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Plant Physiol. (1998) 117: 1463-1471
Visualization of Cavitated Vessels in Winter and Refilled Vessels
in Spring in Diffuse-Porous Trees by Cryo-Scanning Electron
Microscopy1
Yasuhiro Utsumi,
Yuzou Sano*,
Seizo Fujikawa,
Ryo Funada, and
Jun Ohtani
Department of Forest Science (Y.U., Y.S., R.F., J.O.), and
Institute of Low Temperature Science (S.F.), Hokkaido University,
Sapporo 060, Japan
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ABSTRACT |
Xylem cavitation in winter and
recovery from cavitation in the spring were visualized in two species
of diffuse-porous trees, Betula platyphylla var.
japonica Hara and Salix sachalinensis Fr.
Schm., by cryo-scanning electron microscopy after freeze-fixation of
living twigs. Water in the vessel lumina of the outer three annual
rings of twigs of B. platyphylla var.
japonica and of S. sachalinensis
gradually disappeared during the period from January to March, an
indication that cavitation occurs gradually in these species during the
winter. In April, when no leaves had yet expanded, the lumina of most
of the vessels of both species were filled with water. Many vessel
lumina in twigs of both species were filled with water during the
period from the subsequent growth season to the beginning of the next
winter. These observations indicate that recovery in spring occurs
before the onset of transpiration and that water transport through
twigs occurs during the subsequent growing season. We found, moreover,
that vessels repeat an annual cycle of winter cavitation and spring
recovery from cavitation for several years until irreversible
cavitation occurs.
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INTRODUCTION |
In plants "cavitation" refers to the formation of a cavity
within a body of water, usually in the xylem water-transport system (Milburn, 1991 ). All conduits for the transport of water in plants are
potentially vulnerable to cavitation. Cavitation disrupts water
transport and long-term consequences can include reduced growth and
dieback of the plant. Cavitation occurs mainly in response to water
stress or freezing (Tyree and Sperry, 1989), and cavitation caused by
water stress has been explained in terms of air-seeding, as follows.
When the tension inside xylem conduits exceeds a certain critical
value, air is sucked into the lumina of water-filled conduits from
adjacent gas-filled conduits through the pores of intervascular pit
membranes (Zimmermann, 1983; Sperry and Tyree, 1988). By contrast, the
cavitation that is caused by freezing seems to occur as a result of the
low solubility of gases in ice. When frozen sap containing air bubbles
thaws under tension, air bubbles expand in the xylem conduits and
cavitation occurs (Zimmermann, 1983; Sperry, 1993).
In dicotyledonous trees the region of the xylem that functions in water
transport varies among species. In ring-porous trees it is the
earlywood vessels of the current-year xylem that are mainly involved in
water transport (Chaney and Kozlowski, 1977; Ellmore and Ewers, 1986).
The earlywood vessels lose the capacity to function in the transport of
water by the end of each winter, and no refilling with water occurs in
these vessels during the following spring (Zimmermann, 1983).
Consequently, earlywood vessels play a role in water transport during a
single growth season. The cavitation that occurs in earlywood vessels
of ring-porous trees is believed to be irreversible.
In diffuse-porous trees, by contrast to ring-porous trees, water
transport generally occurs in a larger part of the sapwood (Greenidge,
1958; Chaney and Kozlowski, 1977). This observation indicates that
vessels in diffuse-porous trees may continue to function as pathways
for water transport for several years. Two possibilities might explain
how water transport is maintained for several years in the vessels of
diffuse-porous trees. One possibility is that newly formed vessels
might retain the ability to function in water transport for several
years in the absence of cavitation until irreversible cavitation
occurs. Alternatively, functional vessels might repeat a cycle of
cavitation and recovery for several years until irreversible cavitation
occurs. However, these possibilities have not yet been examined.
Seasonal changes in water transport have been
characterized mainly in terms of hydraulic conductivity (Sperry et al.,
1988; Cochard and Tyree, 1990). It has been reported that in
diffuse-porous trees hydraulic conductivity is lower in the winter than
in other seasons (Sperry and Sullivan, 1992; Magnani and Borghetti,
1995), an indication that water transport is disrupted during the
winter in diffuse-porous trees. This method has yielded important
information about quantitative analysis in seasonal changes in water
transport, but it is indirect and does not reveal the location of
cavitated vessels in xylem or the state of water inside vessels
(McCully et al., 1998). In particular, it is difficult to reveal
whether air occupies the entire lumina of vessels or whether only small air bubbles are present inside the vessels.
Cryo-SEM allows fixation of water as ice crystals in cell lumina and
visualization of the precise location of water in the xylem of living
trees (Ohtani and Fujikawa, 1990; Utsumi et al., 1996). However,
during the growing season, water moves from roots to leaves as a
consequence of the negative pressure that is created in the leaf xylem
by transpiration. Zimmermann and Brown (1971) proposed that the water
in vessels is replaced by air when the pressure in these conduits falls
below atmospheric pressure and the conduits are exposed to air. To
prevent this phenomenon during cutting of twigs, we froze the twigs of
living trees in LN2, and stored the samples at subzero
temperatures prior to cryo-SEM. In our previous study, in which we
applied these techniques for an examination of the seasonal progression
of xylem cavitation in Fraxinus mandshurica var.
japonica, we obtained valuable information about the process
and timing of cavitation in the earlywood vessels of a species of
ring-porous trees (Utsumi et al., 1996). In the present study we
attempted to visualize seasonal changes in the distribution of water in
two species of diffuse-porous trees, B. platyphylla var.
japonica Hara and S. sachalinensis Fr. Schm., by
cryo-SEM after freeze-fixation of living twigs to characterize the
seasonal progression of xylem cavitation.
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MATERIALS AND METHODS |
Plant Materials and Sampling
Two mature trees of Betula platyphylla var.
japonica Hara (height, about 8 m; diameter at breast
height, about 15 cm) and of Salix sachalinensis Fr. Schm.
(height, about 15 m; diameter at breast height, about 40 cm)
growing on the campus of Hokkaido University (Sapporo, Japan) were
used. Twig internodes with three to four annual rings were collected at
monthly intervals from the beginning of March, 1996, to the end
of April, 1996, and from the beginning of November, 1996, to the end of
April, 1997. The sample twigs for summer measurements were collected in
August, 1996, only. Four twigs per species were obtained in each
sampling time. In a preliminary investigation, we found that several
sample trees had similar moisture contents.
Samples were collected after the xylem sap had been fixed by freezing
the twigs on living trees by the previously described procedure (Utsumi
et al., 1996). Watertight collars were made with plastic funnels as
containers for LN2, and fitted to the sample
twigs. Then, the collars were filled with LN2 and
the twigs were allowed to freeze for approximately 5 min. Twigs that
contained completely frozen regions (over 5 cm in length) were
immediately removed from the sample trees and stored in a container
with LN2.
Cryo-SEM
The sample twigs that had been stored in LN2
were transferred to a low-temperature room kept at  20°C and were
divided into small specimens (1 cm in length). These specimens were cut
into small blocks (5 × 5 × 5 mm3)
that included part of the outer three annual rings and phloem. One to
four blocks were selected from each twig. Transverse, tangential, or
radial surfaces of the each block were cleanly cut with steel blades on
a sliding microtome to expose cell lumina (Sano et al., 1993, 1995).
Then, the blocks were attached to specimen holders with a drop of
glycerol and further fastened with a screw. The specimen holder with
the sample immersed in LN2 was transferred to a
system for cryo-SEM (model JSM840-a, Jeol) and was fixed on the cold
stage of the freeze-etching unit, which was maintained under a vacuum
of approximately 1 × 10 4 Pa and
equilibrated to 108°C. The specimen was freeze-etched under these
conditions for about 10 min to eliminate contamination by frost, and
then it was rotary-shadowed with a platinum-carbon pellet. The sample
was transferred to the cold stage of the SEM, which was kept at about
160°C, and secondary electron images were observed and recorded at
an accelerating voltage of 5 kV (Fujikawa et al., 1988).
To evaluate seasonal occurrence of cavitation quantitatively, 1.5- × 1.5-mm2 areas containing more than 100 vessel
elements of the outer two annual rings were selected from the cryo-SEM
photographs of the transverse surface of each sample. The number of
water-filled and cavitated vessel elements were counted and the
percentage of cavitated vessel elements was determined.
Environmental Temperatures
Daily minimum and maximum air temperatures and the temperature of
the soil 10 cm below the surface of the ground were recorded at the
Experimental Farm of Hokkaido University, which is located about 1 km
from the site where sample trees were growing from March, 1996, to
March, 1997, for evaluation of the relationship between cavitation and
freezing.
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RESULTS |
Seasonal Changes in the Distribution of Water in Twigs
The distribution of water in twigs was visualized by cryo-SEM.
Seasonal changes in the distribution of water in vessels and fibers of
twigs of B. platyphylla var. japonica and
S. sachalinensis were similar, with the exception of those
in March, when no leaves had yet expanded and current-year xylem had
not yet differentiated. No differences in the distribution of water
were found among annual rings. Figure 1A
shows an example of xylem from the previous year's growth from
B. platyphylla var. japonica. Some vessels were
filled with water (large arrow), whereas others were completely empty (small arrow). Most fibers had no water in their lumina. Similarly, Figure 1B shows an example of xylem from the previous year's growth from S. sachalinensis. Both water-filled vessels and empty
vessels were found. Vessels near the terminal zone of the annual ring, however, consistently had water in their lumina (arrows). On tangential surfaces, almost all vessels were found to be cavitated (Fig. 1, C and
D). Some vessels were completely empty (Fig. 1C, v), whereas other
vessels still had some water in their lumina (Fig. 1D, *). Many fiber
lumina were empty, but a few fibers had some water in their lumina
(Fig. 1C, *). The percentage of cavitated vessel elements was about
80% in B. platyphylla var. japonica and about
70% in S. sachalinensis in a given area of the outer two
annual rings (Fig. 2).
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| Figure 1.
Cryo-SEM photographs of Betula
platyphylla var. japonica and Salix
sachalinensis in March. A, Transverse surface of the xylem from
the previous year's growth of B. platyphylla var.
japonica. Some vessels were filled with water (large
arrow), whereas others were completely empty (small arrow). B,
Transverse surface of the xylem from the previous year's growth of
S. sachalinensis. Some vessels were filled with water;
others contained no water. Vessels near the terminal zone of an annual
ring contained water in their lumina (arrows). C, Tangential surface of
B. platyphylla var. japonica. Vessels (v)
contained no water. Drops of water (*) were present in fiber lumina
(f). D, Tangential surface of B. platyphylla var.
japonica. A drop of water (*) can be seen in a vessel
lumen (v).
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| Figure 2.
Seasonal changes of percentage of cavitated vessel
elements during the period from March, 1996, to April, 1997. Means for
four twigs per one species are shown with 95% confidence intervals.
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In April, when the leaves had still not yet expanded, almost all of the
vessels of B. platyphylla var. japonica (Fig.
3A) and S. sachalinensis (Fig.
3B) were filled with water. Cell division in the cambium had begun in
S. sachalinensis, but not in B. platyphylla var.
japonica. Figure 3C shows an example of the xylem from the previous year's growth of S. sachalinensis. The vessel
lumina were completely filled with water and the lumina of axial and ray parenchyma cells were filled with cytoplasm (arrows). In contrast to samples collected in March, almost all vessel lumina were completely filled with water, as seen in the radial view (Fig. 3D, v). The percentage of cavitated vessel elements was near 0% in both species (Fig. 2).
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| Figure 3.
Cryo-SEM photographs of B. platyphylla var. japonica and S. sachalinensis in April. A, Transverse surface of the xylem from
the previous year's growth of B. platyphylla var.
japonica. All vessels (v) were filled with water. B,
Transverse surface of the xylem from the previous year's growth of
S. sachalinensis. All vessels were filled with water. C,
Transverse surface of S. sachalinensis. All vessels were
filled with water. Axial and ray parenchyma cells were filled with
cytoplasm (arrows). D, Radial surface of S. sachalinensis. The vessel shown was completely filled with
water.
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In August, leaves were fully expanded and new wood was being formed. In
the xylem that had been formed during the previous year and the year
prior to that, most vessels were filled with water, but a few vessels
were completely or partially cavitated. Most wood fibers had no water
in their lumina. In the newly forming current-year xylem, most vessels
and wood fibers were filled with either water or cytoplasm (Fig.
4A). Wood fibers without water in their
lumina were found only in the initial zone of the current-year's annual ring (Fig. 4B, arrows). The percentage of cavitated vessel elements was about 10% in both species (Fig. 2).
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| Figure 4.
Cryo-SEM photographs of S. sachalinensis in August. A, Transverse surface of the newly
forming current-year xylem. Most vessels and fibers were filled with
water or cytoplasm. B, Initial zone of newly forming current-year
xylem. All vessels (v) were filled with water. Fibers without water in
their lumina were also found (arrows).
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During the period from November to February, when all leaves had
fallen, the percentage of cavitated vessel elements gradually increased
(Fig. 2). The amount of water retained within vessels differed among
the cavitated vessels, but such differences were independent of the
time of sampling. In November, many vessels were filled with water,
whereas almost all wood fiber lumina were empty (Fig.
5, A and B). No apparent differences were
observed between November and December. In January, the numbers of
cavitated vessel elements increased (Figs. 2 and 5C). Furthermore, both water-filled wood fibers (Fig. 5D, large arrow) and empty fibers were observed (Fig. 5D, small arrow). In February, the number of
cavitated vessel elements increased still further (Figs. 2 and 5E).
Almost no wood fibers had water in their lumina (Fig. 5F). Resembling
results from 1996, most vessel lumina had no water in March, 1997, and
were refilled with water in April, 1997 (Fig. 2).
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| Figure 5.
Cryo-SEM photographs of B. platyphylla var. japonica in winter. A,
Transverse surface of current-year xylem in November. Most vessels were
filled with water, whereas almost all fiber lumina were empty. B,
Current-year xylem in November. Vessels (v) were filled with water. C,
Transverse surface of previous-year xylem in January. Some vessels were
filled with water but others contained no water. D, Previous-year xylem
in January. Both water-filled fibers (large arrow) and empty fibers
(small arrow) were present. E, Transverse surface of previous-year
xylem in February. Most vessels were empty. F, Previous-year xylem in
February. Most vessels and fibers contained no water.
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The results of this study are schematically illustrated in Figure
6.
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| Figure 6.
A schematic representation of seasonal changes in
the distribution of water in vessel and wood-fiber lumina of B. platyphylla var. japonica. The double-headed
arrow shows a newly formed annual ring.
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Environmental Temperatures
To study the relationship between cavitation and stress due to
freezing, we analyzed seasonal change in air and soil temperatures. Figure 7 shows the daily maximum and
minimum air temperatures, as well as soil temperatures, recorded at the
Experimental Farm of Hokkaido University from March, 1996, to March,
1997. From March, 1996, to April, 1996, the temperature profiles
(including that of the soil) increased rapidly. The first subzero
minimum temperature was recorded in late October, and the first subzero maximum temperature was recorded in mid November, 2 d before the sampling date. During the subsequent winter, the daily minimum air
temperature decreased to and remained below 10°C on 12 separate days. No subzero soil temperatures were recorded during this period.
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| Figure 7.
Changes in air and soil temperatures during the
period from March, 1996, to April, 1996, and October, 1996, to March,
1997. Soil temperatures were measured 10 cm beneath the surface of the
soil.
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DISCUSSION |
From January to March, the number of cavitated vessels increased
steadily in the outer three annual rings of twigs of B. platyphylla var. japonica and S. sachalinensis (Figs. 1, 2, and 5). In January, cavitation was
found in only a few vessels but by March, the number of cavitated
vessels had greatly increased. These results indicate that xylem
cavitation starts in early winter and progresses steadily during the
winter in both of the species examined. Gradual progression of
cavitation is in contrast to the simultaneous cavitation of earlywood
vessel in ring-porous trees. In our previous study, which was designed
to monitor the seasonal progression of cavitation in F. mandshurica var. japonica (a ring-porous tree) and
which was performed by the same methods used in this study, all of the earlywood vessels were simultaneously cavitated in early winter (Utsumi
et al., 1996).
During the period from December to March, the daily minimum air
temperature fell below 10°C on several occasions (Fig. 7). This
infrequent incidence of low temperatures might have been sufficient to
freeze the sap in vessel lumina; in fact, it is likely that the sap was
frozen and thawed several times during the winter. In diffuse-porous
trees, repeated cycles of freezing and thawing might result in the
progression of cavitation. Differences in the progression of cavitation
between diffuse-porous trees and ring-porous trees have been observed
by many investigators in studies of the seasonal progression of
cavitation by determinations of hydraulic conductivity. In
dicotyledonous trees, hydraulic conductivity decreases in the winter
(Sperry and Sullivan, 1992; Magnani and Borghetti, 1995; Pockman and
Sperry, 1997). The extent of the loss of hydraulic conductivity depends
on the species. In general, loss of hydraulic conductivity is less
extensive in diffuse-porous than in ring-porous trees (Sperry, 1993;
Hacke and Sauter, 1996). Moreover, in a study of ring-porous trees, the
first hard frost induced an abrupt loss of hydraulic conductivity (Cochard and Tyree, 1990).
Such differences in the progression and extent of cavitation caused by
freezing appear to be due to differences in conduit diameter (Tyree et
al., 1994; Cochard and Tyree, 1990). Ewers (1985) examined the
stability of freezing-induced air bubbles in water contained in glass
capillary tubes of various diameters. In these experiments, when the
water in narrow capillary tubes was frozen and thawed, air bubbles
formed during freezing and disappeared soon after thawing. These
capillary tubes were of similar diameter to the large earlywood
tracheids of conifers. By contrast, air bubbles formed during freezing
in large glass capillary tubes, with diameters similar to those of
earlywood vessels of ring-porous trees, were present for a long time
after thawing. Evidence suggesting similar tendencies has been obtained in other plant materials. It has been reported that most conifers are
entirely resistant to cavitation caused by freeze-thaw cycles, whereas
dicotyledonous trees are vulnerable to such cavitation (Hammel, 1967;
Sperry et al., 1994). The decrease in hydraulic conductivity in
diffuse-porous trees was reported to be smaller than that in
ring-porous trees during the winter (Sperry and Sullivan, 1992). In the
present study vessels near the terminal zone of the annual rings of
S. sachalinensis, which had relatively small diameters,
retained water in March (Fig. 1B), although about 70% of vessel
elements were cavitated in the outer two annual rings (Fig. 2).
Our cryo-SEM observations provide some crucial information about the
process and timing of refilling of vessels. In April, when the leaves
had not yet expanded, almost all of the vessel lumina of twigs of
B. platyphylla var. japonica and S. sachalinensis were completely refilled with water (Fig. 3). Most
of these refilled vessels retained water in their lumina in August.
These results indicate that spring recovery from winter cavitation
prior to leaf expansion and water transport occurs in most vessels in
twigs during the subsequent growth season. In general, water transport in plants has mainly been explained by the so-called cohesion theory
(Dixon, 1914; Kramer and Kozlowski, 1960; Kozlowski, 1961). Leaves had
not yet expanded in April, however, when the vessels had already been
refilled with water. Recovery from winter cavitation clearly occurred
before the onset of transpiration in both species examined.
Root pressure is considered to play a major role in the spring recovery
from xylem cavitation (Sholander et al., 1955; Sperry et al., 1987,
1988). Positive pressures have been measured in many woody species
(O'Malley and Milburn, 1983; Steudle, 1994; Hacke and Sauter, 1996).
Such positive root pressure could dissolve the gas in the sap and push
undissolved gas out of the vessels until cavitated vessels become
filled with water (Sperry et al., 1987). However, it has been noted
that root pressure is insufficient to push water up to the crown of a
mature tall tree (Steudle, 1995). In addition, recovery from cavitation
in the absence of root pressure has been suggested in conifers
(Borghetti et al., 1991; Grace, 1993; Sperry, 1993). Borghetti et al.
(1991) suggested that capillary action might help to refill tracheids.
In our experiments no measurements were made of the root pressure,
therefore it is not possible to state the mechanisms of the refilling
of cavitated vessels. If spring recovery from winter cavitation was
caused by root pressure, refilling of cavitated vessels would progress upward from the basal portion of trunk to crown. To evaluate the contribution of root pressure to the refilling, it is necessary to
examine the differences in the distribution of water among heights.
We observed changes in the distribution of water in the wood fibers of
the newly forming current-year xylem during the growth season. In
August, water or cytoplasm was present in lumina of newly forming wood
fiber, and had disappeared by early winter. The disappearance of water
from the wood fibers started in the initial zone of the current-year
annual ring and progressed toward the terminal zone of the annual ring
(Fig. 4). A similar result was observed in F. mandshurica
var. japonica (Utsumi et al., 1996). The disappearance of
water from wood fibers would be associated with their maturation.
We also found changes in the distribution of water in mature wood
fibers in winter. In January, when the current-year xylem had
completely matured and some vessels had been cavitated, some fiber
lumina were refilled with water. This phenomenon was not confined to
the current-year xylem but was also observed in older annual rings.
Utsumi et al. (1996) reported that in F. mandshurica var.
japonica, wood fibers surrounding current-year earlywood vessels were refilled with water when these vessels were cavitated in
November. They proposed that water might migrate from newly formed
earlywood vessels to the wood fibers around the vessels when cavitation
occurred. In B. platyphylla var. japonica and S. sachalinensis, it is also possible that water might move
from vessels to wood fibers when cavitation occurs in winter, as seems to be the case in F. mandshurica var. japonica.
However, the wood fibers that surrounded vessels were not always filled
with water in the two species examined in this study (Fig. 5, C and D).
The appearance of water-filled wood fibers seemed to be unrelated to
the arrangement of vessels. More detailed information about the
relationship between the cavitation of vessels and the refilling of
wood fibers with water might provide some clues to the mechanisms of
cavitation that is caused by freezing.
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FOOTNOTES |
1
This study was supported in part by a
Grant-in-Aid for Scientific Research (no. 08456083) from the Ministry
of Education, Science, and Culture, Japan.
*
Corresponding author; e-mail pirika{at}for.agr.hokudai.ac.jp; fax
81-11-736-1791.
Received January 26, 1998;
accepted May 19, 1998.
| |
ABBREVIATIONS |
Abbreviations:
LN2, liquid nitrogen.
SEM, scanning
electron microscopy.
| |
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Top
Abstract
Introduction