The seeds of gymnosperms are naked, meaning that theyare not completely enclosed within another structure, butare borne at the tip of a shoot, or on the surface of a bract orscale. The seeds often appear enclosed because in conifers (suchas pine) they are contained in a seed cone. Unlike angiosperms,most of which are insect pollinated (entomophily), the majority ofgymnosperms are wind pollinated (anemophily).

Conifers are a small group of gymnosperms that dominatenorth temperate forests. All are wind pollinated, but an array ofmechanisms have evolved to increase pollination success. Forexample, the integument tip of the ovulemay be modified for pollen collection; pol-lination drops secreted from the ovule mayaid in scavenging pollen; pollen may havewings (sacci); and seed cones at receptiv-ity may have shapes and orientations thatdirect pollen to the receptive surfaces.

Conifer origin and reproductive diversityConifers evolved from the progymnospermsin the Late Devonian and were at their mostdiverse and abundant during the MesozoicEra1. Early pollen cones (microsporangiatestrobili) were simple structures consistingof an axis with modified leaves (micro-sporophylls) that bore microsporangia. Seedcones (megasporangiate strobili or mega-strobili) were compound, consisting of anaxis bearing modified leaves (bracts) in theaxil of which developed a shoot that boreone to many erect ovules. The ovules, afterpollination and fertilization, formed seeds.The axillary fertile shoots varied in differ-ent taxa. Early forms such as the Voltzialeshad radially symmetrical fertile shoots bear-ing several scales and erect ovules. Subse-quent taxa showed a flattening of the fertileshoot, fusion of the scales, shortening ofthe ovule and cone axes and inversion ofthe ovules. The fossil record is fairly com-plete but there is disagreement about af-finities among taxa. Most modern familiesare recognizable by the Late Triassic, andfamiliar genera such as Pinus date fromapproximately 130 million years ago.

Modern conifers are commonly placedin seven families listed here according totheir time of origin from the earliest tomost recent: Podocarpaceae; Araucariaceae;Cupressaceae; Taxodiaceae; Taxaceae;

Pinaceae; and Cephalotaxaceae. Some taxonomists combine theCupressaceae and Taxodiaceae or place the Taxaceae in a separateorder. There are approximately 550 conifer species in 53 genera2.Most are north temperate, such as the Pinaceae, but others aretropical or found primarily in the southern hemisphere, such as thePodocarpaceae and Araucariaceae.

One might expect an essential feature like pollination to showlittle diversity in such a small taxon. However, conifers are a veryancient group and there have been repeated climatic changes thatprobably restricted and isolated species for long periods of time3.

479

trends in plant sciencereviews

December 1998, Vol. 3, No. 121360 - 1385/98/$ see front matter 1998 Elsevier Science. All rights reserved. PII: S1360-1385(98)01337-5

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 lagsbehind our knowledge of this process in angiosperms. In part this is because conifers are notconsidered to be high priority crops and, unlike many cultivated flowers, conifer seed cones aregenerally neither large nor colorful. The use of genetics to improve tree growth has primarily beenthrough selection and asexual propagation rather than breeding, and because incompatibility isnot thought to occur in conifer pollination systems, concern about pollination has primarily beenwith regard to seed production. Here we examine the ancestral wind-pollination mechanismin conifers and discuss how the process may have evolved to improve pollination success.

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

This has led to diversity in certain traits,such as pollen, megastrobili and pollinationmechanisms, not only among genera withina family, but occasionally between specieswithin a genus.

Megastrobilus and pollen morphologyMegastrobilus orientation and morphologyare important features for wind pollination.In a series of classic experiments, Niklas4,5

studied the aerodynamics of pollen-graindeposition based on models of fossil seedplants and living megastrobili of conifersand cycads (non-coniferous gymnosperms).In most conifer megastrobili at pollinationthere are a complex system of air eddiesgenerated by the cones geometry and thatof the individual bract and scale com-plexes6. The megastrobilus channels pollenaround the cone, and pollen settles on tobracts or scales or passes down around thecone axis. Minute surface features mayaffect where the pollen comes to rest.

The morphology of the pollen plays animportant part in the pollination mecha-nism. Conifer pollen varies in diameter fromapproximately 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 non-saccate (Fig. 1)7. Although conifer pollenis generally larger than pollen from mostangiosperm species, it is light for its sizeand can be carried long distances. Maxi-mum dispersal distances in the Pinaceae are3001300 km in strong air currents8. The air-filled sacci present in about 50% of coniferspecies reduce the density of the pollen,but their primary function is flotation.

480

trends in plant sciencereviews

December 1998, Vol. 3, No. 12

Fig. 2. Light micrographs of three types of seed cones (megastrobili) representing threepollination mechanisms. (a) Juniperus with fused bract-scales (Bs), one central ovule and apollination drop (arrow). Scale bar 5 1 mm. (b) Picea with broad flat scales (S) and separ-ate, 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.

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 pollensink into the pollination drop which is exuded from upright or variably oriented ovules. (b) Pollen with sacci float upwards into the pollinationdrop exuded from inverted ovules. (c) The pollination drop is absent or not exuded from the micropyle in some genera of Pinaceae and pollenfloat into the ovule in rainwater. (d) Pollen have lost the ability to float and are taken into the inverted ovule by engulfment. (e) Pollen grainsgerminate extra-ovularly and pollen tubes grow into the ovule.

Some Pinaceae(Abies)

Some Pinaceae(Pseudotsuga, Larix)

Some Pinaceae(some Tsuga) and

Araucariaceae

Some Pinaceae(Pinus, Picea,

Cedrus and some Tsuga),Podocarpaceae

Cupressaceae,Taxodiaceae, Taxaceae,

Cephalotaxaceae andsome Podocarpaceae

Megastrobilus and pollen morphologyand pollination mechanisms are, of course,linked, often in intriguing ways. Here wediscuss five pollination mechanisms, someof which show considerable variation. Simi-lar mechanisms have evolved independentlyin unrelated taxa.

Pollination mechanismsPollination drop, non-saccate pollen andovules without preferred orientationThe least specialized pollination mechanismis found in four of the seven conifer fam-ilies: Cupressaceae, Taxodiaceae, Cephalo-taxaceae and Taxaceae. All four familieshave small, non-saccate pollen (Fig. 1).The first three families have megastrobili,whereas Taxaceae have separate ovulesthat are commonly erect at pollination orwithout preferred orientation (variable),but not pendant. Megastrobili have fusedbract-scale complexes (Fig. 2) and theovules are flask shaped, variable in numberand attached in the axil of the bract-scale.Ovules lie at an angle to the axis and mayadopt a vertical or horizontal orientationdepending on cone orientation. The integu-ment tip has a narrow neck and a small,unspecialized micropyle.

A pollination drop has been observed inmany species in these families (Fig. 3)9.Light and scanning electron microscopyhave been used for these studies (Fig. 4),but the destructive sampling required hasmade it difficult to determine the sequenceof pollination drop emergence and recession.Time-lapse cinematography of Chamae-cyparis nootkatensis trees revealed one ex-ample of the sequence10. Megastrobili openand ovules become fully exposed for about2 days; then in the early morning a pollination drop is exudedfrom the micropyle of some ovules (Fig. 4). If no pollen is ap-plied, the drops remain until mid-day and then slowly recede intothe micropyle. If pollen is dusted onto the receptive cone the dropsrecede within 20 min. Pollen dusted onto the cone enters the dropsimmediately, signalling an end to active secretion and allowingrapid evaporation (Fig. 4). There is no evidence of active reab-sorption of the drops by ovular tissue. If cones are not pollinatedthe drops repeatedly emerge then recede each day for severaldays, then the bract scales thicken and cover the ovules sealing thecone. Pollinated ovules no longer secrete drops. In field-grownThuja plicata, unpollinated cones enclosed in isolation bags con-tinued to secrete drops diurnally for 1520 days, until the coneswere completely closed, whereas naturally pollinated cones secretedrops for only 45 days11. Anatomical studies in Chamaecyparisand Thuja show that the drop is secreted from the nucellar tip. Sur-face cells become vacuolate, release the clear vacuolar contentsand then collapse, creating a cavity, the pollen chamber, in thenucellar tip. After pollen is taken in, cells lining the micropylarcanal enlarge to form a collar that seals the ovule.

Water in the form of rain or dew may assist in pollination. InThuja, an epicuticular wax layer on the bract scale causes water tobead; beads roll down the surface, picking up pollen, and then con-tact the ovules where the water fuses with the pollination drops11.

The action of water droplets in scavenging pollen and transfer-ing it to the ovules suggests that an internally produced pollinationdrop was not essential in early conifers in the warm and humidhabitats that existed during much of their early evolution3.

We presume that this simple pollination mechanism existed inthe Mesozoic conifers, and is the ancestral mechanism from whichother forms evolved. A prerequisite for this process appears to bethe existence of non-saccate pollen that would sink into the polli-nation or water drops. The driving force for evolutionary changemay have been the occurrence of dry periods and subsequentlower pollen to ovule ratios that would favor large pollinationdrops and more efficient mechanisms for scavenging pollen fromcone surfaces.

Pollination drops, saccate pollen and inverted ovulesA mechanism that combines pollination drops, saccate pollen andinverted ovules is found in the Pinaceae and Podocarpaceae (Fig. 3).In some Mesozoic conifers, ovules became inverted, the ovule stalkshortened bringing the inverted ovule close to the megastrobilusaxis, and ovules fused with the ovuliferous scale1. With few excep-tions, megastrobili in the Pinaceae are upright at pollination (Fig. 2).The two ovules per ovuliferous scale are inverted, and fused to theadaxial surface of the scale close to the axis. Receptive megastrobiliof most Pinaceae are shaped so that they channel pollen towards

481

trends in plant sciencereviews

December 1998, Vol. 3, No. 12

Fig. 4. Scanning electron micrographs of portions of fresh megastrobili at pollination. (a) Chamaecyparis showing all ovules, some with pollination drops (Pd) exuded from themicropyle (arrow) of the ovule. Scale bar 5 200 mm. (b) Chamaecyparis integument tipshowing pollination drop after pollen has entered the drop leaving marks on the surface(arrow). Scale bar 5 35 mm. (c) Pinus integument tip showing the micropyle (M) andmicropylar arms (Ma) that secrete microdroplets (arrow) to which pollen (P) adheres. Scalebar 5 20 mm. (d) Picea integument tip with a large pollination drop emerging from themicropyle and filling the space between the micropylar arms. Scale bar 5 20 mm.

the cone axis and micropyles5. In many genera, as ovules developthe integument tip elongates and forms two prongs (micropylararms), between which is a small micropyle. The micropyle facesdownwards (Figs 3 and 4) so pollen cannot simply fall in12.

This pollination mechanism is best described in Picea1214. Mega-strobili become erect and burst from their bud scales, the bracts andscales reflex and become receptive for pollination. Megastrobiliappear receptive (Fig. 2) for 2 weeks, but take in pollen for ap-proximately only 1 week. At receptivity the epidermal cells of themicropylar arms secrete microdroplets to which pollen adheres(Fig. 4). Pollen also comes to rest on other cone surfaces, most ofwhich are covered with minute hairs or wax rodlets such that anywater entering the megastrobilus beads on these surfaces. Rain-water can move down the surfaces carrying pollen towards themicropyle. A large pollination drop is then exuded from the micro-pyle, filling the space between the arms (Figs 3 and 4), often con-tacting the cone axis or adjacent scales. The saccate pollen (similarto that in Fig. 1b) enters the pollination drop and floats up into themicropyle to the surface of the nucellus (Fig. 5). The arms thenwither and the scales thicken, closing the megastrobilus whichthen becomes pendant. Experiments using pipettes filled with sugarsolutions to simulate pollination drops have shown that saccatepollen is scavenged from surfaces and floats upwards, whereasnon-saccate pollen remains on the surface12,14. This demonstratesthat the sacci function as flotation devices for inverted ovules.

The function of sacci in flotation was recently demonstrated in aspecies of spruce (Picea orientalis) in which megastrobili are pen-dant at pollination; thus the ovules are upright, in contrast to otherspruces (Fig. 5). In this species, the pollen is saccate, but does notfloat up into a simulated pollination drop; instead it sinks into thedrop on an erect ovule. Upon close examination using confocaland transmission electron microscopy, it was found that the sacci,although normal in appearance, are more porous than sacci onpollen from other spruce species. Upon wetting, swelling of thepollen body displaces the air within the sacci and the pollen func-tions as non-saccate pollen15. Most species of Picea freely hybrid-ize, but oriental spruce does not. One reason for this is now clear saccate pollen of other spruces would not sink into the erectovules of oriental spruce, and the functionally non-saccate ori-ental spruce pollen would not float up into the pollination drop ofinverted ovules (Fig. 5). Saccate pollen and inverted ovules in thePinaceae are considered to be the ancestral form from which theupright ovules of oriental spruce have evolved. Oriental spruce isnative to the Caucasus Mountains and has been isolated fromother spruces. This isolation has allowed evolutionary change inboth the pollination mechanism and in vegetative characters. Inthis species, as in many other conifers, the key innovation16 necess-ary for the origin of the new taxon seems to be a change in thepollination mechanism.

Most members of the Podocarpaceae studied to date have a pol-lination mechanism similar in function, but not structure, to Pin-aceae17. In the Podocarpaceae, all megastrobili morphologies arebased on a consistent unit, involving a uniovulate complex in theaxil of a fertile bract. The ovule is inverted in all but two genera.Cone position is closely correlated with leaf type in most Podo-carpaceae: terminal cones are associated with scale-like leaves,and lateral cones with bifacially-flattened, linear leaves. Highlyderived genera within the Podocarpaceae have a reduced numberof ovules per megastrobilus, and fusion of ovulate structures, suchas the integument and epimatium, occurs. There is some debateover whether the epimatium is homologous to the ovuliferousscale, or a sterile part of the seed-scale complex. Most genera as-sociate a fleshy structure (axil, epimatium or peduncle) with themature ovule. There are usually two inverted ovules per unit, eachproducing a pollination drop, and pollen is saccate. Where ovulesare erect, the ovule axis bends downward soon after pollination sothat the micropyle faces downward18. In members of the Podo-carpaceae with inverted ovules, the pollination drop extends beyondthe micropyle and makes contact with megastrobilus surfaces in avariety of configurations depending on the shape of the wettablecone surface. Saccate pollen is scavenged from these surfaces bythe pollination drop, and the floating pollen then passes into themicropyle towards the nucellus17,19.

No pollination drops, saccate pollen and inverted ovulesThere are several reports of rainwater supplementing the pollinationdrop in the Pinaceae14,20, the Cupressaceae11 and the Podocar-paceae18. 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 evolu-tionary step in which rainwater appears to serve the function of apollination drop. The integument tip forms a short funnel, oftenwith fluted edges, around a large micropyle21. Microdrops form onthe inner surface of the funnel and the saccate pollen adheres tothis surface. In Abies amabilis the wettable internal surfaces of thecone are directly below the funnel-shaped tip of the invertedovule. Rainwater forms beads on many surfaces and moves downtowards the axis near the wettable surfaces. Here the water accu-mulates to form a large drop or column joining the funnel and the

482

trends in plant sciencereviews

December 1998, Vol. 3, No. 12

Fig. 5. (a) Megastrobili of Picea glauca are erect at pollinationand ovules are inverted. Saccate pollen floats up into the polli-nation drop and into the micropyle. (b) Picea orientalis megastro-bili are pendant at pollination and ovules are nearly erect. Thepollen is saccate but porous and it floats only briefly before sink-ing into the pollination drop and into the micropyle. Adapted, withpermission, from Ref. 15.

subjacent scale (Fig. 3). Buoyant pollenfloats into the micropyle in the accumu-lated drop. In this mechanism the integu-ment tip has been simplified and thepollination drop appears to have been lost,with rainwater taking over its function.Remnants of a pollination drop may be se-creted from the nucellar apex to stimulatepollen germination.

Engulfment of non-saccate pollen andreduction of the pollination dropIn Pseudotsuga and Larix (Pinaceae) theovule is inverted and the integument tipforms two unequal lobes; the adaxial lobeis larger and both lobes develop unicellularpapillae. The micropyle is a narrow slitbetween the two lobes and no pollinationdrop is exuded from the micropyle (Fig. 3).The structure is called a stigmatic area17, ortip22. The cones are upright at pollinationand pollen passes down the smooth, adax-ial surface of the bract and is funneled tothe stigmatic tip, where they become en-tangled in or adhere to the papillae (Fig. 6).The cones are open and collect pollen forseveral days, then the cells on the outer sur-face of the stigmatic tip elongate and cellsaround the micropyle collapse. As a resultthe papillae and attached pollen are drawninto the micropyle, in much the same wayas a sea anemone engulfs its prey (Fig. 6).

Once pollen is within the micropylarcanal the processes in Pseudotsuga22 andLarix23 differ. In Pseudotsuga, pollen mayremain entangled in the papillae just insidethe sealed micropyle or be released into themicropylar canal. Within a day the pollenhydrates and the exine bursts. Then overseveral weeks, the intine elongates severalhundred micrometres down the micropylarcanal and makes contact with the nucellar apex where a narrowpollen tube forms and penetrates the nucellus. Recently, secretionshave been shown to arise from the inner wall of the integument,the nucellar apex and the megagametophyte. These secretionsmay stimulate pollen elongation and tube formation24. In Larix,engulfed pollen hydrates and sheds its exine within days, but doesnot elongate. Instead, it remains at the distal end of the micropylarcanal for 56 weeks; then a fluid secretion fills the micropylarcanal and the pollen is carried to the nucellar apex, where a pollentube forms and penetrates the nucellus23.

Extra-ovular pollen germination, non-saccate pollen and nopollination dropIn three quite unrelated taxa all of the Araucariaceae, mostTsuga species within the Pinaceae, and Saxegothaea in the Podo-carpaceae the loss of the pollination drop coupled with extremesiphonogamy, has evolved in a parallel fashion. Pollen lands on asurface of the megastrobilus (integument bract, scale or axis) whereit germinates and, usually after some delay, the long pollen tubegrows into the ovule (Fig. 3). In Araucaria, pollen has been reportedto land and germinate on the fused bract-scale, penetrate the epi-dermis, and grow under the surface before emerging and proceedingto the single proximal adaxial ovule. Upon reaching the ovule the

pollen tube enters the large, open micropyle and penetrates the nu-cellus25. In early studies of Agathis australis, the mechanism ap-peared to be similar to that of Araucaria26; it differed in that thepollen tubes appeared to grow under the bract-scale surface andpermeate cortical and vascular tissues until they reached the ovulewhere they emerged to enter the micropyle. A recent study of A. australis from the same location in New Zealand has not bornethis out27. This later study indicates that the non-saccate pollencomes to rest near the cone axis, the ovule tip elongates and pressesthe exposed nucellus apex (Fig. 6) against the cone axis. Pollenpressed between the nucellus and cone axis germinates and thenbranches before penetrating the nucellus. Another study of tropicalA. borneensis indicates that pollen tubes penetrate the ovule in manylocations and not just through the exposed nucellus. In Saxegothaeathe nucellus is extruded through the micropyle28, as observed in A. australis.

In Tsuga (Pinaceae) there are two pollination mechanisms. Thegenus is divided into two sections, Micropeuce, which contains atleast ten extant species and Hesperopeuce, which contains one ortwo remnant extant species and many recently extinct species.Pollination in T. heterophylla has been studied extensively29, andis considered to be typical of the Micropeuce. The mechanism showsremarkable co-evolution of megastrobilate and pollen structures.

483

trends in plant sciencereviews

December 1998, Vol. 3, No. 12

Fig. 6. Scanning electron micrographs of portions of megastrobili at pollination. (a) Pseudo-tsuga stigmatic tip at receptivity showing the two lobes with unicellular papillae and slit-likemicropyle between (arrow). Pollen (P) has begun to adhere to papillae on the abaxial lobe.Scale bar 5 75 mm. (b) Pseudotsuga stigmatic tip after engulfment of the pollen. Somepollen (arrow) has been left outside the micropyle. Scale bar 5 100 mm. (c) Tsuga hetero-phylla bract surface (right) with cobweb-like epicuticular wax threads to which spines ofpollen attach (arrow). Scale bar 5 10 mm. (d) Ovule tip of Agathis showing large U-shapedmicropyle (arrow) with tongue-like nucellus (N) protruding with a distal nucellar flap (Nf) towhich pollen attaches. Scale bar 5 100 mm.

Pollen is non-saccate, although rudimentary sacci are present asfrills on the exine. The pollen is unique for conifers in that it iscovered with short spines (Fig. 1). At pollination, the bract is ex-posed beyond the scale (Fig. 2) and its exposed abaxial surface iscovered by a web-like epicuticular wax. This allows pollen to ad-here to the bract surface (Fig. 6), but few enter the megastrobilusor adhere to the scale. The bracts collect pollen for 12 weeks,then the scales overgrow the bracts and encase the pollen. Thepollen remains in this position for about 6 weeks while the mega-strobilate cone enlarges considerably. The pollen then germinatesand each grain forms a long pollen tube that grows over the bractsurface towards the ovules on a subjacent scale. The ovules havea simple, funnel-shaped integument tip, large micropyle and shortmicropylar canal. Several pollen tubes may grow into each micro-pyle and penetrate the nucellus. It is not known what attractspollen tubes to the nucellus, here or in the Araucariaceae. The polli-nation mechanism of T. heterophylla is the most efficient known inconifers and ensures a high rate of pollination success and seed set29.

The Hesperopeuce, represented by T. mertensiana, have sac-cate pollen and a pollination mechanism that is more similar toPicea12 or Cedrus20 than other hemlocks. The integument tip hastwo flaps on which pollen lands. Secretion of a pollination drop issuspected, but has not been convincingly recorded because thespecies grows at high altitudes and fresh specimens are difficult toobtain. The integument flaps appear to fold over to trap the pollen.Upon germination, the pollen tube has only a short distance togrow to reach the nucellus30. Two such different pollination mecha-nisms in one genus is unique within the conifers, and may be theresult of prolonged isolation over time. It also suggests that theloss of the ancestral pollination drop may have occurred severaltimes in unrelated taxa.

The nature of the pollination dropThe pollination drop, which in different taxa may be prominent,reduced or absent, was first observed in the mid-1800s. Chemicalanalysis has shown it to be a weak sugar solution, consisting ofsucrose, glucose and fructose at a total concentration of between110% (Refs 31,32) or glucose and fructose at a total concen-tration of about 8% (Ref. 12). The solution also contains variousamino acids, peptides and organic acids32,33. Early studies did notconsider secretion of the pollination drop to be an active secretoryprocess31,32 and it was likened to gluttation in Pinus31. More recentstudies have shown it to be an active secretory process12,23, similarto nectar production in angiosperms. However, the volume of thepollination drop is too great to be produced by the nucellar tipalone; suggested secretory sources include other tissues such asthe megagametophyte and integument. In addition, a small polli-nation drop may be augmented by rainwater or dew.

ConclusionsThe conifers are a small group of primitive seed plants that appearat first glance to be conservative in their morphological and repro-ductive traits. However, close inspection reveals five major typesof pollination mechanism that vary in structure and function (Fig.3) while achieving the same result the capture of airborne pollenand its transport into the megastrobilus or ovule. The most primitiveand widespread of these mechanisms makes use of a pollinationdrop. Here, there has been co-evolution of pollen and ovules non-saccate pollen occurs in species that have erect ovules, whereassaccate pollen occurs in species with inverted ovules. Reductionin size or loss of the pollination drop has been accompanied byadaptive changes in the integument tip that allow it to engulf pol-len; such adaptations include making use of rainwater or allowingpollen tubes to grow into the ovule. Subtle changes in the pollination

mechanism lead to reproductive isolation and resulting divergencein other traits. The changes seen among the conifers probably aroseas a result of the frequent isolation of genera or species broughtabout by geoclimatic changes, especially in north temperate regionsover millions of years a conclusion supported by the abundanceof endemic and monotypic conifer genera and species.

Few conifer pollination mechanisms include incompatibilitymechanisms as seen in angiosperms. Pollen discrimination maybe limited to saccate or non-saccate traits and the resulting abilityto float or sink in pollination drops, or to restrictions imposed bypollen size or wall morphology. The incompatibility mechanismsthat exist are late acting and occur within the ovule. Such late-actingincompatibility mechanisms are also common in woody perennialangiosperms some are late prezygotic, others postzygotic. Theclassical view that conifers have only postzygotic incompatibilitymechanisms (inviability), may have to be rethought. Recent re-search has demonstrated that primitive prezygotic incompatibilitymechanisms exist in conifers34. Future experiments and molecularstudies on these different pollination mechanisms may reveal thefull nature of incompatibility in conifers.

AcknowledgementsWe thank the research assistants and graduate students who overmany years have contributed to our understanding of pollinationin conifer species. These include Marje Molder, Anna Colangeli,Margaret Blake, Vivienne Wilson, Erika Anderson, Tajudin Komarand Luke Chandler. Most of the research has been supported by a Natural Sciences and Engineering Research Council of Canadagrant (A1982) to J.N. Owens.

References1 Miller, C.N. (1978) Mesozoic conifers, Bot. Rev. 43, 2172802 Silba, J. (1984) An International Census of the Coneriferae, I. Phytologia

Memoirs, H.N. and A.L. Moldenke, USA3 Florin, R. (1951) Evolution in Cordaites and conifers, Acta Horti Bergiani 15,

2853884 Niklas, K.J. (1981) Airflow patterns around some early seed plant ovules and

capules: Implications concerning efficiency in wind pollination, Am. J. Bot.68, 635650

5 Niklas, K.J. (1982) Simulated and empiric wind pollination patterns of coniferovulate cones, Proc. Natl. Acad. Sci. U. S. A. 79, 510514

6 Niklas, J.K. and Norstog, K. (1984) Aerodynamics and pollen graindepositional patterns on cycad megastrobili: Implications on the reproductionof three cycad genera (Cycas, Dioon and Zamia), Bot. Gaz. 145, 92104

7 Owens, J.N. and Simpson, S.J. (1986) Pollen from conifers native to BritishColumbia, Can. J. For. Res. 16, 955967

8 Potter, L.D. and Rowley, J. (1960) Pollen rain and vegetation, San AugustinPlains, New Mexico, Bot. Gaz. 112, 125

9 Takaso, T. (1990) Pollination drop time at the Arnold Arboretum, Arnoldia50, 27

10 Owens, J.N., Simpson, S. and Molder, M. (1980) The pollination mechanismin yellow cypress (Chamaecyparis nootkatensis), Can. J. For. Res. 10,564572

11 Colangeli, A.M. and Owens, J.N. (1990) The relationship between time ofpollination, pollination efficiency and cone size in western redcedar (Thujaplicata), Can. J. For. Res. 69, 439443

12 Owens, J.N., Simpson, S.J. and Caron, G. (1987) The pollination mechanismof Engelmann spruce (Picea engelmannii Parry), Can. J. Bot. 65, 14391450

13 Runions, C.J., Catalano, G.L. and Owens, J.N. (1995) Pollination mechanismof seed orchard interior spruce, Can. J. For. Res. 25, 14341444

14 Runions, C.J. and Owens, J.N. (1996) Pollen scavenging and rain involvementin the pollination mechanism of interior spruce, Can. J. Bot. 74, 115124

15 Runions, C.J. et al. Pollination of Picea orientalis (Pinaceae): saccusmorphology governs pollen buoyancy, Am. J. Bot. (in press)

484

trends in plant sciencereviews

December 1998, Vol. 3, No. 12

Biology is experiencing the age ofmodel systems1. Our present under-standing of genetics would have beenvery different if laboratories throughout theworld had not agreed to concentrate their ef-forts on the fruit fly Drosophila melanogasterat the beginning of the century. Similarly,different branches of biology have adopted

distinct organisms as being particularly con-venient for the type of study at hand. As a con-sequence, we have considerable knowledge ofthe physiology of mice, the developmentalbiology of sea urchins, the molecular biologyof Escherichia coli, and an understanding ofdisease resistance in tobacco. There are, ofcourse, limits to this strategy of focusing on a

reduced number of organisms. Although it hasbeen possible to understand their biology indepth, it is also clear that we are forfeiting any-thing more than a superficial knowledge of theoverwhelming majority of living organisms.

Fortunately, research in evolutionary biol-ogy can help to broaden the scope of ourinvestigations. All organisms were derivedfrom a single common ancestor, which is whythey share the same genetic/molecular ma-chinery. Thus, we can apply what we learnabout a small number of organisms to the ma-jority at least as long as we do not extrapo-late too far from our starting point in eitherecological or phylogenetic space. The realquestion is how many model systems we need,and how far these generalizations can reason-ably be extended.

Arabidopsis as a model systemArabidopsis thaliana (L.) Heynh. is a smallannual, white-flowered member of the Brassi-caceae family, and is allied to other cruciferssuch as mustard, Brassica napus and broccoli.Arabidopsis thaliana was first adopted as amodel system in plant genetics in the 1950s,largely as a target for mutagenesis studies2.More recently, A. thaliana has been the focusof physiological, developmental and geneticresearch that has made it the reference pointfor plant molecular biology3.

485

trends in plant scienceperspectives

December 1998, Vol. 3, No. 121360 - 1385/98/$ see front matter 1998 Elsevier Science. All rights reserved. PII: S1360-1385(98)01343-0

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 dropin relation to cone morphology in Podocarpaceae: a novel reproductivemechanism, Am. J. Bot. 78, 12891303

20 Takaso, T. and Owens, J.N. (1995) Pollination drop and microdrop secretionsin Cedrus, Int. J. Plant Sci. 156, 640649

21 Singh, H. and Owens, J.N. (1982) Sexual reproduction in grand fir (Abiesgrandis), Can. J. Bot. 60, 21972214

22 Owens, J.N., Simpson, S.J. and Molder, M. (1981) The pollination mechanismand 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 pollinationmechanism and prezygotic and postzygotic events affect seed production inLarix occidentalis, Can. J. For. Res. 24, 917927

24 Takaso, T. and Owens, J.N. (1996) Postpollination-prezygotic ovularsecretions 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 AraucariaJuss., Aust. J. Bot. 32, 583594

26 Eames, A.J. (1913) The morphology of Agathis australis, Ann. Bot. 27, 13627 Owens, J.N. et al. (1995) The reproductive biology of Kauri (Agathis australis).

I. Pollination and prefertilization development, Int. J. Plant Sci. 156, 25726928 Singh, H. (1978) Embryology of Gymnosperms, Gebrder Borntraeger

29 Colangeli, A.M. and Owens, J.N. (1989) Postdormancy seed-conedevelopment and the pollination mechanism in western hemlock (Tsugaheterophylla), Can. J. For. Res. 19, 4453

30 Owens, J.N. and Blake, M.D. (1983) Pollen morphology and development ofthe 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 undden Mechanismus seiner Sekretion, Planta 52, 587599

33 Serdi-Benkaddour, R. and Chesnoy, L. (1985) Secretion and composition ofthe 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 agymnosperm, in Proceedings: Reproductive Biology 96 in Systematics,Conservation and Economic Botany (15 Sept. 1996), Royal BotanicalGardens, 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 BiosphereResearch 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 evolutionarygenetics of ArabidopsisMassimo Pigliucci

The crucifer Arabidopsis thaliana has been the subject of intense research intomolecular and developmental genetics. One of the consequences of havingthis wealth of physiological and molecular data available, is that ecologistsand evolutionary biologists have begun to incorporate this model system intotheir studies. Current research on A. thaliana and its close relatives ablyillustrates the potential for synergy between mechanistic and organismalbiology. On the one hand, mechanistically oriented research can be placed inan historical context, which takes into account the particular phylogenetichistory and ecology of these species. This helps us to make sense ofredundancies, anomalies and sub-optimalities that would otherwise be difficultto interpret. On the other hand, ecologists and evolutionary biologists nowhave the opportunity to investigate the physiological and molecular basis forthe phenotypic changes they observe. This provides new insight into themechanisms that influence evolutionary change.