The importance of qualitative and quantitative anatomical traits in distinguishing species of the series Crataegus subseries Erianthae in Iran

Document Type : Research Paper

Authors

1 Research Institute of Forests and Rangelands, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran

2 Central Herbarium of Tehran University, Center of Excellence in Phylogeny of Living Organisms, School of Biology, College of Science, University of Tehran, Tehran, Iran

3 Research Institute of Forests and Rangelands, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran.

4 School of Biology, College of Science, University of Tehran, Tehran, Iran.

10.22092/ijb.2025.368384.1510

Abstract

Anatomical traits (leaf and epidermal cells) of 10 Crataegus species belonging to the series Crataegus subseries Erianthae were examined for a taxonomic evaluation. Anatomical characteristics were categorized into qualitative and quantitative traits. All data were analyzed using PCA and clustering methods. The results showed that qualitative such as anticlinal walls of lower epidermal cells, the shape of the vascular bundle of the midrib, the ventral shape of midribs, the stomatal type, and the mesophyll type are more effective than quantitative traits in species identification. Some quantitative traits such as the thickness of the middle vein, the ratio of length to width of the first layer of palisade parenchyma, and the ratio of length to width of the second layer of palisade parenchyma can also be used in species separation. In the species related to high altitudes, the width of the first layer of palisade parenchyma was much less than the species of low altitudes. Crataegus babakhanloui and C. aminii, which did not differ significantly in terms of qualitative traits, differed in several quantitative traits such as the length of the first layer of palisade parenchyma and the length of the long axis of stomata. Among various species and specimens, the highest length of the long axis of stomata was observed in C. aminii and the lowest belonged to specimens in C. meyeri. Crataegus khatamsazae and C. hatamii. These species were described as new species based on morphological and micromorphological differences. Our results showed differences in their quantitative and qualitative anatomical traits.

Keywords


Article Title [Persian]

اهمیت صفات تشریحی کمی و کیفی در تمایز گونه‌های سری Crataegus زیر سری Erianthae در ایران

Authors [Persian]

  • بهنام حمزه 1
  • فریده عطار 2
  • روح انگیز ,عباس عظیمی 3
  • فاطمه آوخ حاجی شیرکیایی 4
1 دانشیار، مؤسسه تحقیقات جنگلها و مراتع کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، تهران، ایران
2 استاد، دانشکده زیست شناسی، دانشکدگان علوم ، دانشگاه تهران، تهران، ایران
3 محقق مؤسسه تحقیقات جنگلها و مراتع، سازمان تحقیقات، آموزش و ترویج کشاورزی، تهران، ایران
4 دانش آموخته دانشکده زیست‌شناسی، دانشکدگان علوم، دانشگاه تهران، تهران، ایران
Abstract [Persian]

صفات تشریحی (سلول‌های برگ و اپیدرم) 10 گونه زالزالک متعلق به زیرسریErianthae  برای ارزیابی تاگزونومیکی مورد بررسی قرار گرفت. ویژگی‌های تشریحی به دو گروه صفات کمی و کیفی تفکیک شدند. تمامی داده‎ها با استفاده از روش‌های PCA و خوشه‌بندی تجزیه و تحلیل شدند. نتایج نشان داد که صفات کیفی مانند شکل دیواره آنتی‌کلینال اپیدرم تحتانی، شکل دسته‌های آوندی رگبرگ میانی، شکل سطح شکمی رگبرگ میانی، تیپ روزنه‌ای و تیپ مزوفیل در تشخیص گونه‌ها موثرتر از صفات کمی هستند. همچنین از برخی از صفات کمی مانند ضخامت رگبرگ میانی، نسبت‌های طول به عرض اولین و دومین لایه پارانشیم نردبانی، می‌توان در جداسازی گونه‌ها استفاده کرد. عرض اولین لایه پارانشیم نردبانی در گونه‌های مربوط به ارتفاعات بالا بسیار کم‌تر از گونه‌های ارتفاعات پایین بود. دو گونه C. babakhanloui و C. aminii که از نظر صفات کیفی اختلاف چندانی نداشتند، در تعدادی از صفات کمی مانند طول اولین لایه پارانشیم نردبانی و طول محور بلند روزنه بسیار متفاوت بودند. طول محور بلند روزنه در گونه C. aminii با اختلاف بسیار زیاد بیشترین مقدار و در جمعیت‌های گونه C. meyeri کم‌ترین مقدار را داشت. دو گونه C. khatamsazae و C. hatamii که با داشتن اختلافاتی از نظر صفات مورفولوژیکی و میکروفولوژیکی به‌عنوان گونه جدید به فلور ایران معرفی شده بودند، از نظر صفات کیفی و کمی آناتومی نیز اختلاف داشتند.

Keywords [Persian]

  • آناتومی برگ
  • تاگزونومی
  • ارتفاع
  • PCA
  • خوشه بندی
Albarouki, E. & Peterson, A. 2007: Molecular and morphological characterization of Crataegus L. species (Rosaceae) in southern Syria. -Botanical Journal of the Linnean Society 53: 255-263. https://doi.org/10.1111/j.1095-8339.2007.00607.x
Anten, N.P., Alcalá-Herrera, R., Schieving F. & Onoda, Y. 2010: Wind and mechanical stimuli differentially affect leaf traits in Plantago major. -New Phytol 188: 554-564. https://doi.org/10.1111/j.1469-8137.2010.03379.x
Abbas-Azimi, R., Jalili, A., Bakhshi-Khaniki, Gh., Sobhanian, H. & Matinizadeh, M. 2020: Effect of latitude and longitude on quantitative changes of some anatomical and morphological features of Alnus subcordata C. A. Mey. leaves in Hyrcanian Forests. -Iranian Journal of Botany 26(1): 75-91. https://doi.org/10.22092/ijb.2020.343127.1285
Bayramzadeh, V. 2011: Stomatal characteristics of Fagus orientalis Lipsky in geographically separated locations in the Caspian forests of northern Iran. -Research Journal of Environmental Sciences 11(5): 836-840. https://doi.org/10.3923/rjes.2011.836.840
Campbell, C.S., Evans, R.C., Morgan, D.R. Dickinson, T.A. & Arsenault, M.P. 2007: Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): Limited resolution of a complex evolutionary history. -Plant Syst. Evol. 266: 119-145. https://doi.org/10.1007/s00606-007-0545-y
Chitwood, D.H. 2016: Climate and developmental plasticity: interannual variability in grapevine leaf morphology. -Plant Physiol. 170: 1480-1491. https://doi.org/10.1104/pp.15.01825
Christensen, K.I. 1992: Revision of Crataegus sect. Crataegus and nothosect. Crataeguineae (Rosaceae-Maloideae) in the Old World. -Systematic Botany Monographs 35: 1-199. https://doi.org/10.2307/25027810
Chwil, M., Konarska, A., & Weryszko-Chmielewska, E. 2006: Diversity of the floral nectaries surface of four Crataegus L. species. -Acta Agrobotanica 59(1): 29-39. https://doi.org/10.5586/aa.2006.003
Demiray, H. 2007: Calcium oxalate crystals of some Crataegus (Rosaceae) species growing in Aegean region. -Biologia, Bratislava 62/1: 46-50. https://doi.org/10.2478/s11756-007-0004-9
Dickinson, T.A. & Phipps, J.B. 1985: Degree and pattern of variation in Crataegus section Crus-galli in Ontario. -Sys. Bot. 10: 322-337. https://doi.org/10.2307/2418596
Dickinson, T., Lo, E. & Talent, N. 2007: Polyploidy, Reproductive Biology, and Rosaceae: understanding evolution and making classifications. -Plant Syst. Evol. 266: 59-78. https://doi.org/10.1007/s00606-007-0541-2
Dilcher, D.L. 1974: Approach to the Identification of Angiosperms Leaf Remains. -Botanical Review 40: 1-157. https://doi.org/10.1007/BF02860067
Ganeva, T.S., Uzunova, K.R. & Koleva, D. 2009: Comparative leaf epidermis investigation in species of genus Crataegus L. (Rosaceae) from Bulgaria. -Feddes Repertorium 120 (3-4): 169-184. https://doi.org/10.1002/fedr.200811105
Gladkova, V.N. 1968: Karyological studies of the genera Crataegus L. and Cotoneaster Medic. (Maloideae) as related to their taxonomy. -Botanicheskii Zhurnal 53: 1203-1273.
Guerin, G.R., Wen, H. & Lowe, A.J. 2012: Leaf morphology shift linked to climate change. -Biology Letters 8: 882-886. https://doi.org/10.1098/rsbl.2012.0458
Hadač, E. & Chrtek, J. 1980: A contribution to the Iraqi Rosaceae. Candollea 35: 311-328.
Hamzeh’ee, B., Attar, F., Assareh, M.H., Maassoumi, A.A., Kazempour Osaloo, S., Christensen, K.I. 2014: Taxonomic notes on Crataegus, ser. Crataegus, subser. Erianthae (Rosaceae), new species and record, using morphology and micromorphological evidence. -Nordic Journal of Botany 32: 26-37. https://doi.org/10.1111/j.1756-1051.2012.01737.x
Hamzeh’ee, B., Attar, F., Assareh, M.H., Maassoumi, A.A. & Kazempour Osaloo, S. 2016: Comparative micromorphological characteristics of lower leaf epidermis and seed surface in two series of Crataegus L. (Rosaceae) and their taxonomical role. -Iranian Journal of Botany 22: 126-137. https://doi.org/10.1111/j.1756-1051.2012.01737.x
Holmgren, P.K., Holmgren, N.H., & Barnett, L.C. 1990: Index Herbariorum I: The Herbaria of the world, 8th ed. Regnum Veg. 20.
Ichie, T., Inoue, Y., Takahashi, N., Kamiya, K. & Kenzo, T. 2016: Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. -Journal of Plant Research 129(4): 625-635. https://doi.org/10.1007/s10265-016-0795-2
Jia, X.D., Lü, H.Y., Wu, L.M., Yang, Y.N., Huang, R.H., Wang, H. & Niu, X. 2024: Response of leaf functional traits and anatomical structure to altitude in Crataegus songarica K. Koch in Tianshan wild fruit forest. -Plant Science Journal 42(2): 150-159. https://doi.org/10.11913/PSJ.2095-0837.23157
Jones, D.A. & Wilkins, D.A. 1971: Variation and adaptation in plant species. -Heinemann Educational Books Ltd, London, UK, 184 pp.
Jones, S.B. & Luchsinger, A.G. 1979: Plant Systematics. McGraw-Hill, New York, 292 pp.
Katarzyna, M. 2012: Variation of leaf shape of Salix herbacea in Europe. -Plant Syst. Evol. 298: 1597- 1607. https://doi.org/10.1007/s00606-012-0662-0
Khatamsaz, M. 1991: The genus Crataegus L. (Rosaceae) in Iran. -Iranian Journal of Botany 5: 47-56.
Khatamsaz, M. 1992: Rosaceae. In: Assadi, M. & al. (eds.), Flora of Iran, No. 6. Research Institute of Forests and Rangelands, Tehran, Iran (Persian).
Körner, C., Neumayer, M., Menendez-Riedl, S.P. & Smeets-Scheel, A. 1989: Functional morphology of mountain plants. -Flora 182(5-6): 353-383. https://doi.org/10.1016/S0367-2530
Lo., E., Stefanovic, S.S., Christensen, K.I. & Dickinson, A. 2009: Evidence for genetic association between East Asian and western North American Crataegus L. (Rosaceae) and rapid divergence of the eastern North American lineages based on multiple DNA sequences. -Molecular Phylogenetics and Evolution Journal 51: 157-168. https://doi.org/10.1016/j.ympev.2009.01.018
Lo, E., Stefanovic, S.S. & Dickinson, T.A. 2007: Molecular reappraisal of relationships between Crataegus and Mespilus (Rosaceae, Pyreae) two genera or one? -Systematic Botany 32: 596-616. https://doi.org/10.1600/036364407782250562
Lo, E., Stefanovic, S.S. & Dickinson, T.A. 2010: Reconstructing reticulation history in a phylogenetic framework and the potential of allopatric speciation driven by polyploidy in an agamic complex in Crataegus (Rosaceae). -Evolution 64: 3593-3608. https://doi.org/10.1111/j.1558-5646.2010.01063.x
Meier, I.C., & Leuschner, C. 2008: Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability. -Ecosystems 11(5): 655-669. https://doi.org/10.1007/s10021-008-9135-2
Metcalfe, C.R. & Chalk, L. 1957: Anatomy of dicotyledons, Vol. 1. 806 pp. Oxford. London.
Muir, C.D. 2018: Light and growth form interact to shape stomatal ratio among British angiosperms. -New Phytologist 218(1): 242-252. https://doi.org/10.1111/nph.14956
Nieto-Ángel, R., Pérez-Ortega, S., Núñez-Colín, CA., Martinez-Solís, J. & Gonzáles-Andrés, F. 2009: Seed and endocarp traits as markers of the biodiversity of regional sources of germplasm of tejocote (Crataegus spp.) from Central and Southern Mexico. -Scientia Horticulturae 121: 166–170. https://doi.org/10.1016/j.scienta.2009.01.034
Nisa, S. U., Shah, S. A., Mumtaz, A.S. & Sultan, A. 2019: Stomatal novelties in Vincetoxicum arnottianum (Asclepiadeae: Asclepiadoideae: Apocynaceae). -Flora 260, 151464. https://doi.org/10.1016/j.flora.2019.151464
Novruzova, Z.A., Kasumova, T.A. & Abbasova, V.S. 1990: Comparative anatomical analysis of the hawthorns (Crataegus L.) of Azerbaijan. Izvestiya Akademii Nauk Azerbaĭdzhanskoĭ SSR, Biologicheskie Nauki 9-14.
Paridari, I.C., Jalali, S.G., Sonboli, A. & Zarafshar, M. 2012: Leaf, Stomata and Trichome Morphology of the species in Carpinus Genus. -Taxonomy and Biosystematics 4(10): 11-26 (in Persian).
Potter, D., Eriksson, T., Evans, R.C., Oh, S., Smedmark, J.E.E., Morgan, D.R., Kerr, M., Robertson, K.R., Arsenault, M., Dickinson, T.A. & Campbell, C.S. 2007: Phylogeny and classification of Rosaceae. -Plant Syst. Evol. 266, 5-43. https://doi.org/10.1007/s00606-007-0539-9
Pyakurel, A. & Wang, J.R. 2014: Leaf morphological and stomatal variations in paper birch populations along environmental gradients in Canada. -American Journal of Plant Sciences 1508-1520. https://doi.org/10.4236/ajps.2014.511166
Riedl, H. 1969: Crataegus L. In: Rechinger, K.H. (ed.), Flora Iranica, Rosaceae 1, 66: 49-65. - Akademische Druck-u Verlagsanstalt., Graz, Austria.
Royer, D.L.& Wilf, P. 2006: Why do toothed leaves correlate with cold climates? gas exchange at leaf margins provides new insights into a classic paleotemperature proxy. -Int. J. Plant Sci. 167: 11-18. https://doi.org/10.1086/497995
Ruzin, E.S. (1999). Plant Microtechnique and Microscopy. Oxford University Press, New York.
Saribas, M.&  Yaman, B. 2005: Wood Anatomy of Crataegus tanacetifolia (Lam.) Pers. (Rosaceeae), Endemic to Turkey. -International Journal of Botany 2: 158-162. https://doi.org/10.3923/ijb.2005.158.162
Sass, J.E. 1951: Botanical microtechnique. Ames, Iowa State College Press 228 p.
Shahbaz, S.E. 2009: Taxonomic evidence from leaves, fruits, and leaf cuticular structure to delimit taxa of Crataegus in Dohuk province. The 2nd Kurdistan Conference on Biological Sciences, J. Duhok Univ., Vol. 12, No. 1 (Special Issue), pp. 80-90.
Talent, N. & Dickinson, TA. 2005: Polyploidy in Crataegus and Mespilus (Rosaceae, Maloideae): evolutionary inferences from flow cytometry of nuclear DNA amount. -Can. J. Bot. 83: 1268- 1304. https://doi.org/10.1139/b05-088
Tonggui, W., Zhang, P., Zhang, L., Wang, G.G. & Mukui, Y. 2016: Morphological response of eight Quercus species to simulated wind load. -PLoS One 11: 1-14. https://doi.org/10.1371/journal.pone.0163613
Velízquez‐Rosas, N., Meave, J. & Vízquez‐Santana, S. 2002: Elevational Variation of Leaf Traits in Montane Rain Forest Tree Species at La Chinantla, Southern México1. -Biotropica 34(4): 534-546. https://doi.org/10.1111/j.17447429.2002.tb00572.x
Xu, F., Guo, W., Xu, W., Wei, Y. & Wang, R. 2009: Leaf morphology correlates with water and light availability: what consequences for simple and compound leaves? -Progress in Natural Science 19 (12): 1789-1798. https://doi.org/10.1016/j.pnsc.2009.10.001
Zarafshar, M., Akbarinia, M., Yosefzade H. & Sattarian, A. 2009: Leaf and seed morphological trait in Celtis australis L. in different geographical conditions. -Iranian J. Rangelands and Forest Plant Breed Genet Res. 17: 88-99.
Zhi-Duan, C. & Zhi-Yun, Z. 1991: A study on foliar epidermis in Betulaceae. -Plant Syst. Evol. 29(2): 156-163.