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Genetic Diversity Analyses of Scrophularia erzincanica and Scrophularia fatmae (Scrophulariaceae) Populations Distributed in Eastern Anatolia of Türkiye

Year 2023, Volume: 16 Issue: 2, 436 - 452, 31.08.2023

Faruk Yıldız , Halil İbrahim Türkoğlu , Engin Kılıç , Nalan Yıldırım , Ali Kandemir

https://doi.org/10.18185/erzifbed.1260729

Abstract

Scrophularia fatmae Kandemir & İlhan and Scrophularia erzincanica R.R. Mill (Scrophulariaceae) are endemic species to Erzincan/ Turkiye. IUCN categories in S. erzincanica and S. fatmae are EN and CR. In the present study, we investigated levels of genetic variation and genetic structure of three populations of S. erzincanica, and two populations of S. fatmae in Erzincan using ISSR markers. For this aim, 10 primers amplified 116 total bands, with 104 (89.6 %) being polymorphic, from five populations composed of 75 individuals. The UPGMA cluster analysis demonstrated a significant correlation between genetic variations and geographic distances. The distribution area and population size of S. fatmae, which has adapted to the alpine region, is smaller. In addition, S. fatmae has a higher tendency to self-pollination. S. erzincanica has a larger population. The number of effective pollinators in S. erzincanica and S. fatmae are three and one, respectively. With the contribution of these reasons, when we compare S. fatmae and S. erzincanica species according to the results of the research, it is seen that genetic diversity is higher in S. erzincanica. The genetic data obtained as a result of present study may be used in the development of conservation strategies for other rare and endangered plant species, in addition to S. erzincanica and S. fatmae species.

Keywords

Endemic plant ISSR Population genetic S. erzincanica S. fatmae

Supporting Institution

TÜBİTAK

Project Number

218Z002

Thanks

The research was carried out with the support of TÜBİTAK within the scope of the 1001 project numbered 218Z002. We thank TÜBİTAK for their support.

References

  • [1] Pasdaran A., Hamedi A. (2017). The genus Scrophularia: a source of iridoids and terpenoids with a diverse biological activity, Pharmaceutical Biology, 55 (1), 2211-2233.
  • [2] Uzunhisarcikli M.E., Doğan Güner E., Özbek F., Ekici M. (2019). Scrophularia vernalis: a new species record from Turkey and its comparison with Scrophularia chrysantha (Scrophulariaceae). Phytotaxa, 397 (1), 91-98.
  • [3] Kandemir A., İlhan V., Korkmaz M., Karacan S. (2014). Scrophularia fatmae (Scrophulariaceae): Doğu Anadolu Bölgesi’nden sıra dışı yeni bir Sıracaotu (Scrophularia L.) türü, Bağbahçe Bilim Dergisi, 1 (1), 11-17.
  • [4] Uzunhisarcikli M.E., Güner E.D., Ekici M. (2018). Synopsis of the genus Scrophularia (Scrophulariaceae) in Turkey, Phytotaxa, 333 (2), 151-187.
  • [5] Babür H., Kandemir A. (2019). Scrophulariaceae (Sıracaotugiller) familyasına ait Erzincan’a özgü bazı türlerin polen morfolojileri, Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 9 (4), 1931-1936.
  • [6] Kiliç E., Yildiz F., Türkoğlu H.İ., Kandemir A., Doğan N.Y., Bekdemir M. (2020). Sürek Sıracaotu Scrophularia erzincanica R.R. Mill (Scrophulariaceae) ’nin polinatörleri ve zararlı böcekleri üzerine bir araştırma, Bağbahçe Bilim Dergisi, 7 (3), 1-11.
  • [7] Özbek F., Uzunhisarcikli M. E., Ekici M., Güner E.D., Pinar N.M. (2020) Seed morphology of the genus Scrophularia L. (Scrophulariaceae) from Turkey and its taxonomic implications, Phytotaxa, 434 (1), 35-64.
  • [8] Kandemir A., Sevindi C., Korkmaz M., Çelikoğlu Ş. (2015). Erzincan Türkiye’ye özgü endemik bitki taksonlarının IUCN tehdit kategorileri, Bağbahçe Bilim Dergisi, 2 (1), 43-65.
  • [9] Aagaard J. E., Krutovski K.V., Strauss S.H. (1998) RAPDs and allozymes exhibit similar levels of diversity and differentiation among populations and races of Douglas-fir, Heredity., 81, 69–78.
  • [10] Chase M.W., Kesseli R.V., Bawa K. (1996). Microsatellite markers for population and conservation genetics of tropical trees, American Journal of Botany. 83, 51–57.
  • [11] Zheng Z.L. (2010). Studies on genetic diversity and construction of fingerprinting of Magnolia officinalis, Doctoral dissertation, Fujian Agriculture and forestry university.
  • [12] Xiong M., Tian S., Zhang Z., Fan D., Zhang Z. (2014). Population genetic structure and conservation units of Sinomanglietia glauca (Magnoliaceae), Biodiversity Science, 22 (4): 476-484.
  • [13] Culley T.M., Wolfe A.D. 2001: Population genetic structure of the cleistogamous plant species Viola pubescens Aiton (Violaceae), as indicated by allozyme and ISSR molecular markers. Heredity. 86: 545-556.
  • [14] Mattioni C., Casasoli M., Gonzalea M., Ipinza R., Villani F. (2002). Comparison of ISSR and RAPD markers to characterize three Chilean Nothofagus species, Theor. Appl. Genet., 104, 1064–1070.
  • [15] Yu H.H., Yang Z.L., Sun B., Liu R.N., Yang X. (2011). Genetic diversity and relationship of the endangered plant Magnolia officinalis (Magnoliaceae) assessed with ISSR polymorphisms, Biochem. Syst. Ecol., 39: 71−78.
  • [16] Zietkiewicz E., Rafalski A., Labuda D. (1994). Genome Finger printing by Simple Sequence Repeat (SSR)-anchored Polymerase Chain Reaction Amplification, Genomics, 20 (2): 176-183
  • [17] Chen D., Zhang X., Wang Y., Li L. (2012). Genetic diversity of Scrophularia ningpoensis based on SCoT analysis, Zhongguo Zhong yao za zhi= Zhongguo zhongyao zazhi= China journal of Chinese materia medica, 37(16), 2368-2372.
  • [18] Primack, R. B. (2012). Koruma Biyolojisi, Çeviri editörleri Dönmez, A. A. ve Dönmez, E. O., Hacettepe Üniversitesi Yayınları, Ankara.
  • [19] Cornwell W. K., Pearse W. D., Dalrymple R. L., Zanne A. E. (2019). What we (don't) know about global plant diversity, Ecography, 42(11), 1819-1831.
  • [20] Sunar S., Aksakal O., Yildirim N., Agar G., Gulluce M., Sahin F. (2009). Genetic diversity and relationships detected by FAME and RAPD analysis among Thymus species growing in eastern Anatolia region of Turkey, Rom. Biotechnol. Lett., 14, 4313–4318.
  • [21] Yeh F.C., Yang R.C., Boyle T.B., Ye Z.H., Mao J.X. (1997). Popgene, the user-friendly shareware for population genetic analysis, Molecular biology and biotechnology centre, University of Alberta, Canada, 10, 295-301.
  • [22] Rohlf J. (1997). Numerical taxonomy and multivariate analysis system NTSYS-pc v2. 01b, Dept Ecology and Evolution, State University of New York, NY, USA.
  • [23] Nei M. (1972). Genetic distance between populations, The American Naturalist, 106 (949), 283-291.
  • [24] Qiu Y.X., Hong D.Y., Fu C.X., Cameron K.M. (2004). Genetic variation in the endangered and endemic species Changium smyrnioides (Apiaceae), Biochem. Syst. Ecol., 32 (6), 583–596.
  • [25] Cao P.J., Yao Q.F., Ding B.Y., Zeng H.Y. (2006). Genetic diversity of Sinojackia dolichocarpa (Styracaceae), a species endangered and endemic to China, detected by inter-simple sequence repeat (ISSR), Biochemical Systematics and Ecology, 34 (3), 231–239.
  • [26] Shao J.W., Chen W.L., Peng Y.Q., Zhu G.P. (2009). Genetic diversity within and among populations of the endangered and endemic species Primula merrilliana in China, Biochem. Syst. Ecol., 37 (6), 699-706.
  • [27] Sunar S., Yildirim N., Sengül M., Ağar G. (2016). Genetic Diversity and Relationships Detected by ISSR and RAPD Analysis Among Aethionema Species Growing in Eastern Anatolia (Turkey), Comptes Rentus Biologies, 339 (3-4), 147-151.
  • [28] Schmidt K., Jensen K. (2000). Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components, American Jour. Botany, 87 (5), 678-689.
  • [29] Park J., Kim M., Park K.R. (2010). Genetic variation in endangered Scrophularia takesimensis (Scrophulariaceae) from Ulleung Island, Botanical Studies, 51 (3), 371-376.
  • [30] Torres E., Iriondo J. M., Pérez C. (2003). Genetic structure of an endangered plant, Antirrhinum microphyllum (Scrophulariaceae): allozyme and RAPD analysis, American J. Botany, 90 (1), 85-92.
  • [31] Jiménez J.F., Sánchez-Gómez P., Güemes J., Werner O., Rosselló J.A. (2002). Genetic variability in a narrow endemic snapdragon (Antirrhinum subbaeticum, Scrophulariaceae) using RAPD markers, Heredity, 89 (5), 387-393.
  • [32] Selseleha M., Hadiana J., Ebrahimib S.N., Sonbolic A., Georgievd M.I., Mirjalilia M.H. (2019). Metabolic diversity and genetic association between wild populations of Verbascum songaricum (Scrophulariaceae), Industrial Crops & Products, 137, 112–125.
  • [33] Liu X.L., Qian Z.G., Liu F.H., Yang Y.W., Pu C.X. (2011). Genetic diversity within and among populations of Neopicrorhiza scrophulariiflora (Scrophulariaceae) in China, an endangered medicinal plant, Biochem. Syst. Ecol., 39 (4-6), 297-301.
  • [34] Yang S., Chen C., Zhao Y., Xi W., Zhou X., Chen B., Fu C. (2010). Association between Chemical and Genetic Variation of Wild and Cultivated Populations of Scrophularia ningpoensis Hemsl., Planta Medica, 77 (08), 865-871.
  • [35] Torres-Diaz C., Ruiz E., Gonzalez F., Fuentes G., Cavieres L.A. (2007). Genetic diversity in Nothofagus alessandrii (Fagaceae), an endangered endemic tree species of the coastal Maulino forest of central Chile, Annals of Botany, 100 (1), 75–82.
  • [36] Hamrick J. L., Godt M. J. W., Sherman-Broyles S. L. (1992). Factors influencing levels of genetic diversity in woody plant Species, New Forests., 6, 95-124.
  • [37] He T.H., Rao G.Y., You R.L.S., Zhang D.M. (2000). Genetic diversity of widespread Ophiopogon intermedius (Liliaceae s.l.) a comparison with endangered O. xylorrhizus, Bio. Conserv., 96 (2), 253–257.
  • [38] Hamrick J.L., Murawski D.A. (1990). The breeding structure of tropical tree populations, Plant Species Biology., 5 (1), 157-165.
  • [39] Peterson A., Bartish I.V., Peterson J. (2007). Effects of population size on genetic diversity, fitness and pollinator community composition in fragmented populations of Anthericum liliago L., Plant Ecology, 198 (1), 101-110.
  • [40] Erhardt A. 1993: Pollination of the edelweiss, Leontopodium alpinum, Botanical Journal of the Linnean Society., 111 (2), 229-240.
  • [41] Körner C. (2003). Alpine Plant Life Functional Plant Ecology of High Mountain Ecosystems (2nd Edition). Berlin: Springer-Verlag Berlin Heidelberg, New York.
  • [42] Petrova G., Petrov S., Delcheva M., Bancheva S. (2017). Genetic diversity and conservation of Bulgarian endemic Verbascum tzar-borisii (Scrophulariaceae), Annales Botanici Fennici, 54 (4-6), 307–316.
  • [43] Ballesteros-Mejia L., Lima N.E., Lima-Ribeiro M.S., Collevatti R.G. (2016). Pollination mode and mating system explain patterns in genetic differentiation in neotropical plants, PLoS One, 11 (7), e0158660.
  • [44] Yildiz F. (2021). An investigation of the effects of pollinator varieties, genetic diversity and reproductive success in different pollination applications of Scrophularia fatmae Kandemir & İlhan (Scrophulariaceae) and Scrophularia erzincanica R. R. Mill. (Scrophulariaceae), PhD Thesis, Erzincan Binali Yıldırım University, https://tez.yok.gov.tr/UlusalTezMerkezi/tezSorgu SonucYeni.jsp

Year 2023, Volume: 16 Issue: 2, 436 - 452, 31.08.2023

Faruk Yıldız , Halil İbrahim Türkoğlu , Engin Kılıç , Nalan Yıldırım , Ali Kandemir

https://doi.org/10.18185/erzifbed.1260729

Abstract

Scrophularia fatmae Kandemir & İlhan ve Scrophularia erzincanica R.R. Mill (Scrophulariaceae) Erzincan/Türkiye'ye özgü endemik türlerdir. S. erzincanica ve S. fatmae'de ki IUCN kategorileri sırasıyla EN ve CR'dir. Bu çalışmada, ISSR belirteçlerini kullanarak Erzincan'daki üç S. erzincanica popülasyonunun ve iki S. fatmae popülasyonunun genetik varyasyon seviyelerini ve genetik yapısı araştırılmıştır. Bu amaçla 10 primer, 75 bireyden oluşan beş popülasyondan 104'ü (%89.6) polimorfik olmak üzere toplam 116 bandı amplifiye edildi. UPGMA küme analizi, genetik varyasyonlar ve coğrafi mesafeler arasında anlamlı bir ilişki olduğunu göstermiştir. Alpin bölgesine uyum sağlamış olan S. fatmae'nin yayılış alanı ve populasyon büyüklüğü daha küçüktür. Ek olarak, S. fatmae'nin kendi kendine tozlaşma eğilimi daha yüksektir. S. erzincanica daha büyük bir popülasyona sahiptir. S. erzincanica ve S. fatmae'de etkili tozlayıcı sayısı sırasıyla üç ve birdir. Bu sebeplerin de katkısı ve araştırma sonuçlarına göre S. fatmae ve S. erzincanica türleri karşılaştırıldığında S. erzincanica'da genetik çeşitliliğin daha fazla olduğu görülmektedir. Bu çalışma sonucunda elde edilen genetik veriler, S. erzincanica ve S. fatmae türlerinin yanı sıra diğer nadir ve tehlike altındaki bitki türleri için koruma stratejilerinin geliştirilmesinde kullanılabilir.

Project Number

218Z002

References

  • [1] Pasdaran A., Hamedi A. (2017). The genus Scrophularia: a source of iridoids and terpenoids with a diverse biological activity, Pharmaceutical Biology, 55 (1), 2211-2233.
  • [2] Uzunhisarcikli M.E., Doğan Güner E., Özbek F., Ekici M. (2019). Scrophularia vernalis: a new species record from Turkey and its comparison with Scrophularia chrysantha (Scrophulariaceae). Phytotaxa, 397 (1), 91-98.
  • [3] Kandemir A., İlhan V., Korkmaz M., Karacan S. (2014). Scrophularia fatmae (Scrophulariaceae): Doğu Anadolu Bölgesi’nden sıra dışı yeni bir Sıracaotu (Scrophularia L.) türü, Bağbahçe Bilim Dergisi, 1 (1), 11-17.
  • [4] Uzunhisarcikli M.E., Güner E.D., Ekici M. (2018). Synopsis of the genus Scrophularia (Scrophulariaceae) in Turkey, Phytotaxa, 333 (2), 151-187.
  • [5] Babür H., Kandemir A. (2019). Scrophulariaceae (Sıracaotugiller) familyasına ait Erzincan’a özgü bazı türlerin polen morfolojileri, Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 9 (4), 1931-1936.
  • [6] Kiliç E., Yildiz F., Türkoğlu H.İ., Kandemir A., Doğan N.Y., Bekdemir M. (2020). Sürek Sıracaotu Scrophularia erzincanica R.R. Mill (Scrophulariaceae) ’nin polinatörleri ve zararlı böcekleri üzerine bir araştırma, Bağbahçe Bilim Dergisi, 7 (3), 1-11.
  • [7] Özbek F., Uzunhisarcikli M. E., Ekici M., Güner E.D., Pinar N.M. (2020) Seed morphology of the genus Scrophularia L. (Scrophulariaceae) from Turkey and its taxonomic implications, Phytotaxa, 434 (1), 35-64.
  • [8] Kandemir A., Sevindi C., Korkmaz M., Çelikoğlu Ş. (2015). Erzincan Türkiye’ye özgü endemik bitki taksonlarının IUCN tehdit kategorileri, Bağbahçe Bilim Dergisi, 2 (1), 43-65.
  • [9] Aagaard J. E., Krutovski K.V., Strauss S.H. (1998) RAPDs and allozymes exhibit similar levels of diversity and differentiation among populations and races of Douglas-fir, Heredity., 81, 69–78.
  • [10] Chase M.W., Kesseli R.V., Bawa K. (1996). Microsatellite markers for population and conservation genetics of tropical trees, American Journal of Botany. 83, 51–57.
  • [11] Zheng Z.L. (2010). Studies on genetic diversity and construction of fingerprinting of Magnolia officinalis, Doctoral dissertation, Fujian Agriculture and forestry university.
  • [12] Xiong M., Tian S., Zhang Z., Fan D., Zhang Z. (2014). Population genetic structure and conservation units of Sinomanglietia glauca (Magnoliaceae), Biodiversity Science, 22 (4): 476-484.
  • [13] Culley T.M., Wolfe A.D. 2001: Population genetic structure of the cleistogamous plant species Viola pubescens Aiton (Violaceae), as indicated by allozyme and ISSR molecular markers. Heredity. 86: 545-556.
  • [14] Mattioni C., Casasoli M., Gonzalea M., Ipinza R., Villani F. (2002). Comparison of ISSR and RAPD markers to characterize three Chilean Nothofagus species, Theor. Appl. Genet., 104, 1064–1070.
  • [15] Yu H.H., Yang Z.L., Sun B., Liu R.N., Yang X. (2011). Genetic diversity and relationship of the endangered plant Magnolia officinalis (Magnoliaceae) assessed with ISSR polymorphisms, Biochem. Syst. Ecol., 39: 71−78.
  • [16] Zietkiewicz E., Rafalski A., Labuda D. (1994). Genome Finger printing by Simple Sequence Repeat (SSR)-anchored Polymerase Chain Reaction Amplification, Genomics, 20 (2): 176-183
  • [17] Chen D., Zhang X., Wang Y., Li L. (2012). Genetic diversity of Scrophularia ningpoensis based on SCoT analysis, Zhongguo Zhong yao za zhi= Zhongguo zhongyao zazhi= China journal of Chinese materia medica, 37(16), 2368-2372.
  • [18] Primack, R. B. (2012). Koruma Biyolojisi, Çeviri editörleri Dönmez, A. A. ve Dönmez, E. O., Hacettepe Üniversitesi Yayınları, Ankara.
  • [19] Cornwell W. K., Pearse W. D., Dalrymple R. L., Zanne A. E. (2019). What we (don't) know about global plant diversity, Ecography, 42(11), 1819-1831.
  • [20] Sunar S., Aksakal O., Yildirim N., Agar G., Gulluce M., Sahin F. (2009). Genetic diversity and relationships detected by FAME and RAPD analysis among Thymus species growing in eastern Anatolia region of Turkey, Rom. Biotechnol. Lett., 14, 4313–4318.
  • [21] Yeh F.C., Yang R.C., Boyle T.B., Ye Z.H., Mao J.X. (1997). Popgene, the user-friendly shareware for population genetic analysis, Molecular biology and biotechnology centre, University of Alberta, Canada, 10, 295-301.
  • [22] Rohlf J. (1997). Numerical taxonomy and multivariate analysis system NTSYS-pc v2. 01b, Dept Ecology and Evolution, State University of New York, NY, USA.
  • [23] Nei M. (1972). Genetic distance between populations, The American Naturalist, 106 (949), 283-291.
  • [24] Qiu Y.X., Hong D.Y., Fu C.X., Cameron K.M. (2004). Genetic variation in the endangered and endemic species Changium smyrnioides (Apiaceae), Biochem. Syst. Ecol., 32 (6), 583–596.
  • [25] Cao P.J., Yao Q.F., Ding B.Y., Zeng H.Y. (2006). Genetic diversity of Sinojackia dolichocarpa (Styracaceae), a species endangered and endemic to China, detected by inter-simple sequence repeat (ISSR), Biochemical Systematics and Ecology, 34 (3), 231–239.
  • [26] Shao J.W., Chen W.L., Peng Y.Q., Zhu G.P. (2009). Genetic diversity within and among populations of the endangered and endemic species Primula merrilliana in China, Biochem. Syst. Ecol., 37 (6), 699-706.
  • [27] Sunar S., Yildirim N., Sengül M., Ağar G. (2016). Genetic Diversity and Relationships Detected by ISSR and RAPD Analysis Among Aethionema Species Growing in Eastern Anatolia (Turkey), Comptes Rentus Biologies, 339 (3-4), 147-151.
  • [28] Schmidt K., Jensen K. (2000). Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components, American Jour. Botany, 87 (5), 678-689.
  • [29] Park J., Kim M., Park K.R. (2010). Genetic variation in endangered Scrophularia takesimensis (Scrophulariaceae) from Ulleung Island, Botanical Studies, 51 (3), 371-376.
  • [30] Torres E., Iriondo J. M., Pérez C. (2003). Genetic structure of an endangered plant, Antirrhinum microphyllum (Scrophulariaceae): allozyme and RAPD analysis, American J. Botany, 90 (1), 85-92.
  • [31] Jiménez J.F., Sánchez-Gómez P., Güemes J., Werner O., Rosselló J.A. (2002). Genetic variability in a narrow endemic snapdragon (Antirrhinum subbaeticum, Scrophulariaceae) using RAPD markers, Heredity, 89 (5), 387-393.
  • [32] Selseleha M., Hadiana J., Ebrahimib S.N., Sonbolic A., Georgievd M.I., Mirjalilia M.H. (2019). Metabolic diversity and genetic association between wild populations of Verbascum songaricum (Scrophulariaceae), Industrial Crops & Products, 137, 112–125.
  • [33] Liu X.L., Qian Z.G., Liu F.H., Yang Y.W., Pu C.X. (2011). Genetic diversity within and among populations of Neopicrorhiza scrophulariiflora (Scrophulariaceae) in China, an endangered medicinal plant, Biochem. Syst. Ecol., 39 (4-6), 297-301.
  • [34] Yang S., Chen C., Zhao Y., Xi W., Zhou X., Chen B., Fu C. (2010). Association between Chemical and Genetic Variation of Wild and Cultivated Populations of Scrophularia ningpoensis Hemsl., Planta Medica, 77 (08), 865-871.
  • [35] Torres-Diaz C., Ruiz E., Gonzalez F., Fuentes G., Cavieres L.A. (2007). Genetic diversity in Nothofagus alessandrii (Fagaceae), an endangered endemic tree species of the coastal Maulino forest of central Chile, Annals of Botany, 100 (1), 75–82.
  • [36] Hamrick J. L., Godt M. J. W., Sherman-Broyles S. L. (1992). Factors influencing levels of genetic diversity in woody plant Species, New Forests., 6, 95-124.
  • [37] He T.H., Rao G.Y., You R.L.S., Zhang D.M. (2000). Genetic diversity of widespread Ophiopogon intermedius (Liliaceae s.l.) a comparison with endangered O. xylorrhizus, Bio. Conserv., 96 (2), 253–257.
  • [38] Hamrick J.L., Murawski D.A. (1990). The breeding structure of tropical tree populations, Plant Species Biology., 5 (1), 157-165.
  • [39] Peterson A., Bartish I.V., Peterson J. (2007). Effects of population size on genetic diversity, fitness and pollinator community composition in fragmented populations of Anthericum liliago L., Plant Ecology, 198 (1), 101-110.
  • [40] Erhardt A. 1993: Pollination of the edelweiss, Leontopodium alpinum, Botanical Journal of the Linnean Society., 111 (2), 229-240.
  • [41] Körner C. (2003). Alpine Plant Life Functional Plant Ecology of High Mountain Ecosystems (2nd Edition). Berlin: Springer-Verlag Berlin Heidelberg, New York.
  • [42] Petrova G., Petrov S., Delcheva M., Bancheva S. (2017). Genetic diversity and conservation of Bulgarian endemic Verbascum tzar-borisii (Scrophulariaceae), Annales Botanici Fennici, 54 (4-6), 307–316.
  • [43] Ballesteros-Mejia L., Lima N.E., Lima-Ribeiro M.S., Collevatti R.G. (2016). Pollination mode and mating system explain patterns in genetic differentiation in neotropical plants, PLoS One, 11 (7), e0158660.
  • [44] Yildiz F. (2021). An investigation of the effects of pollinator varieties, genetic diversity and reproductive success in different pollination applications of Scrophularia fatmae Kandemir & İlhan (Scrophulariaceae) and Scrophularia erzincanica R. R. Mill. (Scrophulariaceae), PhD Thesis, Erzincan Binali Yıldırım University, https://tez.yok.gov.tr/UlusalTezMerkezi/tezSorgu SonucYeni.jsp
There are 44 citations in total.

Details

Primary Language English
Subjects Engineering
Journal Section Makaleler
Authors

Faruk Yıldız 0000-0003-1937-6748

Halil İbrahim Türkoğlu 0000-0002-1400-2993

Engin Kılıç 0000-0002-6838-5977

Nalan Yıldırım 0000-0002-5344-5367

Ali Kandemir 0000-0003-1902-9631

Project Number 218Z002
Early Pub Date August 24, 2023
Publication Date August 31, 2023
Published in Issue Year 2023 Volume: 16 Issue: 2

Cite

APA Yıldız, F., Türkoğlu, H. İ., Kılıç, E., Yıldırım, N., et al. (2023). Genetic Diversity Analyses of Scrophularia erzincanica and Scrophularia fatmae (Scrophulariaceae) Populations Distributed in Eastern Anatolia of Türkiye. Erzincan University Journal of Science and Technology, 16(2), 436-452. https://doi.org/10.18185/erzifbed.1260729
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