Current Biology Vol 21 No 14
R540
Dispatches
Stomata: Active Portals for Flourishing on Land
Two studies suggest early land plants could actively control stomata,
facilitating gas exchange while limiting water loss, a critical adaption to life
on land.
John L. Bowman
The conquest of land by plants was an
evolutionary process that began more
than 450 million years ago (MYA) [13]
with far-reaching consequences for
Earths climate and ecology. Molecular
phylogenetic and paleobotanical
ultrastructural data indicate that land
plants evolved from freshwater algae
[4,5] (Figure 1). The terrestrial
environment presented numerous
challenges for plants with aquatic
ancestry. Plants very early evolved an
impermeable outer coating called
a cuticle, possibly present in their
semi-emergent algal ancestors [4], that
prevents desiccation but also prevents
direct gas exchange. For plants larger
than a few cell layers thick, the reduction
in gas exchange severely limits the
availability of CO2 required for
photosynthesis, and most land plants
have microscopic valves called stomata
in their epidermis to both facilitate gas
exchange and limit water loss. Stomata
are composed of two specialized
epidermal cells called guard cells that
face each other. Increasing turgor
pressure causes the guard cells to
deform, opening a pore between them,
while loss of turgor results in closure
of the pore. In extant vascular land
plants, stomata operate to allow
plants to maximize carbon gain by
photosynthesis while limiting water
loss in transpiration under changing
environmental conditions [6].
Extant land plants include three
non-vascular lineages, the liverworts,
mosses and hornworts, collectively
known as bryophytes (Figure 1). The
remaining extant land plants are
together known as the vascular plants as
they all share an internal, highly complex
water-conducting tissue called xylem.
The earliest vascular plants were much
less morphologically and anatomically
complex than extant vascular plants,
lacking roots and leaves. Intriguingly,
stomata occur on both the sporophyte
and gametophyte generations of the
400 million year old Rhynie Chert flora,
which date to the origin of vascular
plants, raising the possibility that early
vascular plants may have had stomata in
both generations [7]. Stomata in these
ancient plants occurred on naked
stem-like axes with small central strands
of conducting cells and opened to
internal air spaces as in extant vascular
plants, suggesting a role in gas
exchange [7]. Active control of stomata,
as occurs in extant vascular plants, in
response to numerous environmental
cues, including light and CO2
concentration, and the drought hormone
abscisic acid (ABA), would presumably
have proven beneficial for controlling
rates of water loss from early Paleozoic
plants with limited rooting and water-
conducting systems [8]. This would have
been especially important since early
vascular plants likely experienced both
restricted water supply and high
evaporative demand when they were
exposed to full sunlight before the
evolution of plant communities large
enough to cast shade.
While active control of stomata in
response to environmental conditions
is clearly beneficial, there has been little
evidence for, or against, active stomatal
control in early land plants. Three recent
studies [911] examine the physiology
and genetics of stomatal function
in lycophytes, the basal lineage of
vascular plants, and in mosses, one
of the bryophyte lineages.
Ruszala et al. [9], as reported in a
recent issue of Current Biology, provide
convincing evidence that the lycophyte
Selaginella uncinata exhibits active
stomatal control in response to
environmental conditions. In
Selaginella, as in other land plants, ABA
accumulates in periods of reduced
water availability and is involved in
establishing tolerance to desiccation.
Addition of physiological
concentrations of ABA caused
dose-dependent stomatal closure and
dose-dependent inhibition of stomatal
opening in response to light in
S. uncinata, similar to responses
observed in flowering plants. In
addition, stomatal apertures
decreased in response to elevated
CO2 concentrations in S. uncinata, as
do those of flowering plants and the
fern Phyllitis scolopendrum [12]. In
contrast, Brodribb and McAdam [10]
did not observe significant active
stomatal control in response to the
environmental conditions in lycophytes
and ferns they tested. The reason for the
discrepancy between the two studies is
not obvious, although Ruszala et al. [9]
speculate that there may be either
species-specific differences or
differences in growth conditions.
The bryophyte lineages emerged and
diversified prior to the origin of vascular
plants, with the liverworts being the
sister group to all other land plants
(Figure 1). The bryophytes are
haploid-dominant plants (unlike
vascular plants). There are no stomata
reported in the liverworts. However,
stomata do occur in the diploid
generation (sporophytes) of mosses and
in both haploid and diploid generations
of hornworts [1317]. In the diploid
sporophyte bodies, the stomata open to
internal air spaces as in vascular plants.
Stomata on the sporophytes of
hornworts are believed to function in gas
exchange and also exhibit closure in
response to ABA [18]. In mosses it is less
clear, as there is one report of stomatal
responses to ABA and darkness [19] and
another that concludes the opposite
[15]. Stomata have also been shown to
be involved in specialized processes in
bryophytes, such as facilitating the
explosive spore dispersal mechanism of
the aquatic moss Sphagnum [13] and
serving as an entry portal for symbiotic
cyanobacteria in the haploid bodies
of hornworts [16], with the stomatal
physiology largely uninvestigated in
these cases.
In the third study, also reported in
Current Biology, Chater et al. [11] utilize
the power of genetics to demonstrate
that stomata, which develop on the
sporophyte of the moss Physcomitrella
patens, actively respond to ABA. In
Physcomitrella, stomatal closure was
observed in response to ABA and CO2
in a manner similar to that observed
previously for hornworts and vascular
Dispatch
R541
Figure 1. The evolution of stomata and responsiveness to environmental stimuli.
Stomata arose early in the evolution of land plants, possibly to facilitate photosynthetic gas
exchange while limiting water loss. From their inception, they may have been regulated, at
least in the sporophyte, by ABA, a hormone whose association with water stress predates
the evolution of stomata [20]. Stomata may have originally been present on both the gameto-
phyte and sporophyte and subsequently lost in the lineages of extant mosses and vascular
plants, or alternatively, a single origin in sporophyte generation and one or more separate
origins in the gametophyte generation.
plants. Consistent with a role for ABA
in stomatal closure, at least one gene
family member for each of the core
components of the ABA signaling
pathway is expressed in the
Physcomitrella sporophyte. OPEN
STOMATA 1 (OST1), which encodes
a serine/threonine protein kinase, is
a key gene involved in the ABA
signaling network responsible for
stomatal closure in Arabidopsis. Using
gene-targeting techniques, Chater
et al. [11] created a loss-of-function
allele of a Physcomitrella homolog,
PpOST1, and strikingly, the Ppost1-1
mutants exhibited attenuated stomatal
responses to ABA, confirming the
conclusion based on physiological
experiments.
In combination, the results of
Ruszala et al. [9] and Chater et al. [11]
suggest the biochemical mechanism
for turgor-driven stomatal closure is
conserved from mosses to flowering
plants (Figure 1). While other scenarios
are possible, the most parsimonious
explanation is that active control of
stomatal responses to environmental
conditions arose once in the common
ancestor of mosses and flowering
plants, essentially concomitantly with
the evolution of stomata themselves.
The ability to regulate stomatal
apertures provided substantial
physiological advantages, allowing
early land plants to balance gas
exchange and water retention. As early
land plants had limited root/rhizoid
systems anchored in soils likely lacking
water-holding capacity and were
exposed periodically to direct sunlight,
the ability to actively control stomatal
apertures may have been a crucial step
allowing plants to achieve permanent
hydration and effectively colonize
diverse terrestrial habitats.
Given the above scenario, key
questions remain. Were stomata
originally found on both the
gametophyte and sporophyte
generations of early land plants
(Figure 1), as is the case in extant
hornworts and proposed for some
extinct early vascular plants? And,
critically, what was the origin of the
specialized guard cells that form
stomata? The fossil record has not
provided information on the changes to
epidermal cells that led to the evolution
of stomata [7]. It is possible that clues
to the underlying ancestral genetic
machinery may be found in extant
liverworts, which lack typical stomata
but possess complex air pores that
facilitate gas exchange.
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School of Biological Sciences, Monash
University, Melbourne, Victoria 3800,
Australia.
E-mail: john.bowman@monash.edu
DOI: 10.1016/j.cub.2011.06.021