The use of physiological, biochemical and morpho-anatomical traits in tree breeding for improved water-use efficiency of Quercus robur L.
Aim of study: In the present paper the nature and level of co-dependence between leaf functional traits and intrinsic water-use efficiency (WUEi) were studied in one-year-old Quercus robur L. seedlings, grown in a common garden experiment under moderate drought conditions. The study was established to identify those traits that might potentially be utilized to improve leaf-level WUEi, and therefore be used in breeding programmes to enhance drought adaptation of Q. robur.
Area of study: The study was carried out at the common garden site within the UNESCO Biosphere Reserve Mura-Drava-Danube.
Material and methods: The study involved one-year-old seedlings of eight half-sib lines of Q. robur. Eighteen leaf parameters were analyzed; i.e. physiological, biochemical, morphological and anatomical. The data were processed using multivariate statistical methods: a) principal component analysis, b) stepwise regression analysis, and c) path coefficient analysis.
Main results: The results showed that leaf stomata traits, particularly stomatal density (SD), and leaf dry mass per unit leaf area (LMA) were the most important traits, closely associated with WUEi. Stomatal density achieved the highest score on PC1 (0.825), in which WUEi had the highest loading (0.920), as well. SD was also included first in stepwise regression model.
Research highlights: These results demonstrate that under moderate water stress WUEi in Q. robur half-sib lines were mainly the result of the plants’ structural acclimation to surrounding environmental conditions.
Keywords: Quercus robur L.; half-sib line; intrinsic water-use efficiency; leaf functional traits.
Aasamaa K, Sober A, Rahi M, 2001. Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Aust J Plant Physiol 28(8): 765-774. https://doi.org/10.1071/PP00157
Andersson M, Milberg P, Bergman K, 2011. Low pre-death growth rates of oak (Quercus robur L.) - Is oak death a long-term process induced by dry years?. Ann For Sci 68(1): 159-168. https://doi.org/10.1007/s13595-011-0017-y
Arnao MB, 2000. Some methodological problems in the determination of antioxidant activity using chromogen radicals: A practical case. Trends Food Sci Tech 11(11): 419-421. https://doi.org/10.1016/S0924-2244(01)00027-9
Avramova V, Abdelgawad H, Vasileva I, Petrova AS, Holek A, Mariën J, Asard H Beemster GTS, 2017. High antioxidant activity facilitates maintenance of cell division in leaves of drought tolerant maize hybrids. Front Plant Sci 8: 84. https://doi.org/10.3389/fpls.2017.00084
Bayramzadeh V, Funada R, Kubo T, 2008. Relationships between vessel element anatomy and physiological as well as morphological traits of leaves in Fagus crenata seedlings originating from different provenances. Trees-Struct Funct 22(2): 217-224. https://doi.org/10.1007/s00468-007-0178-3
Benzie IFF, Strain JJ, 1996. The ferric reducing ability of plasma as a measure of "antioxidant power": the FRAP assay. Anal Biochem 239(1): 70-76. https://doi.org/10.1006/abio.1996.0292
Bojović M, Nikolić N, Borišev M, Pajević S, Horák R, Pavlović L, Vaštag E, 2017. The effect of drought stress and recovery on pedunculate oak populations grown in semi-controlled conditions. Topola 199/200: 193-207.
Bradford MM, 1976. A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2): 248-254. https://doi.org/10.1006/abio.1976.9999
Brendel O, Le Thiec D, Scotti-Saintagne C, Bodénès C, Kremer A, Guehl J-M, 2008. Quantitative trait loci controlling water use efficiency and related traits in Quercus robur L. Tree Genet Genomes 4(2): 263-278. https://doi.org/10.1007/s11295-007-0107-z
Bresson CC, Vitasse Y, Kremer A, Delzon S, 2011. To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiol 31(11): 1164-1174. https://doi.org/10.1093/treephys/tpr084
Čater M, Batič F, 2006. Groundwater and light conditions as factors in the survival of pedunculate oak (Quercus robur L.) seedlings. Eur J For Res 125(4): 419-426. https://doi.org/10.1007/s10342-006-0134-6
Čater, 2015. A 20-year overview of Quercus robur L. mortality and crown conditions in Slovenia. Forests 6(3): 581-593. https://doi.org/10.3390/f6030581
Cerovic ZG, Masdoumier G, Ben Ghozlen N, Latouche G, 2012. A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids. Physiol Plant 146(3): 251-260. https://doi.org/10.1111/j.1399-3054.2012.01639.x
Chang C, Yang M, Wen H, Chern J, 2002. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10(3): 178-182
Chaves MM, Maroco JP, Pereira JS, 2003. Understanding plant responses to drought - from genes to the whole plant. Funct Plant Biol 30: 239-264. https://doi.org/10.1071/FP02076
Cochard H, Bréda N, Granier A, Aussenac G, 1992. Vulnerability to air embolism of three European oak species (Quercus petraea (Matt) Liebl, Q pubescens Willd, Q robur L). Ann For Sci 49(3): 225-233. https://doi.org/10.1051/forest:19920302
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD, 2004. Breeding for high water-use efficiency. J Exp Bot 55(407): 2447-2460. https://doi.org/10.1093/jxb/erh277
de Almeida Silva M, dos Santos CM, Labate CA, Guidetti-Gonzalez S, de Santana Borges J, Cesar Ferreira L, DeLima RO, Fritsche-Neto R, 2012. Breeding for water use efficiency. In: Plant breeding for abiotic stress tolerance; Fritsche-Neto R, Borém A (eds). pp: 87-102. Springer-Verlag, Berlin, Germany. https://doi.org/10.1007/978-3-642-30553-5_6
Dewey DR, Lu KH, 1959. A correlation and path analysis of components of crested wheatgrass seed production. Agron J 51(9): 515-518. https://doi.org/10.2134/agronj1959.00021962005100090002x
Dow GJ, Bergmann DC, Berry JA, 2014. An integrated model of stomatal development and leaf physiology. New Phytol 201(4): 1218-1226. https://doi.org/10.1111/nph.12608
Drobyshev I, Linderson H, Sonesson K, 2007. Temporal mortality pattern of pedunculate oaks in southern Sweden. Dendrochronologia 24(2-3): 97-108. https://doi.org/10.1016/j.dendro.2006.10.004
Fang Y, Xiong L, 2015. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72(4): 673-689. https://doi.org/10.1007/s00018-014-1767-0
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA, 2009. Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29(1): 185-212. https://doi.org/10.1051/agro:2008021
Flexas J, Medrano H, 2002. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89(2): 183-189. https://doi.org/10.1093/aob/mcf027
Flexas J, Niinemets U, Galle A, Barbour MM, Centritto M, Diaz-Espejo A, Douthe C, Galmes J, Ribas-Carbo M, Rodriguez PL, et al., 2013. Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117(1-3): 45-59. https://doi.org/10.1007/s11120-013-9844-z
Franks P, Farquhar G, 2007. The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol 143(1): 78-87. https://doi.org/10.1104/pp.106.089367
Gallé A, Feller U, 2007. Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery. Physiol Plant 131(3): 412-421. https://doi.org/10.1111/j.1399-3054.2007.00972.x
Ghasemzadeh A, Jaafar HZE, 2011. Effect of CO2 enrichment on synthesis of some primary and secondary metabolites in ginger (Zingiber officinale Roscoe). Int J Mol Sci 12(2): 1101-1114. https://doi.org/10.3390/ijms12021101
Golparvar AR, Karimi M, 2012. Determination of the best indirect selection criteria for improvement of seed and oil yield in canola cultivars (Brassica napus L.). Bulgarian Journal of Agricultural Science 18(3): 330-333.
Hassiotou F, Renton M, Ludwig M, Evans JR, Veneklaas EJ, 2010. Photosynthesis at an extreme end of the leaf trait spectrum: how does it relate to high leaf dry mass per area and associated structural parameters? J Exp Bot 61(11): 3015-3028. https://doi.org/10.1093/jxb/erq128
Hensley K, Mou S, Pye QN, 2003. Nitrite determination by colorimetric and fluorometric Griess diazotization assays. In: Methods in pharmacology and toxicology: methods in biological oxidative stress; Hensley K, Floyd RA (eds). pp: 185-193. Humana Press Inc., Totowa, NJ, USA.
Hetherington AM, Woodward FI, 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901-906. https://doi.org/10.1038/nature01843
Holland N, Richardson AD, 2009. Stomatal length correlates with elevation of growth in four tem¬perate species. J Sustain For 28(1): 63-73. https://doi.org/10.1080/10549810802626142
Hui Z, ZhengBin Z, HongBo S, Ping X, Foulkes MJ, 2008. Genetic correlation and path analysis of transpiration efficiency for wheat flag leaves. Environ Exp Bot 64(2): 128-134. https://doi.org/10.1016/j.envexpbot.2007.11.001
Ilgin M, Caglar S, 2009. Comparison of leaf stomatal features in some local and foreign apricot (Prunus armeniaca L.) genotypes. Afr J Biotechnol 8(6): 1074-1077.
Jones HG, 1977. Transpiration in barley lines with differing stomatal frequencies. J Exp Bot 28(1): 162-168. https://doi.org/10.1093/jxb/28.1.162
Kardel F, Wuyts K, Babanezhad M, Vitharana UWA, Wuytack T, Potters G, Samson R, 2010. Assessing urban habitat quality based on specific leaf area and stomatal characteristics of Plantago lanceolata L. Environ Pollut 158(3): 788-794. https://doi.org/10.1016/j.envpol.2009.10.006
Kelleher CT, de Vries SMG, Baliuckas V, Bozzano M, Frydl J, Gonzalez Goicoechea P, Ivankovic M, Kandemir G, Koskela J, Kozioł C, et al., 2015. Approaches to the conservation of forest genetic resources in Europe in the context of climate change. European Forest Genetic Resources Programme (EUFORGEN), Bioversity International, Rome, Italy. 46 pp.
Kim D, Jeond S, Lee CY, 2003. Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem 81(3): 321-326. https://doi.org/10.1016/S0308-8146(02)00423-5
Kooyers NJ, 2015. The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci 234: 155-162. https://doi.org/10.1016/j.plantsci.2015.02.012
Kovacevic B, Guzina V, Kraljevic-Balalic M, Ivanovic M, Nikolić-Đorić E, 2008. Evaluation of early rooting traits of eastern cottonwood that are important for selection tests. Silvae Genet 57(1-6): 13-21. https://doi.org/10.1515/sg-2008-0003
Kovačević B, 2014. Variability of leaf morphometric characters in Populus nigra populations in the Danube Basin. In: Variability of European black poplar (Populus nigra L.) in the Danube Basin; Tomović Z, Vasić I (eds). pp: 52-85. Public Enterprise "Vojvodinašume", Novi Sad, Serbia.
Krstić J, Orlović S, Galić Z, Pilipović A, Stojnić S, 2014. Seasonal changes in leaf gas exchange parameters in Platanus acerifolia Willd. and Acer pseudoplatanus L. seedlings on undeveloped alluvial soil (fluvisol). Šumarstvo 1-2: 163-178.
Lawson T, Blatt MR, 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164(4): 1556-1570. https://doi.org/10.1104/pp.114.237107
Li CC, 1975. Path analysis - A primer. Pacific Grove, California. 346 pp.
Liović B, Tomašić Ž, Dubravac T, Licht R, Turk M, 2019. The effect of polypropylene tree shelters on growth and survival of pedunculate oak seedlings (Quercus robur L.). South-east Eur For 10(1): 89-96. https://doi.org/10.15177/seefor.19-07
Lui C, Liu Y, Ke Guo K, Zheng Y, Li G, Yu L, Yang R, 2010. Influence of drought intensity on the response of six woody karst species subjected to successive cycles of drought and rewatering. Physiol Plant 139(1): 39-54. https://doi.org/10.1111/j.1399-3054.2009.01341.x
Mészáros I, Veres S, Kanalas P, Oláha V, Szȍllȍsi E, Sárvári E, Lévai L, Lakatos G, 2007. Leaf growth and photosynthetic performance of two co-existing oak species in contrasting growing seasons. Acta Silv Lign Hung 3: 7-20.
Miller N, Rice-Evans C, 1997. Factors influencing the antioxidant activity determined by the ABTS radical cation assay. Free Radic Res 26(3): 195-199. https://doi.org/10.3109/10715769709097799
Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu J, 2006. Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Letters 580(28-29): 6537-6542. https://doi.org/10.1016/j.febslet.2006.11.002
Muir CD, Conesa MA, Roldan EJ, Arantzazu Molins A., Galmes J, 2017. Weak coordination between leaf structure and function among closely related tomato species. New Phytol 213: 1642-1653. https://doi.org/10.1111/nph.14285
Nahar S, Vemireddy LR, Sahoo L, Tanti B, 2018. Antioxidant protection mechanisms reveal significant response in drought-induced oxidative stress in some traditional rice of Assam, India. Rice Sci 25(4): 185-196. https://doi.org/10.1016/j.rsci.2018.06.002
Niinemets U, 2001. Global‐scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82(2): 453-469. https://doi.org/10.1890/0012-9658(2001)082[0453:GSCCOL]2.0.CO;2
Novriyanti E, Watanabe M, Makoto K, Takeda T, Hashidoko Y, Koike T, 2012. Photosynthetic nitrogen and water use efficiency of acacia and eucalypt seedlings as afforestation species. Photosynthetica 50(2): 273-281. https://doi.org/10.1007/s11099-012-0033-7
Ohsumi A, Kanemura T, Homma K, Horie T, Shiraiwa T, 2007. Genotypic variation of stomatal conductance in relation to stomatal density and length in rice (Oryza sativa L.). Plant Prod Sci 10(3): 322-328. https://doi.org/10.1626/pps.10.322
Pearce DW, Millard S, Bray DF, Rood SB, 2006. Stomatal characteristics of riparian poplar species in a semi-arid environment. Tree Physiol 26(2): 211-218. https://doi.org/10.1093/treephys/26.2.211
Petridis A, Therios I, Samouris G, Koundouras S, Giannakoula A, 2012. Effect of water deficit on leaf phenolic composition, gas exchange, oxidative damage and antioxidant activity of four Greek olive (Olea europaea L.) cultivars. Plant Physiol Bioch 60: 1-11. https://doi.org/10.1016/j.plaphy.2012.07.014
Pita P, Cañas I, Soria F, Ruiz F, Toval G, 2005. Use of physiological traits in tree breeding for improved yield in drought-prone environments. The case of Eucalyptus globulus. Invest Agrar: Sist Recur For 14(3): 383-393. https://doi.org/10.5424/srf/2005143-00931
Popović B, Štajner D, Tumbas-Šaponjac V, Orlović S, 2016. Water stress induces changes in polyphenol profile and antioxidant capacity in poplar plants (Populus spp.). Plant Physiol Biochem 105: 242-250. https://doi.org/10.1016/j.plaphy.2016.04.036
Popović M, Šuštar V, Gričar J, Štraus I, Torkar G, Kraigher H, de Marco A, 2016. Identification of environmental stress biomarkers in seedlings of European beech (Fagus sylvatica) and Scots pine (Pinus sylvestris). Can J For Res 46(1): 58-66. https://doi.org/10.1139/cjfr-2015-0274
Pyakurel A, Wang JR, 2014. Leaf morphological and stomatal variations in paper birch populations along environmental gradients in Canada. Am J Plant Sci 5(11): 1508-1520. https://doi.org/10.4236/ajps.2014.511166
Raftoyannis Y, Radoglou K, Halivopoulos G, 2006. Ecophysiology and survival of Acer pseudoplatanus L. Castanea sativa Miller. and Quercus frainetto Ten. seedlings on a reforestation site in northern Greece. New For 31(2): 151-163. https://doi.org/10.1007/s11056-004-7365-5
R Core Team, 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/
Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ, 2014. Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol 28: 37-45. https://doi.org/10.1111/1365-2435.12162
Reich PB, Walters MB, Ellswort DS, 1992. Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecolog Monogr 62(3): 365-392. https://doi.org/10.2307/2937116
Roussel M, Le Thiec D, Montpied, P, Ningre N, Guehl, J, Brendel O, 2009. Diversity of water use efficiency among Quercus robur genotypes: contribution of related leaf traits. Ann For Sci 66(4): 408. https://doi.org/10.1051/forest/2009010
Sánchez-Gómez D, Robson TM, Gascó A, Gil-Pelegrín E, Aranda I, 2013. Differences in the leaf functional traits of six beech (Fagus sylvatica L.) populations are reflected in their response to water limitation. Environ Exp Bot 87: 110-119. https://doi.org/10.1016/j.envexpbot.2012.09.011
Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Cervilla LM, Blasco B, Rios JJ, Rosales MA, Romero L, Ruiz JM, 2010. Genotypic differences in some physiological parameters symptomatic for oxidative stress under moderate drought in tomato plants. Plant Sci 178: 30-40. https://doi.org/10.1016/j.plantsci.2009.10.001
Schiop ST, Al Hassan M, Sestras AF, Boscaiu M, Sestras RE, Vicente O, 2015. Identification of salt stress biomarkers in romanian carpathian populations of Picea abies (L.) Karst. PLoS ONE 10: e0135419. https://doi.org/10.1371/journal.pone.0135419
Štajner D, Orlović S, Popović MB, Kebert M, Galić Z, 2011. Screening of drought oxidative stress tolerance in Serbian melliferous plant species. Afr J Biotechnol 10(9): 1609-1614.
Štajner D, Orlović S, Popović B, Kebert M, Stojnić S, Klašnja B, 2013. Chemical parameters of oxidative stress adaptability in beech. Journal of Chemistry 2013; doi: 10.1155/2013/592695. https://doi.org/10.1155/2013/592695
Stojanović D, Matović B, Orlović S, Kržič A, Trudić B, Galić Z, Stojnić S, Pekeč S, 2014. Future of the main important forest tree species in Serbia from the climate change perspective. South-east Eur For 5(2): 117-124. https://doi.org/10.15177/seefor.14-16
Stojanović D, Levanič T, Matović B, Orlović S, 2015. Growth decrease and mortality of oak floodplain forests as a response to change of water regime and climate. Eur J For Res 134(3): 555-567. https://doi.org/10.1007/s10342-015-0871-5
Stojnić S, Trudić B, Galović V, Šimunovački Đ, Đorđević B, Rađević V, Orlović S, 2014. Conservation of Pedunculate oak (Quercus robur L.) genetic resources in the Public Enterprise "Vojvodinašume". Topola 193-194: 47-71.
Stojnić S, Orlović S, Živković U, von Wuehlisch G, Miljković D, 2015a. Phenotypic plasticity of European beech (Fagus sylvatica L.) stomatal features under water deficit assessed in provenance trial. Dendrobiology 73: 163-173. https://doi.org/10.12657/denbio.073.017
Stojnić S, Orlović S, Miljković D, Galić Z, Kebert M, von Wuehlisch G, 2015b. Provenance plasticity of European beech leaf traits under differing environmental conditions at two Serbian common garden sites. Eur J For Res 134(6): 1109-1125. https://doi.org/10.1007/s10342-015-0914-y
Stojnić S, Pekeč S, Kebert M, Pilipović A, Stojanović D, Stojanović M, Orlović S, 2016. Drought effects on physiology and biochemistry of pedunculate oak (Quercus robur L.) and hornbeam (Carpinus betulus L.) saplings grown in urban area of Novi Sad, Serbia. South-east Eur For 7(1): 57-63. https://doi.org/10.15177/seefor.16-03
Thomas FM, Blank R, Hartmann G, 2002. Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. For Path 32 (4-5): 277-307. https://doi.org/10.1046/j.1439-0329.2002.00291.x
Thurstone LL, 1969. Multiple-factor analysis. 8th impression. University of Chicago Press, Chicago, USA. 535 pp.
TIBCO Software Inc, 2017. Statistica (data analysis software system), version 13. URL: http://statistica.io
Topić M, Borišev M, Župunski M, Tomičić M, Nikolić N, Pajević S, Krstić B, Pilipović A, 2012. Recovery responses of photosynthesis, transpiration, and WUE in black poplar clones following water deficits. Topola 189-190: 29-38.
Verryn SD, 2008. Breeding for wood quality - a perspective for the future. New Zeal J For Sci 38(1): 5-13.
Wonnacott TH, Wonnacott RJ, 1981. Regression: a second course in statistics. John Wiley & Sons. 556 pp.
Wu X, Bao W, 2012. Statistical analysis of leaf water use efficiency and physiology traits of winter wheat under drought condition. J Integr Agr 11(1): 82-89. https://doi.org/10.1016/S1671-2927(12)60785-8
Yul Yoo C, Pence HE, Hasegawa PM, Mickelbart MV, 2009. Regulation of transpiration to improve crop water use. Crit Rev Plant Sci 28: 410-431. https://doi.org/10.1080/07352680903173175
© INIA. Manuscripts published are the property of the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, and quoting this source is a requirement for any partial or full reproduction.
Forest Systems is an Open Access Journal. All articles are distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the license CC-by must be expressly stated in this way when necessary.