Abstract
Acclimation of light sensitivity of hydraulic conductance of shoots of silver birch (Betula pendula) and hybrid aspen (Populus × wettsteinii) to growth environments with three different air humidities was studied. Hydraulic conductance of shoots kept for 1–2 h in darkness (D) or in light (L) was measured by the pressure chamber method, and light sensitivity was defined as a significant difference between D and L shoots. Light sensitivity of shoots grown in three different air humidities was found to vary. Amongst shoots grown in current natural air, only the hydraulic conductance of the whole shoot and that of the leaf blades of birch upper foliage were significantly light sensitive. Amongst shoots grown in decreased air humidity, hydraulic conductance of the whole shoot, the leaf blades, and the stem and petioles of birch upper foliage, the conductance of the whole shoot and the leaf blades of birch lower foliage, and the conductance of the whole shoot of aspen upper foliage were light sensitive. None of the shoots grown in increased air humidity were significantly light sensitive. We predict that light sensitivity will become more widespread among species in regions where air humidity decreases as a result of global climate change, and vice versa. Low white light always caused the same increase in hydraulic conductance as high white light, and blue and white light always caused an increase in conductance about two times greater than red light, indicating that growth environment did not markedly modify the mechanism of light sensitivity.
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Aasamaa K, Sõber A (2005) Seasonal courses of maximum hydraulic conductance in shoots of six temperate deciduous tree species. Funct Plant Biol 32:1077–1087. doi:10.1071/FP05088
Aasamaa K, Sõber A (2010) Sensitivity of stem and petiole hydraulic conductance of deciduous trees to xylem sap ion concentration. Biol Plant 54:299–307. doi:10.1007/s10535-010-0052-9
Aasamaa K, Sõber A (2012) Light sensitivity of shoot hydraulic conductance in five temperate deciduous tree species. Funct Plant Biol 39:661–669. doi:10.1071/FP12047
Aasamaa K, Sõber A, Hartung W, Niinemets Ü (2004) Drought acclimation of two deciduous tree species of different layers in a temperate forest canopy. Trees 18:93–101. doi:10.1007/S00468-003-0285-8
Aasamaa K, Niinemets Ü, Sõber A (2005) Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny. Tree Physiol 25:1409–1418. doi:10.1093/treephys/25.11.1409
Aasamaa K, Heinsoo K, Holm B (2010) Biomass production, water use and photosynthesis of Salix clones grown in a wastewater purification system. Biomass Bioenergy 34:897–905. doi:10.1016/j.biombioe.2010.01.035
Adaskaveg JE, Shaw DA, Ogawa JM (1990) A mist generator and environmental monitoring system for field studies on shothole disease of almond. Plant Dis 74:558–562. doi:10.1094/PD-74-0558
Baaziz KB, Lopez D, Rabot A, Combes D, Gousset A, Bouzid S, Cochard H, Sakr S, Venisse J-S (2012) Light-mediated Kleaf induction and contribution of both the PIP1s and PIP2s aquaporins in five tree species: walnut (Juglans regia) case study. Tree Physiol 32:423–434. doi:10.1093/treephys/tps022
Bakker JC (1991) Effects of humidity on stomatal density and its relation to leaf conductance. Sci Hortic 48:205–212. doi:10.1016/0304-4238(91)90128-L
Bañon S, Ochoa J, Franco JA, Alarcón JJ, Sánchez-Blanco MJ (2006) Hardening of oleander seedlings by deficit irrigation and low air humidity. Environ Exp Bot 56:36–43. doi:10.1016/j.envexpbot.2004.12.004
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 Physiol 143:122–133. doi:10.1104/pp.106.090092
Cunningham SC (2006) Effects of vapour pressure deficit on growth of temperate and tropical evergreen rainforest trees of Australia. Acta Oecol 30:399–406. doi:10.1016/j.actao.2006.05.009
Eensalu E, Kupper P, Sellin A, Rahi M, Sõber A, Kull O (2008) Do stomata operate at the same relative opening range along a canopy profile of Betula pendula? Funct Plant Biol 35:103–110. doi:10.1071/FP07258
Ellenberg H (1996) Vegetation of Central Europe with the Alps in ecological, dynamic and historical view, 5th edn (in German). Eugen Ulmer, Stuttgart
Fanourakis D, Carvalho SMP, Almeida DPF, Heuvelink E (2011) Avoiding high relative air humidity during critical stages of leaf ontogeny is decisive for stomatal functioning. Physiol Plant 142:274–286. doi:10.1111/j.1399-3054.2011.01475.x
Gascó A, Nardini A, Salleo S (2004) Resistance to water flow through leaves of Coffea arabica is dominated by extra-vascular tissues. Funct Plant Biol 31:1161–1168. doi:10.1071/FP04032
Guyot G, Scoffoni C, Sack L (2012) Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control. Plant Cell Environ 35:857–871. doi:10.1111/j.1365-3040.2011.02458.x
Heino R, Tuomenvirta H, Vuyglinsky VS, Gustafsson BG, Alexandersson H, Bärring L, Briede A, Cappelen J, Chen D, Falarz M, Forland EJ, Haapala J, Jaagus J, Kitaev L, Kont A, Kuusisto E, Lindrström G, Meier HEM, Mietus M, Moberg A, Myrberg K, Niedzwiedz T, Nordli O, Omstedt A, Orviku K, Pruszak Z, Rimkus E, Russak V, Schrum C, Suursaar Ü, Vihma T, Weisse R, Wibig J (2008) Past and current climate change. In: Bolle H-J, Menenti M, Rasool I (eds) Assessment of climate change for the Baltic Sea basin. Springer, Heidelberg, pp 35–131
Hendrey GR, Ellsworth DE, Lewin KF, Nagy J (1999) A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Global Change Biol 5:293–309. doi:10.1046/j.1365-2486.1999.00228.x
In B-C, Sato K, Ito K, Inamoto K, Doi M, Mori G (2006) Influences of preharvest relative humidity on yield, vase life and transpiration of cut roses. Environ Control Biol 44:257–263
Jones HG (2007) Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance. J Exp Bot 58:119–130. doi:10.1093/jxb/erl118
Karger DN, Kluge J, Abrahamczyk S, Salazar L, Homeier J, Lehnert M, Amoroso VB, Kessler M (2012) Bryophyte cover on trees as proxy for air humidity in the tropics. Ecol Indic 20:277–281. doi:10.1016/j.ecolind.2012.02.026
Kim YX, Steudle E (2007) Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. J Exp Bot 58:4119–4129. doi:10.1093/jxb/erm270
Kim YX, Steudle E (2009) Gating of aqùaporins by light and reactive oxygen species in leaf parenchyma cells of the midrib of Zea mays. J Exp Bot 60:547–556. doi:10.1093/jxb/ern299
Kupper P, Sõber J, Sellin A, Lõhmus K, Tullus A, Räim O, Lubenets K, Tulva I, Uri V, Zobel M, Kull O, Sõber A (2011) An experimental facility for free air humidity manipulation (FAHM) can alter water flux through deciduous tree canopy. Environ Exp Bot 72:432–438. doi:10.1016/j.envexpbot.2010.09.003
Kuwagata T, Ishikawa-Sakurai J, Hayashi H, Nagasuga K, Fukushi K, Ahamed A, Takasugi K, Katsuhara M, Murai-Hatano M (2012) Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. Plant Cell Physiol 53:1418–1431. doi:10.1093/pcp/pcs087
Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579. doi:10.1093/aob/mcn244
Lee J, Holbrook NM, Zwieniecki MA (2012) Ion induced changes in the structure of bordered pit membranes. Front Plant Sci 3:55. doi:10.3389/fpls.2012.00055
Lendzion J, Leuschner C (2008) Growth of European beech (Fagus sylvatica L.) saplings is limited by elevated atmospheric vapour pressure deficits. For Ecol Manage 256:648–655. doi:10.1016/j.foreco.2008.05.008
Lendzion J, Leuschner C (2009) Temperate forest herbs are adapted to high air humidity—evidence from climate chamber and humidity manipulation experiments in the field. Can J For Res 39:2332–2342. doi:10.1139/X09-143
Leuschner C (2002) Air humidity as an ecological factor for woodland herbs: leaf water status, nutrient uptake, leaf anatomy, and productivity of eight species grown at low or high vpd levels. Flora 197:262–274. doi:10.1078/0367-2530-00040
Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624. doi:10.1146/annurev.arplant.59.032607.092734
Mortensen LM, Ottosen C-O, Gislerød HR (2001) Effects of air humidity and K:Ca ratio on growth, morphology, flowering and keeping quality of pot roses. Sci Hortic 90:131–141. doi:10.1016/S0304-4238(00)00251-X
Nardini A, Pitt F (1999) Drought resistance of Quercus pubescens as a function of root hydraulic conductance, xylem embolism and hydraulic architecture. New Phytol 143:485–493. doi:10.1046/j.1469-8137.1999.00476.x
Nardini A, Salleo S, Andri S (2005) Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus L. cv Margot). Plant, Cell Environ 28:750–759. doi:10.1111/j.1365-3040.2005.01320.x
Nardini A, Grego F, Trifilò P, Salleo S (2010) Changes of xylem sap ionic content and stem hydraulics in response to irradiance in Laurus nobilis. Tree Physiol 30:628–635. doi:10.1093/treephys/tpq017
Nardini A, Pedá G, Salleo A (2012) Alternative methods for scaling leaf hydraulic conductance offer new insights into the structure–function relationships of sun and shade leaves. Funct Plant Biol 39:394–401. doi:10.1071/FP12020
Newman JA, Anand M, Henry HA, Hunt SL, Gedalof Z (2011) Climate change biology. CABI, Wallingford
Pantin F, Simonneau T, Muller B (2012) Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny. New Phytol 196:349–366. doi:10.1111/j.1469-8137.2012.04273.x
Pospíšilová J (1996) Effect of air humidity on the development of functional stomatal apparatus. Biol Plant 38:197–204. doi:10.1007/BF02873846
Powell GW, Bork EW (2005) Simulated aspen understory microclimate effects on alfalfa growth. Agron J 97:1361–1366. doi:10.2134/agronj 2005.0048
Rockwell FE, Holbrook NM, Zwieniecki MA (2011) Hydraulic conductivity of red oak (Quercus rubra L.) leaf tissue does not respond to light. Plant Cell Environ 34:565–579. doi:10.1111/j.1365-3040.2011.02263.x
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). J Vis Exp 70:e4179. doi:10.3791/4179
Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. J Exp Bot 53:2177–2184. doi:10.1093/jxb/erf069
Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26:1343–1356. doi:10.1046/j.0016-8025.2003.01058.x
Salleo S, Raimondo F, Trifilò P, Nardini A (2003) Axial-to-radial water permeability of leaf major veins: a possible determinant of the impact of vein embolism on leaf hydraulics? Plant Cell Environ 26:1749–1758. doi:10.1046/j.1365-3040.2003.01092.x
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 Environ 31:1803–1812. doi:10.1111/j.1365-3040.2008.01884.x
Sellin A, Kupper P (2005a) Effects of light availability versus hydraulic constraints on stomatal responses within a crown of silver birch. Oecologia 142:388–397. doi:10.1007/s00442-004-1748-3
Sellin A, Kupper P (2005b) Variation in leaf conductance of silver birch: effects of irradiance, vapour pressure deficit, leaf water status and position within a crown. For Ecol Manage 206:153–166. doi:10.1016/j.foreco.2004.10.059
Sellin A, Kupper P (2007) Effects of enhanced hydraulic supply for foliage on stomatal responses in little-leaf linden (Tilia cordata Mill.). Eur J For Res 126:241–251. doi:10.1007/s10342-006-0140-8
Sellin A, Lubenets K (2010) Variation of transpiration within a canopy of silver birch: effect of canopy position and daily versus nightly water loss. Ecohydrology 3:467–477. doi:10.1002/eco.133
Sellin A, Õunapuu E, Kupper P (2008) Effects of light intensity and duration on leaf hydraulic conductance and distribution of resistance in shoots of silver birch (Betula pendula). Physiol Plant 134:412–420. doi:10.1111/j.1399-3054.2008.01142.x
Sellin A, Eensalu E, Niglas A (2010a) Is distribution of hydraulic constraints within tree crowns reflected in photosynthetic water-use efficiency? An example of Betula pendula. Ecol Res 25:173–183. doi:10.1007/s11284-009-0641-2
Sellin A, Õunapuu E, Karusion A (2010b) Experimental evidence supporting the concept of light-mediated modulation of stem hydraulic conductance. Tree Physiol 30:1528–1535. doi:10.1093/treephys/tpq091
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 Environ 34:1079–1087. doi:10.1111/j.1365-3040.2011.02306.x
Sellin A, Õunapuu E, Kaurilind E, Alber M (2012) Size-dependent variability of leaf and shoot hydraulic conductance in silver birch. Trees 26:821–831. doi:10.1007/s00468-011-0656-5
Sellin A, Tullus A, Niglas A, Õunapuu E, Karusion A, Lõhmus K (2013) Humidity-driven changes in growth rate, photosynthetic capacity, hydraulic properties and other functional traits in silver birch (Betula pendula). Ecol Res 28:523–535. doi:10.1007/s11284-013-1041-1
Simmons AJ, Willett KM, Jones PD, Thorne PW, Dee DP (2010) Low-frequency variations in surface atmospheric humidity, temperature, and precipitation: inferences from reanalyses and monthly gridded observational data sets. J Geophys Res 115:D01110. doi:10.1029/2009JD012442
Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Tullus A, Kupper P, Sellin A, Parts L, Sõber J, Tullus T, Lõhmus K, Sõber A, Tullus H (2012) Climate change at northern latitudes: rising atmospheric humidity decreases transpiration, N-uptake and growth rate of hybrid aspen. PLoS ONE 7:e42648. doi:10.1371/journal.pone.0042648
Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot 23:267–282. doi:10.1093/jxb/23.1.267
Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R (1999) Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiol 120:11–21. doi:10.1104/pp.120.1.11
Tyree MT, 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? J Exp Bot 56:737–744. doi:10.1093/jxb/eri045
van Doorn WG, Hiemstra T, Fanourakis D (2011) Hydrogel regulation of xylem water flow: an alternative hypothesis. Plant Physiol 157:1642–1649. doi:10.1104/pp.111.185314
Voicu MC, Zwiazek JJ (2011) Diurnal and seasonal changes of leaf lamina hydraulic conductance in bur oak (Quercus macrocarpa) and trembling aspen (Populus tremuloides). Trees 25:485–495. doi:10.1007/s00468-010-0524-8
Voicu MC, Zwiazek JJ, Tyree MT (2008) Light response of hydraulic conductance in bur oak (Quercus macrocarpa) leaves. Tree Physiol 28:1007–1015. doi:10.1093/treephys/28.7.1007
Zhang G, Leclerc MY, Karipot A (2010) Local flux-profile relationships of wind speed and temperature in a canopy layer in atmospheric stable conditions. Biogeoscience 7:3625–3636. doi:10.5194/bgd-7-4505-2010
Zhang Y, Equiza MA, Zheng Q, Tyree MT (2011) The impact of long-term water stress on relative growth rate and morphology of needles and shoots of Metasequoia glyptostroboides seedlings: research toward identifying mechanistic models. Physiol Plant 143:10–20. doi:10.1111/j.1399-3054.2011.01482.x
Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062. doi:10.1126/science.1057175
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The study was financed by the Estonian Ministry of Science and Education (target-financed themes no. 0170021s08, 0182734s06 and SF0180025s12), by the Estonian Science Foundation (Grants No. 6969, 7736, 8719 and 9186) and by the Academy of Finland (Project No. 1252548).
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Aasamaa, K., Kõivik, K., Kupper, P. et al. Growth environment determines light sensitivity of shoot hydraulic conductance. Ecol Res 29, 143–151 (2014). https://doi.org/10.1007/s11284-013-1104-3
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DOI: https://doi.org/10.1007/s11284-013-1104-3