Tree Physiology 35, 451–452
doi:10.1093/treephys/tpv042
Commentary
Evolution in the smallest valves (stomata) guides even
the biggest trees
Timothy J. Brodribb1,2 and Scott A.M. McAdam1
1Department
of Plant Science, University of Tasmania, Hobart, Tasmania, Australia; 2Corresponding author ([email protected])
Received April 23, 2015; accepted May 7, 2015; handling Editor Danielle Way
The regal stature of the redwood sister-giants, Sequoia and
Sequoiadendron, makes them internationally renowned icons of
size and longevity. Yet an examination of the evolutionary history
of the sequoiid clade (which includes the dawn redwood—
Metasequoia) quickly dispels the impression that these trees are
an immutable part of the landscape. Fossil data show that these
species are relicts of a lineage that once extended North to the
Arctic Circle and as far south as Australia (­Hill and Brodribb
1999, ­Ahuja and Neale 2002), and like many other basal lineages of the Cupressaceae, the three extant sequoiid genera
have been subject to systematic extinction that has left only
monotypic representatives alive today. Similar to other basal
Cupressaceae, Sequoia and Sequoiadendron are confined to
humid forest or fog belts, a habitat that appears to be very vulnerable to climate warming and associated drought (­Pounds
et al. 1999). This is an important context because an extreme
drought event is currently occurring across the entire range of
both species, raising pertinent questions about how effectively
these species are able to manage water stress. Of particular
concern is whether this current drought represents a threat to
the survival of trees. Answering such a question demands quantitative knowledge of what constitutes a damaging level of water
stress in these species. A study by Ambrose et al. (2015) in this
issue of Tree Physiology provides some answers to this critical
question, while at the same time providing new insights into the
surprisingly different ways these sister-species respond to water
stress.
of what type of drought conditions are likely to cause plants to
suffer and die. This is a tricky job because death by drought in
large trees is often a sad, drawn out process, whereby plants can
decline and die years after an original triggering water-stress
event (­Anderegg et al. 2013). A lot of interest has thus been
focused on the concept of hydraulic failure as an explanation for
plant death, because a water potential threshold at which the
water transport system begins to catastrophically fail can be
determined in excised plant material without the need for
lengthy experiments droughting whole plants. Confirmation that
death by cavitation-induced hydraulic failure is a reality in trees
(­Brodribb and Cochard 2009), and that the distribution of tree
species is limited by their ability to resist cavitation (­Choat et al.
2012), provides some hope of defining a general index of desiccation tolerance for all trees. The problem with this method,
even if we stay above ground and ignore the possibility plants
may run out of carbon (­McDowell et al. 2008), is that the rate
of drying during drought is determined largely by the stomata.
For this reason, the countdown to mortality progresses at a
tempo set by stomatal function. Ultimately, the xylem vulnerability determines a lethal threshold in terms of soil or plant water
content, while stomatal function regulates the rate at which this
lethal threshold is approached during periods of drought. For
this reason, any attempt to quantify the susceptibility of species
to drought must consider the physiology of both stomatal and
xylem tissues, as done by Ambrose et al. (2015) in their evaluation of Sequoia and Sequoiadendron.
Countdown to death
Divergent possibilities
With climate change in rapid progress there is an increasing
urgency for tree physiologists to provide quantitative predictions
The interaction of xylem and stomatal behaviour is part of a
recently popular ‘strategic framework’ used to separate plant
© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
452 Brodribb and McAdam
a­ daptation to water stress into two behavioural types (­isohydry
and anisohydry), which derive from contrasting stomatal sensitivities to water potential (­Tardieu and Davies 1992, ­Skelton
et al. 2015). Isohydry is characterized by species with stomata
that close early during water stress, while anisohydric species
have stomata that close very gradually during the development of
water stress, allowing water loss and photosynthesis to proceed
as plant water potential falls. These two different stomatal behaviours are associated with different benefits during water stress
(Figure 1) but it has been argued that both strategies have
accompanying trade-offs that permit the co-existence of both
functional types in dry forests (­McDowell et al. 2008). However,
despite an acceptance of the ecological significance of these
functional types, little is known about the prevalence of stomatal
iso- or anisohydry in forests, though there are suggestions that a
spectrum of responses can be observed (­Klein 2014). Among
conifers it has been shown that contrasting iso/anisohydric
stress–response behaviours are linked to divergent trends in both
xylem vulnerability to cavitation, and foliar dynamics of abscisic
acid (ABA) during plant desiccation, with a strong phylogenetic
component determining functional type (­Brodribb et al. 2014).
Importantly, it was shown that dry environments appear to have
forced species to diverge strongly in terms of both stomatal
behaviour and xylem vulnerability, such that a strong expression
of iso- or anisohydric syndromes are more likely confined to dry
environments (­Brodribb et al. 2014).
Given that the dynamics of ABA levels during water stress are
likely to be a key determinant of stomatal behavioural type
Figure 1. Plants in dry climates employ one of two divergent strategies
for closing stomata and preventing desiccation during periods of acute
water stress, isohydry or anisohydry. Isohydric plants utilize high levels
of ABA to close stomata (­Brodribb et al. 2014), at the cost of an early
loss of photosynthetic assimilation (A) during drought, and a slow recovery of gas exchange after rainfall. In contrast, anisohydric plants utilize
low leaf water potentials (Ψl) to close stomata during acute water stress,
bearing the cost of expensive (high-density, cavitation-resistant) xylem,
and/or cavitation during prolonged drought. Two dry habitat species
representing these divergent strategies are shown, Pinus edulis (isohydry
in Utah, USA) and Juniperus thurifera (anisohydry in the Atlas Mountains,
Morocco).
Tree Physiology Volume 35, 2015
(­Brodribb and McAdam 2013), the divergence between iso- and
anisohydric behaviours may be under the control of relatively
few genes, namely those regulating ABA synthesis or catabolism. In this respect, the study of Sequoia and Sequoiadendron
during imposed water stress presented in this issue by Ambrose
et al. (2015) provides a fascinating example of incipient divergence in drought-response strategies. Both species are at the
very moderate end of the stomatal or xylem functional spectrum,
suggesting that neither is particularly resilient in terms of resisting drought. However, there is a clear difference in the water
potential exposure of these two species, with Sequoiadendron
behaving like most of the ‘old’ Cupressaceae (­Brodribb et al.
2014), as a water-conserving isohydric trees, while Sequoia
appears to be diverging down the path of anisohydry. This surprising pattern suggests that these two old sisters still have
some important stories to tell us about survival under water
stress.
References
Ahuja MR, Neale DB (2002) Origins of polyploidy in coast redwood
(Sequoia sempervirens (D. Don) Endl.) and relationship of coast redwood to other genera of Taxodiaceae. Silvae Genet 51:93–100.
Ambrose AR, Baxter WL, Wong CS, Næsborg RR, Williams CB, Dawson
TE (2015) Contrasting drought-response strategies in California redwoods. Tree Physiol 35:453–469.
Anderegg WRL, Plavcová L, Anderegg LDL, Hacke UG, Berry JA, Field CB
(2013) Drought’s legacy: multiyear hydraulic deterioration underlies
widespread aspen forest die-off and portends increased future risk.
Glob Change Biol 19:1188–1196.
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery
and point of death in water-stressed conifers. Plant Physiol
149:575–584.
Brodribb TJ, McAdam SAM (2013) Abscisic acid mediates a divergence in
the drought response of two conifers. Plant Physiol 162:1370–1377.
Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent
pathways. Proc Natl Acad Sci USA 111:14489–14493.
Choat B, Jansen S, Brodribb TJ et al. (2012) Global convergence in the
vulnerability of forests to drought. Nature 491:752–755.
Hill RS, Brodribb TJ (1999) Southern conifers in time and space. Aust J
Bot 47:639–696.
Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and
anisohydric behaviours. Funct Ecol 28:1313–1320.
McDowell N, Pockman WT, Allen CD et al. (2008) Mechanisms of plant
survival and mortality during drought: why do some plants survive
while others succumb to drought? New Phytol 178:719–739.
Pounds JA, Fogden MPL, Campbell JH (1999) Biological response to
climate change on a tropical mountain. Nature 398:611–615.
Skelton RP, West AG, Dawson TE (2015) Predicting plant vulnerability to
drought in biodiverse regions using functional traits. Proc Natl Acad
Sci USA 112:5744–5749.
Tardieu F, Davies WJ (1992) Stomatal response to abscisic acid is a
function of current plant water status. Plant Physiol 98:540–545.