sábado, 20 de marzo de 2010

Meristem fate and bulbil formation in Titanotrichum (Gesneriaceae)

Titanotrichum oldhamii (a monotypic genus from Taiwan, Okinawa, and
adjacent regions of China) has inflorescences bearing either showy
yellow flowers or asexual bulbils. Asexual reproduction by bulbils is
important in natural populations, and bulbil production increases in
August and September at the end of the flowering season (which runs
from June to the end of September). The bulbils are small (1–2.5 mm
long) and numerous. They consist of a small portion of stem
(bract-stem) topped by opposite storage bracts that enclose a minute
apical meristem. A secondary root develops from the side of the
bract-stem. The floral meristem of T. oldhamii has three possible
fates: (1) bulbil formation, (2) flower formation, or (3) bracteose
proliferation. Bracteose proliferation rarely occurs and appears to be
a developmental transition between the bulbiliferous and racemose
inflorescence forms. It is strongly reminiscent of the floricaula and
squamosa mutants of Antirrhinum. In the bulbiliferous form a single
floral primordium, which would normally produce one flower, gives rise
to 50–70 bulbils by repeated subdivision of the meristem. This form of
bulbil production appears to be unique to Titanotrichum. Occasionally
a floral meristem divides, but the subdivision forms multiflowered
units of up to four flowers rather than bulbils, suggesting that
meristem fate is reversible up to the first or second meristem
subdivision. In Titanotrichum, therefore, primordium fate is
apparently not determined at inception but becomes irreversibly
determined shortly after the appearance of developmental
characteristics of the floral or bulbil pathway.

Key Words: bracteose proliferation • bulbil • China • floral meristem
• floricaula • gemmae • Gesneriaceae • Japan • squamosa • Taiwan •
Titanotrichum oldhamii • vivipary
Titanotrichum oldhamii Soler. (Gesneriaceae) was first discovered in
1864 by Richard Oldham, collecting for the Royal Botanic Gardens Kew,
during his trip to Formosa (now Taiwan) (Hemsley, 1890 , 1895 ;
Solereder, 1909 ; Sealy, 1949 ). Titanotrichum oldhamii was
cultivated in Europe as an ornamental for its distinctively deep
yellow corolla tube with lobes blotched dark crimson-brown. The
inflorescence of T. oldhamii is an indeterminate raceme, although the
family Gesneriaceae, to which it belongs, usually produces pair-flower
cymes (Weber, 1973 , 1978 , 1982 , 1995 ; Pan et al., 2002 ).
It grows in shaded habitats along creeks, particularly on dripping
cliffs or moist limestone slopes in dense forest and on rocks near
caves and waterfalls. It is not a common plant but has a scattered
distribution in Taiwan, the Fujien province of China, and the Ryukyu
Islands of Japan (Henry, 1898 ; Hayata, 1908 , 1911 ; Hemsley, 1909
; Walker, 1976 ; Wang et al., 1998 ). Interestingly, although it
produces many flowers in the wild, it rarely sets seed and appears to
rely largely on asexual reproduction by bulbils and rhizomes. Genetic
variation and the failure of seed set are being studied at Edinburgh
(C.-N. Wang, unpublished data).
Gesneriaceae species are known for their great range of morphological
variation, resulting from variation in meristem behavior (Jong and
Burtt, 1975 ; Möller and Cronk, 2001 ). While in most Gesneriaceae
the unusual meristem behavior affects only vegetative parts (Burtt,
1970 ; Tsukaya, 1997 ; Imaichi et al., 2000 ), Titanotrichum is
unusual in having variable meristem behavior in reproductive parts.
There are many plants in which all or some flowers of an inflorescence
are converted into asexual bulbils. In most cases, a single floral
meristem is replaced by a single bulbil (e.g., Polygonum viviparum L.,
Ranunculus ficaria L., Saxifraga cernua L., Allium spp., Festuca
vivipara (Rosenv.) E. B. Alexeev.; Kerner, 1904 ; Troll, 1964 ;
Engell, 1973 ; Arizaga and Ezcurra, 1995 ; Briggs and Walters, 1997
; Diggle, 1997 ). In Titanotrichum however, a single floral meristem
is replaced by a cluster of 50–70 bulbils (Stapf, 1911 ; Hayata, 1912
). In Mimulus gemmiparus W. A. Weber, it is not the floral meristem
but the adjacent proximal meristem (dormant in other species of
Mimulus) that develops into a bulbil (Weber, 1972 ; Moody et al.,
1999 ). Pseudovivipary, often found in alpine or arctic habitats, is
often assumed to be an adaptation to poor sexual reproduction under
extreme conditions (Kerner, 1904 ; Youngner, 1960 ). In contrast,
Titanotrichum grows in a subtropical area with a favorable
environment, although sometimes in deep shade.
As part of a wider study of reproduction in this species, the
morphology of bulbil development was investigated. Titanotrichum is
unique in producing large numbers of bulbils in place of a single
flower. We were therefore interested in answering the following
questions: (1) how a single floral meristem is replaced with numerous
bulbil meristems, (2) how an inflorescence changes from flower to
bulbil production, and (3) how bulbils differ from seeds as functional
reproductive units.
Source of plant material and growth conditions
We investigated 26 natural populations of Titanotrichum from Taiwan,
China, and the Okinawa Islands of Japan during the summer of 1999 and
2000. The 145 accessions of living material collected from these
locations were first cultivated at the Institute of Botany, Academia
Sinica, Taipei, and then moved to the Royal Botanic Garden, Edinburgh,
where they were grown between 18°C (night) and 20°C (day) in a
controlled climate glasshouse.
Because Titanotrichum rarely produces seed, mature seeds were obtained
from a pollination experiment in Yangmingshan National Park (25°09' N,
121°33' E), Taipei region, during the summer of 1999. Seed germination
requires light and was carried out under constant lighting in petri
dishes at 22°C and 90% relative humidity in controlled environment
growth cabinets, on wet filter paper. Growth experiments were
conducted in walk-in growth rooms manufactured by Swann Technology
(Royston, UK) with controllable temperature and daylength. Lighting
was provided by 13-W cool white fluorescent tubes.
Fixation of plant tissue
Different stages of the inflorescence shoot, seedlings, and
germinating bulbils were fixed overnight in FAA (18 parts of 70%
ethanol : 1 part glacial acetic acid : 1 part formalin) and taken
through an ethanol series to 100% acetone dehydration before
proceeding to critical point drying (CPD) with an Emitech K850 machine
(Ashford, UK). The dried samples were immediately mounted on aluminium
stubs using carbon discs and coated twice with gold palladium for 2
min (from different angles) in an Emscope SC500 sputter coater (Quorum
Technologies, Newhaven, UK). To see the development of the meristem
clearly, most bracts and bracteoles were removed, especially in the
young inflorescence, using fine forceps either before fixation or,
less satisfactorily, after CPD.
Scanning electron microscopy
Specimens were examined with a Zeiss DSM scanning electron microscope
(Oberkochen, Germany) at a working distance of between 9 and 14 mm and
an accelerating voltage of 5 kV.


Distribution of flowers and bulbils on inflorescences, in individuals,
and in populations
The inflorescence of Titanotrichum oldhamii is basically racemose,
with spirally arranged bracts, each subtending a single axillary
flower with two bracteoles (Figs. 1, 2A). Occasionally inflorescence
branches or multiflowered units of up to four flowers (each with two
bracteoles) may arise at some nodes (from serial multiple buds in the
axil of the same bract). Titanotrichum produces normal racemose
inflorescences of this type during the summer, but at the end of the
season (i.e., the end of August), the upper part of the raceme starts
to convert to the production of bulbils. Bulbil clusters, bulbil
clusters around flowers, or new bulbil-bearing inflorescence branches
are formed in the axils of the bracts in the place of single flowers.
Three different types of inflorescence can be seen at this stage: (1)
bulbils and flowers mixed, (2) bulbils only, and (3) bracteose
proliferation (consisting of repeated production of bracts rather than
flowers or bulbils) with some flowers (Fig. 2B–C). In addition, bulbil
clusters also proliferate in the axils of existing flowers in the
lower part of the inflorescence (Fig. 2D). Within 2 or 3 wk, tens of
thousands of bulbils may fall from one individual and are ready to
grow. Production of different inflorescence types appears to be under
environmental rather than genetic control, because it may vary on the
same individual from year to year. Most individuals, both in the field
and glasshouse, start with flowering inflorescences but end up
converting to bulbil production and initiating new bulbil
inflorescences. Juvenile plants (i.e., 1 yr old) growing in dense
shade are an exception, as they produce only bulbils during the
flowering season.
Development of the inflorescence
Titanotrichum oldhamii is a persistent rhizomatous herb. Several
shoots can arise from the rhizome, and during early vegetative growth,
a pair of two unequal leaves is produced at each node, resulting in a
decussate phyllotaxy typical of the Gesneriaceae and other Lamiales
such as Antirrhinum (Carpenter et al., 1995 ; Vincent et al., 1995
). When it enters the reproductive phase, it converts to spiral
phyllotaxy, in which a single "floral" meristem initiates at each
node, with a single bract. In most related plants, such as
Antirrhinum, these floral primordia would develop straightforwardly
into flowers with whorls of floral organs arising from the meristems
sequentially (e.g., Bradley et al., 1996a ). However, in
Titanotrichum the developmental fate of these meristems is labile,
changing during the season. Three different fates can be observed at
the apex of the inflorescence (Fig. 3): (1) flower formation (Fig.
3B), (2) bulbil formation (Fig. 3E), and (3) bracteose proliferation
(Fig. 3H). Transitional states and reversals are also seen, suggesting
that the meristems are uncommitted in very early development.

When flowers are to be formed, the shoot apex elongates and
well-spaced floral primordia are initiated (Fig. 3A, B). The
"pentagon-shaped" primordium appears at node 10–12 and indicates
pentamerous organ-whorl development and hence flower induction (Fig.
3B). The terminology of floral stages used here follows that used for
Antirrhinum (Carpenter et al., 1995 ). If meristems switch to bulbil
production and bracteose proliferation, shoot apex organogenesis
appears more compressed. Bulbil primordia are distinguishable from
true floral primordia shortly after the "loaf" stage (node 5–7) (Fig.
3C, F, I), as the "pentagon" stage does not form. Instead, in bulbil
development, three subsidiary meristems form (node 9–10) (Fig. 4E, F:
m1–m3). In bracteose proliferation, more than two bract primordia
initiate (Fig. 4I–L, + ß).

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Fig. 4. Scanning electron micrographs of the developing floral
meristems. (A–D) Flower formation; (E–H) bulbil cluster formation;
(I–L) bracteose proliferation. Abbreviations: FM = the primary floral
meristem, Se = sepals, Br = subtending bract, , ß, = bracteoles
(first, second, and third pairs, respectively). In the production of
bulbil clusters, the floral meristem has been divided into terminal
and three subsidiary meristems, which are denoted by TM, M1, M2, and
M3. See text for explanation. Bars = 100 µm. (M–X) Later stages of
developing floral meristems. (M–P) Flower formation; (Q–T) bulbil
proliferation; (U–X) bracteose proliferation. Abbreviations: C =
petals, S = stamen, St = staminode, G = gynoecium. In bulbil cluster
formation, the terminal (TM) and three subsidiary meristems (M1–M3),
eventually form four major primordia (P0–P3) for clusters of bulbils.
In bracteose proliferation, a fourth pair of bracteoles are formed (),
in addition to , ß, and . Bars = 100 µm

Floral development
When the floral meristem enters the floral development pathway, the
primordium is at first laterally elongated (Fig. 3C). It then produces
two opposite bracteoles in succession, which remain slightly unequal
in size (Fig. 4A). The floral apex then becomes pentagonal, and all
the sepals are initiated synchronously, although the abaxial two are
somewhat larger (Fig. 4B–D). Later, the five petal primordia are
initiated nearly synchronously, alternating with the sepals (Fig. 4M).
The four functional stamen initials appear at almost the same time as
the petal primordia (the single staminode arises later) (Fig. 4N–P).
Development of bulbil clusters and the phenomenon of bracteose proliferation
The floral meristems of T. oldhamii can apparently convert to the
production of bulbil primordia or into multibract units immediately
after their two lateral bracteoles initiate (Fig. 4I, K). When primary
meristems enter the bracteole-producing developmental pathway, the two
bracteoles continue to enlarge, and the meristems continue to produce
more bracteoles (Fig. 4L, U–X). This phenomenon we call "bracteose
proliferation," and it does not lead to the production of any
reproductive units. Bracteose proliferation appears to be an
intermediate state between pathways for flower and bulbil production,
as it entails production of bracts like those associated with flowers,
but proliferation of units similar to that associated with bulbil
production. In addition, bracteose proliferation usually occurs
temporally between flower and bulbil production.
In contrast, the initiation of bulbils is more complicated. After the
two bracteoles develop, three subsidiary meristems arise laterally to
the primary meristem in the axils of the bract and bracteoles (Fig.
4F, G). Then all the meristems proliferate (two new meristems arise on
the flanks of existing meristems repeatedly) to generate the numerous
bulbil primordia (Fig. 4H, Q–S). Thus, each floral meristem might give
rise eventually to 50–70 bulbils (Fig. 4T). Bulbils can also arise
from new meristems formed in the axils of bracts and bracteoles as
well as by proliferation of the main axillary meristem.
It is possible to find mixed conditions in which flowers and bulbils
have both arisen from the same meristem (Fig. 5), indicating that
meristems are not committed to a single pathway at initiation. One to
four flowers with associated surrounding bulbils may arise from a
single floral meristem (Fig. 5C–F). These multiflowered units suggest
that flowers form after the development of multiple meristems
characteristic of the bulbil developmental pathway, and therefore that
the bulbil developmental pathway is alterable to the floral pathway,
at least at an early stage of development.
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Fig. 5. (A–F) Flowers and bulbil clusters within the same floral
meristem. Up to four flowers (F1–F4) may initiate with bulbils (Bul)
surrounding them. Bars = 200 µm. See Fig. 4 for meaning of other

The inflorescence of Titanotrichum therefore varies between a simple
raceme and a more complicated structure with multiple axillary
meristems and inflorescence branches.
Germination of seeds and bulbils
The seeds of Titanotrichum are minute (0.6 mm long, 0.15 mm wide),
narrowly ovate to spindle-shaped, with the seed coat shrunken into
folds around the embryo (Fig. 6A). Seeds germinate in 7–10(–14) d at
22°C under constant climatic conditions. The germination rate is very
variable but is usually about 75%. With the elongation of the
hypocotyl, the radicle normally emerges through the micropylar region
7–8 d after sowing (Fig. 6D). Thereafter, the hypocotyl continues to
elongate, and a ring of rhizoids is formed at the base of the
hypocotyl. These rhizoids probably assist in water absorption before
the primary root develops and serve to anchor the seedling (Fig. 6B,
C). At 2 wk the cotyledons are fully expanded and green. Many Old
World Gesneriaceae show accrescent growth of one cotyledon
(anisocotyly). In Titanotrichum most of the seedlings expand their
cotyledons at the same rate during their growth, although some
(20–40%) had slightly unequal expansion at a very early stage of
germination, apparently due to an initial difference in cotyledon
size. True anisocotyly shows accrescence in one cotyledon after
initial cotyledon expansion, due to the formation of a basal meristem
in one cotyledon. This does not appear to happen in Titanotrichum,
which is therefore strictly isocotylous. After cotyledon expansion,
the primary root elongates and the first pair of true leaves is
initiated (Fig. 6E). Although the adult plant is densely covered with
multicellular hairs, the seedling has a few glandular hairs only.
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Fig. 6. The process of seed (A–E) and bulbil (F–J) germination.
Abbreviations: Cot = cotyledons, Hc = hypocotyl, B = bracts, BS =
bract stem, sR = bulbil root, L = bulbil leaves, I = bulbil internode,
and AM = apical meristem. Bars = 200 µm

Compared to seeds, bulbils "germinate" very easily, taking 1 wk and,
unlike seedlings, can live for 1–2 mo on wet filter paper without
nutrients. The bulbil germination rate is higher than that of seeds,
at 95%.
Bulbil germination in Titanotrichum is somewhat different to that of
seedlings. Each bulbil has two "storage" bracts and oil bodies are
visible in this tissue as droplets within the cells (in cross section
under the light microscope). These bracts form a V-shape at the top of
a short "bract stem" (Fig. 6F). In comparison to the seed, it is
relatively large (1.5 mm long, 0.5 mm wide). When a bulbil is about to
germinate, it forms a ring of rhizoids to take up water (like those in
true seedlings) (Fig. 6G, H). Then, on the side of the bract stem, a
root primordium begins to initiate (Fig. 6H). Furthermore, a first
pair of leaves ("bulbil leaves") start to develop between the two
storage bracts (Fig. 6I). The bulbil leaves continue to grow on an
elongating "bulbil internode" (Fig. 6I). A second pair of leaves
arises from the apical meristem between the bulbil leaves 1 wk after
the start of germination (Figs. 6J, 7).
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Fig. 7. A bulbil-germinated "seedling." The remains of the V-shaped
bulbil can be seen at the base

Environmental control
In the field, bulbil production of Titanotrichum begins at the end of
summer, apparently when daylength begins to shorten. Around the end of
August, daylength in its native habitat declines slowly to <12 h
(eventually to 10 h on the shortest day of the year). The mean daily
temperature falls too, typically from 30°C to 22°C, but seldom drops
below 20°C. To investigate the control of bulbil production further we
made observations on 4–5 individuals of each of six clones (from five
populations) grown under controlled conditions. In every case when
offspring from the same genotype were placed into different
daylength/temperature growth cabinets, plants in long daylength
conditions and low temperature (16 h daylight and constant temperature
at 18°C) had slowed floral development but no inhibition of the
initiation and development of bulbil inflorescences. Individuals in
artificial long day conditions but moderate temperature (16 h daylight
and 23°C) reduced production of bulbiliferous inflorescences, and
flowering inflorescences predominated. In short days, flowers are not
produced, but bulbils are produced vigorously at both temperatures (8
h daylight).

Plasticity of meristem behavior
Titanotrichum has inflorescence meristems that can revert to
vegetative growth (bulbil formation and bracteose proliferation) (Fig.
8). Moreover, many individuals can produce bulbil-only inflorescences
while other inflorescences are still flowering. Occasionally,
individuals may have their inflorescences transformed from flower
production (with flowers at the base) to the production of bulbil
primordia or bracteose proliferation (sometimes the multibracteole
units may produce enlarged bracts or even leaves) and then revert back
to flowering again at the top. This variation suggests that after
inflorescence induction, the inflorescence meristem of Titanotrichum
is constantly regulated by the interaction of genetic and
environmental signals.
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Fig. 8. Meristem fate during development in three different
pathways: flower formation, bulbil proliferation, and bracteose
proliferation. Pale shading indicates bracts, darker shading
meristems. See Fig. 4 for meaning of abbreviations

The floral and bulbil meristems are indistinguishable up to the end of
the loaf stage (Fig. 3C, F, I). Apparently, the meristems are
uncommitted at this early stage and are developmentally plastic when
formed. There seems to be a directional phase change in the fate of
primordia within the inflorescence: flowers form at the beginning of
the flowering season, then bulbil formation replaces flowers at the
top of the inflorescence. Bulbils are also produced from the axillary
meristems in the bracts and bracteoles of existing flowers. The
existence of multiflower units, formed after the multiple meristems
have developed at the start of the bulbil pathway, suggests that the
meristems are not irrevocably committed at this stage and can revert
back to flower formation. Occasionally, bracteose proliferation
occurs, in which multiple bracteoles form in a whorl surrounding the
undifferentiated floral meristem.
The meristem plasticity of Titanotrichum is perhaps unsurprising
because the Gesneriaceae as a whole displays unusually variable
meristem behavior. Some genera of the Gesneriaceae, such as
Streptocarpus (Jong and Burtt, 1975 ; Möller and Cronk, 2001 ), vary
enormously in basic morphology. Three major growth forms occur in
Streptocarpus: caulescent, unifoliate, and rosulate (Jong and Burtt,
1975 ). Unifoliates have no shoot apical meristem. Instead, they have
a single cotyledon with a basal meristem and a separate meristem in
the midrib. The variable behavior of the vegetative meristem in
Streptocarpus is uncoupled from that of the reproductive meristems,
however. Reproductive meristems remain unchanged, producing normal
pair-flower cymes like other members of the Gesneriaceae.
Developmental switches and meristem transitions
Developmental and genetic studies on meristem behavior in mutants of
Antirrhinum and Arabidopsis provide cases analogous to that in
Titanotrichum. For instance, the squamosa (squa) mutant of Antirrhinum
majus L. is characterized by excessive formation of bracts and the
production of fewer and deformed flowers (Huijser et al., 1992 ).
Similarly, the floricaula (flo) mutant of Antirrhinum, homologous to
the leafy (lfy) mutant of Arabidopsis, produces indeterminate shoots
bearing further bracts (instead of flowers) in the axils of bracts
(Coen et al., 1990 ). These phenotypes combined (as in the flo/squa
double mutant) are similar to the bracteose proliferation form in
Titanotrichum. The development of the floral meristem in the squa or
flo mutant is similar to the wild type until the loaf stage, but the
meristem then fails to form sepals in a whorl. Instead, bracteole
primordia form at the end of the loaf structure. This meristem may
give rise to an indeterminate inflorescence with a spiral array of
bracteoles (flo) or remain with two lateral bracteoles plus two
ventral primordia without floral parts (squa).
Because these phenotypes are artificial mutations, they are not
developmentally plastic as in Titanotrichum. Nevertheless, the
similarity of developmental stages in both flo and squa with the
bracteose proliferation form of Titanotrichum is striking (Figs. 4X,
8). Thus Gesner-FLO and Gesner-SQUA may be candidate genes for the
regulation of the bracteose proliferation phenotype in Titanotrichum.
The cluster of bulbil primordia produced at one floral meristem can be
likened to a compressed inflorescence side branch (Fig. 4G). Again the
Gesner-FLO gene may play a role in this because FLO promotes
transitions between floral and vegetative (branching) phases.
Moreover, the TERMINAL FLOWER-1 (TFL-1) gene of Arabidopsis (Araki,
2001 ) and the homologous CENTRORADIALIS (CEN) gene of Antirrhinum
are known to influence whether the inflorescence is determinate or
indeterminate (Bradley et al., 1996b ). Overexpression of TFL-1 in
Arabidopsis results in a prolonged vegetative phase and a highly
branched inflorescence (Ratcliffe et al., 1998 ; Schmitz and Theres,
1999 ). Similarly, work on meristem reversion of Impatiens suggests
that FIMBRIATA (FIM) affects the formation of the whorled phyllotaxy
and defines the boundaries of different organ-identity genes (Pouteau
et al., 1998a ). Environmental changes can cause the Impatiens
balsamina L. flower axis to revert back to a vegetative meristem,
resulting in deformed flowers and leaves (bracts) (Pouteau et al.,
1997 , 1998b ). Floral meristems in Impatiens can therefore also
adopt different fates.
Bulbil formation is scattered widely in angiosperms. Many species,
such as Saxifraga cernua (Saxifragaceae), Ranunculus ficaria
(Ranunculaceae), and Remusatia vivipara Schott (Araceae) share with
Titanotrichum the ability to initiate bulbils in place of the floral
meristem (Kerner, 1904 ). Mimulus gemmiparus too, although it
produces its propagules from lateral meristems (the distal axillary
bud adjacent to the floral bud), has an essentially similar pattern of
development (Moody et al., 1999 ). Thus there may be an analogous
developmental switch common to bulbil formation in diverse species.
Titanotrichum is unusual in that this developmental switch
incorporates successive meristem divisions to produce numerous bulbils
from one primordium. Nothing comparable to this is found elsewhere in
Similarity between bulbils and seedlings
With the obvious exception of the two prominent bracts, the
Titanotrichum V-shaped bulbil possesses a number of similarities to
the seeds. On "germination," a pair of bulbil leaves arises on an
elongated bulbil-internode (Fig. 6I). Root initiation in the bulbil is
secondary (the root primordium grows endogenously from the side of the
bract stem). On the other hand, the seed germinates with a true
radicle (primary root), which is persistent in Titanotrichum, although
the development of a secondary root seedling, after primary root
abortion, is common in many other Old World Gesneriaceae species (Fig.
6D and E). There is no "anisocotyly" in bulbil germination, the bract
and leaf pairs produced on germination being equal. Wang et al. (2002)
recently observed seedlings from two individuals of T. oldhamii and
concluded that it is anisocotylous. Our observations have not revealed
any differential growth of the cotyledons after initial expansion,
resulting from the action of a basal meristem (anisocotyly). The
initial expansion may however be slightly unequal. To clarify this, it
would be useful to examine whether there is an unequal cell division
rate in the two cotyledons, as demonstrated by Tsukaya (1997) in
Moody et al. (1999) , following Troll, defined the vegetative
propagules of Mimulus gemmiparus as brood bulbils (with storage in the
leaf component), distinct from brood tubers (storage in the stem
component). The storage bracts of Titanotrichum are part of the wide
range in form of the storage organs of vegetative propagules. For
instance, in Dioscoreaceae (Passam et al., 1982 ) and in Globba
(Zingiberaceae), the vegetative propagules are tuber-like, while in
Allium (Alliaceae), globular propagules form at the base of umbel
pedicels. The propagules of Saxifraga (Saxifragaceae) have enclosing
bracts and replace flowers within the inflorescence. Mimulus
gemmiparus (Scrophulariaceae) closely parallels Titanotrichum by
possessing V-shaped storage bracts (Moody et al., 1999 ). In
Titanotrichum however, the whole floral meristem has been replaced by
a cluster of bulbils, allowing Titanotrichum to produce large numbers
of bulbils, whereas in Mimulus (Moody et al., 1999 ), only one
propagule arises (from the proximal axillary buds).
Ecological significance of bulbil production
Bulbil production is the common state of all natural populations of
Titanotrichum when autumn approaches (at the beginning of September).
Because Titanotrichum usually grows near water, these tiny bulbils
disperse by flotation very easily. When attempting to trace the origin
of young clonal populations along ditches or tributaries, it is always
possible to locate a putative progenitor colony or plant upstream.
Bulbils may also be more easily carried by animals (including humans)
than seeds. The pointed storage bracts, which have long trichomes,
readily catch on human clothing and probably on animal fur. Plants
that regenerate from bulbils grow vigorously and establish quickly.
They can produce rhizomes in a shorter period than seedlings, which is
important for surviving drought or the death of aboveground growth.
Although flowers are produced freely in almost all natural
populations, seeds are hardly ever set. Propagation by bulbils is thus
the major means of mass reproduction and dispersal for Titanotrichum
in the wild, especially since seeds are rarely set, perhaps because of
a lack of effective pollinators (C.-N. Wang, personal observation).
Bulbils are unusual in tropical or subtropical plants (with certain
exceptions such as Remusatia vivipara). Titanotrichum is therefore
interesting in being a subtropical plant that uses bulbil propagation
as its main reproductive strategy. Titanotrichum often grows in dense
shade in which inflorescence growth and flower production is reduced.
Individuals under dense shade tend to produce more bulbils relative to
flowers compared to individuals in full light. Furthermore, field
observations suggest that seedlings rarely establish in deep shade,
and most regeneration is by the more robust bulbil-produced juvenile
plants and by rhizomatous spread.
It is notable that bulbil formation in glasshouse conditions in
Edinburgh is much more pronounced than that in the wild. Almost every
leaf axil initiates a bulbil inflorescence resulting in massive bulbil
production. We attribute this to low glasshouse temperatures (18°C
maximum) and to the rapid decline of daylength after mid-autumn that
occurs in Edinburgh. From observations in the wild and from
examination of herbarium specimens collected in autumn and winter in
Taiwan, the situation in the wild is less marked, and bulbiliferous
inflorescences do not so dramatically replace normal flowers and
vegetative shoots.
Significance of bulbil production for conservation
Seed set is very low in natural populations of Titanotrichum in
Taiwan, adjacent regions of China, and the Ryukyu Islands of Japan,
which suggests that bulbil production is the major reproductive
strategy for nearly all populations despite regular flower production.
In the open, large bees and butterflies sometimes visit the flowers.
However, in deep shade, insects rarely visit Titanotrichum flowers,
even though other flowering plants nearby, such as Begonia spp., are
regularly visited by pollinating insects. Although sexual reproduction
appears to be infrequent, occasional seed set and gene flow between
populations may be important in maintaining population viability.
Surveys of the genetic variation within and between populations are
needed in order to determine the extent of clonality and ascertain
whether the genetic variation is lower in marginal or threatened
Hecho por : Willson A Mendoza C
C.I: 16.959.604

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