Abstract
Key message
In urban shrub trees, the species-specific photosynthetic response and water-use properties are related to the xylem anatomy of the petiole.
Abstract
It is becoming essential to select urban tree species based on drought response in warm temperate regions, because water limitation is prone to occur in an urban environment, and furthermore, urban warming along with global warming intensifies drought stress even in relatively humid regions. We focused on leaf photosynthesis, water use efficiency, and leaf water relations as key factors for the evaluation of drought response in urban trees, and compared their responses to drought stress and re-watering (recovery) in five major urban shrub tree species planted in Japan. In addition, species-specific xylem anatomical traits in the leaf petiole were evaluated. The five species showed diverse responses to drought and recovery. Rhaphiolepis umbellata possessed both the highest photosynthesis (A) and highest intrinsic water use efficiency (A/gs) under drought, as well as full recovery in the midday leaf water potential (Ψmid). These results suggest that R. umbellata is the most favorable species as an urban tree among the five species. In contrast, A and A/gs in Rhododendron obtusum were only 19% and 55%, respectively, of those in R. umbellata under drought, along with incomplete recovery in Ψmid. The responses of A, A/gs, and Ψmid for the other three species were intermediate between R. umbellata and R. obtusum. We found that during recovery, the species-specific coordination between photosynthesis and leaf hydraulic traits was mediated by stomatal regulation. The species with large stomatal conductance had both high photosynthesis and high leaf hydraulic conductance, along with a large vessel area in the leaf petiole. The selection of trees with consideration of the drought response, along with appropriate watering management, will improve the photosynthetic ability, and thus, will enhance CO2 absorption by urban trees.
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References
Aasamaa K, Sõber 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. https://doi.org/10.1071/pp00157
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898. https://doi.org/10.1104/pp.107.101352
Carriquí M, Cabrera HM, Conesa M, Coopman RE, Douthe C, Gago J, Gallé A, Galmés J, Ribas-Carbo M, Tomás M, Flexas J (2015) Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study. Plant Cell Environ 38:448–460. https://doi.org/10.1111/pce.12402
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol 193:713–720. https://doi.org/10.1111/j.1469-8137.2011.03984.x
Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol. https://doi.org/10.1093/treephys/6.4.393
Delzon S (2015) New insight into leaf drought tolerance. Funct Ecol 29:1247–1249. https://doi.org/10.1111/1365-2435.12500
Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ 27:137–153. https://doi.org/10.1111/j.1365-3040.2004.01140.x
Ethier GJ, Livingston NJ, Harrison DL, Black TA, Moran JA (2006) Low stomatal and internal conductance to CO2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves. Plant Cell Environ 29:2168–2184. https://doi.org/10.1111/j.1365-3040.2006.01590.x
Fini A, Ferrini F, Frangi P, Amoroso G, Piatti R (2009) Withholding irrigation during the establishment phase affected growth and physiology of norway maple (Acer platanoides) and linden (tilia spp.). Arboric Urban For 35:241–251
Flexas J, Scoffoni C, Gago J, Sack L (2013) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. J Exp Bot 64:3965–3981. https://doi.org/10.1093/jxb/ert319
Flexas J, Díaz-Espejo A, Conesa MA, Coopman RE, Douthe C, Gago J, Gallé A, Galmés J, Medrano H, Ribas-Carbo M, Tomàs M, Niinemets Ü (2016) Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant Cell Environ 39:965–982. https://doi.org/10.1111/pce.12622
Gilbert ME, Zwieniecki MA, Holbrook NM (2011) Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. J Exp Bot 62:2875–2887. https://doi.org/10.1093/jxb/erq461
Hochberg U, Degu A, Gendler T, Fait A, Rachmilevitch S (2015) The variability in the xylem architecture of grapevine petiole and its contribution to hydraulic differences. Funct Plant Biol 42:357. https://doi.org/10.1071/FP14167
Holloway-Phillips MM, Brodribb TJ (2011) Contrasting hydraulic regulation in closely related forage grasses: implications for plant water use. Funct Plant Biol 38:594–605. https://doi.org/10.1071/FP11029
Jacobsen AL, Brandon Pratt R, Venturas MD, Hacke UG (2019) Large volume vessels are vulnerable to water-stress-induced embolism in stems of poplar. IAWA J 40:4–22. https://doi.org/10.1163/22941932-40190233
Kagotani Y, Fujino K, Kazama T, Hanba YT (2013) Leaf carbon isotope ratio and water use efficiency of urban roadside trees in summer in Kyoto city. Ecol Res 28:725–734. https://doi.org/10.1007/s11284-013-1056-7
Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transplant 48:452–458. https://doi.org/10.1038/bmt.2012.244
Kannenberg SA, Novick KA, Phillips RP (2019) Anisohydric behavior linked to persistent hydraulic damage and delayed drought recovery across seven North American tree species. New Phytol 222:1862–1872. https://doi.org/10.1111/nph.15699
Kataoka K, Matsumoto F, Ichinose T, Taniguchi M (2009) Urban warming trends in several large Asian cities over the last 100 years. Sci Total Environ 407:3112–3119. https://doi.org/10.1016/j.scitotenv.2008.09.015
Kiyomizu T, Yamagishi S, Kume A, Hanba YT (2019) Contrasting photosynthetic responses to ambient air pollution between the urban shrub Rhododendron × pulchrum and urban tall tree Ginkgo biloba in Kyoto city: stomatal and leaf mesophyll morpho-anatomies are key traits. Trees 33:63–77. https://doi.org/10.1007/s00468-018-1759-z
Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct Ecol 28:1313–1320. https://doi.org/10.1111/1365-2435.12289
Klein T, Zeppel MJB, Anderegg WRL, Bloemen J, De Kauwe MG, Hudson P, Ruehr NK, Powell TL, von Arx G, Nardini A (2018) Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs. Ecol Res 33:839–855. https://doi.org/10.1007/s11284-018-1588-y
Kogami H, Kogami H, Hanba YT, Hanba YT, Kibe T, Kibe T, Terashima I, Terashima I, Masuzawa T, Masuzawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant Cell Environ 24:529–538. https://doi.org/10.1046/j.1365-3040.2001.00696.x
Markesteijn L, Poorter L, Paz H, Sack L, Bongers F (2011) Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits. Plant Cell Environ 34:137–148. https://doi.org/10.1111/j.1365-3040.2010.02231.x
McCarthy MP, Best MJ, Betts RA (2010) Climate change in cities due to global warming and urban effects. Geophys Res Lett 37:1–5. https://doi.org/10.1029/2010GL042845
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytol 178:719–739. https://doi.org/10.1111/j.1469-8137.2008.02436.x
Medrano H, Flexas J, Galmés J (2009) Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms. Plant Soil 317:17–29. https://doi.org/10.1007/s11104-008-9785-z
Meineke EK, Frank SD (2018) Water availability drives urban tree growth responses to herbivory and warming. J Appl Ecol 55:1701–1713. https://doi.org/10.1111/1365-2664.13130
Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Le Thiec D, Bréchet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides x Populus nigra. New Phytol 169:765–777. https://doi.org/10.1111/j.1469-8137.2005.01630.x
Osone Y, Kawarasaki S, Ishida A, Kikuchi S, Shimizu A, Yazaki K, Aikawa S, Yamaguchi M, Izuta T, Matsumoto GI (2014) Responses of gas-exchange rates and water relations to annual fluctuations of weather in three species of urban street trees. Tree Physiol 34:1056–1068. https://doi.org/10.1093/treephys/tpu086
Peguero-Pina JJ, Sancho-Knapik D, Flexas J, Galmés J, Niinemets Ü, Gil-Pelegrín E (2016) Light acclimation of photosynthesis in two closely related firs (Abies pinsapo Boiss. and Abies alba Mill.): the role of leaf anatomy and mesophyll conductance to CO2. Tree Physiol 36:300–310. https://doi.org/10.1093/treephys/tpv114
Percival GC, Keary IP, AL-Habsi S (2006) An assessment of the drought tolerance of Fraxinus genotypes for urban landscape plantings. Urban For Urban Green 5:17–27. https://doi.org/10.1016/j.ufug.2006.03.002
Reddy KS, Sekhar KM, Reddy AR (2017) Genotypic variation in tolerance to drought stress is highly coordinated with hydraulic conductivity-photosynthesis interplay and aquaporin expression in field-grown mulberry (Morus spp.). Tree Physiol 37:926–937. https://doi.org/10.1093/treephys/tpx051
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Shelden MC, Vandeleur R, Kaiser BN, Tyerman SD (2017) A comparison of petiole hydraulics and aquaporin expression in an anisohydric and isohydric cultivar of grapevine in response to water-stress induced cavitation. Front Plant Sci 8:1–17. https://doi.org/10.3389/fpls.2017.01893
Sun Y, Zhang X, Ren G, Zwiers FW, Hu T (2016) Contribution of urbanization to warming in China. Nat Clim Change 6:706–709. https://doi.org/10.1038/nclimate2956
Tamaoki D, Karahara I, Schreiber L, Wakasugi T, Yamada K, Kamisaka S (2006) Effects of hypergravity conditions on elongation growth and lignin formation in the inflorescence stem of Arabidopsis thaliana. J Plant Res 119:79–84. https://doi.org/10.1007/s10265-005-0243-1
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432. https://doi.org/10.1093/jxb/49.Special_Issue.419
Tayasu I, Hirasawa R, Ogawa NO, Ohkouchi N, Yamada K (2011) New organic reference materials for carbon- and nitrogen-stable isotope ratio measurements provided by Center for Ecological Research, Kyoto University, and Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology. Limnology 12:261–266. https://doi.org/10.1007/s10201-011-0345-5
Terashima I, Hanba YT, Tholen D, Niinemets Ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116. https://doi.org/10.1104/pp.110.165472
Tomás M, Medrano H, Brugnoli E, Escalona JM, Martorell S, Pou A, Ribas-Carbó M, Flexas J (2014) Variability of mesophyll conductance in grapevine cultivars under water stress conditions in relation to leaf anatomy and water use efficiency. Aust J Grape Wine Res 20:272–280. https://doi.org/10.1111/ajgw.12069
Tosens T, Nishida K, Gago J, Coopman RE, Cabrera M, Carriquí M, Laanisto L, Morales L, Nadal M, Rojas R, Talts E, Tomas M, Hanba Y, Niinemets Ü, Flexas J (2016) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol 209:1576–1590. https://doi.org/10.1111/nph.13719
Tsuji S, Nakashizuka T, Kuraji K, Kume A, Hanba YT (2020) Sensitivity of stomatal conductance to vapor pressure deficit and its dependence on leaf water relations and wood anatomy in nine canopy tree species in a Malaysian wet tropical rainforest. Trees Struct Funct. https://doi.org/10.1007/s00468-020-01998-5
Wang XM, Wang XK, Su YB, Zhang HX (2019) Land pavement depresses photosynthesis in urban trees especially under drought stress. Sci Total Environ 653:120–130. https://doi.org/10.1016/j.scitotenv.2018.10.281
Warren CR (2008) water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not. J Exp Bot 31:1–8. https://doi.org/10.1093/jxb/erm314
Weissert LF, Salmond JA, Schwendenmann L (2017) Photosynthetic CO2 uptake and carbon sequestration potential of deciduous and evergreen tree species in an urban environment. Urban Ecosyst. https://doi.org/10.1007/s11252-016-0627-0
Xiong D, Flexas J, Yu T, Peng S, Huang J (2017) Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytol 213:572–583. https://doi.org/10.1111/nph.14186
Zanne AE, Westoby M, Falster DS, Ackerly DD, Loarie SR, Arnold SEJ, Coomes DA (2010) Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity. Am J Bot 97:207–215. https://doi.org/10.3732/ajb.0900178
Acknowledgements
This work was supported by a Grant-in-Aid for Scientific Research (15K00566, 19H04281), the Sumitomo Foundation (103230), Adaptable & Seamless Technology Transfer Program through Target-driven R&D (AS262Z01258N). The leaf stable carbon isotope ratio was measured at the Research Institute for Humanity and Nature. We appreciate Dr. Ichiro Tayasu and Riyo Hirasawa for supporting the isotope measurements.
Funding
This work was supported by a Grant-in-Aid for Scientific Research (15K00566, 19H04281), the Sumitomo Foundation (103230), Adaptable & Seamless Technology Transfer Program through Target-driven R&D (AS262Z01258N).
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Fig. S1 Correlation matrix among the variables, obtained under pre-drought, drought and recovery conditions. Mean values for each species were used for the analysis (n = 5). Values indicate Pearson's correlation coefficients, where each cell is colorized based on the values of the coefficients. Fig. S2 Effect of the three conditions, pre-drought, drought, and recovery, on the gas exchange and leaf traits used for the principal component analysis in Fig. 5. The principal component scores for the drought and re-water conditions were re-calculated using the normalized values and factor loadings of the pre-drought condition. The species are Forsythia suspensa (Fsus), Rhaphiolepis umbellata (Rumb), Camellia hiemalis (Chie), Rhododendoron pulchrum (Rpul), and Rhododendoron obtusum (Robt).Supplementary file1 (PDF 169 KB)
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Horike, H., Kinoshita, T., Kume, A. et al. Responses of leaf photosynthetic traits, water use efficiency, and water relations in five urban shrub tree species under drought stress and recovery. Trees 37, 53–67 (2023). https://doi.org/10.1007/s00468-021-02083-1
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DOI: https://doi.org/10.1007/s00468-021-02083-1