. The reproductive cycle in Podocarpus totara,
Am. J. Bot. (in press)
19 Tomlinson, P.B., Braggins, J.E. and Rattenbury, J.A. (1991) Pollination drop
in relation to cone morphology in Podocarpaceae: a novel reproductive
mechanism, Am. J. Bot. 78, 12891303
20 Takaso, T. and Owens, J.N. (1995) Pollination drop and microdrop secretions
in Cedrus, Int. J. Plant Sci. 156, 640649
21 Singh, H. and Owens, J.N. (1982) Sexual reproduction in grand fir (Abies
grandis), Can. J. Bot. 60, 21972214
22 Owens, J.N., Simpson, S.J. and Molder, M. (1981) The pollination mechanism
and the optimal time of pollination in Douglas-fir (Pseudotsuga menziesii),
Can. J. For. Res. 11, 3650
23 Owens, J.N., Morris, S. and Catalano, G. (1994) How the pollination
mechanism and prezygotic and postzygotic events affect seed production in
Larix occidentalis, Can. J. For. Res. 24, 917927
24 Takaso, T. and Owens, J.N. (1996) Postpollination-prezygotic ovular
secretions into the micropylar canal in Pseudotsuga menziesii (Pinaceae),
J. Plant Res. 109, 147160
25 Haines, R.J., Prakash, N. and Nikles, D.G. (1984) Pollination in Araucaria
Juss., Aust. J. Bot. 32, 583594
26 Eames, A.J. (1913) The morphology of Agathis australis, Ann. Bot. 27, 136
27 Owens, J.N. et al. (1995) The reproductive biology of Kauri (Agathis australis).
I. Pollination and prefertilization development, Int. J. Plant Sci. 156, 257269
28 Singh, H. (1978) Embryology of Gymnosperms, Gebrder Borntraeger

29 Colangeli, A.M. and Owens, J.N. (1989) Postdormancy seed-cone

development and the pollination mechanism in western hemlock (Tsuga
heterophylla), Can. J. For. Res. 19, 4453
30 Owens, J.N. and Blake, M.D. (1983) Pollen morphology and development of
the pollination mechanisms in Tsuga heterophylla and T. mertensiana, Can. J.
Bot. 61, 30413048
31 McWilliam, J.R. (19958) The role of the micropyle in the pollination of Pinus,
Bot. Gaz. (Chicago) 120, 109117
32 Ziegler, H. (1959) Uber die Zusammensetzung des bestaubungstropfens und
den Mechanismus seiner Sekretion, Planta 52, 587599
33 Serdi-Benkaddour, R. and Chesnoy, L. (1985) Secretion and composition of
the pollination drop in the Cephalotaxus drupacea (Gymnosperm,
Cephalotaxeae), in Sexual Reproduction in Higher Plants (Cristi, M., Gori, P.
and Pacini, E., eds), pp. 345350, Springer-Verlag
34 Runions, C.J. and Owens, J.N. Evidence of prezygotic self-incompatibility in a
gymnosperm, in Proceedings: Reproductive Biology 96 in Systematics,
Conservation and Economic Botany (15 Sept. 1996), Royal Botanical
Gardens, Kew, UK (in press)

John N. Owens* is at the Centre for Forest Biology,

PO Box 3020 STN CSC, Victoria, BC, Canada V8W 3N5;
Tokushiro Takaso is at the Iromote Station, Tropical Biosphere
Research Centre, University of the Ryukyus, 870 Uehara,
Taketomi-cho, Okinawa 907-1541, Japan;
C. John Runions is in the Section of Ecology and Systematics,
Corson Hall, Cornell University, Ithaca, NY 14853-2701, USA.

*Author for correspondence (tel 11 250 721 7113;

fax 11 250 721 6611; e-mail jowens@uvic.ca).

Ecological and evolutionary

genetics of Arabidopsis
Massimo Pigliucci
The crucifer Arabidopsis thaliana has been the subject of intense research into
molecular and developmental genetics. One of the consequences of having
this wealth of physiological and molecular data available, is that ecologists
and evolutionary biologists have begun to incorporate this model system into
their studies. Current research on A. thaliana and its close relatives ably
illustrates the potential for synergy between mechanistic and organismal
biology. On the one hand, mechanistically oriented research can be placed in
an historical context, which takes into account the particular phylogenetic
history and ecology of these species. This helps us to make sense of
redundancies, anomalies and sub-optimalities that would otherwise be difficult
to interpret. On the other hand, ecologists and evolutionary biologists now
have the opportunity to investigate the physiological and molecular basis for
the phenotypic changes they observe. This provides new insight into the
mechanisms that influence evolutionary change.

iology is experiencing the age of

model systems1. Our present understanding of genetics would have been
very different if laboratories throughout the
world had not agreed to concentrate their efforts on the fruit fly Drosophila melanogaster
at the beginning of the century. Similarly,
different branches of biology have adopted

distinct organisms as being particularly convenient for the type of study at hand. As a consequence, we have considerable knowledge of
the physiology of mice, the developmental
biology of sea urchins, the molecular biology
of Escherichia coli, and an understanding of
disease resistance in tobacco. There are, of
course, limits to this strategy of focusing on a

1360 - 1385/98/$ see front matter 1998 Elsevier Science. All rights reserved. PII: S1360-1385(98)01343-0

reduced number of organisms. Although it has

been possible to understand their biology in
depth, it is also clear that we are forfeiting anything more than a superficial knowledge of the
overwhelming majority of living organisms.
Fortunately, research in evolutionary biology can help to broaden the scope of our
investigations. All organisms were derived
from a single common ancestor, which is why
they share the same genetic/molecular machinery. Thus, we can apply what we learn
about a small number of organisms to the majority at least as long as we do not extrapolate too far from our starting point in either
ecological or phylogenetic space. The real
question is how many model systems we need,
and how far these generalizations can reasonably be extended.
Arabidopsis as a model system
Arabidopsis thaliana (L.) Heynh. is a small
annual, white-flowered member of the Brassicaceae family, and is allied to other crucifers
such as mustard, Brassica napus and broccoli.
Arabidopsis thaliana was first adopted as a
model system in plant genetics in the 1950s,
largely as a target for mutagenesis studies2.
More recently, A. thaliana has been the focus
of physiological, developmental and genetic
research that has made it the reference point
for plant molecular biology3.
December 1998, Vol. 3, No. 12

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