Partitioning hydraulic resistance in Sorghum bicolor leaves reveals unique correlations with stomatal conductance during drought
Troy W. Ocheltree A C D , Jesse B. Nippert B , Mary Beth Kirkham C and P. Vara V. Prasad C
+ Author Affiliations
- Author Affiliations
A Department of Forest Resources, University of Minnesota, 1530 Cleveland Avenue N., St. Paul, MN 55108, USA.
B Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, USA.
C Department of Agronomy, Kansas State University, 2004 Throckmorton Hall, Manhattan, KS 66506, USA.
D Corresponding author. Email: ochel005@umn.edu
Functional Plant Biology 41(1) 25-36 https://doi.org/10.1071/FP12316
Submitted: 25 October 2012 Accepted: 31 May 2013 Published: 30 July 2013
Abstract
The hydraulic architecture of leaves represents the final path along which liquid water travels through the plant and comprises a significant resistance for water movement, especially for grasses. We partitioned leaf hydraulic resistance of six genotypes of Sorghum bicolor L. (Moench) into leaf specific hydraulic resistance within the large longitudinal veins (r*LV) and outside the large veins (r*OLV), and correlated these resistances with the response of stomatal conductance (gs) and photosynthesis (A) to drought. Under well-watered conditions, gs was tightly correlated with r*OLV (r2 = 0.95), but as soil moisture decreased, gs was more closely correlated with r*LV (r2 = 0.97). These results suggest that r*OLV limits maximum rates of gas exchange, but the ability to efficiently move water long distances (low r*LV) becomes more important for the maintenance of cell turgor and gas exchange as soil moisture declines. Hydraulic resistance through the leaf was negatively correlated with evapotranspiration (P < 0.001) resulting in more conservative water use in genotypes with large leaf resistance. These results illustrate the functional significance of leaf resistance partitioning to declining soil moisture in a broadly-adapted cereal species.
Additional keywords: drought tolerance, leaf hydraulic conductance, stomatal conductance, plant anatomy.
References
Ackerson RC, Krieg DR, Miller TD, Zartman RE (1977) Water relations of field grown cotton and sorghum: temporal and diurnal changes in leaf water, osmotic, and turgor potentials. Crop Science 17, 76–80.| Water relations of field grown cotton and sorghum: temporal and diurnal changes in leaf water, osmotic, and turgor potentials.Crossref | GoogleScholarGoogle Scholar |
Altus D, Canny M (1985) Water pathways in wheat leaves. 1. The division of fluxes between different vein types. Australian Journal of Plant Physiology 12, 173–181.
| Water pathways in wheat leaves. 1. The division of fluxes between different vein types.Crossref | GoogleScholarGoogle Scholar |
Altus D, Canny M, Blackman D (1985) Water pathways in wheat leaves. 2. Water-conducting capacities and vessel diameters of different vein types, and the behavior of the integrated vein network. Australian Journal of Plant Physiology 12, 183–199.
| Water pathways in wheat leaves. 2. Water-conducting capacities and vessel diameters of different vein types, and the behavior of the integrated vein network.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 |
Brodribb TJ, Feild TS (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant, Cell & Environment 23, 1381–1388.
| Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132, 2166–2173.
| Stomatal closure during leaf dehydration, correlation with other leaf physiological traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVantbc%3D&md5=5e37abae6f351712a8923a2cc0de35c9CAS | 12913171PubMed |
Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiology 137, 1139–1146.
| Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislOqs7k%3D&md5=55177ec044765c553099af456f809236CAS | 15734905PubMed |
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=0f0bcc31dbcd41cfef4c9194f51ea13dCAS | 17556506PubMed |
Buckley TN (2005) The control of stomata by water balance. New Phytologist 168, 275–292.
| The control of stomata by water balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Smu7bI&md5=00245a1e868c3b96f4891c3b2c5e03d0CAS | 16219068PubMed |
Cochard H, Froux F, Mayr S, Coutand C (2004a) Xylem wall collapse in water-stressed pine needles. Plant Physiology 134, 401–408.
| Xylem wall collapse in water-stressed pine needles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVansrg%3D&md5=bd03e75e841f5ac5767b930dfcdd0f98CAS | 14657404PubMed |
Cochard H, Nardini A, Coll L (2004b) Hydraulic architecture of leaf blades: where is the main resistance? Plant, Cell & Environment 27, 1257–1267.
| Hydraulic architecture of leaf blades: where is the main resistance?Crossref | GoogleScholarGoogle Scholar |
Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiology 143, 122–133.
| Putative role of aquaporins in variable hydraulic conductance of leaves in response to light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1OgtQ%3D%3D&md5=ca60fb78d4d509f18ded15ad80a7ed30CAS | 17114274PubMed |
Comstock JP (2000) Correction of thermocouple psychrometer readings for the interaction of temperature and actual water potential. Crop Science 40, 709–712.
| Correction of thermocouple psychrometer readings for the interaction of temperature and actual water potential.Crossref | GoogleScholarGoogle Scholar |
DeLucia E, Schlesinger W (1991) Resource-use efficiency and drought tolerance in adjacent Great-Basin and Sierran plants. Ecology 72, 51–58.
| Resource-use efficiency and drought tolerance in adjacent Great-Basin and Sierran plants.Crossref | GoogleScholarGoogle Scholar |
Fernández R, Reynolds J (2000) Potential growth and drought tolerance of eight desert grasses: lack of a trade-off? Oecologia 123, 90–98.
| Potential growth and drought tolerance of eight desert grasses: lack of a trade-off?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 |
Girma F, Krieg D (1992) Osmotic adjustment in Sorghum. 2. Relationship to gas-exchange rates. Plant Physiology 99, 583–588.
| Osmotic adjustment in Sorghum. 2. Relationship to gas-exchange rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XkvVOjtrs%3D&md5=0e4946dc6640053437b28a4bae655515CAS | 16668926PubMed |
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26, 689–701.
| Scaling of angiosperm xylem structure with safety and efficiency.Crossref | GoogleScholarGoogle Scholar | 16510385PubMed |
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=71889aaa95e1898406faa35ca70ea226CAS | 19542196PubMed |
Holloway-Phillips MM, Brodribb T (2011a) Minimum hydraulic safety leads to maximum water-use efficiency in a forage grass. Plant, Cell & Environment 34, 302–313.
| Minimum hydraulic safety leads to maximum water-use efficiency in a forage grass.Crossref | GoogleScholarGoogle Scholar |
Holloway-Phillips MM, Brodribb TJ (2011b) Contrasting hydraulic regulation in closely related forage grasses: implications for plant water use. Functional Plant Biology 38, 594–605.
| Contrasting hydraulic regulation in closely related forage grasses: implications for plant water use.Crossref | GoogleScholarGoogle Scholar |
Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell & Environment 24, 113–121.
| Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine.Crossref | GoogleScholarGoogle Scholar |
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=5e6ace0e516b0dc1b973eb80fbad3816CAS |
Jones MM, Turner NC (1978) Osmotic adjustment in leaves of sorghum in response to water deficits. Plant Physiology 61, 122–126.
| Osmotic adjustment in leaves of sorghum in response to water deficits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtVWkuro%3D&md5=0b9272e71ca1e31a2644f35cdc6edb6bCAS | 16660224PubMed |
Kim YX, Steudle E (2007) Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. Journal of Experimental Botany 58, 4119–4129.
| Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlymtbs%3D&md5=903fedded05b1bc76b82739a48132d51CAS | 18065766PubMed |
Kodama N, Cousins A, Tu KP, Barbour MM (2011) Spatial variation in photosynthetic CO2 carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum × Secale) relates to mesophyll conductance and the Péclet effect. Plant, Cell & Environment 34, 1548–1562.
| Spatial variation in photosynthetic CO2 carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum × Secale) relates to mesophyll conductance and the Péclet effect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yms7nI&md5=6c6f8a756ea3a15e0370d97809ead878CAS |
Marenco RA, Siebke K, Farquhar GD, Ball MC (2006) Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum. Functional Plant Biology 33, 1103–1113.
| Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum.Crossref | GoogleScholarGoogle Scholar |
Markesteijn L, Poorter L, Bongers F, Paz H, Sack L (2011) Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance. New Phytologist 191, 480–495.
| Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance.Crossref | GoogleScholarGoogle Scholar | 21477008PubMed |
Martre P, Cochard H, Durand JL (2001) Hydraulic architecture and water flow in growing grass tillers (Festuca arundinacea Schreb.). Plant, Cell & Environment 24, 65–76.
| Hydraulic architecture and water flow in growing grass tillers (Festuca arundinacea Schreb.).Crossref | GoogleScholarGoogle Scholar |
McCulloh K, Sperry J, Adler F (2003) Water transport in plants obeys Murray’s law. Nature 421, 939–942.
| Water transport in plants obeys Murray’s law.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVKgtbw%3D&md5=79966ef6e576430222a94ffa60978736CAS | 12607000PubMed |
McKown AD, Cochard H, Sack L (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. American Naturalist 175, 447–460.
| Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution.Crossref | GoogleScholarGoogle Scholar | 20178410PubMed |
Meinzer FC (2002) Co-ordination of vapour and liquid phase water transport properties in plants. Plant, Cell & Environment 25, 265–274.
| Co-ordination of vapour and liquid phase water transport properties in plants.Crossref | GoogleScholarGoogle Scholar |
Meinzer F, Grantz D (1990) Stomatal and hydraulic conductance in growing sugarcane – stomatal adjustment to water transport capacity. Plant, Cell & Environment 13, 383–388.
| Stomatal and hydraulic conductance in growing sugarcane – stomatal adjustment to water transport capacity.Crossref | GoogleScholarGoogle Scholar |
Meinzer FC, Goldstein G, Jackson P, Holbrook NM, Gutiérrez MV, Cavelier J (1995) Environmental and physiological regulation of transpiration in tropical forest gap species: the influence of boundary layer and hydraulic properties. Oecologia 101, 514–522.
| Environmental and physiological regulation of transpiration in tropical forest gap species: the influence of boundary layer and hydraulic properties.Crossref | GoogleScholarGoogle Scholar |
Mott KA (2007) Leaf hydraulic conductivity and stomatal responses to humidity in amphistomatous leaves. Plant, Cell & Environment 30, 1444–1449.
| Leaf hydraulic conductivity and stomatal responses to humidity in amphistomatous leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhsrbO&md5=adc62657a1d9823faa21e4c0c3225a1dCAS |
Nardini A, Salleo S (2005) Water stress-induced modifications of leaf hydraulic architecture in sunflower: co-ordination with gas exchange. Journal of Experimental Botany 56, 3093–3101.
| Water stress-induced modifications of leaf hydraulic architecture in sunflower: co-ordination with gas exchange.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GlsbbO&md5=17590d968758405fb1107ab5defa1b22CAS | 16246857PubMed |
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, Salleo S, Andri S (2005) Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus L. cv Margot). Plant, Cell & Environment 28, 750–759.
| Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus L. cv Margot).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVaku7o%3D&md5=aff3a036aded6805d1a4efe0696542b5CAS |
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 |
Ocheltree TW, Nippert JB, Prasad PVV (2012) Changes in stomatal conductance along grass blades reflect changes in leaf structure. Plant, Cell & Environment 35, 1040–1049.
| Changes in stomatal conductance along grass blades reflect changes in leaf structure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zosVGhtQ%3D%3D&md5=2b19592a101b9bd8c8ae20b35e4c03ceCAS |
Peak D, Mott KA (2011) A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant, Cell & Environment 34, 162–178.
| A new, vapour-phase mechanism for stomatal responses to humidity and temperature.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2011) R: A language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/
Ruzin SE (1999) ‘Plant microtechnique and microscopy.’ (Oxford University Press: New York)
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, 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=3f502b84989933bacc5535c1045bdb19CAS | 16669766PubMed |
Sack L, Melcher P, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53, 2177–2184.
| The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1KgtLg%3D&md5=83c383fd6a58330126fe336037d6e958CAS | 12379784PubMed |
Sack L, Streeter C, Holbrook NM (2004) Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiology 134, 1824–1833.
| Hydraulic analysis of water flow through leaves of sugar maple and red oak.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKmtrY%3D&md5=b1e95c6fb92ab6c48927d46b96be5d8bCAS | 15064368PubMed |
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 |
Sadok W, Sinclair TR (2010) Transpiration response of ‘slow-wilting’ and commercial soybean (Glycine max (L.) Merr.) genotypes to three aquaporin inhibitors. Journal of Experimental Botany 61, 821–829.
| Transpiration response of ‘slow-wilting’ and commercial soybean (Glycine max (L.) Merr.) genotypes to three aquaporin inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSrtbY%3D&md5=d19da63b337bbb76f8d8211c5b0bed9cCAS | 19969533PubMed |
Saliendra N, Sperry J, Comstock J (1995) Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis. Planta 196, 357–366.
| Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXls1Wqs7s%3D&md5=d033b6be43cd09f4a2dacef12c531bf9CAS |
Scoffoni C, Pou A, Aasamaa K, Sack L (2008) The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods. Plant, Cell & Environment 31, 1803–1812.
| The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods.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=d56e102ae2e901a986ceb4a54baa6ed3CAS | 21511989PubMed |
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=47d8b0752057897d1ff441203c1fa497CAS | 18333998PubMed |
Sperry JS, Hacke UG (2002) Desert shrub water relations with respect to soil characteristics and plant functional type. Functional Ecology 16, 367–378.
| Desert shrub water relations with respect to soil characteristics and plant functional type.Crossref | GoogleScholarGoogle Scholar |
Sperry J, Donnelly J, Tyree M (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11, 35–40.
| A method for measuring hydraulic conductivity and embolism in xylem.Crossref | GoogleScholarGoogle Scholar |
Sperry J, Adler F, Campbell G, Comstock J (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant, Cell & Environment 21, 347–359.
| Limitation of plant water use by rhizosphere and xylem conductance: results from a model.Crossref | GoogleScholarGoogle Scholar |
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419–432.
Trifilò P, Nardini A, Lo Gullo M, Salleo S (2003) Vein cavitation and stomatal behaviour of sunflower (Helianthus annuus) leaves under water limitation. Physiologia Plantarum 119, 409–417.
| Vein cavitation and stomatal behaviour of sunflower (Helianthus annuus) leaves under water limitation.Crossref | GoogleScholarGoogle Scholar |
Tsuda M, Tyree M (2000) Plant hydraulic conductance measured by the high pressure flow meter in crop plants. Journal of Experimental Botany 51, 823–828.
| Plant hydraulic conductance measured by the high pressure flow meter in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsLY%3D&md5=19854ec3a656993197ecd43e60ce4188CAS | 10938875PubMed |
Tyree MT, Zimmerman MH (2002) Xylem Structure and the Ascent of Sap. (Springer-Verlag: Berlin)
Tyree M, Nardini A, Salleo S, Sack L, El Omari B (2005) The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? Journal of Experimental Botany 56, 737–744.
| The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2ruro%3D&md5=414a45f8fb0c695279023a14a7d4f2e4CAS | 15582928PubMed |
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant, Cell & Environment 28, 800–812.
| Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport.Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM (2002) Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25, 1445–1450.
| Hydraulic architecture of leaf venation in Laurus nobilis L.Crossref | GoogleScholarGoogle Scholar |
