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A SALUTE TO DR. MELVIN T. TYREE |
Plant Physiology
wishes to extend its hearty congratulations to Dr. Melvin
T. Tyree for his award of the prestigious Marcus Wallenberg Prize (Fig.
1). Sometimes
offhandedly described as "The Nobel Prize for Forestry," the
purpose of the Marcus Wallenberg Prize is to recognize, encourage, and
stimulate groundbreaking scientific achievements that contribute
significantly to the broadening of knowledge and to technical advances
within the fields of basic and applied forestry. Dr. Tyree was awarded
the 19th Marcus Wallenberg Prize for his numerous contributions
concerning the transport of water in trees. Dr. Tyree's scientific
work has been fundamental to the understanding of stress-induced
disruptions of water transport in trees. Through both his theoretical
contributions and his development and refinement of physiological
methods, he has made fundamental contributions to our understanding of
the importance of xylem cavitation in the ecology and physiology of
trees. Dr. Tyree's research also offers profound insight into the
evolution of wood structure and on the distribution of trees in forests
around the world.
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King Carl Gustaf of Sweden presented the 19th Marcus
Wallenberg Prize to Dr. Tyree (left) at a ceremony held in Stockholm on
September 26, 2002.
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Dr. Tyree has been a long-time contributor to Plant
Physiology and has written upon such a wide variety of topics
that it is impossible to do justice to his scientific contributions in two short pages. This tribute focuses solely on the contributions for
which he is perhaps best known
his studies of xylem embolisms.
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Mechanism of Xylem Embolism |
Water in the xylem is usually under tension, and this tension
increases as soil moisture decreases or transpiration rate increases. If the tension in the water column becomes too great, embolisms (gas
bubbles) form within the xylem vessel, and cavitation (breaking of the
water column) occurs, rendering the xylem conduit in which it occurs permanently or temporarily dysfunctional. The shock waves
produced by these rapid cavitation events can even be measured ultrasonically and under field conditions (Tyree and Dixon,
1983
). Numerous hypotheses have been put forward to explain how
water stress causes embolisms. The leading explanation is the
"air-seeding" hypothesis, which proposes that embolisms are
triggered by air aspirated into a vessel via pits in the wall where it
adjoins an air space. Once inside the vessel, the air disrupts the
cohesion of the water column, thereby causing a sudden retraction of
the water column and leaving behind a vessel filled with
water vapor and air. In support of the "air-seeding" hypothesis,
Sperry and Tyree (1988) found in their study of
sugar maples (Acer saccharum) that the pressure
difference between internal water-filled and air-filled vessels was
theoretically sufficient to cause air entry via pits. Moreover, a
specific treatment, namely the perfusion of the stem with a solution of
calcium and oxalate, increased (by means unknown) the permeability of
intervessel pits to the injection of air. Consistent with the "air
seeding" hypothesis, the calcium/oxalate treatment also caused xylem
vessels to cavitate at less negative pressures.
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The Refilling of Embolized Vessels |
The mechanisms underlying xylem recovery following drought- or
freezing-induced cavitation remain controversial. The leading paradigm
suggests that embolism removal occurs by gas dissolution in the
surrounding water. Since water in plants is saturated with air at
atmospheric pressure, this paradigm requires that the embolism be above
atmospheric pressure for the gases to redissolve. Indeed, most studies
have reported that embolism dissolution ceases when the gas pressure is
at or below atmospheric pressure. Various studies by Tyree and his
co-workers have lent support to this idea (Tyree and Yang
1992; Yang and Tyree 1992; Lewis et al., 1994). In most instances, gas in an embolism will exceed the
atmospheric pressure whenever the threshold xylem pressure is greater
than 
15 kPa. This condition is achieved in many plants
that develop root pressure at night or in the early spring. The problem
is that many species do not exhibit root pressure, including the gymnosperms and forest trees. Root pressure may facilitate the recovery
of embolized xylem conduits in herbs, shrubs, and small trees, but it
is unlikely to be a major factor in xylem recovery in tall trees
because of its dissipation by gravity. Thus, it is surprising that
embolisms do dissolve in plant species with little or no
root pressure. More recently, Tyree et al. (1999) studied the recovery of hydraulic conductivity after the induction of
embolisms in woody stems of laurel (Laurus nobilis), a
species that shows no detectable root pressure. They confirmed previous reports that the recovery of hydraulic conductivity in laurel occurs
even though the xylem pressure potential was less than 1 MPa.
Cryoscanning electron microscopic images revealed vessels in all three
states of presumed refilling: (a) mostly water with a little air, (b)
mostly air with a little water, or (c) water droplets extruding from
vessel pits adjacent to living cells. Although the xylem sap collected
by perfusion of excised stem segments showed elevated levels of several
ions during refilling, radiographic probe microanalysis of refilling
vessels revealed non-detectable levels of dissolved solutes. Based on
the these findings, Tyree et al. (1999) abjured, based
on physical grounds, all the proposed hypotheses that attempt to
explain xylem embolism repair while surrounding vessels are at a xylem
pressure potential of less than 1 MPa. They conclude that none of the
existing paradigms adequately explains their results. A genuine mystery!
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Vulnerabilty to Embolism and Plant Distribution |
Dr. Tyree has been the leading champion of the idea that
vulnerability to embolisms may be a major factor in determining plant distribution. An important aspect of embolisms is that even one embolism will decrease the hydraulic conductivity of the plant, thereby
creating even greater tension in the remaining functional xylem
conduits. Some of these, in turn, may start to form embolisms, and soon
this catastrophic process spirals out of control. In fact, Tyree and
Sperry (1988) have argued that many woody plants normally operate near the point of catastrophic xylem dysfunction. Vulnerability to embolisms caused by drought or freezing may go a long
way toward explaining species distributions. Oaks
(Quercus spp.), for example, seem to operate close to
the point of xylem dysfunction, but oaks protect against embolism by
stomatal regulation that keeps water potentials above those that would
cause "run-away" embolisms. Tyree and Cochard (1996)
concluded that embolism plays little role in the drought tolerance of
oaks since drought-induced embolism occurs at more negative water
potentials than are known to cause damage (e.g. reduced growth). On the
other hand, frost-induced embolism may explain species distributions in
cold climates.
In recent years, Dr. Tyree's research has turned increasingly toward
elucidating the role of xylem embolism formation within the context of plant ecology and evolution. For example, Tyree et al.
(1994) have argued that although the efficiency of water transport increases in vessels with increasing diameter, the
vulnerability of large diameter vessels to frost-induced embolism
is dramatically increased. Thus, there is a selection for small
diameter vessels in cold climates. The relationship between vessel
diameter and vulnerability of large diameter vessels to drought-induced
embolism is much weaker. The correlation is too weak to permit
comparative physiologists to predict vulnerability based on vessel
diameter, but the correlation is strong enough to be of some
evolutionary significance.
Perhaps some of the widest vessels are found in tropical lianas.
This raises the question of whether lianas are especially prone to the
formation of xylem embolisms in nature. Given that tropical rain
forests are generally moist and frost-free, it is not clear that
lianas are exposed in nature to conditions that would favor the
formation of embolisms. Alternatively, it is possible that embolisms do
occur in tropical lianas, but the refilling of xylem vessels by root
pressure may be particularly effective in tropical lianas. To shed
light on this question, Ewers et al. (1997) measured
pre-dawn xylem pressures in 32 Panamanian species of vines
to determine if pressures were sufficient to allow for possible
refilling of embolized vessels. In all 29 dicotyledons examined, the
xylem pressures were not sufficient to refill embolized vessels in the
upper stems. In contrast, two of the smaller, non-dicotyledonous vines,
the climbing fern Lygodium venustrum and the vine-like bamboo Rhipidocladum racemiflorum, had xylem pressures
sufficient to push water to the apex of the plants. Therefore, a root
pressure mechanism to reverse embolisms in stem xylem could apply to
some but not to most of the climbing plants that were studied.
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A SALUTE TO DR....
Mechanism of Xylem Embolism