{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,16]],"date-time":"2026-02-16T17:03:05Z","timestamp":1771261385102,"version":"3.50.1"},"reference-count":55,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2019,8,2]],"date-time":"2019-08-02T00:00:00Z","timestamp":1564704000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Chaonian Feng","award":["164010104"],"award-info":[{"award-number":["164010104"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Symmetry"],"abstract":"<jats:p>Leaf shape can reflect the survival and development of plants in different environments. In particular, leaf area, showing a scaling relationship with other leaf-shape indices, has been used to evaluate the extent of salt stress on plants. Based on the scaling relationships between leaf area and other leaf-shape indices in experiments at different levels of salt stress, we could examine which leaf-shape indices are also related to salt stress. In the present study, we explored the effects of different salt concentration treatments on leaf dry mass per unit area (LMA), the quotient of leaf perimeter and leaf area (QPA), the quotient of leaf width and length (QWL), the areal quotient (AQ) of left and right sides of a leaf and the standardized index (SI) for bilateral symmetry. We treated Pyrus betulifolia Bunge under NaCl salt solution of 2\u2030, 4\u2030 and 6\u2030, respectively, with fresh water with no salt as the control. The reduced major axis (RMA) was used to fit a linear relationship of the log-transformed data between any leaf trait measures and leaf area. We found that leaf fresh weight and dry weight decrease with salt concentration increasing, whereas the exponents of leaf dry weight versus leaf area exhibit an increasing trend, which implies that the leaves expanding in higher salt environments are prone to have a higher cost of dry mass investment to increase per unit leaf area than those in lower salt environments. Salt concentration has a significant influence on leaf shape especially QWL, and QWL under 6\u2030 concentration treatment is significantly greater than the other treatments. However, there is no a single increasing or decreasing trend for the extent of leaf bilateral symmetry with salt concentration increasing. In addition, we found that the scaling exponents of QPA versus leaf area for four treatments have no significant difference. It indicates that the scaling relationship of leaf perimeter versus leaf area did not change with salt concentration increasing. The present study suggests that salt stress can change leaf functional traits especially the scaling relationship of leaf dry weight versus leaf area and QWL, however, it does not significantly affect the scaling relationships between leaf morphological measures (including QPA and the extent of leaf bilateral symmetry) and leaf area.<\/jats:p>","DOI":"10.3390\/sym11080991","type":"journal-article","created":{"date-parts":[[2019,8,2]],"date-time":"2019-08-02T11:58:16Z","timestamp":1564747096000},"page":"991","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Effects of Salt Stress on the Leaf Shape and Scaling of Pyrus betulifolia Bunge"],"prefix":"10.3390","volume":"11","author":[{"given":"Xiaojing","family":"Yu","sequence":"first","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4696-0130","authenticated-orcid":false,"given":"Peijian","family":"Shi","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cang","family":"Hui","sequence":"additional","affiliation":[{"name":"Centre for Invasion Biology, Department of Mathematical Sciences, Stellenbosch University, Matieland 7602, South Africa"},{"name":"Mathematical and Physical Biosciences, African Institute for Mathematical Sciences, Cape Town 7945, South Africa"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lifei","family":"Miao","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Changlai","family":"Liu","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qiuyue","family":"Zhang","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chaonian","family":"Feng","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,8,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1146\/annurev.arplant.59.032607.092911","article-title":"Mechanisms of salinity tolerance","volume":"59","author":"Munns","year":"2008","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_2","unstructured":"Ghassemi, F., Jakeman, A.J., and Nix, H.A. (1995). Salinisation of Land and Water Resources: Human Causes, Extent, Management and Case Studies, University of New South Wales Press Ltd."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/S1360-1385(00)01838-0","article-title":"Plant salt tolerance","volume":"6","author":"Zhu","year":"2001","journal-title":"Trends Plant Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00425-003-1105-5","article-title":"Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance","volume":"218","author":"Wang","year":"2003","journal-title":"Planta"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1126\/science.218.4571.443","article-title":"Plant productivity and environment","volume":"218","author":"Boyer","year":"1982","journal-title":"Science"},{"key":"ref_6","unstructured":"Gruissem, W., Buchannan, B., and Jones, R. (2000). Responses to Abiotic Stresses. Biochemistry and Molecular Biology of Plants, American Society of Plant Physiologists."},{"key":"ref_7","unstructured":"Zhao, K.F., Li, F.C., and Zhang, F.S. (2013). Halophytes in China, Science Press."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1093\/jxb\/erh003","article-title":"Improving crop salt tolerance","volume":"55","author":"Flowers","year":"2004","journal-title":"J. Exp. Bot."},{"key":"ref_9","unstructured":"Zhao, K.F., and Fan, H. (2005). Saline Plants and Their Adaptive Physiology to Saline Habitats, Science Press."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1046\/j.1439-037X.2002.00537.x","article-title":"Effect of salinity stress on growth and nutrient composition of three soybean (Glycine max L. Merrill) cultivars","volume":"188","author":"Essa","year":"2002","journal-title":"J. Agron. Crop Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1007\/s11738-006-0037-7","article-title":"Changes in peroxidase activities and soluble proteins in strawberry varieties under salt-stress","volume":"28","author":"Gulen","year":"2006","journal-title":"Acta Physiol. Plant"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1023\/A:1023060211546","article-title":"Behaviour of antioxidant defense system in the adaptive response to salt stress in Helianthus annuus L. cells","volume":"40","author":"Davenport","year":"2003","journal-title":"Plant Growth Regul."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1093\/jxb\/erl216","article-title":"Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment","volume":"58","author":"Kim","year":"2007","journal-title":"J. Exp. Bot."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/0168-9452(96)04325-7","article-title":"Differences in the physiological responses of two clones of Eucalyptus microtheca selected for their salt tolerance","volume":"114","author":"Morabito","year":"1996","journal-title":"Plant Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1111\/j.1365-3040.1993.tb00840.x","article-title":"Physiological processes limiting plant growth in saline soils: Some dogmas and hypotheses","volume":"16","author":"Munns","year":"1993","journal-title":"Plant Cell Environ."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1126\/science.aal4760","article-title":"Global climatic drivers of leaf size","volume":"357","author":"Wright","year":"2017","journal-title":"Science"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1007\/s11104-007-9337-y","article-title":"The upscaling of transpiration from individual trees to areal transpiration in tree belts","volume":"297","author":"Crosbie","year":"2007","journal-title":"Plant Soil"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1086\/405156","article-title":"Transpiration and energy exchange","volume":"41","author":"Gates","year":"1966","journal-title":"Q. Rev. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.3732\/ajb.1100106","article-title":"Differences in the scaling of area and mass of Ginkgo biloba (Ginkgoaceae) leaves and their relevance to the study of specific leaf area","volume":"98","author":"Niklas","year":"2011","journal-title":"Am. J. Bot."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"11556","DOI":"10.1007\/s11356-018-1446-z","article-title":"Effect of biochar on growth and ion contents of bean plant under saline condition","volume":"25","author":"Torabian","year":"2018","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/s00442-008-1131-x","article-title":"Leaf size and leaf display of thirty-eight tropical tree species","volume":"158","author":"Poorter","year":"2008","journal-title":"Oecologia"},{"key":"ref_22","first-page":"40","article-title":"Estimation of leaf area in cup plant (Silphium perfoliatum) using different leaf traits","volume":"22","author":"Jucsor","year":"2018","journal-title":"J. Horticul. For. Biotechnol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3897\/phytokeys.113.30330","article-title":"Similarity analysis between species of the genus Quercus L. (Fagaceae) in southern Italy based on the fractal dimension","volume":"113","author":"Musarella","year":"2018","journal-title":"PhytoKeys"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zhang, X., Zhao, W., Luo, H., Chen, L., Peng, J., and Fan, J. (2019). Plant recognition via leaf shape and margin features. Multimed. Tools Appl., in press.","DOI":"10.1007\/s11042-019-07846-0"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"928","DOI":"10.1046\/j.1365-2664.2003.00843.x","article-title":"Monitoring salt stress in grapevines: Are measures of plant trait variability useful?","volume":"40","author":"Sinclair","year":"2003","journal-title":"J. Appl. Ecol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"231","DOI":"10.20870\/oeno-one.2014.48.4.1692","article-title":"Effects of salinity on leaf mineral composition and salt injury symptoms of some Iranian wild grapevine (Vitis vinifera L. ssp. sylvestris) genotypes","volume":"48","author":"Baneh","year":"2014","journal-title":"OENO One"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1071\/FP11057","article-title":"The evolution and functional significance of leaf shape in the angiosperms","volume":"38","author":"Nicotra","year":"2011","journal-title":"Funct. Plant Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2109","DOI":"10.1098\/rspb.2007.0417","article-title":"The scaling of leaf area and mass: The cost of light interception increases with leaf size","volume":"274","author":"Milla","year":"2007","journal-title":"Proc. R. Soc. B"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"8891","DOI":"10.1073\/pnas.0701135104","article-title":"\u2018\u2018Diminishing returns\u2019\u2019 in the scaling of functional leaf traits across and within species groups","volume":"104","author":"Niklas","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1851","DOI":"10.1590\/0001-3765201720170077","article-title":"Leaf area estimation from linear measurements in different ages of Crotalaria juncea plants","volume":"89","author":"Toebe","year":"2017","journal-title":"An. Acad. Bras. Ci\u00eanc."},{"key":"ref_31","unstructured":"Montgomery, E.G. (1911). Correlation studies in corn. Annual Report No. 24, Agricultural Experimental Station."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Shi, P.J., Liu, M.D., Yu, X.J., Gielis, J., and Ratkowsky, D.A. (2019). Proportional relationship between leaf area and the product of leaf length and width of four types of special leaf shapes. Forests, 10.","DOI":"10.3390\/f10020178"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"430","DOI":"10.2134\/agronj1974.00021962006600030027x","article-title":"Length-width method for estimating leaf area of rice","volume":"66","author":"Palaniswamy","year":"1974","journal-title":"Agron. J."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Wang, P., Ratkowsky, D.A., Xiao, X., Yu, X.J., Su, J.L., Zhang, L.F., and Shi, P.J. (2018). Taylor\u2019s power law for leaf bilateral symmetry. Forests, 9.","DOI":"10.3390\/f9080500"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1111\/j.1469-8137.2010.03476.x","article-title":"Structural and hydraulic correlates of heterophylly in Ginkgo biloba","volume":"189","author":"Leigh","year":"2011","journal-title":"New Phytol."},{"key":"ref_36","unstructured":"Bailey, L.H. (1917). Pyrus, Standard Cyclopedia of Horticulture."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1086\/281206","article-title":"Geographical distribution of the genus Pyrus and trends and factors in its evolution","volume":"78","author":"Rubtsov","year":"1944","journal-title":"Am. Nat."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/S0304-4238(99)00141-7","article-title":"Effects of sodium chloride on survival and stem elongation of two Asian pear rootstock seedlings","volume":"85","author":"Okubo","year":"2000","journal-title":"Sci. Hortic."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2503\/jjshs.75.1","article-title":"Selection of dwarfing pear rootstock clones from Pyrus betulaefolia and P. calleryana seedlings","volume":"75","author":"Robbani","year":"2006","journal-title":"J. Jpn. Soc. Hortic. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0304-4238(99)00145-4","article-title":"Growth, flowering and leaf properties of pear cultivars grafted on two Asian pear rootstock seedlings under NaCl irrigation","volume":"85","author":"Okubo","year":"2000","journal-title":"Sci. Hortic."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"47","DOI":"10.2503\/hrj.6.47","article-title":"Enhancement in salt tolerance of Japanese pear by using Pyrus betulaefolia rootstock","volume":"6","author":"Matsumoto","year":"2007","journal-title":"Hortic. Res. (Jpn.)"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2503\/jjshs1.81.1","article-title":"Recent advances in research on Japanese pear rootstocks","volume":"81","author":"Tamura","year":"2012","journal-title":"J. Jpn. Soc. Hortic. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"856","DOI":"10.3389\/fpls.2015.00856","article-title":"Capturing spiral radial growth of conifers using the superellipse to model tree-ring geometric shape","volume":"6","author":"Shi","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Shi, P.J., Ratkowsky, D.A., Li, Y., Zhang, L.F., Lin, S.Y., and Gielis, J. (2018). A general leaf area geometric formula exists for plants: Evidence from the simplified Gielis equation. Forestry, 9.","DOI":"10.3390\/f9110714"},{"key":"ref_45","first-page":"e00666","article-title":"Lamina shape does not correlate with lamina surface area: An analysis based on the simplified Gielis equation","volume":"19","author":"Su","year":"2019","journal-title":"Glob. Ecol. Conserv."},{"key":"ref_46","unstructured":"R Core Team (2015). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: http:\/\/www.R-project.org."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Shi, P.J., Zheng, X., Ratkowsky, D.A., Li, Y., Wang, P., and Cheng, L. (2018). A simple method for measuring the bilateral symmetry of leaves. Symmetry, 10.","DOI":"10.3390\/sym10040118"},{"key":"ref_48","first-page":"81","article-title":"Responses and adaptation of xylem hydraulic conductivity to salt stress in Populus euphratica","volume":"31","author":"Zhou","year":"2015","journal-title":"Chin. J. Plant Ecol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1146\/annurev.pp.31.060180.001053","article-title":"Mechanisms of salt tolerance in non-halophytes","volume":"31","author":"Greenway","year":"1980","journal-title":"Annu. Rev. Plant Physiol."},{"key":"ref_50","first-page":"143","article-title":"Whole-plant responses to salinity","volume":"13","author":"Munns","year":"1986","journal-title":"Aust. J. Plant Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1007\/BF00195744","article-title":"Growth and development of sorghum leaves under conditions of NaCl stress","volume":"191","author":"Bernstein","year":"1993","journal-title":"Planta"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1006\/anbo.1997.0519","article-title":"Crown spread patterns for five deciduous broad-leaved woody species ecological significance of the retention patterns of larger branches","volume":"80","author":"Sumida","year":"1997","journal-title":"Ann. Bot."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1093\/aob\/mcf042","article-title":"Spatial arrangement of branches in relation to slope and neighbourhood competition","volume":"89","author":"Sumida","year":"2002","journal-title":"Ann. Bot."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"27","DOI":"10.2307\/2389648","article-title":"Allometry of saplings and understorey trees of a Panamanian forest","volume":"4","author":"King","year":"1990","journal-title":"Funct. Ecol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/0169-5347(89)90103-1","article-title":"Ecological significance of above-ground architectural patterns in woody plants: A question of cost-benefit relationships","volume":"4","year":"1989","journal-title":"Trends Ecol. Evol."}],"container-title":["Symmetry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-8994\/11\/8\/991\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:12:56Z","timestamp":1760188376000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-8994\/11\/8\/991"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8,2]]},"references-count":55,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2019,8]]}},"alternative-id":["sym11080991"],"URL":"https:\/\/doi.org\/10.3390\/sym11080991","relation":{},"ISSN":["2073-8994"],"issn-type":[{"value":"2073-8994","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,2]]}}}