The role of leaf hydraulic conductance dynamics on the timing of leaf senescence
Juan Pablo Giraldo A B , James K. Wheeler A , Brett A. Huggett A and N. Michele Holbrook A
+ Author Affiliations
- Author Affiliations
A Harvard University, Department of Organismic and Evolutionary Biology, 16 Divinity Avenue, Cambridge, MA 02138, USA.
B Corresponding author. Email: jgiraldo@post.harvard.edu
Functional Plant Biology 41(1) 37-47 https://doi.org/10.1071/FP13033
Submitted: 10 February 2013 Accepted: 27 June 2013 Published: 14 August 2013
Abstract
We tested the hypothesis that an age-dependent reduction in leaf hydraulic conductance (Kleaf) influences the timing of leaf senescence via limitation of the stomatal aperture on xylem compound delivery to leaves of tomato (Solanum lycopersicum L.), the tropical trees Anacardium excelsum Kunth, Pittoniotis trichantha Griseb, and the temperate trees Acer saccharum Marsh. and Quercus rubra L. The onset of leaf senescence was preceded by a decline in Kleaf in tomato and the tropical trees, but not in the temperate trees. Age-dependent changes in Kleaf in tomato were driven by a reduction in leaf vein density without a proportional increase in the xylem hydraulic supply. A decline in stomatal conductance accompanied Kleaf reduction with age in tomato but not in tropical and temperate tree species. Experimental manipulations that reduce the flow of xylem-transported compounds into leaves with open stomata induced early leaf senescence in tomato and A. excelsum, but not in P. trichantha, A. saccharum and Q. rubra leaves. We propose that in tomato, a reduction in Kleaf limits the delivery of xylem-transported compounds into the leaves, thus making them vulnerable to senescence. In the tropical evergreen tree A. excelsum, xylem-transported compounds may play a role in signalling the timing of senescence but are not under leaf hydraulic regulation; leaf senescence in the deciduous trees A. trichanta, A. saccharum and Q. rubra is not influenced by leaf vascular transport.
Additional keywords: chlorophyll, leaf anatomy, leaf phenology, photosynthesis, tomato, vascular transport.
References
Aasamaa K, Niinemets U, Sober A (2005) Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny. Tree Physiology 25, 1409–1418.| Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny.Crossref | GoogleScholarGoogle Scholar | 16105808PubMed |
Albacete A, Martínez-Andújar C, Ghanem ME, Acosta M, Sánchez-Bravo J, Asins MJ, Cuartero J, Lutts S, Dodd IC, Pérez-Alfocea F (2009) Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato. Plant, Cell & Environment 32, 928–938.
| Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2jsb0%3D&md5=8d8968b04d1c348e8d823c7638e13300CAS |
Berlyn GP, Miksche JP (1976) Botanical microtechnique and cytochemistry. (Iowa State University Press: Ames, Iowa)
Blackman CJ, Brodribb TJ, Jordan GJ (2009) Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant, Cell & Environment 32, 1584–1595.
| Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species.Crossref | GoogleScholarGoogle Scholar |
Boonman A, Prinsen E, Gilmer F, Schurr U, Peeters AJM, Voesenek L, Pons TL (2007) Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients. Plant Physiology 143, 1841–1852.
| Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFWjtbY%3D&md5=b5d3f00c4df91e82c6ff9d2f2dfc19feCAS | 17277095PubMed |
Boonman A, Prinsen E, Voesenek L, Pons TL (2009) Redundant roles of photoreceptors and cytokinins in regulating photosynthetic acclimation to canopy density. Journal of Experimental Botany 60, 1179–1190.
| Redundant roles of photoreceptors and cytokinins in regulating photosynthetic acclimation to canopy density.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFShs7s%3D&md5=76e5e4e3bc94586ddb48ae2a4ffafd70CAS | 19240103PubMed |
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149, 575–584.
| Hydraulic failure defines the recovery and point of death in water-stressed conifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Wqtb4%3D&md5=1263655147532700e5bc4b8701254f2dCAS | 19011001PubMed |
Brodribb TJ, Holbrook NM (2003a) Changes in leaf hydraulic conductance during leaf shedding in seasonally dry tropical forest. New Phytologist 158, 295–303.
| Changes in leaf hydraulic conductance during leaf shedding in seasonally dry tropical forest.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Holbrook NM (2003b) 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 (2006) Declining hydraulic efficiency as transpiring leaves desiccate: two types of response. Plant, Cell & Environment 29, 2205–2215.
| Declining hydraulic efficiency as transpiring leaves desiccate: two types of response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaitA%3D%3D&md5=3b48a1de64db28b3db03cef1f723c0dfCAS |
Brodribb TJ, Holbrook NM (2007) Forced depression of leaf hydraulic conductance in situ: effects on the leaf gas exchange of forest trees. Functional Ecology 21, 705–712.
| Forced depression of leaf hydraulic conductance in situ: effects on the leaf gas exchange of forest trees.Crossref | GoogleScholarGoogle Scholar |
Brodribb T, Holbrook N, Zwieniecki M, 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 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 |
Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence – a genomics approach. Plant Biotechnology Journal 1, 3–22.
| The molecular analysis of leaf senescence – a genomics approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptV2ktrs%3D&md5=914208c7a9972399529c5b1cf380e554CAS | 17147676PubMed |
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 |
Cochard H, Nardini A, Coll L (2004) 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 |
Estrella N, Menzel A (2006) Responses of leaf colouring in four deciduous tree species to climate and weather in Germany. Climate Research 32, 253–267.
| Responses of leaf colouring in four deciduous tree species to climate and weather in Germany.Crossref | GoogleScholarGoogle Scholar |
Gan SS, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986–1988.
| Inhibition of leaf senescence by autoregulated production of cytokinin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xlt12q&md5=9ee325b03921b5ebf5a01004bde3024bCAS |
Gan SS, Amasino RM (1996) Cytokinins in plant senescence: from spray and pray to clone and play. BioEssays 18, 557–565.
| Cytokinins in plant senescence: from spray and pray to clone and play.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvVWktLc%3D&md5=12aad31f9f8ccf7d1b47458dcf888b2bCAS |
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 |
Ghanem ME, Albacete A, Martinez-Andujar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Perez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). Journal of Experimental Botany 59, 3039–3050.
| Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslalsb4%3D&md5=3e3f157ff2706135d5a71fcb168e321fCAS | 18573798PubMed |
Giraldo JP, Holbrook NM (2011) Physiological mechanisms underlying the seasonality of leaf senescence and renewal in seasonally dry tropical forests trees. In ‘Seasonally dry tropical forests: ecology and conservation’. (Eds R Dirzo, H Young, H Mooney, G Ceballos) pp. 129–140. (Island Press: Washington DC)
Guo YF, Gan SS (2005) Leaf senescence: signals, execution, and regulation. In ‘Current topics in developmental biology’. (Eds G Schatten) Vol. 71, pp. 83–112. (Elsevier Academic Press: San Diego)
Hensel LL, Grbic V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. The Plant Cell 5, 553–564.
Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. Journal of Plant Physiology 158, 1317–1323.
| Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosl2mu7k%3D&md5=1f74e675c6e54d2057df27e863603443CAS |
Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annual Review of Plant Biology 57, 55–77.
| Chlorophyll degradation during senescence.Crossref | GoogleScholarGoogle Scholar | 16669755PubMed |
Kaldenhoff R, Fischer M (2006) Aquaporins in plants. Acta Physiologica (Oxford, England) 187, 169–176.
| Aquaporins in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVCgurs%3D&md5=58b3ad214d324c26cf53fd78dfd8198bCAS |
Kaldenhoff R, Ribas-Carbo M, Flexas J, Lovisolo C, Heckwolf M, Uehlein N (2008) Aquaporins and plant water balance. Plant, Cell & Environment 31, 658–666.
| Aquaporins and plant water balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvFehur8%3D&md5=e5452be32662aba1cff66727d201fa34CAS |
Lee DW, O’Keefe J, Holbrook NM, Feild TS (2003) Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecological Research 18, 677–694.
| Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVClt70%3D&md5=245a0897b56a3bf510320f08d1a85f1eCAS |
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annual Review of Plant Biology 58, 115–136.
| Leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVahs70%3D&md5=af29ba153b44fac5167ae4448786c096CAS | 17177638PubMed |
Lo Gullo MA, Noval LC, Salleo S, Nardini A (2004) Hydraulic architecture of plants of Helianthus annuus L. cv. Margot: evidence for plant segmentation in herbs. Journal of Experimental Botany 55, 1549–1556.
| Hydraulic architecture of plants of Helianthus annuus L. cv. Margot: evidence for plant segmentation in herbs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlOqu7w%3D&md5=1fca5c17333a2a28048449d7b53c96faCAS | 15181104PubMed |
Lo Gullo MA, Nardini A, Trifilo P, Salleo S (2005) Diurnal and seasonal variations in leaf hydraulic conductance in evergreen and deciduous trees. Tree Physiology 25, 505–512.
| Diurnal and seasonal variations in leaf hydraulic conductance in evergreen and deciduous trees.Crossref | GoogleScholarGoogle Scholar | 15687099PubMed |
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 |
McLaughlin SB, Wimmer R (1999) Calcium physiology and terrestrial ecosystem processes. New Phytologist 142, 373–417.
| Calcium physiology and terrestrial ecosystem processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFGrs7c%3D&md5=2ab8ff8025642a5697b555557ddba9e1CAS |
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 |
Miller A, Schlagnhaufer C, Spalding M, Rodermel S (2000) Carbohydrate regulation of leaf development: prolongation of leaf senescence in Rubisco antisense mutants of tobacco. Photosynthesis Research 63, 1–8.
| Carbohydrate regulation of leaf development: prolongation of leaf senescence in Rubisco antisense mutants of tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymtLY%3D&md5=7e25588100aba0781079ea036b85f3d3CAS | 16252160PubMed |
Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Functional Plant Biology 31, 203–216.
| Die and let live: leaf senescence contributes to plant survival under drought stress.Crossref | GoogleScholarGoogle Scholar |
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, Gortan E, Ramani M, Salleo S (2008) Heterogeneity of gas exchange rates over the leaf surface in tobacco: an effect of hydraulic architecture? Plant, Cell & Environment 31, 804–812.
| Heterogeneity of gas exchange rates over the leaf surface in tobacco: an effect of hydraulic architecture?Crossref | GoogleScholarGoogle Scholar |
Nardini A, Raimondo F, Lo Gullo MA, Salleo S (2010) Leafminers help us understand leaf hydraulic design. Plant, Cell & Environment 33, 1091–1100.
Ono K, Watanabe A (1997) Levels of endogenous sugars, transcripts of rbcS and rbcL, and of Rubisco protein in senescing sunflower leaves. Plant & Cell Physiology 38, 1032–1038.
| Levels of endogenous sugars, transcripts of rbcS and rbcL, and of Rubisco protein in senescing sunflower leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtlyltrc%3D&md5=0f5a2bd758081203e5f15f44b3b42fdeCAS |
Ono K, Nishi Y, Watanabe A, Terashima I (2001) Possible mechanisms of adaptive leaf senescence. Plant Biology 3, 234–243.
| Possible mechanisms of adaptive leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFGhsb4%3D&md5=91c21dced2924155b110d6aa49753ea5CAS |
Pourtau N, Mares M, Purdy S, Quentin N, Ruel A, Wingler A (2004) Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 219, 765–772.
| Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1GlurY%3D&md5=a892b47b4d46986d3d6319a62ab6007dCAS | 15118859PubMed |
Richmond AE, Lang A (1957) Effect of kinetin on protein content and survival of detached Xanthium leaves. Science 125, 650–651.
| Effect of kinetin on protein content and survival of detached Xanthium leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2sXkslOktA%3D%3D&md5=c8c026c8ec96992bf36d6dfdc9418095CAS |
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675–709.
| Sugar sensing and signaling in plants: conserved and novel mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKht7k%3D&md5=51c252f22fd5eba6aecaf76c949f2ee7CAS | 16669778PubMed |
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 PJ, 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 |
Salleo S, Nardini A, Lo Gullo MA, Ghirardelli LA (2002) Changes in stem and leaf hydraulics preceding leaf shedding in Castanea sativa L. Biologia Plantarum 45, 227–234.
| Changes in stem and leaf hydraulics preceding leaf shedding in Castanea sativa L.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C, Sack L, PrometheusWiki contributors (2010) ‘Quantifying leaf vein traits.’ PrometheusWiki. Available at: http://www.publish.csiro.au/prometheuswiki/tiki-pagehistory.php?page=Quantifying leaf vein traits&preview=14
Sigurdsson BD (2001) Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study. Trees – Structure and Function 15, 403–413.
| Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Perry AH, Sullivan JEM (1991) Pit membrane degradation and air-embolism formation in aging xylem vessels of Populus tremuloides Michx. Journal of Experimental Botany 42, 1399–1406.
| Pit membrane degradation and air-embolism formation in aging xylem vessels of Populus tremuloides Michx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsFKksA%3D%3D&md5=a1cba4c79af8af9e3734f0a464d40a58CAS |
Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistivity in xylem conduits. Plant, Cell & Environment 28, 456–465.
| Comparative analysis of end wall resistivity in xylem conduits.Crossref | GoogleScholarGoogle Scholar |
Swartzberg D, Dai N, Gan S, Amasino R, Granot D (2006) Effects of cytokinin production under two SAG promoters on senescence and development of tomato plants. Plant Biology 8, 579–586.
| Effects of cytokinin production under two SAG promoters on senescence and development of tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSktbjF&md5=87849b452102a878ead6093ae39dbc34CAS | 16883480PubMed |
Thomas H, Ougham H, Canter P, Donnison I (2002) What stay-green mutants tell us about nitrogen remobilization in leaf senescence. Journal of Experimental Botany 53, 801–808.
| What stay-green mutants tell us about nitrogen remobilization in leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFSntLo%3D&md5=643d76fd286b1ad0a0c4de16c32d3530CAS | 11912223PubMed |
van Doorn WG (2008) Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? Journal of Experimental Botany 59, 1963–1972.
| Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFWku7g%3D&md5=817628c9df842dfc432d65ce06e45ea3CAS | 18453532PubMed |
Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Functional Ecology 6, 469–475.
| The relation of foliar phenology to xylem embolism in trees.Crossref | GoogleScholarGoogle Scholar |
Wingler A, Mares M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytologist 161, 781–789.
| Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Woo HR, Goh CH, Park JH, de la Serve BT, Kim JH, Park YI, Nam HG (2002) Extended leaf longevity in the ore4–1 mutant of Arabidopsis with a reduced expression of a plastid ribosomal protein gene. The Plant Journal 31, 331–340.
| Extended leaf longevity in the ore4–1 mutant of Arabidopsis with a reduced expression of a plastid ribosomal protein gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntFelsb4%3D&md5=2775e68cdfbac239d42a5c70e83fc36fCAS | 12164812PubMed |
Wright SJ (1991) Seasonal drought and the phenology of understory shrubs in a tropical moist forest. Ecology 72, 1643–1657.
| Seasonal drought and the phenology of understory shrubs in a tropical moist forest.Crossref | GoogleScholarGoogle Scholar |
Wright SJ, Cornejo FH (1990) Seasonal drought and leaf fall in a tropical forest. Ecology 71, 1165–1175.
| Seasonal drought and leaf fall in a tropical forest.Crossref | GoogleScholarGoogle Scholar |
Wright SJ, Vanschaik CP (1994) Light and the phenology of tropical trees. American Naturalist 143, 192–199.
| Light and the phenology of tropical trees.Crossref | GoogleScholarGoogle Scholar |
Ye Q, Holbrook NM, Zwieniecki MA (2008) Cell-to-cell pathway dominates xylem-epidermis hydraulic connection in Tradescantia fluminensis (Vell. Conc.) leaves. Planta 227, 1311–1319.
| Cell-to-cell pathway dominates xylem-epidermis hydraulic connection in Tradescantia fluminensis (Vell. Conc.) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1Ght78%3D&md5=c520177fddea64ffa7eeeae276dadf77CAS | 18273638PubMed |
Zhang YX, Equiza MA, Zheng QS, Tyree MT (2012) Factors controlling plasticity of leaf morphology in Robinia pseudoacacia L. II: the impact of water stress on leaf morphology of seedlings grown in a controlled environment chamber. Annals of Forest Science 69, 39–47.
| Factors controlling plasticity of leaf morphology in Robinia pseudoacacia L. II: the impact of water stress on leaf morphology of seedlings grown in a controlled environment chamber.Crossref | GoogleScholarGoogle Scholar |
Zimmermann MH (1983) ‘Xylem structure and the ascent of sap.’ (Springer-Verlag: Berlin)
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 |
