Vein density is independent of epidermal cell size in Arabidopsis mutants
Madeline R. Carins Murphy A , Graham J. Dow B , Gregory J. Jordan A and Timothy J. Brodribb A C
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.
B Department of Biology, Boston University, 5 Cummington Mall, Boston, MA 02 215, USA.
C Corresponding author. Email: timothyb@utas.edu.au
Functional Plant Biology 44(4) 410-418 https://doi.org/10.1071/FP16299
Submitted: 24 August 2016 Accepted: 10 November 2016 Published: 9 January 2017
Abstract
Densities of leaf minor veins and stomata are co-ordinated within and across vascular plants. This maximises the benefit-to-cost ratio of leaf construction by ensuring stomata receive the minimum amount of water required to maintain optimal aperture. A ‘passive dilution’ mechanism in which densities of veins and stomata are co-regulated by epidermal cell size is thought to facilitate this co-ordination. However, unlike stomata, veins are spatially isolated from the epidermis and thus may not be directly regulated by epidermal cell expansion. Here, we use mutant genotypes of Arabidopsis thaliana (L.) Heynh. with altered stomatal and epidermal cell development to test this mechanism. To do this we compared observed relationships between vein density and epidermal cell size with modelled relationships that assume veins and stomata are passively diluted by epidermal cell expansion. Data from wild-type plants were consistent with the ‘passive dilution’ mechanism, but in mutant genotypes vein density was independent of epidermal cell size. Hence, vein density is not causally linked to epidermal cell expansion. This suggests that adaptation favours synchronised changes to the cell size of different leaf tissues to coordinate veins and stomata, and thus balance water supply with transpirational demand.
Additional keywords: pavement cells, xylem, vascular tissue.
References
Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216, 841–853.Avsian-Kretchmer O, Cheng J-C, Chen L, Moctezuma E, Sung ZR (2002) Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiology 130, 199–209.
| Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntFOrtr4%3D&md5=95bd22ad7caee0593eca416d093804ebCAS |
Balcerowicz M, Hoecker U (2014) Auxin – a novel regulator of stomata differentiation. Trends in Plant Science 19, 747–749.
| Auxin – a novel regulator of stomata differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2lt7jN&md5=875c87a6d14aa8bb4c367549f33e8111CAS |
Brodribb TJ, Jordan GJ (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist 192, 437–448.
| Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist 165, 839–846.
| Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
| Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=4f04ed96d6b9423f9048f7253d491de9CAS |
Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199, 559–570.
| Unified changes in cell size permit coordinated leaf evolution.Crossref | GoogleScholarGoogle Scholar |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35, 1407–1418.
| Differential leaf expansion can enable hydraulic acclimation to sun and shade.Crossref | GoogleScholarGoogle Scholar |
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 & Environment 37, 124–131.
| Acclimation to humidity modifies the link between leaf size and the density of veins and stomata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjurfN&md5=833a1be8197dcdd3234905d986eb9b97CAS |
Carins Murphy MR, Jordan GJ, 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, 1127–1138.
| Cell expansion not cell differentiation predominantly co-ordinates veins and stomata within and among herbs and woody angiosperms grown under sun and shade.Crossref | GoogleScholarGoogle Scholar |
Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 547–555.
| Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltV2rtbs%3D&md5=e20275e2fb10e65b98f19e17c382dc82CAS |
Dong J, MacAlister CA, Bergmann DC (2009) BASL controls asymmetric cell division in Arabidopsis. Cell 137, 1320–1330.
| BASL controls asymmetric cell division in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Dow GJ, Bergmann DC (2014) Patterning and processes: how stomatal development defines physiological potential. Current Opinion in Plant Biology 21, 67–74.
| Patterning and processes: how stomatal development defines physiological potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ensbfK&md5=360d89f74f7ae1fc059fcdc39ed5afd6CAS |
Dow GJ, Bergmann DC, Berry JA (2014a) An integrated model of stomatal development and leaf physiology. New Phytologist 201, 1218–1226.
| An integrated model of stomatal development and leaf physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVehu74%3D&md5=3a1348f44df77b54fb6b05e75b3580acCAS |
Dow GJ, Berry JA, Bergmann DC (2014b) The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytologist 201, 1205–1217.
| The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVegsr4%3D&md5=1dd7b2ea9f48a34ecbc9bf12924a1612CAS |
Fiorin L, Brodribb TJ, Anfodillo T (2016) Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves. New Phytologist 209, 216–227.
| Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves.Crossref | GoogleScholarGoogle Scholar |
Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 537–546.
| Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltV2rtbo%3D&md5=ce9f5149e0f6b463db43c583029e34efCAS |
Gälweiler L, Guan CH, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230.
| Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.Crossref | GoogleScholarGoogle Scholar |
Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T (2007) The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes & Development 21, 1720–1725.
| The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXoslSisLg%3D&md5=21b460949ac785d537908e93a2054114CAS |
Hill R (1980) Three new Eocene cycads from eastern Australia. Australian Journal of Botany 28, 105–122.
| Three new Eocene cycads from eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Current Biology 19, 864–869.
| The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVCgtLg%3D&md5=44e3b4cd9a1da26f044e56af69eeebd2CAS |
Jacobs WP (1952) The role of auxin in differentiation of xylem around a wound. American Journal of Botany 39, 301–309.
| The role of auxin in differentiation of xylem around a wound.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG38XlsV2ntQ%3D%3D&md5=63143874d1da492b073641eda2e17be4CAS |
John GP, Scoffoni C, Sack L (2013) Allometry of cells and tissues within leaves. American Journal of Botany 100, 1936–1948.
| Allometry of cells and tissues within leaves.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23, 187–261.
| Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksVGiu7w%3D&md5=8050afbf3e4cefc3f1638841211d6fa1CAS |
Lampard GR, MacAlister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322, 1113–1116.
| Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGgsr7I&md5=d6f9ef3e151f1e6be7bd41cb231c1766CAS |
Lau OS, Bergmann DC (2012) Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication. Development 139, 3683–3692.
| Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsleru7rF&md5=eb814146040ddf6a880a40e98e5b5fafCAS |
Lo Gullo MA, Raimondo F, Crisafulli A, Salleo S, Nardini A (2010) Leaf hydraulic architecture and water relations of three ferns from contrasting light habitats. Functional Plant Biology 37, 566–574.
| Leaf hydraulic architecture and water relations of three ferns from contrasting light habitats.Crossref | GoogleScholarGoogle Scholar |
Martins SCV, Galmés J, Cavatte PC, Pereira LF, Ventrella MC, DaMatta FM (2014) Understanding the low photosynthetic rates of sun and shade coffee leaves: bridging the gap on the relative roles of hydraulic, diffusive and biochemical constraints to photosynthesis. PLoS One 9, e95571
| Understanding the low photosynthetic rates of sun and shade coffee leaves: bridging the gap on the relative roles of hydraulic, diffusive and biochemical constraints to photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126, 2979–2991.
Mayer U, Buttner G, Jurgens G (1993) Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117, 149–162.
Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CVM, Crous KY, de Angelis P, Freeman M, Wingate L (2011) Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology 17, 2134–2144.
| Reconciling the optimal and empirical approaches to modelling stomatal conductance.Crossref | GoogleScholarGoogle Scholar |
Nadeau JA, Sack FD (2002) Control of stomatal distribution on the Arabidopsis leaf surface. Science 296, 1697–1700.
| Control of stomatal distribution on the Arabidopsis leaf surface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlCgtLk%3D&md5=659166ffc7b561b86a4fdcdb512b76e4CAS |
Pant DD, Kidwai PF (1967) Development of stomata in some Cruciferae. Annals of Botany 31, 513–521.
Pantin F, Simonneau T, Rolland G, Dauzat M, Muller B (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiology 156, 803–815.
| Control of leaf expansion: a developmental switch from metabolics to hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrs%3D&md5=b80444fcbfbe3b3a219f40bb2906a240CAS |
Pantin F, Simonneau T, Muller B (2012) Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny. New Phytologist 196, 349–366.
| Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny.Crossref | GoogleScholarGoogle Scholar |
Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annual Review of Plant Biology 63, 591–614.
| Mechanisms of stomatal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1amtrs%3D&md5=c559dcba2771f9314a54cee57d85601eCAS |
Raven JA (1975) Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytologist 74, 163–172.
| Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhsFahtLc%3D&md5=17eac3ba61a5c4fc7a1b1bf95a740ff9CAS |
Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118, 101–121.
| Carrier-mediated auxin transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXltFOisbs%3D&md5=6558d91c0b93e606b16ce2995d3ce43dCAS |
Sachs T (1981) The control of the patterned differentiation of vascular tissues. Advances in Botanical Research 9, 151–262.
| The control of the patterned differentiation of vascular tissues.Crossref | GoogleScholarGoogle Scholar |
Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483–491.
| Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar |
Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philosophical Transactions of the Royal Society of London. Series B, Containing Papers of a Biological Character 216, 1–65.
| On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora.Crossref | GoogleScholarGoogle Scholar |
Šantrůček J, Vráblová M, Šimková M, Hronková M, Drtinová M, Květoň J, Vrábl D, Kubásek J, Macková J, Wiesnerová D, Neuwithová J, Schreiber L (2014) Stomatal and pavement cell density linked to leaf internal CO2 concentration. Annals of Botany 114, 191–202.
| Stomatal and pavement cell density linked to leaf internal CO2 concentration.Crossref | GoogleScholarGoogle Scholar |
Sasidharan R, Chinnappa CC, Voesenek LACJ, Pierik R (2008) The regulation of cell wall extensibility during shade avoidance: a study using two contrasting ecotypes of Stellaria longipes. Plant Physiology 148, 1557–1569.
| The regulation of cell wall extensibility during shade avoidance: a study using two contrasting ecotypes of Stellaria longipes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVSnurnL&md5=ad0e556571d83c8b5311e84452d1e998CAS |
Schopfer P (2006) Biomechanics of plant growth. American Journal of Botany 93, 1415–1425.
| Biomechanics of plant growth.Crossref | GoogleScholarGoogle Scholar |
Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiology 121, 1179–1190.
| Auxin is required for leaf vein pattern in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFyju7k%3D&md5=123422281f0ee83452c70e8f29d3ff70CAS |
Smith S, Weyers JDB, Berry WG (1989) Variation in stomatal characteristics over the lower surface of Commelina communis leaves. Plant, Cell & Environment 12, 653–659.
| Variation in stomatal characteristics over the lower surface of Commelina communis leaves.Crossref | GoogleScholarGoogle Scholar |
Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. The Plant Cell 21, 749–766.
| The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFyltbs%3D&md5=2e0f2de42c095e516046271a9f007f52CAS |
Uggla C, Moritz T, Sandberg G, Sundberg B (1996) Auxin as a positional signal in pattern formation in plants. Proceedings of the National Academy of Sciences of the United States of America 93, 9282–9286.
| Auxin as a positional signal in pattern formation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xlt1CnurY%3D&md5=cc2c770c6b48093e160933b3ade0f8b5CAS |
Verna C, Sawchuk MG, Linh NM, Scarpella E (2015) Control of vein network topology by auxin transport. BMC Biology 13, 94
| Control of vein network topology by auxin transport.Crossref | GoogleScholarGoogle Scholar |
Wuyts N, Palauqui JC, Conejero G, Verdeil JL, Granier C, Massonnet C (2010) High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6, 17
| High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll.Crossref | GoogleScholarGoogle Scholar |
Yang S-J, Sun M, Zhang Y-J, Cochard H, Cao K-F (2014) Strong leaf morphological, anatomical, and physiological responses of a subtropical woody bamboo (Sinarundinaria nitida) to contrasting light environments. Plant Ecology 215, 97–109.
| Strong leaf morphological, anatomical, and physiological responses of a subtropical woody bamboo (Sinarundinaria nitida) to contrasting light environments.Crossref | GoogleScholarGoogle Scholar |
Zhang SB, Guan ZJ, Sun M, Zhang JJ, Cao KF, Hu H (2012) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PLoS One 7, e40080
| Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVaitrc%3D&md5=c7e21cec999d969dabf95f7afd65aae5CAS |
Zhang SB, Sun M, Cao KF, Hu H, Zhang JL (2014) Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS One 9, e84682
| Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity.Crossref | GoogleScholarGoogle Scholar |
