Teasing out elevational trends in infraspecific Prunus taxa: A vein analysis approach.
Prunus microcarpa
leaf dimorphism
leaf venation
plant adaptation
protocol
Journal
Microscopy research and technique
ISSN: 1097-0029
Titre abrégé: Microsc Res Tech
Pays: United States
ID NLM: 9203012
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
05
01
2023
accepted:
16
08
2023
medline:
16
11
2023
pubmed:
29
8
2023
entrez:
29
8
2023
Statut:
ppublish
Résumé
Using 33 specimens collected from across their range in Turkey, we demonstrate that the subspecies of Prunus microcarpa C.A.Mey react very differently to altitude. We first outline a simplified, flexible protocol for sectioning and removing the epidermis of small, difficult-to-image leaves for leaf vein studies. We then used venation analysis software to evaluate the two subspecies of this wild cherry in relation to altitude. We also found key differences in venation features between short-shoot and long-shoot leaves for each taxon. Differences include statistically significant negative correlation between vein density, and positive correlation between areole area and altitude in long-shoot leaves of Prunus microcarpa subsp. microcarpa, while its short-shoot leaves had a positive relationship between maximum areole area, and negative relationship between vein density, numbers of veins and endpoints. Meanwhile, P. microcarpa subsp. tortuosa (Boiss. & Hausskn.) Browicz recorded trends that were largely opposite of this, but beside vein thickness and areole area, were not statistically significant. This difference may be part of each taxon's overarching syndrome of anatomical and morphological adaptations to its external environment. RESEARCH HIGHLIGHTS: Features of vein density and thickness fell, while areole area and vein length rose with altitude in P. microcarpa. P. microcarpa subsp. tortuosa showed opposite trends, but reacted less strongly to altitude. Short-shoot and long-shoot have significantly different venation parameters. Using sections proportionate to leaf size is useful to compare venation of leaves that vary due to dimorphism. We discuss protocol strategies for imaging of difficult leaves for venation analyses.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1699-1711Subventions
Organisme : Istanbul University Scientific Projects Division
ID : FYL-2021-37622
Organisme : Scientific and Technological Research Institution of Turkey
ID : 116Z247
Informations de copyright
© 2023 The Authors. Microscopy Research and Technique published by Wiley Periodicals LLC.
Références
Ashby, E. (1948). Studies in the morphogenesis of leaves. I. An essay on leaf shape. The New Phytologist, 47(2), 153-176.
Boissier, E. (1867). Flora Orientalis: Sive, Enumeratio plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatarum. H. Georg. https://doi.org/10.5962/bhl.title.20323
Bostanci Ordu, P. İ., Çiftçi, A., Mollman, R., Yazıcı, C., Abudurusuli, A., Şık, L., & Erol, O. (2021). Foliar anatomy of some Prunus L. subgen. Cerasus Mill. (Rosaceae) taxa. Nordic Journal of Botany, 39(6), 1-12. https://doi.org/10.1111/njb.03185
Brodribb, T. J., Feild, T. S., & Sack, L. (2010). Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology, 37(6), 488-498.
Browicz, K. (1972). The genus Cerasus Duhamel. In P. H. Davis (Ed.), Flora of Turkey and East Aegean Islands (Vol. 4). Cambridge University Press.
Bühler, J., Rishmawi, L., Pflugfelder, D., Huber, G., Scharr, H., Hülskamp, M., Koornneef, M., Schurr, U., & Jahnke, S. (2015). phenoVein-A tool for leaf vein segmentation and analysis. Plant Physiology, 169(4), 2359-2370. https://doi.org/10.1104/pp.15.00974
Çiftçi, A., Gerçek, Y. C., Mollman, R., Bostancı Ordu, P., Yazıcı, C., Yaprak, A. E., Morgil, H., Şık, L., & Erol, O. (2022). Towards a better understanding of Prunus L.: Molecular and morphological notes on subgenus Cerasus (Mill.) Focke in Turkey. Botanical Journal of the Linnean Society, 202, 346-362. https://doi.org/10.1093/botlinnean/boac080
Costes, E., Crespel, L., Denoyes, B., Morel, P., Demene, M. N., Lauri, P. E., & Wenden, B. (2014). Bud structure, position and fate generate various branching patterns along shoots of closely related Rosaceae species: A review. Frontiers in Plant Science, 5, 666. https://doi.org/10.3389/fpls.2014.00666
Diego, B., & De Bacco, C. (2021). Principled network extraction from images. Royal Society Open Science, 8(7), 8210025210025. https://doi.org/10.1098/rsos.210025
Dirnberger, M., Kehl, T., & Neumann, A. (2015). NEFI: Network extraction from images. Scientific Reports, 5(1), 1-10. https://doi.org/10.1093/oxfordjournals.aob.a083733
Dizeo de Strittmatter, C. (1973). Nueva Tenica de Diafanizacion. Boletin de la Sociedad Argentina de Botanica, 15, 126-129.
Götmark, F., Götmark, E., & Jensen, A. M. (2016). Why be a shrub? A basic model and hypotheses for the adaptive values of a common growth form. Frontiers in Plant Science, 7, 1095. https://doi.org/10.3389/fpls.2016.01095
Hammer, Ø., Harper, D. A., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 9.
Kawai, K., & Okada, N. (2020). Leaf vascular architecture in temperate dicotyledons: Correlations and link to functional traits. Planta, 251(1), 1-12. https://doi.org/10.1007/s00425-019-03295-z
Kolivand, H., Fern, B. M., Saba, T., Rahim, M. S. M., & Rehman, A. (2019). A new leaf venation detection technique for plant species classification. Arabian Journal for Science and Engineering, 44(4), 3315-3327. https://doi.org/10.1007/s13369-018-3504-8
Larese, M. G., Namías, R., Craviotto, R. M., Arango, M. R., Gallo, C., & Granitto, P. M. (2014). Automatic classification of legumes using leaf vein image features. Pattern Recognition, 47(1), 158-168. https://doi.org/10.1016/j.patcog.2013.06.012
Liu, W., Zheng, L., & Qi, D. (2020). Variation in leaf traits at different altitudes reflects the adaptive strategy of plants to environmental changes. Ecology and Evolution, 10(15), 8166-8175. https://doi.org/10.1002/ece3.6519
Maximov, N. A. (1931). The physiological significance of the xeromorphic structure of plants. Journal of Ecology, 19(2), 273-282. https://doi.org/10.2307/2255820
McDonald, P. G., Fonseca, C. R., McC, J., & Westoby, M. (2003). Leaf-size divergence along rainfall and soil-nutrient gradients: Is the method of size reduction common among clades? Functional Ecology, 17(1), 50-57. https://doi.org/10.1046/j.1365-2435.2003.00698.x
Miljković, D., Stefanović, M., Orlović, S., Stanković Neđić, M., Kesić, L., & Stojnić, S. (2019). Wild cherry (Prunus avium (L.) L.) leaf shape and size variations in natural populations at different elevations. Alpine Botany, 129(2), 163-174. https://doi.org/10.1007/s00035-019-00227-1
Mollman, R., Çiftci, A., & Erol, O. (2022). Variable leaf shape on short and long shoots: An elliptic Fourier analysis of Prunus microcarpa C.A.Mey. Brazilian Journal of Botany, 46, 113-125. https://doi.org/10.1007/s40415-022-00857-6
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(6), 804-812. https://doi.org/10.1111/j.1365-3040.2008.01798.x
Newsome, E. L., Brock, G. L., Lutz, J., & Baker, R. L. (2020). Variation within laminae: Semi-automated methods for quantifying leaf venation using phenoVein. Applications in Plant Sciences, 8(5), e11346.
Nicotra, A. B., Leigh, A., Boyce, C. K., Jones, C. S., Niklas, K. J., Royer, D. L., & Tsukaya, H. (2011). The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology, 38(7), 535-552. https://doi.org/10.1071/FP11057
Okie, W. R., & Rieger, M. (2002). Inheritance of venation pattern in Prunus ferganensis x persica hybrids. XXVI International Horticultural Congress: Genetics and Breeding of Tree Fruits and Nuts, 622, pp. 261-264. https://doi.org/10.17660/ActaHortic.2003.622.24
Pagano, M., Corona, P., & Storchi, P. (2016). Image analysis of the leaf vascular network: physiological considerations. Photosynthetica, 54, 567-571.
Pickett, S. T. A., & Kempf, J. S. (1980). Branching patterns in forest shrubs and understory trees in relation to habitat. New Phytologist, 86(2), 219-228. https://doi.org/10.1111/j.1469-8137.1980.tb03191.x
POWO. (2022). Plants of the world online. Facilitated by the Royal Botanic Gardens, Kew. http://www.plantsoftheworldonline.org/ [Visited: 26 Jan. 2022]
Price, C. A., Symonova, O., Mileyko, Y., Hilley, T., & Weitz, J. S. (2011). Leaf extraction and analysis framework graphical user interface: Segmenting and analyzing the structure of leaf veins and areoles. Plant Physiology, 155(1), 236-245. https://doi.org/10.1104/pp.110.162834
Rieger, M., Lo Bianco, R., & Okie, W. R. (2003). Responses of Prunus ferganensis, Prunus persica and two interspecific hybrids to moderate drought stress. Tree Physiology, 23(1), 51-58. https://doi.org/10.1093/treephys/23.1.51
Robertson, K. R., Phipps, J. B., & Rohrer, J. R. (1992). Summary of leaves in the genera of Maloideae (Rosaceae). Annals of the Missouri Botanical Garden, 79(1), 81-94. https://doi.org/10.2307/2399811
Roth-Nebelsick, A., Uhl, D., Mosbrugger, V., & Kerp, H. (2001). Evolution and function of leaf venation architecture: A review. Annals of Botany, 87(5), 553-566. https://doi.org/10.1006/anbo.2001.1391
Rouffa, A. S., & Gunckel, J. E. (1951). Leaf initiation, origin, and pattern of pith development in the Rosaceae. American Journal of Botany, (8)4, 301-307. https://doi.org/10.2307/2438004
Sack, L., & Scoffoni, C. (2013). Leaf venation: Structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist, 198, 983-1000. https://doi.org/10.1111/nph.12253
Schneider, J. V., Negraschis, V., Habersetzer, J., Rabenstein, R., Wesenberg, J., Wesche, K., & Zizka, G. (2018). Taxonomic diversity masks leaf vein-climate relationships: Lessons from herbarium collections across a latitudinal rainfall gradient in West Africa. Botany Letters, 165(3-4), 384-395. https://doi.org/10.1080/23818107.2017.1421480
Scoffoni, C., Rawls, M., McKown, A., Cochard, H., & Sack, L. (2011). Decline of leaf hydraulic conductance with dehydration: Relationship to leaf size and venation architecture. Plant Physiology, 156(2), 832-843. https://doi.org/10.1104/pp.111.173856
Sun, S., Niklas, K. J., Fang, F., Xiang, S., Wu, X., & Yang, X. (2010). Is branching intensity interspecifically related to biomass allocation? A survey of 25 dicot shrub species from an open-growing dry valley. International Journal of Plant Sciences, 171(6), 615-625. https://doi.org/10.1086/653544
Ufimov, R. A., & Dickinson, T. A. (2020). Infrageneric nomenclature adjustments in Crataegus L.(Maleae, Rosaceae). Phytologia, 102(3), 177.
Uhl, D., & Mosbrugger, V. (1999). Leaf venation density as a climate and environmental proxy: A critical review and new data. Palaeogeography, Palaeoclimatology, Palaeoecology, 149(1-4), 15-26. https://doi.org/10.1016/S0031-0182(98)00189-8
Wang, R., Chen, H., Liu, X., Wang, Z., Wen, J., & Zhang, S. (2020). Plant phylogeny and growth form as drivers of the altitudinal variation in woody leaf vein traits. Frontiers in Plant Science, 10, 1735. https://doi.org/10.3389/fpls.2019.01735
Zheng, X., & Wang, X. (2010). Leaf vein extraction based on gray-scale morphology. International Journal of Image, Graphics and Signal Processing, 2(2), 25-31.
Zhu, J., Yao, J., Yu, Q., He, W., Xu, C., Qin, G., Zhu, Q., Fan, D., & Zhu, H. (2020). A fast and automatic method for leaf vein network extraction and vein density measurement based on object-oriented classification. Frontiers in Plant Science, 11, 499.
Zwieniecki, M. A., Boyce, C. K., & Holbrook, N. M. (2004). Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant, Cell & Environment, 27(3), 357-365. https://doi.org/10.1111/j.1365-3040.2003.01153.x