Stomatal conductance scales with petiole xylem traits in Populus genotypes
Caroline A. Brocious A and Uwe G. Hacke A B
+ Author Affiliations
- Author Affiliations
A University of Alberta, Department of Renewable Resources, 442 Earth Sciences Building, Edmonton, AB T6G 2E3, Canada.
B Corresponding author. Email: uwe.hacke@ualberta.ca
Functional Plant Biology 43(6) 553-562 https://doi.org/10.1071/FP15336
Submitted: 28 October 2015 Accepted: 14 April 2016 Published: 12 May 2016
Abstract
Progress has been made in linking water transport in leaves with anatomical traits. However, most of our current knowledge about these links is based on studies that sampled phylogenetically distant species and covered a wide range of leaf size and morphology. Here we studied covariation of leaf anatomical traits and hydraulic capacity in five closely related hybrid poplar genotypes. Variation in stomatal conductance and leaf hydraulic conductance was not linked to vein density or other anatomical lamina properties. A strong correlation was found between stomatal conductance and the transport capacity of the petiole, estimated from the diameter and number of xylem vessels. An inverse relationship existed between leaf size and major vein density. The role of bundle sheath extensions is discussed. Our data suggests that petiole xylem is an important predictor of gas exchange capacity in poplar leaves.
Additional keywords: bundle sheath extensions, leaf anatomy, leaf hydraulics, leaf veins.
References
Adams WW, Cohu CM, Muller O, Demmig-Adams B (2013) Foliar phloem infrastructure in support of photosynthesis. Frontiers in Plant Science 4,| Foliar phloem infrastructure in support of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 23898338PubMed |
Almeida-Rodriguez AM, Hacke UG, Laur J (2011) Influence of evaporative demand on aquaporin expression and root hydraulics in hybrid poplar. Plant, Cell & Environment 34, 1318–1331.
| Influence of evaporative demand on aquaporin expression and root hydraulics in hybrid poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOntbrF&md5=96ae77c7f310142a9a92943c68f0a493CAS |
Berlyn GP, Miksche JP, Sass JE (1976) ‘Botanical microtechnique and cytochemistry.’ (Iowa State University Press: Iowa City, IA, USA)
Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society of London. Series B, Biological Sciences 276, 1771–1776.
| Angiosperm leaf vein evolution was physiologically and environmentally transformative.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=52674169ae1dca1c088306428cad4fedCAS | 17556506PubMed |
Brodribb TJ, Feild TS, Sack L (2010) Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology 37, 488–498.
| Viewing leaf structure and evolution from a hydraulic perspective.Crossref | GoogleScholarGoogle Scholar |
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 | 23647069PubMed |
Buckley TN, Sack L, Gilbert ME (2011) The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiology 156, 962–973.
| The role of bundle sheath extensions and life form in stomatal responses to leaf water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrt7Y%3D&md5=88382bb4bf9b3b443fb4f948ff66ea38CAS | 21459977PubMed |
Buckley TN, John GP, Scoffoni C, Sack L (2015) How does leaf anatomy influence water transport outside the xylem? Plant Physiology 168, 1616–1635.
| How does leaf anatomy influence water transport outside the xylem?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVSrt7nF&md5=6cdc67f72ce816ec84eeeec2c486fe8dCAS | 26084922PubMed |
Caringella MA, Bongers FJ, Sack L (2015) Leaf hydraulic conductance varies with vein anatomy across Arabidopsis thaliana wild-type and leaf vein mutants. Plant, Cell & Environment 38, 2735–2746.
| Leaf hydraulic conductance varies with vein anatomy across Arabidopsis thaliana wild-type and leaf vein mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVOrt7zK&md5=bc0d0cee70cb93bf8b8bb7f115119152CAS |
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology 164, 1600–1618.
| Aquaporins: highly regulated channels controlling plant water relations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsV2jsr4%3D&md5=9280679c4bdf33a07e273d0c68e480d4CAS | 24449709PubMed |
Coomes DA, Heathcote S, Godfrey ER, Shepherd JJ, Sack L (2008) Scaling of xylem vessels and veins within the leaves of oak species. Biology Letters 4, 302–306.
| Scaling of xylem vessels and veins within the leaves of oak species.Crossref | GoogleScholarGoogle Scholar | 18407890PubMed |
DesRochers A, Thomas BR (2003) A comparison of pre-planting treatments on hardwood cuttings of four hybrid poplar clones. New Forests 26, 17–32.
| A comparison of pre-planting treatments on hardwood cuttings of four hybrid poplar clones.Crossref | GoogleScholarGoogle Scholar |
Ellis B, Daly DC, Hickey LJ, Johnson KR, Mitchell JD, Wilf P, Wing SL (2009) ‘Manual of leaf architecture.’ (Cornell University Press Ithaca: NY, USA)
Fox J, Weisberg S (2010) ‘An R companion to applied regression.’ (Sage Publications: Thousand Oaks, CA, USA)
Gebauer R, Vanbeveren SP, Volařík D, Plichta R, Ceulemans R (2016) Petiole and leaf traits of poplar in relation to parentage and biomass yield. Forest Ecology and Management 362, 1–9.
| Petiole and leaf traits of poplar in relation to parentage and biomass yield.Crossref | GoogleScholarGoogle Scholar |
Gleason SM, Blackman CJ, Chang Y, Cook AM, Laws CA, Westoby M (2016) Weak coordination among petiole, leaf, vein, and gas-exchange traits across Australian angiosperm species and its possible implications. Ecology and Evolution 6, 267–278.
| Weak coordination among petiole, leaf, vein, and gas-exchange traits across Australian angiosperm species and its possible implications.Crossref | GoogleScholarGoogle Scholar | 26811791PubMed |
Hao G-Y, Sack L, Wang A-Y, Cao K-F, Goldstein G (2010) Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Functional Ecology 24, 731–740.
| Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species.Crossref | GoogleScholarGoogle Scholar |
Harrell FE, Dupont C (2012) Hmisc: Harrell miscellaneous. R package ver. 3.9–3. Available at http://CRAN.R-project.org/package=Hmisc [Verified 15 November 2015]
Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. Journal of Experimental Botany 60, 2971–2985.
| Role of aquaporins in leaf physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsValsb0%3D&md5=9c3fb498db5accfaeb3b04df781de13cCAS | 19542196PubMed |
Kröber W, Zhang S, Ehmig M, Bruelheide H (2014) Linking xylem hydraulic conductivity and vulnerability to the leaf economics spectrum – a cross-species study of 39 evergreen and deciduous broadleaved subtropical tree species. PLoS One 9, e109211
| Linking xylem hydraulic conductivity and vulnerability to the leaf economics spectrum – a cross-species study of 39 evergreen and deciduous broadleaved subtropical tree species.Crossref | GoogleScholarGoogle Scholar | 25423316PubMed |
Laur J, Hacke UG (2014) Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling. New Phytologist 203, 388–400.
| Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVahtLrO&md5=f5290c10e78fc9fc882c6c8c4777c929CAS | 24702644PubMed |
Nardini A, Pedà G, Rocca NL (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytologist 196, 788–798.
| Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences.Crossref | GoogleScholarGoogle Scholar | 22978628PubMed |
Nardini A, Õunapuu-Pikas E, Savi T (2014) When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes. Functional Plant Biology 41, 972–982.
| When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes.Crossref | GoogleScholarGoogle Scholar |
Plavcová L, Hacke UG (2012) Phenotypic and developmental plasticity of xylem in hybrid poplar saplings subjected to experimental drought, nitrogen fertilization, and shading. Journal of Experimental Botany 63, 6481–6491.
| Phenotypic and developmental plasticity of xylem in hybrid poplar saplings subjected to experimental drought, nitrogen fertilization, and shading.Crossref | GoogleScholarGoogle Scholar | 23095999PubMed |
Pohlert T (2014) ‘The pairwise multiple comparison of mean ranks package (PMCMR), R-package.’ Available at http://CRAN.R-project.org/package=PMCMR [Verified 15 November 2015]
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 | 16637372PubMed |
Sack L, Scoffoni C (2012) Measurement of leaf hydraulic conductance and stomatal conductance and their responses to irradiance and dehydration using the evaporative flux method (EFM). Journal of Visualized Experiments (70), e4179
| Measurement of leaf hydraulic conductance and stomatal conductance and their responses to irradiance and dehydration using the evaporative flux method (EFM).Crossref | GoogleScholarGoogle Scholar |
Sack L, Scoffoni C, McKown AD, Frole K, Rawls M, Havran JC, Tran H, Tran T (2012) Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications 3, 837
| Developmentally based scaling of leaf venation architecture explains global ecological patterns.Crossref | GoogleScholarGoogle Scholar | 22588299PubMed |
Sack L, Scoffoni C, Johnson DM, Buckley TN, Brodribb TJ (2015) The anatomical determinants of leaf hydraulic function. In ‘Functional and ecological xylem anatomy’. pp. 255–271. (Springer: Berlin, Germany)
Salisbury EJ (1913) The determining factors in petiolar structure. New Phytologist 12, 281–289.
| The determining factors in petiolar structure.Crossref | GoogleScholarGoogle Scholar |
Schreiber SG, Hacke UG, Hamann A, Thomas BR (2011) Genetic variation of hydraulic and wood anatomical traits in hybrid poplar and trembling aspen. New Phytologist 190, 150–160.
| Genetic variation of hydraulic and wood anatomical traits in hybrid poplar and trembling aspen.Crossref | GoogleScholarGoogle Scholar | 21223285PubMed |
Schreiber SG, Hacke UG, Chamberland S, Lowe CW, Kamelchuk D, Bräutigam K, Campbell MM, Thomas BR (2016) Leaf size serves as a proxy for xylem vulnerability to cavitation in plantation trees. Plant, Cell & Environment 39, 272–281.
| Leaf size serves as a proxy for xylem vulnerability to cavitation in plantation trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisVyisb4%3D&md5=817f2d5753be989e9a11becfe648b2a0CAS |
Schultz HR, Matthews MA (1993) Xylem development and hydraulic conductance in sun and shade shoots of grapevine (Vitis vinifera L.): evidence that low light uncouples water transport capacity from leaf area. Planta 190, 393–406.
| Xylem development and hydraulic conductance in sun and shade shoots of grapevine (Vitis vinifera L.): evidence that low light uncouples water transport capacity from leaf area.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C (2015) Modelling the outside-xylem hydraulic conductance: towards a new understanding of leaf water relations. Plant, Cell & Environment 38, 4–6.
| Modelling the outside-xylem hydraulic conductance: towards a new understanding of leaf water relations.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C, McKown AD, Rawls M, Sack L (2012) Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state. Journal of Experimental Botany 63, 643–658.
| Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1GitA%3D%3D&md5=1d5cf54afdff99605dc10d76f184cf00CAS | 22016424PubMed |
Shatil-Cohen A, Attia Z, Moshelion M (2011) Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? The Plant Journal 67, 72–80.
| Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsVyrtrg%3D&md5=ef8c0786b2d760c944f7ac7d935cd524CAS | 21401747PubMed |
Sommerville KE, Sack L, Ball MC (2012) Hydraulic conductance of Acacia phyllodes (foliage) is driven by primary nerve (vein) conductance and density. Plant, Cell & Environment 35, 158–168.
| Hydraulic conductance of Acacia phyllodes (foliage) is driven by primary nerve (vein) conductance and density.Crossref | GoogleScholarGoogle Scholar |
Taneda H, Terashima I (2012) Co-ordinated development of the leaf midrib xylem with the lamina in Nicotiana tabacum. Annals of Botany 110, 35–45.
| Co-ordinated development of the leaf midrib xylem with the lamina in Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVaitb8%3D&md5=4843635e8556e18c5736efbf357a7f1cCAS | 22589329PubMed |
Tyree MT, Ewers FW (1991) Tansley review no. 34: the hydraulic architecture of trees and other woody plants. New Phytologist 119, 345–360.
| Tansley review no. 34: the hydraulic architecture of trees and other woody plants.Crossref | GoogleScholarGoogle Scholar |
Xiong D, Yu T, Zhang T, Li Y, Peng S, Huang J (2015) Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza. Journal of Experimental Botany 66, 741–748.
| Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGisLfO&md5=7030c33498c34f2627f3987b2943470cCAS | 25429002PubMed |
Zhang CK, Han L, Slewinski TL, Sun JL, Zhang J, Wang ZY, Turgeon R (2014) Symplastic phloem loading in poplar. Plant Physiology 166, 306–313.
| Symplastic phloem loading in poplar.Crossref | GoogleScholarGoogle Scholar |
Zsögön A, Alves Negrini AC, Peres LEP, Nguyen HT, Ball MC (2015) A mutation that eliminates bundle sheath extensions reduces leaf hydraulic conductance, stomatal conductance and assimilation rates in tomato (Solanum lycopersicum). New Phytologist 205, 618–626.
| A mutation that eliminates bundle sheath extensions reduces leaf hydraulic conductance, stomatal conductance and assimilation rates in tomato (Solanum lycopersicum).Crossref | GoogleScholarGoogle Scholar | 25267094PubMed |
Zwieniecki MA, Brodribb TJ, Holbrook NM (2007) Hydraulic design of leaves: insights from rehydration kinetics. Plant, Cell & Environment 30, 910–921.
| Hydraulic design of leaves: insights from rehydration kinetics.Crossref | GoogleScholarGoogle Scholar |
