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Cell expansion coordinates leaf vein and stomatal density

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Carins Murphy, MR (2016) Cell expansion coordinates leaf vein and stomatal density. PhD thesis, University of Tasmania.

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Abstract

The efficiency with which water is delivered through leaf tissue to sites of
evaporation (the leaf hydraulic conductance) is an important determinant of
photosynthetic capacity. This is because inadequate water supply forces stomata to
close due to plant desiccation. The resulting reduction in stomatal conductance
restricts carbon dioxide (CO2) uptake. An oversupply of water, on the other hand,
results in unprofitable investment in vascular tissue. Accordingly, water supply is
strongly correlated with the demand for water generated by stomata. Recent work
suggests that this balance is achieved in a tropical angiosperm tree by a simple
developmental mechanism in which changes to leaf size co-regulate vein and
stomatal density (major determinants of water supply and demand, respectively).
However, the generality of this mechanism is unknown. Thus, in this thesis I set out
to establish whether there is a general developmental mechanism that allows plants
to maintain a constant ratio between leaf vein and stomatal density. In doing so the
following specific research questions were investigated:
1. Does acclimation to high and low VPD (vapour pressure difference) modify
the relationships between vein density, stomatal density and leaf size?
(Chapter 2)
2. Does leaf or epidermal cell expansion coordinate vein and stomatal density in
herbs and woody angiosperms? (Chapter 3)
3. Does epidermal cell expansion coordinate vein and stomatal density in older
plant lineages like ferns? (Chapter 4)
4. Is vein density directly regulated by epidermal cell expansion? (Chapter 5)
The difference in vapour pressure between leaf tissue and the atmosphere determines
how much water is transpired at any given stomatal conductance. Thus, I
hypothesised in Chapter 2 that plants grown under high VPD would exhibit a
modified relationship between vein and stomatal density resulting in maintenance of
homeostasis in leaf water potential such that there is either a decrease in stomatal
density and no change in vein density, or no change in stomatal density and an
increase in vein density. This would also disrupt previously observed relationships
with leaf size. However, contrary to my hypothesis, I found a small but coordinated
increase in vein and stomatal density in plants grown under high VPD compared with
those grown under low VPD. Furthermore, densities of veins and stomata were
independent of large VPD-induced changes to leaf size and were instead limited by
epidermal cell size (which was fairly insensitive to VPD). This suggests that
significant modification of epidermal cell size is required to produce large changes in
vein and stomatal density.
Thus, to further investigate whether leaf expansion or epidermal cell expansion
coordinates vein and stomatal density more generally among plants I examined
relationships between vein density, stomatal density, leaf size and epidermal cell size
across a diverse range of woody and herbaceous angiosperms grown under sun and
shade conditions (Chapter 3). Contrary to the original premise that differential leaf
expansion coordinates vein and stomatal density, I found that leaf size was
independent of epidermal cell size in most cases and that relationships between vein
density, stomatal density and epidermal cell size were well described by modelled
relationships that assume veins and stomata are passively ‘diluted’ by epidermal cell
expansion. These results demonstrate that coordination of vein and stomatal density
in angiosperms is driven by their co-variation with epidermal cell size.
While this ‘passive dilution’ mechanism seems to be common among angiosperms, it
is not known when it appeared in the vascular plant phylogeny. Furthermore, older
plant lineages like ferns may employ different mechanisms to coordinate vein and
stomatal density because they differ from angiosperms in both current water relations
physiology and evolutionary history. Contrary to this expectation, I found that
relationships between vein density, stomatal density and epidermal cell size across
four ferns species were very similar to those previously observed across angiosperm
species (Chapter 4). However, there was little plasticity in these traits within fern
species and changes to stomatal density across species were actively regulated by
stomatal index, as well as epidermal cell size. Despite this, epidermal cell size was a
strong determinant of vein and stomatal density in ferns (explaining 55.5 % of the
variation in stomatal density versus the 44.5 % explained by stomatal index). Thus,
ferns (like angiosperms) appear to use the co-variance of vein and stomatal density
with epidermal cell expansion to maintain a constant ratio between the abundance of
veins and stomata in the leaf. This suggests that the ‘passive dilution’ mechanism
may be an ancient feature of vascular plants that co-regulates these tissues.
In Chapters 3 and 4 it was proposed that coordination of vein and stomatal density is
achieved through a ‘passive dilution’ mechanism in which densities of veins and
stomata are co-regulated by epidermal cell size. However, unlike stomata, leaf veins
are spatially isolated from the epidermis and it is not known whether they are directly
regulated by epidermal cell expansion. To investigate this I tested whether
relationships between vein density and epidermal cell size in a wild type genotype of
Arabidopsis (Col-0) and seven other genotypes with modified forms of genes that
affect both stomatal development and epidermal cell size were the same as modelled
relationships that assume veins are passively ‘diluted’ by epidermal cell expansion
(Chapter 5). Vein density in wild type plants was correlated with abaxial epidermal
cell size in a way that was consistent with the ‘passive dilution’ mechanism (despite
some deviation from modelled relationships). However, vein density was
independent of variation in epidermal cell size among mutant and transgenic
genotypes. This suggests that epidermal cell size in these genotypes was modified
independently from the rest of the leaf in spite of prior evidence that cell sizes are
correlated within leaves. Thus, vein density is not causally linked to epidermal cell
expansion. Instead the relationship between vein density and epidermal cell size in
wild type plants reflects developmental factors that affect both mesophyll and
epidermal cells, suggesting that adaptation favours coordination of veins and stomata
over independent development of these tissues.
Thus, the overarching finding of this thesis is that the ‘dilution’ of veins and stomata
by differential epidermal cell expansion (and perhaps mesophyll cell expansion)
appears to be a general mechanism capable of maintaining a constant ratio between
vein and stomatal density both within and across a diverse range of vascular plant
species. Leaf cells expand more in the shade than the sun, and more in some species
compared with others, which increases the space between veins and stomata
concomitantly reducing their density. These relationships provide an insight into how
plants construct leaves that can efficiently replace transpired water and maintain
maximum carbon assimilation for the minimum investment in vein and stomatal
infrastructure. Achieving this maximises the energetic return for investments made
during leaf construction increasing the energy available for growth and reproduction.

Item Type: Thesis (PhD)
Keywords: angiosperms, epidermal cell size, ferns, leaf size, light, stomatal density, vein density, VPD
Copyright Information:

Copyright 2015 the Author

Additional Information:

Chapter 2 appears to be the equivalent of the peer reviewed version of the following article: Carins Murphy, MR, Jordan, GJ, Brodribb, TJ (2014) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant cell and environment 37(1), 124-131, which has been published in final form at http://dx.doi.org/10.1111/pce.12136
This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.

Chapter 3 has been removed from the accesible version of the thesis as it appears to be the equivalent of a pre-print version of an article published as: Carins Murphy, MR, Jordan, GJ, and Brodribb, TJ, (2016) Cell expansion not cell differentiation predominantly co-ordinates veins and stomata within and among herbs and woody angiosperms grown under sun and shade. Annals of botany 118(6), 1127-1138.

Date Deposited: 03 Nov 2016 03:41
Last Modified: 14 Nov 2016 01:09
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