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Research Article
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Analysis of the Variations Within Quercus ilex L. and the Evaluation of Morphological Types Based on Chloroplast and Nuclear DNA Sequences

Year 2025, Volume: 28 Issue: 1, 36 - 46, 12.02.2025

Aykut Yılmaz

https://doi.org/10.18016/ksutarimdoga.vi.1478950

Abstract

Quercus ilex, evaluated within evergreen oaks, has a wide geographic distribution in the Mediterranean basin. Hybridization and gene flow are effective and frequently observed mechanisms in Q. ilex. Additionally, weak reproductive barriers between closely related taxa in zones of geographical contact further increase genetic diversity and subsequent taxonomic problems. Two morphological types, known as rotundifolia and ilex, are defined based on the variations between Q. ilex populations appearing as a result of all these factors. However, it is still controversial whether morphological types: ilex and rotundifolia are subspecies of Q. ilex or two separate species. In this study, short DNA sequences that consist of matK gene-partial trnK gene intron of chloroplast DNA and ITS1-5.8S rRNA gene-ITS2 of nuclear DNA were used to overcome such difficulties and to reveal the variations between Q. ilex populations. All Q. ilex populations based on both barcoding regions were determined and examined using the Molecular Evolutionary Genetics Analysis (MEGA 11). The analysis such as base substitutions, variable and parsim-info sites, transitional and transversional base substitution ranges (%), and nucleotide frequencies (%) was performed and transitional substitutions according to the transversional substitutions for both barcoding regions were observed in the high-value. Furthermore, the sequences belonging to nuclear DNA in comparison to other barcoding regions exhibited higher variable and parsim-info sites. Finally, Maximum Parsimony (MP) dendrograms for both barcoding regions were drawn to evaluate the populations belonging to Q. ilex in terms of their variations, phylogenetic-evolutionary relationships, and taxonomic status. Although both barcoding regions support the separation of Q. ilex populations based on different morphological types, matK gene-partial trnK gene intron sequences exhibited clearer and more informative results than ITS1-5.8S rRNA gene-ITS2 sequences.

Keywords

Quercus ilex Morphological type Chloroplast DNA Nuclear DNA MEGA 11

References

  • Amaral-Franco, J. (1990). Quercus L. In: Castroviejo S, Lainz M, Lopez Gonzalez G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L (eds) Flora Iberica. Real Jardin Botanico, CSIC, Madrid, pp 15-36.
  • Bacilieri, R., Ducousso, A., Petit, R. J., & Kremer, A. (1996). Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution, 50, 900-908.
  • Barbero, M., Loisel, R., & Quezel, P. (1992). Biogeography, ecology and history of Mediterranean Quercus ilex ecosystems. Vegetatio, 99-100, 19-34.
  • Bensaci, O. A., Beghami, R., & Gouaref, K. (2021). First report of Apiognomonia errabunda on Quercus ilex in Algeria. Folia Forestalia Polonica, Series A – Forestry, 63 (1), 10-20.
  • Borazan, A., & Babaç, M.T. (2003).Morphometric leaf variation in oaks (Quercus) of Bolu, Turkey. Annales Botanici Fennici, 40, 233-242.
  • de Casas, R. R., Cano, E., Balaguer, L., Perez-Corona, E., Manrique, E., Garcia-Verdugo, C., & Vargas, P. (2007). Taxonomic identity of Quercus coccifera L. in the Iberian Peninsula is maintained in spite of widespread hybridisation, as revealed by morphological, ISSR and ITS sequence data. Flora, 202, 488-499.
  • de Rigo, D., & Caudullo, G. (2016). Quercus ilex in Europe: distribution, habitat, usage and threats. In J. San-Miguel-Ayanz, D. de Rigo, G. Caudullo, T. Houston Durrant, and A. Mauri (Eds.), European Atlas of forest tree species. European Union Publication Office.
  • Govaerts, R., & Frodin, D. G. (1998). World checklist and bibliography of Fagales. Kew: Royal Botanic Gardens, Kew.
  • Hernández‐Agüero, J. A., Ruiz‐Tapiador, I., & Cayuela, L. (2022). What feeds on Quercus ilex L.? A biogeographical approach to studying trophic interactions in a Mediterranean keystone species. Diversity and Distributions, 28(1), 4-24.
  • Jimenez, P., Lopez de Heredia, U., Collada, C., Lorenzo, Z., & Gil, L. (2004). High variability of chloroplast DNA in three Mediterranean evergreen oaks indicates complex evolutionary history. Heredity, 93, 510-515.
  • Kremer, A, Dupouey, J. L., Deans, J. D., Cottrell, J., Csaikl, U., Finkeldey, U., Espinel, S., Jensen, J., Kleinschmit, J., Van Dam, B., Ducousso, A., Forrest, I., de Heredia, U. L., Lowe, A. J., Tutkova, M., Munro, R. C., Steinhoff, S., & Badeau, V. 2002. Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann. For. Sci., 59, 777-787.
  • Lopez de Heredia, U., Jimenez, P., Collada, C., Simeone, M. C., Bellarosa, R., Schirone, B., Cervera, M. T., & Gil, L. (2007). Multimarker phylogeny of three evergreen oaks reveals vicariant patterns in the Western Mediterranean. Taxon, 56, 1209-1220.
  • Lopez De Heredia, U, Sánchez, H., & Soto, Á. (2018). Molecular evidence of bidirectional introgression between Quercus suber and Quercus ilex. iForest, 11, 338-343.
  • Lumaret, R., Mır, C., Mıchaud, H., & Raynal, V. (2002). Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.). Molecular Ecology, 11, 2327-2336.
  • Michaud, H., Toumi, L., Lumaret, R., Li, T. X., Romane, F., & Di Giusto, F. (1995). Effect of geographical discontinuity on genetic variation in Quercus ilex L. (holm-oak). Evidence from enzyme polymorphism. Heredity, 74, 590-606.
  • NCBI, National Centre of Biotechnology Information, https://www.ncbi.nlm.nih.gov/genbank
  • Ortego, J., & Bonal, R. (2010). Natural hybridisation between kermes (Quercus coccifera L.) and holm oaks (Q. ilex L.) revealed by microsatellite markers. Plant Biology, 12, 234-238.
  • Peguero-Pina, J. J., Sancho-Knapik, D., Barrón, E., Camarero, J. J., Vilagrosa, A., & Gil-Pelegrín, E. (2014). Morphological and physiological divergences within Quercus ilex support the existence of different ecotypes depending on climatic dryness. Annals of Botany, 114, 301-313.
  • Petit, R.J., Bodenes, C., Ducousso, A., Roussel, G., & Kremer, A. (2003). Hybridization as a mechanism of invasion in oaks. New Phytologist, 161, 151-164.
  • Rey, M. D., Labella-Ortega, M., Guerrero-Sanchez, V. M., Carleial, R., Castillejo, M. A., Ruggieri, V., & Jorrin-Novo, J. V. (2023). A first draft genome of holm oak (Q. ilex subsp. ballota), the most representative species of the Mediterranean forest and the Spanish agrosylvopastoral ecosystem ‘‘dehesa’’. Frontiers in Molecular Biosciences, 10, 1242943.
  • Saenz de Rivas, C. (1967). Estudios sobre Quercus ilex L. y Quercus rotundifolia Lamk. Anales del Instituto Botánico A. J. Cavanilles, 2, 243-262.
  • Saenz de Rivas, C. (1970). Biometria foliar de una poblacion de Quercus ilex l. subsp. rotundifolia (lamk.) Morais, en El Pardo. Annales del Jardin Botanico de Madrid, 27, 107-114.
  • Schnitzler, J. P., Steinbrecher, R., Zimmer, I., Steigner, D., & Fladung, M. (2004). Hybridization of European oaks (Quercus ilex x Q. robur) results in a mixed isoprenoid emitter type. Plant, Cell and Environment, 27, 585-593.
  • Soto, A., Lorenzo, Z., & Gil, L. (2007). Differences in fine-scale genetic structure and dispersal in Quercus ilex L. and Q. suber L.: Consequences for regeneration of mediterranean open woods. Heredity, 99, 601-607.
  • Sousa, V., Silva, M. E., Louzada, J. L., & Pereira, H. (2021). Wood Density and Ring Width in Quercus rotundifolia Trees in Southern Portugal. Forests, 12, 1499.
  • Suicmez, B., & Avci, M. (2023). Distribution patterns of Quercus ilex from the last interglacial period to the future by ecological niche modelling. Ecology and Evolution, 13, e10606.
  • Tamura, K., Stecher, G., & Kumar, S. 2021. MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7), 3022-3027.
  • Tutın, T. G., Heywood, V. H., Burges, N. A., Moore, D. M., Valentıne, D. H., Walters, S. M., & Webb, D. A. 1964. Flora Europaea. Cambridge University Press, London.
  • Vázquez Pardo, F. M., Ramos Maqueda, S., & Doncel Pérez, E. (2002) Quercus ilex L. and Quercus rotundifolia Lam: Two Different Species. International Oaks, 13, 9-14.
  • Yılmaz, A., Uslu, E., & Babaç, M. T. (2013). Molecular diversity among Turkish oaks (QUERCUS) using random amplified polymorphic DNA (RAPD) analysis. African Journal of Biotechnology, 12(45), 6358-6365.
  • Yılmaz, A., Uslu, E., & Babaç, M. T. (2017). Morphological Variability of Evergreen Oaks (Quercus) in Turkey. Bangladesh Journal of Plant Taxononomy, 24(1), 39-47.
  • Yılmaz, A. (2018). Cytogenetic Relationships of Turkish Oaks. Cytogenetics- Past, Present and Further Perspectives, Chapter 2. Intechopen.

Quercus ilex L. Içerisindeki Varyasyonlarin Analizi ve Kloroplast ve Nükleer DNA Sekanslari Temelinde Morfolojik Tiplerin Değerlendirmesi

Year 2025, Volume: 28 Issue: 1, 36 - 46, 12.02.2025

Aykut Yılmaz

https://doi.org/10.18016/ksutarimdoga.vi.1478950

Abstract

Herdem yeşil meşeler içerisinde değerlendirilen Quercus ilex, Akdeniz temelinde geniş coğrafik dağılıma sahiptir. Hibridizasyon ve gen akışı Q. ilex’de etkili ve sıklıkla gözlenen mekanizmalardır. Ayrıca, coğrafik olarak temaslı bölgelerde, yakın ilişkili taksonlar arasında zayıf üreme bariyerleri, Q. ilex içerisindeki genetik çeşitliliği ve sonrasında taksonomik problemleri arttıran diğer bir önemli durumdur. Rotundifolia ve ilex olarak bilinen iki morfolojik tip, tüm bu faktörlerin sonucu olarak ortaya çıkan, Q. ilex populasyonları arasındaki varyasyonlar temelinde tanımlanır. Ancak, morfolojik tipler: ilex ve rotundifolia nın Q. ilex’in alttürlerimi yoksa iki ayrı türmü olup olmadığı hala tartışmalı durumdur. Bu çalışmada, kloroplast DNA’ya ait matK geni-kısmi trnK gen intronu ve nükleer DNA’ya ait ITS1-5.8S rRNA geni-ITS2 den oluşan kısa DNA sekansları, bu tarz zorlukların üstesinden gelmek ve Q. ilex populasyonları arasındaki varyasyonları ortaya çıkarmak için kullanıldı. Q. ilex’e ait tüm populasyonlar heriki barkodlama bölgesi temelinde belirlendi ve Molecular Evolutionary Genetics Analysis (MEGA 11) kullanarak incelendi. Baz değişimleri, varyasyonlu ve parsim info bölgeler, transisyonel ve transversiyonel baz değişim oranları (%) ve nükleotid frekansları (%) gibi analizler gerçekleştirildi ve her iki barkodlama bölgesi için transisyonel baz değişimlerinin transversiyonel değişimlere göre daha yüksek değerde olduğu gözlemlendi. Ayrıca, nükleer DNA’ya ait sekanslar diğer barkodlama bölgesi ile karşılaştırmada daha yüksek varyasyonlu ve parsim info bölgeler sergiledi. Son olarak her iki barkodlama bölgesi için Maximum Parsimony (MP) dendrogramlar, varyasyonlar, filogenetik-evrimsel ilişkiler ve taksonomik statüler açısından Q. ilex’e ait populasyonları değerlendirmek için çizildi. Her iki barkodlama bölgesi, Q. ilex populasyonlarının farklı morfolojik tipler temelinde ayrımını desteklemesine rağmen, özellikle matK geni-kısmi trnK gen intron sekansları, ITS1-5.8S rRNA geni-ITS2 sekanslarından daha açık ve bilgilendirici sonuçlar sergiledi.

Keywords

Quercus ilex Morfolojik tip Kloroplast DNA Nükleer DNA MEGA 11

References

  • Amaral-Franco, J. (1990). Quercus L. In: Castroviejo S, Lainz M, Lopez Gonzalez G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L (eds) Flora Iberica. Real Jardin Botanico, CSIC, Madrid, pp 15-36.
  • Bacilieri, R., Ducousso, A., Petit, R. J., & Kremer, A. (1996). Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution, 50, 900-908.
  • Barbero, M., Loisel, R., & Quezel, P. (1992). Biogeography, ecology and history of Mediterranean Quercus ilex ecosystems. Vegetatio, 99-100, 19-34.
  • Bensaci, O. A., Beghami, R., & Gouaref, K. (2021). First report of Apiognomonia errabunda on Quercus ilex in Algeria. Folia Forestalia Polonica, Series A – Forestry, 63 (1), 10-20.
  • Borazan, A., & Babaç, M.T. (2003).Morphometric leaf variation in oaks (Quercus) of Bolu, Turkey. Annales Botanici Fennici, 40, 233-242.
  • de Casas, R. R., Cano, E., Balaguer, L., Perez-Corona, E., Manrique, E., Garcia-Verdugo, C., & Vargas, P. (2007). Taxonomic identity of Quercus coccifera L. in the Iberian Peninsula is maintained in spite of widespread hybridisation, as revealed by morphological, ISSR and ITS sequence data. Flora, 202, 488-499.
  • de Rigo, D., & Caudullo, G. (2016). Quercus ilex in Europe: distribution, habitat, usage and threats. In J. San-Miguel-Ayanz, D. de Rigo, G. Caudullo, T. Houston Durrant, and A. Mauri (Eds.), European Atlas of forest tree species. European Union Publication Office.
  • Govaerts, R., & Frodin, D. G. (1998). World checklist and bibliography of Fagales. Kew: Royal Botanic Gardens, Kew.
  • Hernández‐Agüero, J. A., Ruiz‐Tapiador, I., & Cayuela, L. (2022). What feeds on Quercus ilex L.? A biogeographical approach to studying trophic interactions in a Mediterranean keystone species. Diversity and Distributions, 28(1), 4-24.
  • Jimenez, P., Lopez de Heredia, U., Collada, C., Lorenzo, Z., & Gil, L. (2004). High variability of chloroplast DNA in three Mediterranean evergreen oaks indicates complex evolutionary history. Heredity, 93, 510-515.
  • Kremer, A, Dupouey, J. L., Deans, J. D., Cottrell, J., Csaikl, U., Finkeldey, U., Espinel, S., Jensen, J., Kleinschmit, J., Van Dam, B., Ducousso, A., Forrest, I., de Heredia, U. L., Lowe, A. J., Tutkova, M., Munro, R. C., Steinhoff, S., & Badeau, V. 2002. Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann. For. Sci., 59, 777-787.
  • Lopez de Heredia, U., Jimenez, P., Collada, C., Simeone, M. C., Bellarosa, R., Schirone, B., Cervera, M. T., & Gil, L. (2007). Multimarker phylogeny of three evergreen oaks reveals vicariant patterns in the Western Mediterranean. Taxon, 56, 1209-1220.
  • Lopez De Heredia, U, Sánchez, H., & Soto, Á. (2018). Molecular evidence of bidirectional introgression between Quercus suber and Quercus ilex. iForest, 11, 338-343.
  • Lumaret, R., Mır, C., Mıchaud, H., & Raynal, V. (2002). Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.). Molecular Ecology, 11, 2327-2336.
  • Michaud, H., Toumi, L., Lumaret, R., Li, T. X., Romane, F., & Di Giusto, F. (1995). Effect of geographical discontinuity on genetic variation in Quercus ilex L. (holm-oak). Evidence from enzyme polymorphism. Heredity, 74, 590-606.
  • NCBI, National Centre of Biotechnology Information, https://www.ncbi.nlm.nih.gov/genbank
  • Ortego, J., & Bonal, R. (2010). Natural hybridisation between kermes (Quercus coccifera L.) and holm oaks (Q. ilex L.) revealed by microsatellite markers. Plant Biology, 12, 234-238.
  • Peguero-Pina, J. J., Sancho-Knapik, D., Barrón, E., Camarero, J. J., Vilagrosa, A., & Gil-Pelegrín, E. (2014). Morphological and physiological divergences within Quercus ilex support the existence of different ecotypes depending on climatic dryness. Annals of Botany, 114, 301-313.
  • Petit, R.J., Bodenes, C., Ducousso, A., Roussel, G., & Kremer, A. (2003). Hybridization as a mechanism of invasion in oaks. New Phytologist, 161, 151-164.
  • Rey, M. D., Labella-Ortega, M., Guerrero-Sanchez, V. M., Carleial, R., Castillejo, M. A., Ruggieri, V., & Jorrin-Novo, J. V. (2023). A first draft genome of holm oak (Q. ilex subsp. ballota), the most representative species of the Mediterranean forest and the Spanish agrosylvopastoral ecosystem ‘‘dehesa’’. Frontiers in Molecular Biosciences, 10, 1242943.
  • Saenz de Rivas, C. (1967). Estudios sobre Quercus ilex L. y Quercus rotundifolia Lamk. Anales del Instituto Botánico A. J. Cavanilles, 2, 243-262.
  • Saenz de Rivas, C. (1970). Biometria foliar de una poblacion de Quercus ilex l. subsp. rotundifolia (lamk.) Morais, en El Pardo. Annales del Jardin Botanico de Madrid, 27, 107-114.
  • Schnitzler, J. P., Steinbrecher, R., Zimmer, I., Steigner, D., & Fladung, M. (2004). Hybridization of European oaks (Quercus ilex x Q. robur) results in a mixed isoprenoid emitter type. Plant, Cell and Environment, 27, 585-593.
  • Soto, A., Lorenzo, Z., & Gil, L. (2007). Differences in fine-scale genetic structure and dispersal in Quercus ilex L. and Q. suber L.: Consequences for regeneration of mediterranean open woods. Heredity, 99, 601-607.
  • Sousa, V., Silva, M. E., Louzada, J. L., & Pereira, H. (2021). Wood Density and Ring Width in Quercus rotundifolia Trees in Southern Portugal. Forests, 12, 1499.
  • Suicmez, B., & Avci, M. (2023). Distribution patterns of Quercus ilex from the last interglacial period to the future by ecological niche modelling. Ecology and Evolution, 13, e10606.
  • Tamura, K., Stecher, G., & Kumar, S. 2021. MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7), 3022-3027.
  • Tutın, T. G., Heywood, V. H., Burges, N. A., Moore, D. M., Valentıne, D. H., Walters, S. M., & Webb, D. A. 1964. Flora Europaea. Cambridge University Press, London.
  • Vázquez Pardo, F. M., Ramos Maqueda, S., & Doncel Pérez, E. (2002) Quercus ilex L. and Quercus rotundifolia Lam: Two Different Species. International Oaks, 13, 9-14.
  • Yılmaz, A., Uslu, E., & Babaç, M. T. (2013). Molecular diversity among Turkish oaks (QUERCUS) using random amplified polymorphic DNA (RAPD) analysis. African Journal of Biotechnology, 12(45), 6358-6365.
  • Yılmaz, A., Uslu, E., & Babaç, M. T. (2017). Morphological Variability of Evergreen Oaks (Quercus) in Turkey. Bangladesh Journal of Plant Taxononomy, 24(1), 39-47.
  • Yılmaz, A. (2018). Cytogenetic Relationships of Turkish Oaks. Cytogenetics- Past, Present and Further Perspectives, Chapter 2. Intechopen.
There are 32 citations in total.

Details

Primary Language English
Subjects Plant Cell and Molecular Biology
Journal Section RESEARCH ARTICLE
Authors

Aykut Yılmaz 0000-0002-0327-8388

Early Pub Date January 30, 2025
Publication Date February 12, 2025
Submission Date May 5, 2024
Acceptance Date November 8, 2024
Published in Issue Year 2025 Volume: 28 Issue: 1

Cite

APA Yılmaz, A. (2025). Analysis of the Variations Within Quercus ilex L. and the Evaluation of Morphological Types Based on Chloroplast and Nuclear DNA Sequences. Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 28(1), 36-46. https://doi.org/10.18016/ksutarimdoga.vi.1478950
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