Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:
Tree Physiology 15, 491--498
© 1995 Heron Publishing----Victoria, Canada
The role of acrotony in reproductive development in Picea
G. R. POWELL
Faculty of Forestry and Environmental Management, University of New Brunswick, P.O. Box 44555, Fredericton,
New Brunswick E3B 6C2, Canada
Received May 31, 1994
Summary The expression of acrotony (i.e., the increasing
size of comparable lateral shoots toward the apex of the main
shoot) was similar among first-order shoots borne along previous-year leaders of young Picea glauca (Moench) Voss,
Picea mariana (Mill.) B.S.P. and Picea rubens Sarg. trees. The
position and nature (i.e., whether cones, second-order shoots
or non-flushed buds) of lateral axes borne along the first-order
shoots were investigated. Seed cones occurred in proximal to
distal positions, but not in terminal positions, on upper shoots,
in medial to terminal positions on middle shoots, and in distal
to terminal positions on lower shoots. Most non-flushed buds
occurred in proximal positions on middle and lower shoots. In
P. rubens, rate, duration and amount of elongation of first-order
shoots increased acropetally. Thus lower shoots stopped elongating before upper shoots. Evidence of bud differentiation in
P. rubens, as indicated by the presence of initiating leaf primordia, was seen first in sections of terminal buds of upper shoots.
Differentiation of buds then proceeded basipetally along shoots
and among shoots down the crown. Differentiation of buds in
positions where cones are commonly borne became evident
soon after shoot elongation was completed.
Keywords: bud differentiation, Picea glauca, Picea mariana,
Picea rubens, seed cones, shoots, shoot elongation.
Introduction
It is well established that application of gibberellin A4/7 enhances cone production in Picea (Marquard and Hanover
1984a, 1984b, Cecich 1985, Philipson 1985, 1987, Ross 1985,
Bonnet-Masimbert 1987, Hall 1988, Ho 1988, Greenwood et
al. 1991, Owens et al. 1992). However, the underlying physiological bases of the GA4/7-induced enhancement of cone
production remains obscure (e.g., Ross and Pharis 1985, Pharis
et al. 1987), partly because the intricate complexity of tree
crowns has not been considered when designing treatments to
enhance cone production or in interpreting the results of cone
induction experiments. Thus studies have focused on whole
crowns rather than on morphogenetic patterns (i.e., shoot origin, placement, elongation and size, and seed-cone and pollencone placements) among shoots within crowns.
Shoot patterns within a crown are genus specific (e.g., De-
bezac 1965, Powell 1977a, 1988, 1991), and even within a
genus, such as Picea, differences in expression of basic characteristics and responses occur (Greenwood et al. 1991). The
distinctive morphogenetic pattern of shoots in young Picea
trees is strongly acrotonic. In Picea, which exhibits preformed
growth, acrotony is expressed as an increase in size of lateral
structures toward the shoot apex (cf. Champagnat 1978) and is
clearly displayed in the lateral buds along a tree’s leading
shoot. Numbers of bud scales and leaf primordia per lateral bud
increase acropetally (Baxter and Cannell 1978), and this increase, in turn, leads to an acropetal increase in the lengths of
the first-order shoots when the preformed elements grow out
from the buds. All of the buds arise similarly in leaf axils along
a shoot, and so, except for the acrotoneous arrangement, they
are of equal status.
It is on the first-order shoots arising from lateral buds along
a tree leader of the previous year that seed cones commonly
differentiate at first bearing (Marquard and Hanover 1984a,
1984b, Caron and Powell 1990, 1992, 1993). Similar shoots
from lateral buds on subsequent tree leaders bear many cones
in following years (Caron and Powell 1993). In any year, these
first-order shoots represent a population of similar origin and
age (axis age), but of different lengths. Thus the population
provides a basis for inter-shoot comparison free from variables
such as differing branching order or age of parent structure.
With decreasing shoot length, cones are positioned progressively more distally and are terminal on many of the short
shoots (e.g., Powell 1983, Caron 1987, Caron and Powell
1993). Marquard and Hanover (1984b) found that seed cones
of Picea glauca (Moench) Voss were medially situated on the
most-distal, first-order shoots, but underwent a slight acropetal
shift in response to GA4/7 treatment.
In Picea, the lower, shorter shoots cease elongation earlier
than the upper, longer shoots (e.g., Fraser 1966, BonnetMasimbert 1987, Ford et al. 1987). If lateral buds differentiate
when shoots cease elongating (cf. Owens and Molder 1976a,
1976b, 1977, Owens et al. 1977, Harrison and Owens 1983,
Maquard and Hanover 1984b), then buds on shorter shoots
would differentiate before those on longer shoots. Alternatively, because elongation along a shoot is completed first
proximally and last distally, differentiation of lateral buds may
occur progressively along individual shoots. If this is the case,
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POWELL
distal buds on shorter shoots may differentiate at the same time
as more proximally situated buds on longer shoots. Timing
may be important in terms of when particular buds are responsive to imposed treatment and endogenous biochemical gradients.
The interrelationships among elongation, timing and positioning, all occasioned by acrotony, have not been elucidated.
In this study, the acrotonal pattern among first-order shoots
undergoing their first elongation was used as a basis to investigate positional aspects of cone production and temporal aspects of bud differentiation under natural conditions. Three
Picea species were studied, P. glauca, P. mariana (Mill.) B.S.P.
and P. rubens Sarg.
Materials and methods
The 1992 crop of seed cones on Picea species growing in
central New Brunswick was better than average. In May 1993,
20 trees of each species, P. glauca, P. mariana and P. rubens,
were selected in the University of New Brunswick (UNB)
Forest, Fredericton, N.B., or in the Acadia Forest Experiment
Station, 20 km to the east. Selection criteria were: trees 0.7 to
3.7 m tall in 1990, single tree leader in 1990, normal branch
development in 1991 and 1992, and presence of cones that had
matured in 1992 on first-order shoots of 1991 (i.e., shoots that
had extended in 1991 from the 1990 leader).
Each first-order shoot of 1991 was examined in acropetal
sequence (Figure 1A). Recorded were the distance of the shoot
from the base of the 1990 leader and the distance along each
shoot of each non-flushed bud, shoot, seed cone or pollen cone.
The distance data were expressed as percentages of total
lengths of the respective leaders or first-order shoots to facilitate analysis on a comparative basis. The percentages were
Figure 1. Stylized diagrams of upper sections of one side of young
Picea crowns to depict measuring and sampling positions. (A) Leaders
of the last 3 years (ages shown by numbers of lines) with that of 1990
showing how positions of first-order lateral shoots were divided into
10% distance classes from the leader’s base (single arrow), and how
positions of second-order lateral axes along the first-order shoots of
1991 were divided into 20% distance classes from the shoot base.
(B) Leader of 1992 on which lateral buds were divided into lower,
middle and upper positional classes according to relative distances
from the leader’s base (single arrow).
grouped acropetally in 10% classes along the parent leaders
and 20% classes along the first-order shoots (Figure 1A).
Separately, 20 P. rubens between 1 and 2 m tall were selected in the UNB Forest. Each had a single 1992 leader
(Figure 1B) between 20 and 40 cm long and was free from
local competition from other trees. In mid-May 1993, in
acropetal sequence, the length of each bud on each leader was
measured with vernier calipers (nearest 0.1 mm). The bud’s
distance from the base of the leader and its position around the
leader (north, east, south or west quadrant) were recorded.
From among the buds, three lower, three middle and three
upper lateral buds (Figure 1B), and the terminal bud were
selected and marked. To minimize variability, the lateral buds
were selected preferentially from the southern exposure, with
numbers made up as necessary from closest buds on first the
western and then the eastern exposure.
Elongation of marked buds and subsequently the first-order
shoots produced from them was measured each Monday,
Wednesday and Friday. To facilitate tracking of shoot elongation, and particularly of its completion, each measurement was
entered into a computer file on the day it was made and used
to generate growth curves. When elongation of the lower
shoots was deemed from their growth curves to be 95% completed (Day 190), two lower, two middle and two upper shoots
were harvested on each of three additional, randomly chosen
trees. The harvested shoots were labeled and transported in a
cooler (< 10 °C) to the laboratory. Similar collections were
made from other trees when elongation of first, middle (Day
195) and upper shoots (Day 200) on the measured trees was
deemed to be 95% completed. When elongation of the tree
leaders was deemed to be 95% completed (Day 207), shoots,
including tree leaders, were collected from additional trees.
Further collections were made on Days 215, 221 and 229.
For each collected shoot, the distance from the base of the
shoot to each bud (numbered in acropetal sequence) was recorded. Each bud was then carefully excised, placed in formalin/acetic acid/alcohol (FAA) and subjected to reduced
pressure, and then left for a minimum of 2 days. Each labeled
bud was placed in a container and passed through an n-butanol
series into Paraplast in a Histomatic processor. Each Paraplastembedded bud was arranged in molten Paraplast in a boat and
cooled. The resultant blocked buds were mounted on wooden
stubs and serially longitudinally sectioned at 10 µm on a rotary
microtome. The sections were mounted on microscope slides,
stained with safranin and fast green, and covered for subsequent microscopic examination.
To facilitate comparative examination, the medial section
(or most nearly medial section in obliquely sectioned buds)
was photographed at a magnification of 20.5× using a Wild
M400 Macroscrope with Kodak 100 Gold film and a daylight
(blue) filter. A paper print at 72× magnification was made of
each selected section (over 200), and sets of sections of buds
were compared for the successive collection dates.
On Day 221 (August 9), first-order shoots were collected
from two extra trees. Samples of buds from a range of positions
along the shoots were dissected, and flanks of the apical
meristems were examined directly.
ACROTONY AND REPRODUCTIVE DEVELOPMENT IN PICEA
Results
Shoot lengths and distribution of lateral axes along shoots
The seed-cone-bearing P. glauca, P. mariana and P. rubens
trees averaged (mean ± SE) 2.31 ± 0.17, 1.54 ± 0.11 and 1.75
± 0.12 m in height in 1990, respectively. Leading shoots of
1990 were 254 ± 22, 182 ± 23 and 216 ± 27 mm long, but when
adjusted with tree height in 1989 as a covariate, the means
were estimated at 204 ± 21, 218 ± 20 and 228 ± 19 mm,
respectively, and were not significantly different (P = 0.71).
The lateral shoots that elongated in 1991 from buds along the
1990 leading shoots showed distinct acrotony (Figure 2). The
pattern among the shoots was least uniform in P. rubens, which
also had the fewest shoots (from Figure 2). In each species,
shoots were least numerous in the 70 to 90% region along the
leader and near its base, although in P. glauca, there were many
shoots in the 70--80% and 0--10% regions of the leaders (Figure 2). Lengths of shoots on north-, east-, south- and west-facing surfaces were not different for any species (P = 0.75, 0.41
and 0.69 for P. glauca, P. mariana and P. rubens, respectively,
with leader lengths in 1990 as covariates).
Because number of lateral axes borne per shoot was correlated with shoot length (r = 0.941, 0.901 and 0.906 for
P. glauca, P. mariana and P. rubens, respectively), it followed
a similar pattern to that of lateral shoot length along the leading
shoot (Figure 3). Picea glauca bore more lateral axes per unit
length of shoots originating between 30 and 90% of the distance along the leader than did the other species (cf. Figures 2
and 3). Overall, P. glauca bore 0.77 ± 0.01 lateral axis per cm
of shoot, P. mariana 0.75 ± 0.02, and P. rubens 0.66 ± 0.01.
When expressed in terms of position along the bearing
shoot, lateral axes (non-flushed buds, second-order shoots or
cones) occurred all along the upper shoots, but only along the
distal halves of the lower shoots (Figure 4). Proportions of
non-flushed buds increased downward in the crown among the
shoots. The most proximal buds on lower and some upper
Figure 2. Mean lengths of 1991 shoots borne on 1990 leaders of
P. glauca, P. mariana and P. rubens expressed as percentages of
current (1991) leader lengths at different heights (10% distance
classes) along the 1990 leaders. Standard errors are shown as projecting lines from the bars, and numbers on bars indicate numbers of
shoots included in the respective classes (means).
493
shoots did not flush, but non-flushed buds also occurred at all
locations where cones or lateral shoots occurred. Frequency of
occurrence of lateral shoots in mid-shoot positions decreased
downward. Most lateral shoots on upper parent shoots were
situated distally. On lower parent shoots, most new shoots were
terminal.
Cones occurred laterally all along the uppermost shoots, but
not terminally (Figure 4), whereas on lower shoots, cones were
most frequently terminal. Overall, cone positions tended to
become more distal toward the base of the crown. The pattern
of cone occurrence was consistent for all three species (Figure 5); however, the few very short shoots that occurred near
the bases of the leaders of P. mariana and P. rubens (Figure 2)
did not bear cones (Figure 5).
Figure 3. Mean numbers of lateral axes borne per shoot at different
heights (10% distance classes) along 1990 leaders of P. glauca,
P. mariana and P. rubens. Details as in Figure 2.
Figure 4. Mean percentages and standard errors of lateral axes borne
at successive positions (20% distance classes and terminally, T) along
shoots at different heights (10% distance classes) along the leaders of
20 trees of each of three Picea species. The lateral axes are designated
as non-flushed buds (open), seed cones (solid), and extended shoots
(cross-hatched).
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POWELL
Figure 5. Percentages of seed cones borne at successive positions
(20% distance classes and terminally, T) along shoots at different
heights (10% distance classes) along the leaders of P. glauca (open),
P. mariana (solid) and P. rubens (cross-hatched) (n = 20).
Elongation of shoots borne along leaders
In P. rubens, lengths of lateral buds formed in 1992 increased
acropetally along leaders (Figure 6). Terminal buds on leaders
were not as long as distal lateral buds (5.07 ± 0.14 versus 5.98
± 0.07 mm for buds in the 95% distance-class).
Bud elongation became detectable (increase of 0.05 mm)
between Days 141 and 165 (May 21 and June 14, 1993). Bud
burst occurred between Days 162 and 174 (June 11 and 23). It
was achieved for all buds on single leaders in 2 to 7 days. Mean
days by which bud burst was achieved (assessed at 2- and
3-day intervals) on lower, middle and upper lateral buds, and
terminal buds were 169.6a, 170.0a, 169.0a and 168.0b, respectively (the same letter after the means indicates no significant
difference at the 0.05 level), indicating a slight basipetal trend.
Figure 6. Mean lengths of lateral buds borne at different heights (10%
distance classes) on 1992 leaders of 20 P. rubens trees. Standard errors
are shown as projecting lines from the bars, and numbers on bars
indicate the numbers of buds included in the respective classes
(means).
The rate and duration of post-bud-burst, first-order shoot
elongation increased acropetally (Figure 7). Mean days by
which shoot elongation ceased were 204.0a (July 23), 204.9a,
208.4 and 211.3 for lower, middle, upper and terminal shoots,
respectively. Overall, lower shoots completed 95% of their
elongation 2 days before middle shoots, middle shoots 2 days
before upper shoots, and upper shoots 7 days before terminal
shoots (mean days of 192.0 ± 0.4, 194.1 ± 0.2, 196.2 ± 0.3 and
203.1 ± 1.0 for lower, middle, upper and terminal shoots,
respectively). On individual trees, achievement of 95% of final
length of first-order shoots alone and of first-order and terminal shoots together spanned 2 to 12 days and 4 to 18 days,
respectively.
Total post-bud-burst elongation took 34.4 ± 0.7, 34.9 ± 0.7,
39.3 ± 0.7 and 43.3 ± 1.3 days for lower, middle and upper
first-order shoots, and terminal shoots, respectively. The difference between means for lower and middle first-order shoots
was not significant at the 0.05 level.
Differentiation of buds along shoots
Sections of buds collected on Day 190 (July 9) showed no
evidence that differentiation (presence of leaf primordia on the
lower flanks of apical meristems) had occurred. The apical
meristems (apices) were rounded domes to rounded cones with
inner bud scales generally close to the apex surfaces (Figure 8).
Apices of lateral buds were situated at the level of the receptacle bearing the older bud scales, whereas apices of terminal
buds were situated well below the level of the receptacle
bearing older bud scales (e.g., Figures 8A and 8B). This massive receptacle development in terminal buds was most apparent in buds terminating upper shoots. These buds had the
broadest apices. The receptacle was only moderately raised
above the level of the bases of the narrower apices in terminal
buds on lower shoots. Most lateral buds on lower shoots, some
on middle shoots and occasional buds on upper shoots lagged
in development. Their apices were small, rounded domes,
which essentially lacked pith development in their lower parts
and in the tissues beneath. These buds were categorized as
Figure 7. Elongation after bud burst in 1993 of shoots borne along
1992 leaders of 20 P. rubens trees. Values on the curves indicate in
ascending order the mean percentages of the distances along their
respective leaders of three lower, three middle and three upper shoots,
and the new leaders (100% distance) of each tree. Vertical lines on the
curves are standard errors.
ACROTONY AND REPRODUCTIVE DEVELOPMENT IN PICEA
495
Figure 8. Median longitudinal sections of comparable parts of buds
from an upper shoot of one Picea
rubens tree, Day 190, showing over
half of the apical meristem (a), pith
(p) and receptacle (r and arrows)
bearing bud scales (s) (72×). (A) The
6th of 10 lateral buds positioned at
76% of the distance along the shoot,
and (B) the terminal bud.
latent. The pith areas of better-developed buds were distinctive (Figure 8), and the portions in and just below the lower
reaches of the apex stained darkly. The proportion of darkly
stained pith tissues tended to increase acropetally in buds
along individual shoots and upward among shoots.
Collections on Days 195 and 200 (July 14 and 19) showed
increases in proportions of more conical apices among lateral
buds. No indications of initiation of leaf primordia were observed on these apices (Figure 9). The outer flanks of the
broad apices of terminal buds of upper shoots provided the
first evidence of initiation of leaf primordia (Figure 10) as indicated by suggestive staining of surficial and associated
subsurface cells (Figure 10A), and as slight surficial
mounding among such cells (Figure 10B).
Figure 9. Median longitudinal sections of comparable parts of lateral
buds from upper shoots of two Picea
rubens trees (72×). (A) The 11th of
11 buds positioned at 95% of the distance along the shoot on Day 195,
and (B) the 2nd of 11 buds positioned at 45% of the distance along
the shoot on Day 200. Symbols as in
Figure 8.
Figure 10. Median longitudinal sections of comparable parts of terminal
buds from upper shoots of two Picea
rubens trees (72×). (A) Cellular patterns (arrows) suggestive of leaf-primordium initiation on Day 195, and
(B) bulging tissues and cellular patterns (arrows) indicating leaf primordium initiation on Day 200. Other
symbols as in Figure 8.
496
POWELL
Collections on Day 207 (July 26) showed that leaf primordia
had initiated in terminal buds of upper shoots. Leaf primordia
were also evident in terminal buds of some middle (Figure 11A) and lower shoots, and in distal lateral buds (Figure 11B) on upper shoots. By Day 207, dark staining of pith in
the lower reaches of and just below the apex was pronounced,
especially in the terminal and distal lateral buds. Outside the
pith zone, the peripheral flanks of the apex, where leaf
primordia were forming, were three to five cells thick.
By Day 215 (August 3), apices of terminal buds of upper
shoots were developing mammillary tips. Leaf primordia were
evident on lower flanks of apices of buds situated more
basipetally on shoots at all levels. On Day 221 (August 9),
proximally situated buds with well-developed apices (hence,
apparently not latent) showed little evidence of initiation of
leaf primordia (Figure 12A), whereas there was an acropetal
trend in the development of leaf primordia in buds along single
shoots (Figure 12B to 12F). Associated with this development
of leaf primordia, there were increases in apex size, density of
staining in the pith and relative height above the base of the
apex of the bud-scale-bearing receptacle (Figure 12). Buds
collected and dissected on Day 221 showed similar acropetal
trends in development of leaf primordia and in apex size and
shape.
Discussion
Acrotony among directly comparable shoots of similar origin
was expressed similarly in P. glauca, P. mariana and P. rubens. Shoot length was associated with bud size (Figure 6) and
with preformed bud composition (Baxter and Cannell 1978).
Shoot length was also associated with the propensity of the lateral axis to differentiate and develop into a cone or shoot, or
remain as a non-flushed bud. Although the cause of non-flushing of buds was not examined, their distribution (Figure 4)
suggests that most were latent buds. Sections of developing
P. rubens buds confirmed that many buds in more proximal
positions had small apices that appeared inactive. Latent buds,
which have been described in other Picea (e.g., Owens et al.
1977, 1992), represent a reserve of lateral axes that can be activated if more distally situated vegetative structures are destroyed (cf. Powell 1982). Also, in some genera of Pinaceae,
cone buds tend more frequently to take the place of latent buds
than of vegetative buds (Owens 1969, Powell 1977a). The occurrence of the three kinds of buds in Picea warrants further
investigation in relation to position on the shoot and to years of
varying cone abundance (cf. Powell 1977b).
The acrotoneous arrangement of shoots was also associated
with rate and duration of shoot elongation that led to an
acropetal increase in timing of cessation of shoot elongation.
The upper, longer shoots, which started to elongate slightly
earlier, exhibited a much greater rate of elongation and stopped
elongating 4 days later than the lower, shorter shoots. This
Figure 11. Median longitudinal sections of comparable parts of buds
from shoots of two Picea rubens trees
on Day 207 (72×). (A) Terminal bud
from a middle shoot, and (B) the 6th
of 7 lateral buds at 96% of the distance along an upper shoot. Arrows
indicate leaf primordia; other symbols as in Figure 8.
Figure 12. Median longitudinal sections of comparable parts of buds
from an upper shoot of one Picea
rubens tree on Day 221 (51×). (A–E)
2nd, 5th, 8th, 10th and 12th of 12 lateral buds at 34, 49, 71, 95 and 96% of
the distance along the shoot, respectively, and (F) the terminal bud.
ACROTONY AND REPRODUCTIVE DEVELOPMENT IN PICEA
pattern is consistent with that reported for shoots extending
principal branches of the crowns of large Picea trees (e.g.
Fraser 1966, Ford et al. 1987).
Morphological-anatomical evidence of differentiation of
buds on the acrotoneously arranged shoots followed neither
the upward (shorter to longer shoots) pattern of timing, suggested by the notion that differentiation occurs when shoot
elongation ceases, nor the outward (acropetal along shoots)
pattern of timing, suggested by the progressive completion of
elongation along a shoot (see Introduction). The evidence
indicates an opposite or basipetal pattern of timing of bud
differentiation. Terminal buds of upper shoots showed signs of
differentiation first. Differentiation was evident next in terminal buds of middle and some lower shoots, and in distal lateral
buds of upper shoots. Evidence of differentiation then moved
to medial lateral buds of upper shoots and distal lateral buds of
middle shoots, and then to more proximal buds on all shoots.
Mammillary tips to the apices, as described in some differentiating apices in other Picea (Owens and Molder 1976a,
Owens et al. 1977, 1992, Marquard and Hanover 1984b), were
observed only in terminal and distal lateral buds of the upper
and middle shoots, indicating that they are associated with
more vigorous development.
The times when evidence of differentiation became apparent
were associated with cessation of shoot elongation, but not in
a consistent manner. On upper shoots, differentiation of terminal buds became evident when shoots were completing elongation (95% completed). On middle and lower shoots,
differentiation of terminal buds became evident just after completion of shoot elongation. Thus the time when evidence of
differentiation became apparent was dependent on the relative
position of the parent shoot and the relative position of the bud
along the parent shoot.
The consistent pattern of cone distribution in the three Picea
species (Figure 5), coupled with the time when differentiation
became evident, indicates that the buds most likely to differentiate as cones should all show evidence of differentiation at
about the same time, and after shoot elongation has been
completed. Thus measures aimed at enhancing cone differentiation must take place before shoot elongation ends (cf. Marquard and Hanover 1984b, Ross 1985, Ho 1988). Moreover,
because visible evidence of differentiation must follow precursor events within the tissues of the buds or shoots, time must
be allowed for such events to occur after any given cone-enhancing treatment. However, the reaction times to stimuli of
differentiation appear to vary among shoots or among buds
along shoots. Thus the patterns of shoot elongation, of non-differentiation (latency) and differentiation, of sizes of bud apices
along shoots, and of density of staining in the pith in buds
along shoots provide an indication that response times may be
slower on shorter shoots and in proximal positions on longer
shoots. The corollary to this is that the rate of development
appears to be fastest in terminal buds of upper shoots. This, and
the finding that such buds normally do not differentiate as
cones, can be interpreted as a mechanism to ensure continued
vegetative development of the most vigorous shoots, and thus
expansion of the crown by means of the most distal branches
497
of any one year.
This study has demonstrated the complexity yet orderliness
of morphogenetic patterning in populations of similar shoots
in a region of the crown of young Picea trees and has provided
information on where and when changes associated with, or
precursive to, cone differentiation occur. The information
should be of value in designing treatments to enhance cone
production and in interpreting results of experiments on cone
induction.
Acknowledgments
This research was made possible through research grants from the
Natural Science and Engineering Research Council of Canada and the
University of New Brunswick Research Fund. The author thanks J.G.
Floyd, D.W. Gimby, M.H. Hancox and P. Pobihushchy for technical
assistance in the field and laboratory, and W.L. Staples for photographic processing.
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Marquard, R.D. and J.W. Hanover. 1984b. Relationship between gibberellin A4/7 concentration, time of treatment, and crown position
on flowering of Picea glauca. Can. J. For. Res. 14:547--553.
Owens, J.N. 1969. The relative importance of initiation and early
development on cone production in Douglas-fir. Can. J. Bot.
47:1039--1049.
Owens, J.N. and M. Molder. 1976a. Bud development in Sitka spruce.
I. Annual growth cycle of vegetative buds and shoots. Can. J. Bot.
54:313--325.
Owens, J.N. and M. Molder. 1976b. Bud development in Sitka spruce.
II. Cone differentiation and early development. Can J. Bot. 54:766-779.
Owens, J.N. and M. Molder. 1977. Bud development in Picea glauca.
II. Cone differentiation and early development. Can. J. Bot.
55:2746--2760.
Owens, J.N., M. Molder and H. Langer. 1977. Bud development in
Picea glauca. I. Annual growth cycle of vegetative buds and shoot
elongation as they relate to date and temperature sums. Can. J. Bot.
55:2728--2745.
Owens, J.B., J.J. Philipson and D.L.S. Harrison. 1992. The effects of
the duration and timing of drought plus heat plus gibberellin A4/7 on
apical meristem development and coning in Sitka spruce (Picea
sitchensis (Bong.) Carr.). New Phytol. 122:515--528.
Pharis, R.P., J.E. Webber and S.D. Ross. 1987. The promotion of
flowering in forest trees by gibberellin A4/7 and cultural treatments:
a review of possible mechanisms. For. Ecol. Manage. 19:65--84.
Philipson, J.J. 1985. The effect of top pruning, girdling, and gibberellin A4/7 application on the production and distribution of pollen and
seed cones in Sitka spruce. Can. J. For. Res. 15:1125--1128.
Philipson, J.J. 1987. Promotion of cone and seed production by gibberellin A4/7 and distribution of pollen and seed cones on Sitka
spruce in a clone bank. For. Ecol. Manage. 19:147--154.
Powell, G.R. 1977a. Patterns of development in Abies balsamea
crowns and effects of megastrobilus production on shoots and buds.
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review of its morphogenesis and a discussion of its apparent physiological basis. Can. J. For. Res. 7:547--555.
Powell, G.R. 1982. Shoot and bud development in balsam fir: implications for pruning of Christmas trees. For. Chron. 58:168--172.
Powell, G.R. 1983. Red spruce, Picea rubens Sarg. In Reproduction
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2:150--164.
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grafts: effects of heat, drought, gibberellin A4/7 and their timing.
Can. J. For. Res. 15:618--624.
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different mechanisms and techniques, with special reference to
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and J.E. Jackson. Inst. Terrestrial Ecol., Natural Environ. Res.
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© 1995 Heron Publishing----Victoria, Canada
The role of acrotony in reproductive development in Picea
G. R. POWELL
Faculty of Forestry and Environmental Management, University of New Brunswick, P.O. Box 44555, Fredericton,
New Brunswick E3B 6C2, Canada
Received May 31, 1994
Summary The expression of acrotony (i.e., the increasing
size of comparable lateral shoots toward the apex of the main
shoot) was similar among first-order shoots borne along previous-year leaders of young Picea glauca (Moench) Voss,
Picea mariana (Mill.) B.S.P. and Picea rubens Sarg. trees. The
position and nature (i.e., whether cones, second-order shoots
or non-flushed buds) of lateral axes borne along the first-order
shoots were investigated. Seed cones occurred in proximal to
distal positions, but not in terminal positions, on upper shoots,
in medial to terminal positions on middle shoots, and in distal
to terminal positions on lower shoots. Most non-flushed buds
occurred in proximal positions on middle and lower shoots. In
P. rubens, rate, duration and amount of elongation of first-order
shoots increased acropetally. Thus lower shoots stopped elongating before upper shoots. Evidence of bud differentiation in
P. rubens, as indicated by the presence of initiating leaf primordia, was seen first in sections of terminal buds of upper shoots.
Differentiation of buds then proceeded basipetally along shoots
and among shoots down the crown. Differentiation of buds in
positions where cones are commonly borne became evident
soon after shoot elongation was completed.
Keywords: bud differentiation, Picea glauca, Picea mariana,
Picea rubens, seed cones, shoots, shoot elongation.
Introduction
It is well established that application of gibberellin A4/7 enhances cone production in Picea (Marquard and Hanover
1984a, 1984b, Cecich 1985, Philipson 1985, 1987, Ross 1985,
Bonnet-Masimbert 1987, Hall 1988, Ho 1988, Greenwood et
al. 1991, Owens et al. 1992). However, the underlying physiological bases of the GA4/7-induced enhancement of cone
production remains obscure (e.g., Ross and Pharis 1985, Pharis
et al. 1987), partly because the intricate complexity of tree
crowns has not been considered when designing treatments to
enhance cone production or in interpreting the results of cone
induction experiments. Thus studies have focused on whole
crowns rather than on morphogenetic patterns (i.e., shoot origin, placement, elongation and size, and seed-cone and pollencone placements) among shoots within crowns.
Shoot patterns within a crown are genus specific (e.g., De-
bezac 1965, Powell 1977a, 1988, 1991), and even within a
genus, such as Picea, differences in expression of basic characteristics and responses occur (Greenwood et al. 1991). The
distinctive morphogenetic pattern of shoots in young Picea
trees is strongly acrotonic. In Picea, which exhibits preformed
growth, acrotony is expressed as an increase in size of lateral
structures toward the shoot apex (cf. Champagnat 1978) and is
clearly displayed in the lateral buds along a tree’s leading
shoot. Numbers of bud scales and leaf primordia per lateral bud
increase acropetally (Baxter and Cannell 1978), and this increase, in turn, leads to an acropetal increase in the lengths of
the first-order shoots when the preformed elements grow out
from the buds. All of the buds arise similarly in leaf axils along
a shoot, and so, except for the acrotoneous arrangement, they
are of equal status.
It is on the first-order shoots arising from lateral buds along
a tree leader of the previous year that seed cones commonly
differentiate at first bearing (Marquard and Hanover 1984a,
1984b, Caron and Powell 1990, 1992, 1993). Similar shoots
from lateral buds on subsequent tree leaders bear many cones
in following years (Caron and Powell 1993). In any year, these
first-order shoots represent a population of similar origin and
age (axis age), but of different lengths. Thus the population
provides a basis for inter-shoot comparison free from variables
such as differing branching order or age of parent structure.
With decreasing shoot length, cones are positioned progressively more distally and are terminal on many of the short
shoots (e.g., Powell 1983, Caron 1987, Caron and Powell
1993). Marquard and Hanover (1984b) found that seed cones
of Picea glauca (Moench) Voss were medially situated on the
most-distal, first-order shoots, but underwent a slight acropetal
shift in response to GA4/7 treatment.
In Picea, the lower, shorter shoots cease elongation earlier
than the upper, longer shoots (e.g., Fraser 1966, BonnetMasimbert 1987, Ford et al. 1987). If lateral buds differentiate
when shoots cease elongating (cf. Owens and Molder 1976a,
1976b, 1977, Owens et al. 1977, Harrison and Owens 1983,
Maquard and Hanover 1984b), then buds on shorter shoots
would differentiate before those on longer shoots. Alternatively, because elongation along a shoot is completed first
proximally and last distally, differentiation of lateral buds may
occur progressively along individual shoots. If this is the case,
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POWELL
distal buds on shorter shoots may differentiate at the same time
as more proximally situated buds on longer shoots. Timing
may be important in terms of when particular buds are responsive to imposed treatment and endogenous biochemical gradients.
The interrelationships among elongation, timing and positioning, all occasioned by acrotony, have not been elucidated.
In this study, the acrotonal pattern among first-order shoots
undergoing their first elongation was used as a basis to investigate positional aspects of cone production and temporal aspects of bud differentiation under natural conditions. Three
Picea species were studied, P. glauca, P. mariana (Mill.) B.S.P.
and P. rubens Sarg.
Materials and methods
The 1992 crop of seed cones on Picea species growing in
central New Brunswick was better than average. In May 1993,
20 trees of each species, P. glauca, P. mariana and P. rubens,
were selected in the University of New Brunswick (UNB)
Forest, Fredericton, N.B., or in the Acadia Forest Experiment
Station, 20 km to the east. Selection criteria were: trees 0.7 to
3.7 m tall in 1990, single tree leader in 1990, normal branch
development in 1991 and 1992, and presence of cones that had
matured in 1992 on first-order shoots of 1991 (i.e., shoots that
had extended in 1991 from the 1990 leader).
Each first-order shoot of 1991 was examined in acropetal
sequence (Figure 1A). Recorded were the distance of the shoot
from the base of the 1990 leader and the distance along each
shoot of each non-flushed bud, shoot, seed cone or pollen cone.
The distance data were expressed as percentages of total
lengths of the respective leaders or first-order shoots to facilitate analysis on a comparative basis. The percentages were
Figure 1. Stylized diagrams of upper sections of one side of young
Picea crowns to depict measuring and sampling positions. (A) Leaders
of the last 3 years (ages shown by numbers of lines) with that of 1990
showing how positions of first-order lateral shoots were divided into
10% distance classes from the leader’s base (single arrow), and how
positions of second-order lateral axes along the first-order shoots of
1991 were divided into 20% distance classes from the shoot base.
(B) Leader of 1992 on which lateral buds were divided into lower,
middle and upper positional classes according to relative distances
from the leader’s base (single arrow).
grouped acropetally in 10% classes along the parent leaders
and 20% classes along the first-order shoots (Figure 1A).
Separately, 20 P. rubens between 1 and 2 m tall were selected in the UNB Forest. Each had a single 1992 leader
(Figure 1B) between 20 and 40 cm long and was free from
local competition from other trees. In mid-May 1993, in
acropetal sequence, the length of each bud on each leader was
measured with vernier calipers (nearest 0.1 mm). The bud’s
distance from the base of the leader and its position around the
leader (north, east, south or west quadrant) were recorded.
From among the buds, three lower, three middle and three
upper lateral buds (Figure 1B), and the terminal bud were
selected and marked. To minimize variability, the lateral buds
were selected preferentially from the southern exposure, with
numbers made up as necessary from closest buds on first the
western and then the eastern exposure.
Elongation of marked buds and subsequently the first-order
shoots produced from them was measured each Monday,
Wednesday and Friday. To facilitate tracking of shoot elongation, and particularly of its completion, each measurement was
entered into a computer file on the day it was made and used
to generate growth curves. When elongation of the lower
shoots was deemed from their growth curves to be 95% completed (Day 190), two lower, two middle and two upper shoots
were harvested on each of three additional, randomly chosen
trees. The harvested shoots were labeled and transported in a
cooler (< 10 °C) to the laboratory. Similar collections were
made from other trees when elongation of first, middle (Day
195) and upper shoots (Day 200) on the measured trees was
deemed to be 95% completed. When elongation of the tree
leaders was deemed to be 95% completed (Day 207), shoots,
including tree leaders, were collected from additional trees.
Further collections were made on Days 215, 221 and 229.
For each collected shoot, the distance from the base of the
shoot to each bud (numbered in acropetal sequence) was recorded. Each bud was then carefully excised, placed in formalin/acetic acid/alcohol (FAA) and subjected to reduced
pressure, and then left for a minimum of 2 days. Each labeled
bud was placed in a container and passed through an n-butanol
series into Paraplast in a Histomatic processor. Each Paraplastembedded bud was arranged in molten Paraplast in a boat and
cooled. The resultant blocked buds were mounted on wooden
stubs and serially longitudinally sectioned at 10 µm on a rotary
microtome. The sections were mounted on microscope slides,
stained with safranin and fast green, and covered for subsequent microscopic examination.
To facilitate comparative examination, the medial section
(or most nearly medial section in obliquely sectioned buds)
was photographed at a magnification of 20.5× using a Wild
M400 Macroscrope with Kodak 100 Gold film and a daylight
(blue) filter. A paper print at 72× magnification was made of
each selected section (over 200), and sets of sections of buds
were compared for the successive collection dates.
On Day 221 (August 9), first-order shoots were collected
from two extra trees. Samples of buds from a range of positions
along the shoots were dissected, and flanks of the apical
meristems were examined directly.
ACROTONY AND REPRODUCTIVE DEVELOPMENT IN PICEA
Results
Shoot lengths and distribution of lateral axes along shoots
The seed-cone-bearing P. glauca, P. mariana and P. rubens
trees averaged (mean ± SE) 2.31 ± 0.17, 1.54 ± 0.11 and 1.75
± 0.12 m in height in 1990, respectively. Leading shoots of
1990 were 254 ± 22, 182 ± 23 and 216 ± 27 mm long, but when
adjusted with tree height in 1989 as a covariate, the means
were estimated at 204 ± 21, 218 ± 20 and 228 ± 19 mm,
respectively, and were not significantly different (P = 0.71).
The lateral shoots that elongated in 1991 from buds along the
1990 leading shoots showed distinct acrotony (Figure 2). The
pattern among the shoots was least uniform in P. rubens, which
also had the fewest shoots (from Figure 2). In each species,
shoots were least numerous in the 70 to 90% region along the
leader and near its base, although in P. glauca, there were many
shoots in the 70--80% and 0--10% regions of the leaders (Figure 2). Lengths of shoots on north-, east-, south- and west-facing surfaces were not different for any species (P = 0.75, 0.41
and 0.69 for P. glauca, P. mariana and P. rubens, respectively,
with leader lengths in 1990 as covariates).
Because number of lateral axes borne per shoot was correlated with shoot length (r = 0.941, 0.901 and 0.906 for
P. glauca, P. mariana and P. rubens, respectively), it followed
a similar pattern to that of lateral shoot length along the leading
shoot (Figure 3). Picea glauca bore more lateral axes per unit
length of shoots originating between 30 and 90% of the distance along the leader than did the other species (cf. Figures 2
and 3). Overall, P. glauca bore 0.77 ± 0.01 lateral axis per cm
of shoot, P. mariana 0.75 ± 0.02, and P. rubens 0.66 ± 0.01.
When expressed in terms of position along the bearing
shoot, lateral axes (non-flushed buds, second-order shoots or
cones) occurred all along the upper shoots, but only along the
distal halves of the lower shoots (Figure 4). Proportions of
non-flushed buds increased downward in the crown among the
shoots. The most proximal buds on lower and some upper
Figure 2. Mean lengths of 1991 shoots borne on 1990 leaders of
P. glauca, P. mariana and P. rubens expressed as percentages of
current (1991) leader lengths at different heights (10% distance
classes) along the 1990 leaders. Standard errors are shown as projecting lines from the bars, and numbers on bars indicate numbers of
shoots included in the respective classes (means).
493
shoots did not flush, but non-flushed buds also occurred at all
locations where cones or lateral shoots occurred. Frequency of
occurrence of lateral shoots in mid-shoot positions decreased
downward. Most lateral shoots on upper parent shoots were
situated distally. On lower parent shoots, most new shoots were
terminal.
Cones occurred laterally all along the uppermost shoots, but
not terminally (Figure 4), whereas on lower shoots, cones were
most frequently terminal. Overall, cone positions tended to
become more distal toward the base of the crown. The pattern
of cone occurrence was consistent for all three species (Figure 5); however, the few very short shoots that occurred near
the bases of the leaders of P. mariana and P. rubens (Figure 2)
did not bear cones (Figure 5).
Figure 3. Mean numbers of lateral axes borne per shoot at different
heights (10% distance classes) along 1990 leaders of P. glauca,
P. mariana and P. rubens. Details as in Figure 2.
Figure 4. Mean percentages and standard errors of lateral axes borne
at successive positions (20% distance classes and terminally, T) along
shoots at different heights (10% distance classes) along the leaders of
20 trees of each of three Picea species. The lateral axes are designated
as non-flushed buds (open), seed cones (solid), and extended shoots
(cross-hatched).
494
POWELL
Figure 5. Percentages of seed cones borne at successive positions
(20% distance classes and terminally, T) along shoots at different
heights (10% distance classes) along the leaders of P. glauca (open),
P. mariana (solid) and P. rubens (cross-hatched) (n = 20).
Elongation of shoots borne along leaders
In P. rubens, lengths of lateral buds formed in 1992 increased
acropetally along leaders (Figure 6). Terminal buds on leaders
were not as long as distal lateral buds (5.07 ± 0.14 versus 5.98
± 0.07 mm for buds in the 95% distance-class).
Bud elongation became detectable (increase of 0.05 mm)
between Days 141 and 165 (May 21 and June 14, 1993). Bud
burst occurred between Days 162 and 174 (June 11 and 23). It
was achieved for all buds on single leaders in 2 to 7 days. Mean
days by which bud burst was achieved (assessed at 2- and
3-day intervals) on lower, middle and upper lateral buds, and
terminal buds were 169.6a, 170.0a, 169.0a and 168.0b, respectively (the same letter after the means indicates no significant
difference at the 0.05 level), indicating a slight basipetal trend.
Figure 6. Mean lengths of lateral buds borne at different heights (10%
distance classes) on 1992 leaders of 20 P. rubens trees. Standard errors
are shown as projecting lines from the bars, and numbers on bars
indicate the numbers of buds included in the respective classes
(means).
The rate and duration of post-bud-burst, first-order shoot
elongation increased acropetally (Figure 7). Mean days by
which shoot elongation ceased were 204.0a (July 23), 204.9a,
208.4 and 211.3 for lower, middle, upper and terminal shoots,
respectively. Overall, lower shoots completed 95% of their
elongation 2 days before middle shoots, middle shoots 2 days
before upper shoots, and upper shoots 7 days before terminal
shoots (mean days of 192.0 ± 0.4, 194.1 ± 0.2, 196.2 ± 0.3 and
203.1 ± 1.0 for lower, middle, upper and terminal shoots,
respectively). On individual trees, achievement of 95% of final
length of first-order shoots alone and of first-order and terminal shoots together spanned 2 to 12 days and 4 to 18 days,
respectively.
Total post-bud-burst elongation took 34.4 ± 0.7, 34.9 ± 0.7,
39.3 ± 0.7 and 43.3 ± 1.3 days for lower, middle and upper
first-order shoots, and terminal shoots, respectively. The difference between means for lower and middle first-order shoots
was not significant at the 0.05 level.
Differentiation of buds along shoots
Sections of buds collected on Day 190 (July 9) showed no
evidence that differentiation (presence of leaf primordia on the
lower flanks of apical meristems) had occurred. The apical
meristems (apices) were rounded domes to rounded cones with
inner bud scales generally close to the apex surfaces (Figure 8).
Apices of lateral buds were situated at the level of the receptacle bearing the older bud scales, whereas apices of terminal
buds were situated well below the level of the receptacle
bearing older bud scales (e.g., Figures 8A and 8B). This massive receptacle development in terminal buds was most apparent in buds terminating upper shoots. These buds had the
broadest apices. The receptacle was only moderately raised
above the level of the bases of the narrower apices in terminal
buds on lower shoots. Most lateral buds on lower shoots, some
on middle shoots and occasional buds on upper shoots lagged
in development. Their apices were small, rounded domes,
which essentially lacked pith development in their lower parts
and in the tissues beneath. These buds were categorized as
Figure 7. Elongation after bud burst in 1993 of shoots borne along
1992 leaders of 20 P. rubens trees. Values on the curves indicate in
ascending order the mean percentages of the distances along their
respective leaders of three lower, three middle and three upper shoots,
and the new leaders (100% distance) of each tree. Vertical lines on the
curves are standard errors.
ACROTONY AND REPRODUCTIVE DEVELOPMENT IN PICEA
495
Figure 8. Median longitudinal sections of comparable parts of buds
from an upper shoot of one Picea
rubens tree, Day 190, showing over
half of the apical meristem (a), pith
(p) and receptacle (r and arrows)
bearing bud scales (s) (72×). (A) The
6th of 10 lateral buds positioned at
76% of the distance along the shoot,
and (B) the terminal bud.
latent. The pith areas of better-developed buds were distinctive (Figure 8), and the portions in and just below the lower
reaches of the apex stained darkly. The proportion of darkly
stained pith tissues tended to increase acropetally in buds
along individual shoots and upward among shoots.
Collections on Days 195 and 200 (July 14 and 19) showed
increases in proportions of more conical apices among lateral
buds. No indications of initiation of leaf primordia were observed on these apices (Figure 9). The outer flanks of the
broad apices of terminal buds of upper shoots provided the
first evidence of initiation of leaf primordia (Figure 10) as indicated by suggestive staining of surficial and associated
subsurface cells (Figure 10A), and as slight surficial
mounding among such cells (Figure 10B).
Figure 9. Median longitudinal sections of comparable parts of lateral
buds from upper shoots of two Picea
rubens trees (72×). (A) The 11th of
11 buds positioned at 95% of the distance along the shoot on Day 195,
and (B) the 2nd of 11 buds positioned at 45% of the distance along
the shoot on Day 200. Symbols as in
Figure 8.
Figure 10. Median longitudinal sections of comparable parts of terminal
buds from upper shoots of two Picea
rubens trees (72×). (A) Cellular patterns (arrows) suggestive of leaf-primordium initiation on Day 195, and
(B) bulging tissues and cellular patterns (arrows) indicating leaf primordium initiation on Day 200. Other
symbols as in Figure 8.
496
POWELL
Collections on Day 207 (July 26) showed that leaf primordia
had initiated in terminal buds of upper shoots. Leaf primordia
were also evident in terminal buds of some middle (Figure 11A) and lower shoots, and in distal lateral buds (Figure 11B) on upper shoots. By Day 207, dark staining of pith in
the lower reaches of and just below the apex was pronounced,
especially in the terminal and distal lateral buds. Outside the
pith zone, the peripheral flanks of the apex, where leaf
primordia were forming, were three to five cells thick.
By Day 215 (August 3), apices of terminal buds of upper
shoots were developing mammillary tips. Leaf primordia were
evident on lower flanks of apices of buds situated more
basipetally on shoots at all levels. On Day 221 (August 9),
proximally situated buds with well-developed apices (hence,
apparently not latent) showed little evidence of initiation of
leaf primordia (Figure 12A), whereas there was an acropetal
trend in the development of leaf primordia in buds along single
shoots (Figure 12B to 12F). Associated with this development
of leaf primordia, there were increases in apex size, density of
staining in the pith and relative height above the base of the
apex of the bud-scale-bearing receptacle (Figure 12). Buds
collected and dissected on Day 221 showed similar acropetal
trends in development of leaf primordia and in apex size and
shape.
Discussion
Acrotony among directly comparable shoots of similar origin
was expressed similarly in P. glauca, P. mariana and P. rubens. Shoot length was associated with bud size (Figure 6) and
with preformed bud composition (Baxter and Cannell 1978).
Shoot length was also associated with the propensity of the lateral axis to differentiate and develop into a cone or shoot, or
remain as a non-flushed bud. Although the cause of non-flushing of buds was not examined, their distribution (Figure 4)
suggests that most were latent buds. Sections of developing
P. rubens buds confirmed that many buds in more proximal
positions had small apices that appeared inactive. Latent buds,
which have been described in other Picea (e.g., Owens et al.
1977, 1992), represent a reserve of lateral axes that can be activated if more distally situated vegetative structures are destroyed (cf. Powell 1982). Also, in some genera of Pinaceae,
cone buds tend more frequently to take the place of latent buds
than of vegetative buds (Owens 1969, Powell 1977a). The occurrence of the three kinds of buds in Picea warrants further
investigation in relation to position on the shoot and to years of
varying cone abundance (cf. Powell 1977b).
The acrotoneous arrangement of shoots was also associated
with rate and duration of shoot elongation that led to an
acropetal increase in timing of cessation of shoot elongation.
The upper, longer shoots, which started to elongate slightly
earlier, exhibited a much greater rate of elongation and stopped
elongating 4 days later than the lower, shorter shoots. This
Figure 11. Median longitudinal sections of comparable parts of buds
from shoots of two Picea rubens trees
on Day 207 (72×). (A) Terminal bud
from a middle shoot, and (B) the 6th
of 7 lateral buds at 96% of the distance along an upper shoot. Arrows
indicate leaf primordia; other symbols as in Figure 8.
Figure 12. Median longitudinal sections of comparable parts of buds
from an upper shoot of one Picea
rubens tree on Day 221 (51×). (A–E)
2nd, 5th, 8th, 10th and 12th of 12 lateral buds at 34, 49, 71, 95 and 96% of
the distance along the shoot, respectively, and (F) the terminal bud.
ACROTONY AND REPRODUCTIVE DEVELOPMENT IN PICEA
pattern is consistent with that reported for shoots extending
principal branches of the crowns of large Picea trees (e.g.
Fraser 1966, Ford et al. 1987).
Morphological-anatomical evidence of differentiation of
buds on the acrotoneously arranged shoots followed neither
the upward (shorter to longer shoots) pattern of timing, suggested by the notion that differentiation occurs when shoot
elongation ceases, nor the outward (acropetal along shoots)
pattern of timing, suggested by the progressive completion of
elongation along a shoot (see Introduction). The evidence
indicates an opposite or basipetal pattern of timing of bud
differentiation. Terminal buds of upper shoots showed signs of
differentiation first. Differentiation was evident next in terminal buds of middle and some lower shoots, and in distal lateral
buds of upper shoots. Evidence of differentiation then moved
to medial lateral buds of upper shoots and distal lateral buds of
middle shoots, and then to more proximal buds on all shoots.
Mammillary tips to the apices, as described in some differentiating apices in other Picea (Owens and Molder 1976a,
Owens et al. 1977, 1992, Marquard and Hanover 1984b), were
observed only in terminal and distal lateral buds of the upper
and middle shoots, indicating that they are associated with
more vigorous development.
The times when evidence of differentiation became apparent
were associated with cessation of shoot elongation, but not in
a consistent manner. On upper shoots, differentiation of terminal buds became evident when shoots were completing elongation (95% completed). On middle and lower shoots,
differentiation of terminal buds became evident just after completion of shoot elongation. Thus the time when evidence of
differentiation became apparent was dependent on the relative
position of the parent shoot and the relative position of the bud
along the parent shoot.
The consistent pattern of cone distribution in the three Picea
species (Figure 5), coupled with the time when differentiation
became evident, indicates that the buds most likely to differentiate as cones should all show evidence of differentiation at
about the same time, and after shoot elongation has been
completed. Thus measures aimed at enhancing cone differentiation must take place before shoot elongation ends (cf. Marquard and Hanover 1984b, Ross 1985, Ho 1988). Moreover,
because visible evidence of differentiation must follow precursor events within the tissues of the buds or shoots, time must
be allowed for such events to occur after any given cone-enhancing treatment. However, the reaction times to stimuli of
differentiation appear to vary among shoots or among buds
along shoots. Thus the patterns of shoot elongation, of non-differentiation (latency) and differentiation, of sizes of bud apices
along shoots, and of density of staining in the pith in buds
along shoots provide an indication that response times may be
slower on shorter shoots and in proximal positions on longer
shoots. The corollary to this is that the rate of development
appears to be fastest in terminal buds of upper shoots. This, and
the finding that such buds normally do not differentiate as
cones, can be interpreted as a mechanism to ensure continued
vegetative development of the most vigorous shoots, and thus
expansion of the crown by means of the most distal branches
497
of any one year.
This study has demonstrated the complexity yet orderliness
of morphogenetic patterning in populations of similar shoots
in a region of the crown of young Picea trees and has provided
information on where and when changes associated with, or
precursive to, cone differentiation occur. The information
should be of value in designing treatments to enhance cone
production and in interpreting results of experiments on cone
induction.
Acknowledgments
This research was made possible through research grants from the
Natural Science and Engineering Research Council of Canada and the
University of New Brunswick Research Fund. The author thanks J.G.
Floyd, D.W. Gimby, M.H. Hancox and P. Pobihushchy for technical
assistance in the field and laboratory, and W.L. Staples for photographic processing.
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