Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes

Andrea Nardini A C , Eele Õunapuu-Pikas A B and Tadeja Savi A
+ Author Affiliations
- Author Affiliations

A Department of Life Sciences, University of Trieste, Via L. Giorgieri 10, 34127 Trieste, Italy.

B Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 21, 51014 Tartu, Estonia.

C Corresponding author. Email: nardini@units.it

Functional Plant Biology 41(9) 972-982 https://doi.org/10.1071/FP13302
Submitted: 18 October 2013  Accepted: 11 April 2014   Published: 13 May 2014

Abstract

Leaf hydraulic conductance (Kleaf) and drought vulnerability in terms of leaf water potential inducing 50% loss of Kleaf (P50), were assessed in four genotypes of Coffea arabica L. We tested three hypotheses: (1) leaf P50 is lower in small leaves with higher vein densities; (2) lower P50 translates into lower Kleaf, limiting gas exchange rates and higher leaf mass per unit area (LMA); (3) P50 values are coordinated with symplastic drought tolerance. We found partial support for Hypotheses 1 and 3, but not for Hypothesis 2. Significant correlations existed among leaf size, vein network and drought resistance. Smaller leaves displayed higher major vein density, higher Kleaf and more negative P50. Kleaf was correlated with leaf gas exchange rates. A negative relationship was observed between Kleaf and LMA, whereas P50 was found to be positively correlated with LMA. Across coffee genotypes, reduced leaf surface area and increased vein density shifts P50 towards more negative values while not translating into higher LMA or lower Kleaf. Breeding crop varieties for both increased safety of the leaf hydraulic system towards drought-induced dysfunction and high gas exchange rates per unit of leaf area is probably a feasible target for future adaptation of crops to climate change scenarios.

Additional keywords: coffee, gas exchange, leaf area, Leaf mass per unit area.


References

Barnard DM, Meinzer FC, Lachenbruch B, McCulloh KA, Johnson DM, Woodruff DR (2011) Climate-related trends in sapwood biophysical properties in two conifers: avoidance of hydraulic dysfunction through coordinated adjustments in xylem efficiency, safety and capacitance. Plant, Cell & Environment 34, 643–654.
Climate-related trends in sapwood biophysical properties in two conifers: avoidance of hydraulic dysfunction through coordinated adjustments in xylem efficiency, safety and capacitance.Crossref | GoogleScholarGoogle Scholar |

Bindi M, Olesen JE (2011) The responses of agriculture in Europe to climate change. Regional Environmental Change 11, 151–158.
The responses of agriculture in Europe to climate change.Crossref | GoogleScholarGoogle Scholar |

Blackman CJ, Brodribb TJ (2011) Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Functional Plant Biology 38, 118–126.
Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves.Crossref | GoogleScholarGoogle Scholar |

Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytologist 188, 1113–1123.
Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 20738785PubMed |

Blackman CJ, Brodribb TJ, Jordan GJ (2012) Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms. Oecologia 168, 1–10.
Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 21744163PubMed |

Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecology Letters 14, 91–100.
Venation networks and the origin of the leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 21073643PubMed |

Blonder B, Violle C, Enquist BJ (2013) Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides. Journal of Ecology 101, 981–989.
Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides.Crossref | GoogleScholarGoogle Scholar |

Brodribb TJ (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Science 177, 245–251.
Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1Kgsro%3D&md5=0c8d5db001d9b893171dd9bbc23b7e1aCAS |

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 | 15720695PubMed |

Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rates and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
Leaf maximum photosynthetic rates and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=af12f58caacd925d16035eea3ba3533dCAS | 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 |

Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Campanello PI, Villalobos-Vega R, Bustamante M, Miralles-Wilhelm F (2006) Nutrient availability constrains the hydraulic architecture and water relations of savannah trees. Plant, Cell & Environment 29, 2153–2167.
Nutrient availability constrains the hydraulic architecture and water relations of savannah trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVajuw%3D%3D&md5=1a8c1b9ab1cc76be3a8a8ccef9b563c1CAS |

Bucci SJ, Scholz FG, Campanello PI, Montti L, Jimenez-Castillo M, Rockwell FA, La Manna L, Guerra P, Bernal PL, Troncoso O, Enricci J, Holbrook NM, Goldstein G (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiology 32, 880–893.
Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality?Crossref | GoogleScholarGoogle Scholar | 22684354PubMed |

Cavatte PC, Oliveira AAG, Morais LE, Martins SCV, Sanglard LMVP, DaMatta FM (2012) Could shading reduce the negative impacts of drought on coffee? A morphophysiological analysis. Physiologia Plantarum 144, 111–122.
Could shading reduce the negative impacts of drought on coffee? A morphophysiological analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Kjt7w%3D&md5=66fc8083a11c02b2f58a387361d5a94fCAS | 21939445PubMed |

Charra-Vaskou K, Badel E, Burlett R, Cochard H, Delzon S, Mayr S (2012) Hydraulic efficiency and safety of vascular and non-vascular components in Pinus pinaster leaves. Tree Physiology 32, 1161–1170.
Hydraulic efficiency and safety of vascular and non-vascular components in Pinus pinaster leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlymsL%2FP&md5=6f5ce39a84d7ffd15fe856ccb17f8f50CAS | 22907978PubMed |

DaMatta FM (2004) Exploring drought tolerance in coffee: a physiological approach with some insights for plant breeding. Brazilian Journal of Plant Physiology 16, 1–6.
Exploring drought tolerance in coffee: a physiological approach with some insights for plant breeding.Crossref | GoogleScholarGoogle Scholar |

DaMatta FM, Chaves ARM, Pinheiro HA, Ducatti C, Loureiro ME (2003) Drought tolerance of two field-grown clones of Coffea canephora. Plant Science 164, 111–117.
Drought tolerance of two field-grown clones of Coffea canephora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFertrg%3D&md5=fc1835ac9af17c5aef711202cb97d5c9CAS |

Davis AP, Gole TW, Baena S, Moat J (2012) The impact of climate change on indigenous Arabica coffee (Coffea arabica): predicting future trends and identifying priorities. PLoS ONE 7, e47981
The impact of climate change on indigenous Arabica coffee (Coffea arabica): predicting future trends and identifying priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCjurnN&md5=8f8e183ea8b70207c10a00e5f45e9685CAS | 23144840PubMed |

Dias PC, Araujo WL, Moraes GABK, Barros RS, DaMatta FM (2007) Morphological and physiological responses of two coffee progenies to soil water availability. Journal of Plant Physiology 164, 1639–1647.
Morphological and physiological responses of two coffee progenies to soil water availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVOnsr3O&md5=0ebf135f027eaad10cdef6ed581bfe87CAS | 17291628PubMed |

Dunbar-Co S, Sporck MJ, Sack L (2009) Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. International Journal of Plant Sciences 170, 61–75.
Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation.Crossref | GoogleScholarGoogle Scholar |

Edwards EJ (2006) Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae). New Phytologist 172, 479–489.
Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae).Crossref | GoogleScholarGoogle Scholar | 17083678PubMed |

Fichot R, Barigah TS, Chamaillard S, Le Thiec D, Laurans F, Cochard H, Brignolas F (2010) Common trade-offs between xylem resistance to cavitation and other physiological traits do not hold among unrelated Populus deltoides × Populus nigra hybrids. Plant, Cell & Environment 33, 1553–1568.

Froux F, Huc R, Ducrey M, Dreyer E (2002) Xylem hydraulic efficiency versus vulnerability in seedlings of four contrasting Mediterranean tree species (Cedrus atlantica, Cupressus sempervirens, Pinus halepensis and Pinus nigra). Annals of Forest Science 59, 409–418.
Xylem hydraulic efficiency versus vulnerability in seedlings of four contrasting Mediterranean tree species (Cedrus atlantica, Cupressus sempervirens, Pinus halepensis and Pinus nigra).Crossref | GoogleScholarGoogle Scholar |

Gascó A, Nardini A, Salleo S (2004) Resistance to water flow through leaves of Coffea arabica is dominated by extra-vascular tissues. Functional Plant Biology 31, 1161–1168.
Resistance to water flow through leaves of Coffea arabica is dominated by extra-vascular tissues.Crossref | GoogleScholarGoogle Scholar |

Gleason SM, Butler DW, Ziemińska K, Waryszak P, Westboy M (2012) Stem xylem conductivity is key to plant water balance across Australian angiosperm species. Functional Ecology 26, 343–352.
Stem xylem conductivity is key to plant water balance across Australian angiosperm species.Crossref | GoogleScholarGoogle Scholar |

Gortan E, Nardini A, Gascò A, Salleo S (2009) The hydraulic conductance of Fraxinus ornus leaves is constrained by soil water availability and coordinated with gas exchange rates. Tree Physiology 29, 529–539.
The hydraulic conductance of Fraxinus ornus leaves is constrained by soil water availability and coordinated with gas exchange rates.Crossref | GoogleScholarGoogle Scholar | 19203976PubMed |

Hughes FW (2005) Archimedes revisited: a faster, better, cheaper method of accurately measuring the volume of small objects. Physics Education 40, 468–474.
Archimedes revisited: a faster, better, cheaper method of accurately measuring the volume of small objects.Crossref | GoogleScholarGoogle Scholar |

Jacobsen AL, Ewers FW, Pratt RB, Paddock WA, Davis SD (2005) Do xylem fibers affect vessel cavitation resistance? Plant Physiology 139, 546–556.
Do xylem fibers affect vessel cavitation resistance?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgurvN&md5=43c2f622a00f79a8bd8922311b547680CAS | 16100359PubMed |

Johnson DM, Woodruff DR, McCulloh KA, Meinzer FC (2009) Leaf hydraulic conductance, measured in situ, declines and recover daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species. Tree Physiology 29, 879–887.
Leaf hydraulic conductance, measured in situ, declines and recover daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mvhs12isw%3D%3D&md5=751319b9a0ed3db1919e36001527eb86CAS | 19429900PubMed |

Johnson DM, McCulloh KA, Meinzer FC, Woodruff DR, Eissenstat DM (2011) Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species. Tree Physiology 31, 659–668.
Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjgtVCksQ%3D%3D&md5=490e4831d49f7bcdd98410360e223d6cCAS | 21724585PubMed |

Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC (2012) Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance. Plant, Cell & Environment 35, 760–769.
Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFWls7k%3D&md5=7b46664cdef3b405ed8f2131937c6754CAS |

Jordan GJ, Brodribb TJ, Blackman CJ, Weston PH (2013) Climate drives vein anatomy in Proteaceae. American Journal of Botany 100, 1483–1493.
Climate drives vein anatomy in Proteaceae.Crossref | GoogleScholarGoogle Scholar | 23935111PubMed |

Kufa T, Burkhardt J (2011) Variations in leaf water potential in the wild Ethiopian Coffea arabica accessions under contrasting nursery environments. Journal of Agronomy 10, 1–11.
Variations in leaf water potential in the wild Ethiopian Coffea arabica accessions under contrasting nursery environments.Crossref | GoogleScholarGoogle Scholar |

Marraccini P, Vinecky F, Alves GSC, Ramos HJO, Elbelt S, Vieira NG, Carneiro FA, Sujii PS, Alekcevetch JC, Silva VA, DaMatta FM, Ferrao MAG, Leroy T, Pot D, Vieira LGE, da Silva FR, Andrade AC (2012) Differentially expressed genes and proteins upon drought acclimation in tolerant and sensitive genotypes of Coffea canephora. Journal of Experimental Botany 63, 4191–4212.
Differentially expressed genes and proteins upon drought acclimation in tolerant and sensitive genotypes of Coffea canephora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSlsLvJ&md5=b211c2426e83a0180c3d788c3fe6765dCAS | 22511801PubMed |

Méndez-Alonzo R, Ewers FW, Sack L (2013) Ecological variation in leaf biomechanics and its scaling with tissue structure across three mediterranean-climate plant communities. Functional Ecology 27, 544–554.
Ecological variation in leaf biomechanics and its scaling with tissue structure across three mediterranean-climate plant communities.Crossref | GoogleScholarGoogle Scholar |

Meyer FG (1965) Notes on wild Coffea arabica from Southwestern Ethiopia, with some historical considerations. Economic Botany 19, 136–151.
Notes on wild Coffea arabica from Southwestern Ethiopia, with some historical considerations.Crossref | GoogleScholarGoogle Scholar |

Milla R, Reich PB (2007) The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proceedings. Biological Sciences 274, 2109–2115.
The scaling of leaf area and mass: the cost of light interception increases with leaf size.Crossref | GoogleScholarGoogle Scholar |

Müller C, Cramer W, Hare WL, Lotze-Campen H (2011) Climate change risks for African agriculture. Proceedings of the National Academy of Sciences of the United States of America 108, 4313–4315.
Climate change risks for African agriculture.Crossref | GoogleScholarGoogle Scholar | 21368199PubMed |

Nardini A, Salleo S (2003) Effects of the experimental blockage of the major veins on leaf hydraulics and gas exchange of Prunus laurocerasus L. leaves. Journal of Experimental Botany 54, 1213–1219.
Effects of the experimental blockage of the major veins on leaf hydraulics and gas exchange of Prunus laurocerasus L. leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFCju7k%3D&md5=b17715a2977f6ef5f2d76082192a0facCAS | 12654872PubMed |

Nardini A, Salleo S, Raimondo F (2003) Changes in leaf hydraulic conductance correlate with leaf vein embolism in Cercis siliquastrum L. Trees – Structure and Function 17, 529–534.
Changes in leaf hydraulic conductance correlate with leaf vein embolism in Cercis siliquastrum L.Crossref | GoogleScholarGoogle Scholar |

Nardini A, Gortan E, Salleo S (2005) Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species. Functional Plant Biology 32, 953–961.
Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species.Crossref | GoogleScholarGoogle Scholar |

Nardini A, Pedà G, La Rocca N (2012a) 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, Pedà G, Salleo S (2012b) Alternative methods for scaling leaf hydraulic conductance offer new insights into the structure–function relationship of sun and shade leaves. Functional Plant Biology 39, 394–401.
Alternative methods for scaling leaf hydraulic conductance offer new insights into the structure–function relationship of sun and shade leaves.Crossref | GoogleScholarGoogle Scholar |

Nardini A, Battistuzzo M, Savi T (2013) Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. New Phytologist 200, 322–329.
Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsV2ntrvE&md5=cc6435aa6ef3745c77cea6f626ce69c5CAS | 23593942PubMed |

Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469.
Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs.Crossref | GoogleScholarGoogle Scholar |

Õunapuu E, Sellin A (2013) Daily dynamics of leaf and soil-to-branch hydraulic conductance in silver birch (Betula pendula) measured in situ. Plant Physiology and Biochemistry 68, 104–110.
Daily dynamics of leaf and soil-to-branch hydraulic conductance in silver birch (Betula pendula) measured in situ.Crossref | GoogleScholarGoogle Scholar | 23681117PubMed |

Pinheiro HA, DaMatta FM, Chaves AR, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Annals of Botany 96, 101–108.
Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora.Crossref | GoogleScholarGoogle Scholar | 15888500PubMed |

Price CA, Wing S, Weitz JS (2012) Scaling and structure of dicotyledonous leaf venation networks. Ecology Letters 15, 87–95.
Scaling and structure of dicotyledonous leaf venation networks.Crossref | GoogleScholarGoogle Scholar | 22093803PubMed |

Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
Leaf hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhtrs%3D&md5=fff87787c4afc0b47840a2e7e62e7ae9CAS | 16669766PubMed |

Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198, 983–1000.
Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future.Crossref | GoogleScholarGoogle Scholar | 23600478PubMed |

Sack L, Tyree MT, Holbrook NM (2005) Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytologist 167, 403–413.
Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees.Crossref | GoogleScholarGoogle Scholar | 15998394PubMed |

Sack L, Dietrich EM, Streeter CM, Sánchez-Gómez D, Holbrook NM (2008) Leaf palmate venation and vascular redundancy confer tolerance to hydraulic disruption. Proceedings of the National Academy of Sciences of the United States of America 105, 1567–1572.
Leaf palmate venation and vascular redundancy confer tolerance to hydraulic disruption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvFCitLY%3D&md5=b956f14c37faebb0f773c9c0d75f2719CAS | 18227511PubMed |

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 |

Salleo S (1983) Water relations parameters of two Sicilian species of Senecio (groundsel) measured by the pressure-bomb technique. New Phytologist 95, 179–188.
Water relations parameters of two Sicilian species of Senecio (groundsel) measured by the pressure-bomb technique.Crossref | GoogleScholarGoogle Scholar |

Salleo S, Lo Gullo MA, Raimondo F, Nardini A (2001) Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange? Plant, Cell & Environment 24, 851–859.
Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange?Crossref | GoogleScholarGoogle Scholar |

Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011) Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156, 832–843.
Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrk%3D&md5=035989dacb128ea1c13ecb51c3b0b58bCAS | 21511989PubMed |

Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiology 164, 1772–1788.
Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsV2js70%3D&md5=2a1c7230953d346b57e202d917929c07CAS | 24306532PubMed |

Sellin A, Sack L, Õunapuu E, Karusion A (2011) Impact of light quality on leaf and shoot hydraulic properties: a case study in silver birch (Betula pendula). Plant, Cell & Environment 34, 1079–1087.
Impact of light quality on leaf and shoot hydraulic properties: a case study in silver birch (Betula pendula).Crossref | GoogleScholarGoogle Scholar |

Sellin A, Õunapuu E, Kaurilind E, Alber M (2012) Size-dependent variability of leaf and shoot hydraulic conductance in silver birch. Trees – Structure and Function 26, 821–831.
Size-dependent variability of leaf and shoot hydraulic conductance in silver birch.Crossref | GoogleScholarGoogle Scholar |

Silva PEM, Cavatte PC, Morais LE, Medina EF, DaMatta FM (2013) The functional divergence of biomass partitioning, carbon gain and water use in Coffea canephora in response to water supply: implications for breeding aimed at improving drought tolerance. Environmental and Experimental Botany 87, 49–57.
The functional divergence of biomass partitioning, carbon gain and water use in Coffea canephora in response to water supply: implications for breeding aimed at improving drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Simonin KA, Limm EB, Dawson TE (2012) Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain. New Phytologist 193, 939–947.
Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain.Crossref | GoogleScholarGoogle Scholar | 22224403PubMed |

Sinclair TR, Zwieniecki MA, Holbrook NM (2008) Low leaf hydraulic conductance associated with drought tolerance in soybean. Physiologia Plantarum 132, 446–451.
Low leaf hydraulic conductance associated with drought tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktb4%3D&md5=09bd3981785793331151959d973c8c7dCAS | 18333998PubMed |

Smillie IRA, Pike KA, Murchie EH (2012) Variation in vein density and mesophyll cell architecture in a rice deletion mutant population. Journal of Experimental Botany 63, 4563–4570.
Variation in vein density and mesophyll cell architecture in a rice deletion mutant population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1egur7F&md5=0ccdd9552c06e2801ef218dea06d5b92CAS |

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 |

Tausend PC, Goldstein G, Meinzer FC (2000) Water utilization, plant hydraulic properties and xylem vulnerability in three contrasting coffee (Coffea arabica) cultivars. Tree Physiology 20, 159–168.
Water utilization, plant hydraulic properties and xylem vulnerability in three contrasting coffee (Coffea arabica) cultivars.Crossref | GoogleScholarGoogle Scholar | 12651468PubMed |

Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23, 267–282.
The measurement of the turgor pressure and water relations of plants by the pressure-bomb technique.Crossref | GoogleScholarGoogle Scholar |

Tyree MT, Velez V, Dalling JW (1998) Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia 114, 293–298.
Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes.Crossref | GoogleScholarGoogle Scholar |

Vilagrosa A, Morales F, Abadía A, Bellot J, Cochard H, Gil-Pelegrín E (2010) Are symplast tolerance to intense drought conditions and xylem vulnerability to cavitation coordinated? An integrated analysis of photosynthetic, hydraulic and leaf level processes in two Mediterranean drought-resistant species. Environmental and Experimental Botany 69, 233–242.
Are symplast tolerance to intense drought conditions and xylem vulnerability to cavitation coordinated? An integrated analysis of photosynthetic, hydraulic and leaf level processes in two Mediterranean drought-resistant species.Crossref | GoogleScholarGoogle Scholar |

Wright I, Reich P, Westboy M, Ackerly D, Brauch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen J, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=e9071180899e5420611f7642ada4a2a5CAS | 15103368PubMed |

Zwieniecki MA, Boyce CK, Holbrook NM (2004) Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant, Cell & Environment 27, 357–365.
Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves.Crossref | GoogleScholarGoogle Scholar |