Serial Development of Foliar Gemmae in Tortula (Pottiales, Musci ...

Annals of Botany 78 : 305–315, 1996

Serial Development of Foliar Gemmae in Tortula (Pottiales, Musci),

an Ultrastructural Study

ROBERTO LIGRONE†, JEFFREY G. DUCKETT‡ and RAFFAELE GAMBARDELLA*

*Dipartimento di Biologia Vegetale, Uni�ersita[ di Napoli, Via Foria 223, I-80139 Napoli, Italy, †Facolta[ di Scienze

Ambientali del Secondo Ateneo Napoletano, �ia Arena 22, 81100 Caserta, Italy and ‡School of Biological Sciences,

Queen Mary & Westfield College, Mile End Road, London E1 4NS, UK

Received: 19 October 1995 Accepted: 6 March 1996

The development and liberation mechanism of foliar gemmae have been studied by electron microscopy in twomosses, Tortula latifolia Bruch and Tortula papillosa Wils. The gemmae develop on the adaxial surface of matureleaves from single initial cells on both the lamina and costa in T. latifolia but only on the costa in T. papillosa.Elongation of the initial cell is associated with the deposition of a highly extensible new wall whilst the old wall andcuticle in the apical dome rupture. The first division is transverse and separates a short basal cell embedded in thefoliar tissue and a distal cell, or gemma primordium, protruding from the leaf surface. Subsequent divisions of thegemma primordium give rise to a six-to-eight-celled globose gemma with mucilaginous outer walls. During gemmadevelopment the basal cell produces a new wall and elongates again whilst the common wall with the gemma splitsapart centripetally along the boundary between the old and new wall in the basal cell ; plasmodesmal connections aregradually severed and eventually the young gemma remains connected to the basal cell only by mucilage. Afterseparation of the first-formed gemma, the basal cell may expand and produce a second gemma by the samemechanism. The whole process may be repeated several times resulting in the formation of a chain of gemmae stucktogether by mucilage and which are liberated only when the leaves are fully hydrated. Accumulation of abundant lipiddeposits in the gemmae after symplasmic isolation reflects considerable photosynthetic autonomy.

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Key words : Abscission, bryophytes, cell wall formation, plasmodesmata, vegetative reproduction.

INTRODUCTION

Development of new, physiologically independent plants byseparation of younger gametophyte sectors and}or re-generation from mature cells (Giles, 1971; Longton andMiles, 1982; Chopra and Kumra, 1988) are mechanismsessential for the maintenance and expansion of alreadyestablished bryophyte colonies. By contrast diaspores, i.e.biological units of dispersal, are needed for colonization ofnew habitats. Diaspore formation by the sporophyte usuallycovers only a fraction of the life cycle and, moreover, isseasonal and subject to severe ecological and physiologicalconstraints (Longton and Schuster, 1983; Mishler, 1988;Longton, 1990). For this reason reproduction by asexualdiaspores, produced more or less continuously by thegametophyte, is of utmost importance for population spreadin numerous bryophyte taxa (Longton and Schuster, 1983;Mishler, 1988).

Asexual diaspores in bryophytes range from caducous orfragile stems, leaves or perianths, often barely distinguish-able from normal vegetative organs, to highly specializedstructures such as bulbils, tubers and gemmae (Buch, 1911;Correns, 1899; Cavers, 1903; Schuster, 1966, 1984; Duckettand Ligrone, 1992). As initially pointed out by Correns(1899) and reviewed more recently by Duckett and Ligrone(1992), diaspore liberation in mosses may occur either by aschizolytic mechanism, i.e. detachment along cell walls, or a

lysigenic mechanism involving the rupture of a specializedabscission or tmema cell. In contrast, only the schizolyticmechanism has been reported in liverworts (Hughes,1971a, b ; Duckett and Ligrone, 1994).

Until very recently the cytological and physiologicalmechanisms underlying development, liberation and ger-mination of asexual diaspores in bryophytes have beenvirtually ignored. Studies of the mosses Calymperes (Duckettand Ligrone, 1991; Ligrone, Duckett and Egunyomi, 1992),Funaria (Bopp et al., 1991; Sawidis et al., 1991; Schnepf andSawidis, 1991; Schnepf, 1992) and Bryum (Goode et al.,1993) have revealed two basically different patterns oftmema cell (TC) formation and breakage. In Calymperes theTC originates by tip growth, whilst in Funaria and Bryum itis formed by unequal intercalary division. In Funaria andCalymperes a new wall is built beneath the original wall butwhilst in Funaria the TC breaks off by elongation andsubsequent lysis of the new wall, TC breakage in Calymperesresults from sliding apart of the old and new walls. Aspointed out in a recent survey of asexual diaspores in mosses(Duckett and Ligrone, 1992), these are but two examples ofan impressive variety of mechanisms that are still verypoorly understood.

Thus the aims of this paper are to provide the firstdocumentation of the ultrastructural events associated withschizolytic gemma formation and liberation in mosses andto compare these with the ontogeny and separation of

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306 Ligrone et al.—Foliar gemmae in Tortula

catenate foliar gemmae in liverworts. The selected species,Tortula papillosa and T. latifolia are both characterized bythe continuous copious production of foliar gemmae innature (Smith, 1978).

MATERIALS AND METHODS

Plants of Tortula latifolia were collected from Acer roots bythe River Mole, Boxhill, Surrey, UK, whilst the material ofT. papillosa was from Tilia trunks, Roscigno, Salerno, Italy.Gemmiferous leaves of different ages were selected and fixedwith 2% glutaraldehyde1% formaldehyde0±5% tannicacid in 0±05 Na-phosphate buffer, pH 7±0, for 2 h at roomtemperature, followed by 1% osmium tetroxide in the samebuffer, pH 6±8, overnight at 4 °C. The samples were thendehydrated through a graded series of ethanol to propyleneoxide and embedded in Spurr’s resin. Thin sections, cut witha diamond knife, were sequentially stained with 3%methanolic uranyl acetate and lead citrate. The periodicacid}thiocarbohydrazide}silver proteinate (PATAg) testwas performed according to Roland and Sandoz (1969) onsections collected on gold grids. Either periodic acid orthiocarbohydrazide treatment was omitted as controls. Theultrastructural observations were performed with a Jeol100C or a Philips CM12 electron microscope.

For scanning electron microscopy, specimens fixed asabove were dehydrated with ethanol, critical point dried,coated with a layer of gold about 20 nm thick and observedwith a Jeol JMS 35 scanning electron microscope.

OBSERVATIONS

The adaxial surface of mature leaves of both Tortula speciesbears numerous globular gemmae; these are restricted to thenerve in T. papillosa (Fig. 1A, C) or scattered on both themonolayered lamina and nerve in T. latifolia (Fig. 1B).Fully developed gemmae comprise six to eight cells withnumerous starch-containing chloroplasts (Fig. 1D).

Primary gemmae arise from mature photosynthetic leafcells. If present on the costa, these are symplasmicallyconnected to underlying food conducting cells (deuters).The entire sequence of development and liberation isillustrated in Fig. 7.

The first visible indication of the transformation ofmature leaf cells into gemma initials is a change in thedisposition of the chloroplasts (Fig. 1E, F). From apredominantly peripheral location along the periclinal wallsthese become randomly arranged with the consequentdisplacement of the central aggregation of vacuoles (Fig.2A). The initial cells expand outwards and breakage of theadaxial wall and overlying cuticle is associated with thedeposition of new wall material, initially in the apical dome(Fig. 2B, C) and subsequently throughout the cell (Fig.2D). As the initial cell grows the new wall expands whilstthe broken ends of the old wall are left behind (Fig. 2D).During this cellular expansion the nucleus migrates from thelower part of the cell to a more central position, whilst thechloroplasts rapidly increase in number from the four to six

in mature leaf cells. The first division produces a basal cellembedded in the leaf tissue and a distal cell, or gemmaprimordium, protruding from the leaf surface (Fig. 2E).The gemma primordium undergoes further expansion andthen divides by a slightly oblique or longitudinal septumforming two cells that in turn divide into three to four cells.Depending on the orientation of the first septum, thegemma is connected to the basal cell by either one or twocells. While proliferative divisions take place in thedeveloping gemma, the basal cell, initially rather short (Fig.2E), elongates markedly. Elongation involves depositionand subsequent expansion of a new wall layer, first at theupper corners of the cell (Fig. 3A, B, C), later all over thedistal wall, i.e. the wall common to the developing gemma(Fig. 3D).

When the basal cell has elongated by 3–6 µm, i.e. aboutone-third the original height of the initial cell, the distal wallbegins to split. Usually by this stage the gemma has not yetcompleted its development. Separation starts from themargins and proceeds centripetally along the boundarybetween the old and new wall of the basal cell (Figs 3D, Eand 4A). This is particularly evident in T. latifolia where themiddle lamella, i.e. the boundary between the gemma andbasal cell, is relatively clearly discernible (Fig. 4B, C).During separation a new wall layer is also deposited in thegemma cell(s) adjacent to the basal cell. Plasmodesmataconnecting the gemma to the basal cell are not obliteratedby the additional wall layer on either side of the septum(Fig. 4B) and persist until they are disrupted as a result ofthe splitting of the wall (Fig. 4C). Electron-opaque material,probably artifactual in origin, is visible occasionally in thecytoplasmic channel of the plasmodesmata (Fig. 4B). Beforeseparation is complete the last proliferative divisions occurwithin the gemma. Following liberation the old wall betweenthe gemma and the basal cell, i.e. the wall formed during thefirst division in the initial cell, is sloughed off and becomesmucilaginous (Fig. 4D).

The basal cell, now free from the original gemma (Fig.4E), continues growing and becomes the initial of a secondgemma. A new wall is soon deposited beneath the old outerwall which partially degenerates. Different from a primaryinitial, the outer wall is not invested by cuticle (Fig. 2A) andcontains remnants of plasmodesmata truncated during theseparation of the first-formed gemma (Fig. 4F). Duringcellular expansion the old wall is sloughed off from theunderlying new wall (Fig. 5A) and eventually disrupted.Subsequent development follows the same pattern asdescribed above, resulting in the formation of a secondgemma. The process can be repeated several times (Fig. 5B)thus producing a chain of gemmae stuck to each other bymucilage (Fig. 6A, B). The ends of the broken walls form aconcentric series surrounding the initial}basal cell (Fig.5B, C). PATAg staining reveals a distinct multilayeredstructure in the lateral walls of initial}basal cells (Fig. 5D),reflecting successive cycles of gemma formation. After anumber of cycles, usually three to six, the initial cell ceasesactivity. Inactive initials in T. latifolia may be lost with thelast-formed gemma, leaving a cavity on the surface of theleaf (Fig. 5E). Each cycle of gemma formation, except thefirst one, involves the deposition and subsequent rupture of


Ligrone et al.—Foliar gemmae in Tortula 307

F. 1. A–C, Scanning electron micrographs of the adaxial face of gemmiferous leaves in Tortula papillosa (A, C) and T. latifolia (B). The gemmaeare restricted to the costa in the former but are scattered throughout the surface in the latter. C, The rough surface of the gemmae of T. papillosa(at higher magnification) is due to the presence of investing mucilage. D, Transmission electron micrograph of a maturing gemma in T. latifolia.The arrowheads in (C) and (D) indicate the first-formed septum during proliferative divisions of the gemma primordium. E, F, Mature leaf cells

of T. latifolia and T. papillosa, respectively. Note the peripheral location of the chloroplasts (c) around the central vacuoles (v).



F. 2. Primary gemma development in Tortula latifolia. A, Mature superficial cell of the leaf costa becoming transformed into a gemma initial.The outer adaxial wall, covered with a cuticle (arrowheads) is bulging outwards and the chloroplasts (c) have lost their peripheral disposition.n, nucleus. B, At a slightly later stage in gemma development the old outer adaxial wall and cuticle have ruptured (arrowhead) and a new wallis being deposited underneath. n, Nucleus. C, Detail of (B) showing the broken cuticle (cu) and old wall (ow), and the expanding new wall (nw).D, Initial cell during elongation. Remnants of the old wall are visible (arrowheads) around the expanding dome. The nucleus (n) retains its basallocation. E, The first division of the gemma initial separates a short basal cell (bs) and a gemma primordium (gp) that swells markedly. Note the

much more numerous chloroplasts (c) than in mature leaf cells.

two walls, the first during the expansion of the initial cellpreceding division, the second during the expansionassociated with gemma liberation (Fig. 7). During the firstcycle, the first wall that is broken is the original wall of theleaf cell.

Nascent gemmae contain numerous chloroplasts with awell-developed thylakoid system but little or no starch (Figs

1D and 6A, B, C). After symplasmic isolation the gemmaeenter a maturation phase characterized by an initial cellularexpansion due to enlargement of the vacuolar system (Fig.6A). Subsequently the vacuoles reduce in size and abundantlipid reserves accumulate in the cytoplasm (Fig. 6B, C).Electron-opaque vacuolar deposits are sometimes present inmature gemmae of T. latifolia (Fig. 6D). During maturation



F. 3. Gemma liberation in Tortula papillosa. A, Detail of a basal cell (bc) showing the deposition of new wall material around its upper margins.The dotted lines indicate the boundaries between the original outer wall of the leaf cell (1), the second wall formed during expansion of the gemmainitial (2) and a third developing wall layer (3). g, Developing gemma. B, Basal cell which has started elongation prior to producing a secondgemma. The arrowheads indicate where the second wall layer has broken. C, Detail from (B) at higher magnification, showing the new expandinginner wall layer (3) and the broken old wall strata (1 and 2). D, Splitting of the wall (arrowheads) between the basal cell (bc) and gemma (g). nw,

New wall ; ow, old wall. E, Higher magnification from (D). nw, New wall ; ow, old wall.

brown pigmentation of the walls of the gemmae is associatedwith progressively increasing electron-opacity (Fig. 6B, C).Frequently the outer walls are sloughed off and converted

into mucilage whilst new wall layers are deposited insidethem (Fig. 6E). The mucilage maintains the attachment ofthe maturing gemmae to each other and to the parent leaves.



F. 4. Gemma liberation in Tortula latifolia. A, Splitting of the wall (arrows) between the basal cell (bc) and gemma (g). B, C, Details from (A)showing an uninterrupted plasmodesma in the mid region of the wall (B) and truncated plasmodesmata (arrowheads) along the splitting edge ofthe wall. ml, Middle lamella ; ow, old wall ; nw, new wall. D, Advanced stage in gemma liberation. Symplasmic connections have all been severedand the new walls (nw) in the basal cell (bc) and gemma (g) have thickened, whilst the old wall (ow) is becoming disorganized. E, Expanding basalcell after liberation of the first gemma. F, Detail of the outer wall of a basal cell at the same stage as shown in (E), PATAg staining. The olddegenerating wall contains remnants of plasmodesmata (arrowheads). The new expanding wall (nw) is less reactive than the old (ow) to the

PATAg staining.



F. 5. Development of secondary gemmae in Tortula latifolia. A, Fully expanded basal cell. The old wall, now mucilaginous (arrowheads) investsthe expanded new wall (nw). Arrows indicate plasmodesmata in the basal and lateral walls. B, A transverse division produces a new basal cell(bc) and a new gemma primordium (gp). The spindle-shaped nucleus (n) in the gemma primordium is about to undergo mitosis. C, D, Detailsfrom (B), showing a concentric series of broken walls. D, Detail of the lateral wall of a basal cell after PATAg-staining showing at least five distinct

strata. E, A cavity in the leaf surface produced by detachment of a basal cell.



F. 6. Maturation of gemmae in Tortula latifolia. A, Detail of young gemmae during their initial expansion. v, Vacuole ; c, chloroplast. Thearrowheads point to mucilage connecting sister gemmae. B, Maturing gemmae showing the accumulation of lipid (arrowheads) between thevacuoles and increased electron-opacity of the walls. C–E, Details of gemmae at an advanced stage of maturation. C, Abundant lipid accumulationand deposition of additional wall layers. D, Electron-opaque vacuolar deposits (arrowheads) and cytoplasmic lipid droplets. E, Detail from (C)showing a new wall layer (nw) deposited beneath the old wall (ow) that is becoming mucilaginous. The outermost mucilaginous layer (arrow)

derives from the expanded wall of the initial cell.



A B C

D E F

G H I

F. 7. Diagrammatic representation of gemma development andliberation in Tortula. Thick black lines indicate newly formed expandingwalls, and partial shading mucilaginous walls. The circle in the cellsrepresents the nucleus. A, Mature superficial cell of the leaf. B, Onsetof dedifferentiation and deposition of a new wall beneath the outerpericlinal wall. C, Extension of the new wall towards the base of thecell, during the onset of cellular expansion, and breakage of the old walland cuticle. D, Swelling of the initial cell, now completely surroundedby the new wall. E, Transverse division producing a basal cell and agemma primordium. The basal cell is becoming the initial of a secondgemma. F, Elongation of the basal cell associated with deposition of anew wall and breakage of the old wall. Expansion of the gemma and theonset of separation. G, Separation is complete. The oldest wall layersare now mucilaginous. Deposition of a new wall has started in theapical dome of the basal cell. H, Bulging of the new initial cell withexpansion of the new wall and disruption of the old. F, Formation ofa second gemma primordium. The first-formed gemma has been

omitted in (H) and (I).

DISCUSSION

The pattern of gemma formation and liberation in Tortulais a striking example of percurrent proliferation (Hughes,1971b) involving dedifferentiation of mature cells andsubsequent redifferentiation. As a mechanism of multipleformation and liberation of asexual diaspores, percurrentproliferation is common in fungi and algae but among landplants has been described only in mosses (Hughes, 1971b ;Wang, 1990; Duckett and Ligrone, 1992). As in protonemalgemmae in Funaria (Schnepf, 1992) and Calymperes(Ligrone et al., 1992), the elongation of the initial cell offoliar gemmae in Tortula involves the deposition andexpansion of a new wall combined with rupture of the oldwall. This is probably a consequence of the fact that the wallof the mature, fully differentiated cells whence the initialsarise, have very limited extensibility. A similar mechanismhas been observed during side branch formation fromprotonemal subapical cells in Funaria (Schmiedel and

Schnepf, 1979; Schnepf, 1982). In several other instances,e.g. the foliar gemmae in Calymperes (Ligrone et al., 1992)or in the liverwort Odontoschisma (Duckett and Ligrone,1995), the gemma initial is an undifferentiated cell andexpands and elongates without deposition of new layers ofwall material nor rupture of the original walls. During thededifferentiation phase the initial cell of gemmae in Tortulaproduces a new wall, then elongates and divides, whilstduring the short redifferentiation phase the newly producedwall is stabilized and becomes relatively rigid so that it isdisrupted during the following expansion cycle.

Because of the absence of a tmema cell, the foliar gemmaein Tortula are perhaps most appropriately referred to assessile gemmae. From first hand observations on over 20species in the Pottiales (Duckett, Matcham and Ligrone,unpubl. res.) it would appear that such gemmae are acharacteristic of this order in contrast to the closely alliedfamily, the Encalyptaceae, where liberation involves tmemacells. Elsewhere in mosses sessile foliar and}or protonemalgemmae are found in Diphyscium (Duckett, 1994), Mniaceae(Duckett and Ligrone 1994), Cryphaea, Leptodon, Homalia,Myrinia and Grimmiaceae and less commonly than thosewith tmema cells in the Dicranales and Orthotrichaceae.

The deposition of a new wall beneath the pre-exisiting oneplays a major role in the liberation of the gemma. Thisoccurs by schizolytic separation along a weak area at theboundary between the newly deposited wall and theoverlying wall in the basal cell. Separation is probablyinduced by expansion of both the basal cell and adjoininggemma cell(s) and seems not to involve extensive walldegradation as is the case in abscission and fruit maturationin higher plants (Sexton and Roberts, 1982; Zanchin et al.,1993, 1994).

The deposition of a new wall preceding separation of thegemma from the basal cell does not interrupt the plasmo-desmata in the common septum. In contrast severance ofplasmodesmata by deposition of a new wall layer has beenreported in stomatal guard cells (Wille and Lucas, 1984), incells adjoining tmema cells in Funaria protonemata (Schnepfand Sawidis, 1991; Schnepf, 1992) and in the symplasmicisolation of the initial cell of the subsequently multicellularendogenous gemmae in metzgerialean liverworts (Ligroneand Duckett, 1993). In Tortula the persistence of supposedlyfunctional plasmodesmata probably permits physiologicalinteraction until separation is complete and may perhaps beassociated with the gemmae of Tortula developing asdeterminate structures, i.e. becoming dormant at the eight-celled stage. In contrast in Metzgeria the gemmae continueto grow in situ forming juvenile thalli whilst still attached tothe parent plants. The symplasmic connection with food-conducting cells (Ligrone and Duckett, 1994) in the leafnerve may account for the particularly copious productionof gemmae in T. papillosa.

During maturation the gemmae undergo marked cyto-logical changes. The initial expansion, probably due towater uptake from the outside, facilitates the detachment ofthe gemma from the basal cell. The subsequent reduction inthe vacuolar system reflects dehydration preparatory todormancy. As a rule asexual diaspores of bryophytesaccumulate abundant reserves before detachment from the



parental plant, in the form of starch or lipid and protein, thelast two being typical of hornworts and Blasia, taxaassociated with nitrogen-fixing cyanobacteria (Verdus, 1978,1983; Ligrone and Lopes, 1989; Ligrone et al., 1992;Ligrone and Duckett, 1993; Duckett and Renzaglia, 1988).The gemmae of Tortula are unusual because they lackreserves immediately after severance of the symplasmicconnections with the plant but subsequently accumulateabundant lipid deposits. This indicates that during matu-ration the gemmae possess considerable photosyntheticactivity whose products are mainly converted into lipid.Although the foliar gemmae of Tortula and junger-mannialean liverworts are both produced in chains theyhave little else in common either developmentally or in themanner in which they are dispersed; they are yet anotherexample in the ever growing catalogue of developmentalanalogues found in bryophytes (Crandall-Stotler, 1984;Duckett and Renzaglia, 1988; Renzaglia and Duckett,1988).

Both in Tortula and in jungermannialean liverworts thegemmae develop by endogenous proliferative division(s) ofunicellular primordia formed exogenously by formativedivision of an initial cell. [For a detailed consideration offormative and proliferative divisions see Gunning (1982) ;the former, usually not definite in number, produceundifferentiated, but often determinate cells, the latter aredefinite in number and immediately precede the finaldifferentiation of tissues and organs.] However, whilst inTortula and other moss taxa the chains of gemmae arisefrom regular alternation of formative and proliferativedivisions, in jungermannialean liverworths an acropetalsequence of formative divisions of the initial cell produces abranched chain of gemma primordia that subsequentlyundergo an endogenous proliferative divison, or sometimesmore than one, in basipetal succession (Duckett andLigrone, 1995; Hughes, 1971a ; Schuster, 1966, 1984).Suppression of the proliferative division leads to theliberation of unicellular gemmae in certain taxa, e.g.Scapania (Schuster 1966, 1984). Conversely, inmetzgerialean liverworts the initial cell has no formativeactivity and after symplasmic isolation it divides endogen-ously producing an isolate multicellular gemma (Ligroneand Duckett, 1993).

In jungermannialean liverworts, where the original wallsof the gemma primordium remain intact, shallow de-tachment scars are visible on both gemmae and parent leafcells ; in Tortula, where the walls become mucilaginous andexpansion during maturation is more pronounced, thesescars are absent. Whereas in liverworts the walls of thematuring gemmae become firmly textured and waterrepellant, the increasingly mucilaginous walls in Tortulabecome progressively looser in texture and hydrophilic.These different properties almost certainly relate to theconditions under which the gemmae of the two groups areliberated and dispersed. In liverworts the foliar gemmae,which are exposed at all times, may be dispersed eitherfloating on water films under wet conditions, or by windwhen the plants are dry. In Tortula gemma liberation anddispersal occurs only when the plants are fully hydratedsince in the dry state appression and incurving of the leaves

(Smith, 1978) shuts off their gemma-producing adaxialsurfaces. It is also noteworthy that gemmae adhesion to newsubstrata will be maximal when the investitive of mucilageis fully hydrated.

Mature gemmae of both Tortula latifolia and T. papillosacan survive drought for several months in nature and atleast 2 years in laboratory and germinate to produceprotonemata within 48 h after rehydration (Duckett andLigrone, 1992). These are properties shared with theprotonemal brood cells in a further pottialean genus, Aloina(Goode et al., 1994), both kinds of diaspores possessingthick multistratose walls and abundant lipid reserves.Extreme resistance to drought, immediate germination,abundant lipid reserves and continuous productionthroughout the vegetative season, whenever the gameto-phyte is fully hydrated, indicate that the gemmae of Tortulaare highly effective propagules for rapid and successfulcolonization of new habitats.

ACKNOWLEDGEMENTS

This study was supported by CNR as a part of a BilateralResearch Project Italy}United Kingdom. R. Ligrone thanksQueen Mary & Westfield College for laboratory facilitiesduring his sabbatical leave in 1992–3. The observations werein part performed at the CIRVB (University of Naples‘‘Federico II ’’, Italy).

LITERATURE CITED

Bopp M, Quader H, Thoni C, Sawidis T, Schnepf E. 1991. Filament

disruption in Funaria protonemata: formation and disintegration

of tmema cells. Journal of Plant Physiology 137 : 273–284.

Buch H. 1911. UX ber die Brutorgane der Lebermoose. Helsingfors :

J. Simelii Arvingars Boktryckeriaktiebolag.

Cavers F. 1903. On asexual reproduction and regeneration in Hepaticae.

New Phytologist 2 : 121–133, 155–165.

Chopra RN, Kumra PK. 1988. Biology of bryophytes. New Delhi : Wiley

& Sons.

Correns C. 1899. Untersuchungen uX ber die Vermehrung der Laubmoose

durch Brutorgane und Stecklinge. Jena: G. Fisher.

Crandell-Stotler B. 1984. Musci, hepatics and anthocerotes—an essay

on analogues. In: Schuster RM, ed. New manual of bryology Vol.

2. Nichinan, Japan: Hattori Botanical Laboratory, 1093–1129.

Duckett JG. 1994. Studies of protonemal morphogenesis in mosses. V.

Diphyscium foliosum. (Hedw). Mohr (Buxbaumiales). Journal of

Bryology 18 : 223–238.

Duckett JG, Ligrone R. 1991. Gemma germination and morphogenesis

of a highly differentiated gemmiferous protonema in the tropical

moss Calymperes (Calymperaceae, Musci). Cryptogamic Botany

2/3 : 219–228.

Duckett JG, Ligrone R. 1992. A survey of diaspore liberation

mechanisms and germination patterns in mosses. Journal of

Bryology 17 : 335–354.

Duckett JG, Ligrone R. 1994. Studies of protonemal morphogenesis in

mosses. III. The perennial gemmiferous protonema of Rhizomnium

punctatum (Hedw). Kop. Journal of Bryology 18 : 13–26.

Duckett JG, Ligrone R. 1995. The formation of catenate foliar gemmae

and the origin of oil bodies in the liverwort Odontoschisma

denudatum (Mart.) Dum. (Jungermanniales) : a light and electron

microscope study. Annals of Botany 76 : 405–419.

Duckett JG, Renzaglia KS. 1988. Cell and molecular biology of

bryophytes : ultimate limits to the resolution of phylogenetic



problems. In: Newton ME, Wanstall PJ, eds. Bryology : modernresearch and ways forward. Botanical Journal of the LinneanSociety 98 : 225–246.

Giles KL. 1971. Dedifferentiation and regeneration in bryophytes : aselective review. New Zealand Journal of Botany 9 : 689–694.

Goode JA, Alfano F, Stead AD, Duckett JG. 1993. The formation ofaplastidic abscission (Tmema) cells and protonemal disruption inthe moss Bryum tenuisetum Limpr. is associated with transversearrays of microtubules and microfilaments. Protoplasma 174 :158–172.

Goode JA, Stead AD, Ligrone R, Duckett JG. 1994. Studies ofprotonemal morphogenesis in mosses. IV. Aloina (Pottiales).Journal of Bryology 18 : 27–41.

Gunning BES. 1982. The root of the water fern Azolla–cellular basis ofdevelopment and multiple roles of cortical microtubules. In:Subtelny S, ed. De�elopmental order : its origin and regulation.Symposium for the Society of De�elopmental Biology 40 : 379–422.New York: AR Liss.

Hughes SJ. 1971a. On conidia of fungi, and gemmae of algae,bryophytes, and pteridophytes. Canadian Journal of Botany 49 :1319–1339.

Hughes SJ. 1971b. Percurrent proliferations in fungi, algae and mosses.Canadian Journal of Botany 49 : 215–231.

Ligrone R, Duckett JG. 1993. Formation of endogenous gemmae in thesimple thalloid liverworts Metzgeria and Riccardia (Metzgeriales).Giornale Botanico Italiano 127 : 328–330.

Ligrone R, Duckett JG. 1994. Cytoplasmic polarity and endoplasmicmicrotubules associated with the nucleus and organelles areubiquitous features of food-conducting cells in bryoid mosses(Bryophyta). New Phytologist 127 : 601–614.

Ligrone R, Duckett JG, Egunyomi A. 1992. Foliar and protonemalgemmae in the tropical moss Calymperes (Calymperaceae) : anultrastructural study. Cryptogamic Botany 2 : 317–329.

Ligrone R, Lopes C. 1989. Ultrastructure, development and cyto-chemistry of storage cells in the ‘tubers ’ of Phaeoceros lae�isProsk. (Anthocerotophyta). New Phytologist 112 : 317–325.

Longton RE. 1990. Sexual reproduction in bryophytes in relation tophysical factors of the environment. In: Chopra RN, Bhatla SC,eds. Bryophyte de�elopment : physiology and biochemistry. BocaRaton, USA: CRC Press, 139–166.

Longton RE, Miles CJ. 1982. Studies on the reproductive biology ofmosses. Journal of the Hattori Botanical Laboratory 52 : 219–240.

Longton RE, Schuster RM. 1983. Reproductive biology. In: SchusterRM, ed. New manual of bryology Vol. 1. Nichinan, Japan: HattoriBotanical Laboratory, 386–462.

Mishler BD. 1988. Reproductive ecology of bryophytes. In: LovettDoust J, Lovett Doust L, eds. Plant reproducti�e ecology : patternsand strategies. New York: Oxford University Press, 285–305.

Renzaglia KS, Duckett JG. 1988. Different developmental processesunderlie spermatozoid architecture in mosses, hepatics andhornworts. Journal of the Hattori Botanical Laboratory 64 :219–235.

Roland JC, Sandoz D. 1969. De! tection cytochimique des sites deformation des polysaccharides pre! -membranaires dans les cellulesve! ge! tales. Journal de Microscopie 8 : 263–268.

Sawidis T, Quader H, Bopp M, Schnepf E. 1991. Presence and absenceof the preprophase band in moss protonemata: a clue tounderstanding its function. Protoplasma 163 : 156–161.

Schmiedel G, Schnepf E. 1979. Side branch formation and orientationin the caulonema of the moss, Funaria hygrometrica : normaldevelopment and fine structure. Protoplasma 100 : 367–383.

Schnepf E. 1982. Morphogenesis in moss protonemata. In: Lloyd CW,ed. The cytoskeleton in plant growth and de�elopment. London:Academic Press, 321–344.

Schnepf E. 1992. Structure and development of tmema cells inprotonemata of Funaria hygrometrica (Bryophyta). CryptogamicBotany 3 : 35–39.

Schnepf E, Sawidis T. 1991. Filament disruption in Funariaprotonemata: occlusion of plasmodesmata. Botanica Acta 104 :98–102.

Schuster RM. 1966. The Hepaticae and Anthocerotae of North AmericaVol. 1. New York: Columbia University Press.

Schuster RM. 1984. Comparative anatomy and morphology of theHepaticae. In: Schuster RM, ed. New manual of bryology Vol. 2.Nichinan, Japan: Hattori Botanical Laboratory, 760–891.

Sexton R, Roberts JA. 1982. Cell biology of abscission. Annual Re�iewof Plant Physiology 33 : 133–162.

Smith AJE. 1978. The moss flora of Britain and Ireland. Cambridge:Cambridge University Press.

Verdus MC. 1978. E! tude ultrastructurale des propagules de Campylopusintroflexus (Hedw.) Brid. (Bryopsida, Dicranales). Bulletin de laSocieteU botanique de France 31 : 33–40.

Verdus MC. 1983. Ultrastructure des propagules protonematiques deDicranoweisia cirrata (Hedw.) Lindb. Journal of the HattoriBotanical Laboratory 54 : 95–105.

Wang CJK. 1990. Ultrastructure of percurrently proliferating conidio-genous cells and classification. Studies in Mycology 32 : 49–64.

Wille AC, Lucas WJ. 1984. Ultrastructural and histochemical studieson guard cells. Planta 160 : 129–142.

Zanchin A, Bonghi C, Casadoro G, Ramina A, Rascio N. 1993.

Abscission in leaf and fruit explants of Prunus persica (L.) Batsch.New Phytologist 123 : 555–565.

Zanchin A, Bonghi C, Casadoro G, Ramina A, Rascio N. 1994. Cellenlargement and cell separation during peach fruit development.International Journal of Plant Science 155 : 49–56.


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