Assessment of Durian Diversity and Its Wild Relatives (Durio spp.) Based on Leaf Morphology and Molecular Marker

Abstract

Durian (Durio spp.) is native to Southeast Asia and has potential for development. However, some species are threatened due to deforestation and extensive land conversion. This study aimed to determine the genetic diversity and relationships of durian and wild relatives (Durio spp.) on the Indonesia Island Borneo using a leaf morphology and DNA barcoding (matK) marker. In this study, 15 durian samples from this region were used, excluding ‘Monthong’ (Durio zibethinus) and ‘Bengang’ (Neesia strigosa) as the outgroups from the GenBank database. The leaf morphology was analyzed descriptively, whereas the genetic diversity was by the nucleotide diversity index (π%). The relationship of durians was revealed by the maximum likelihood (ML) method and examined with the bootstrap statistics for 1000 replicates, also confirmed by the PCA (principal component analysis). Based on the leaf morphology, the durians are divided into five forms, i.e., obovate-lanceolate, elliptic, ovate, oblong, and linear-oblong. ‘Pampaken’ and ‘Pampaken Burung Kecil’ indicated the earliest form (obovate-lanceolate), whereas the linear-oblong was by ‘Kamundai.’ Following the molecular marker, it was seen that the durians have low genetic diversity (π%) with only 0.015. However, phylogenetically, the durians were separated into four similar clades or groups for ML and PCA. In this instance, it has appeared that most of the durians evaluated in the current study have close relationships, except for the taxa with the farthest relationship. The results provide valuable information for the local and global durian conservation mission, including future breeding programs.

Keywords

• Breeding program
• Conservation
• DNA barcoding
• Genetic diversity
• Phylogeny

References

1. Acquaah, G. (2015). Conventional plant breeding principles and techniques. In: Advances in Plant Breeding Strategies: Breeding, Biotechnology and Molecular Tools (J. M. Al Khayri et al., eds), Springer International Publishing, pp. 115–158.
2. Acquaah, G. (2015). Conventional plant breeding principles and techniques. In: Advances in Plant Breeding Strategies: Breeding, Biotechnology and Molecular Tools (J. M. Al Khayri et al., eds), Springer International Publishing, pp. 115–158.
3. Aloqalaa, D. A., Kowalski, D. R., Błazej, P., Wnetrzak, M., Mackiewicz, D., & Mackiewicz, P. (2019). The impact of the transversion/transition ratio on the optimal genetic code graph partition. 10th International Conference on Bioinformatics Models, Methods and Algorithms, Proceedings; Part of 12th International Joint Conference on Biomedical Engineering Systems and Technologies, BIOSTEC 2019, pp. 55–65.
4. Aloqalaa, D. A., Kowalski, D. R., Błazej, P., Wnetrzak, M., Mackiewicz, D., & Mackiewicz, P. (2019). The impact of the transversion/transition ratio on the optimal genetic code graph partition. 10th International Conference on Bioinformatics Models, Methods and Algorithms, Proceedings; Part of 12th International Joint Conference on Biomedical Engineering Systems and Technologies, BIOSTEC 2019, pp. 55–65.
5. Aziz, N. A. A., & Jalil, A. M. M. (2019). Bioactive compounds, nutritional value, and potential health benefits of indigenous durian (Durio zibethinus Murr.): A review. Foods, 8(3), 1–18. https://doi.org/10.3390/foods8030096
6. Aziz, N. A. A., & Jalil, A. M. M. (2019). Bioactive compounds, nutritional value, and potential health benefits of indigenous durian (Durio zibethinus Murr.): A review. Foods, 8(3), 1–18. https://doi.org/10.3390/foods8030096
7. Barthet, M. M., Pierpont, C. L., & Tavernier, E. K. (2020). Unraveling the role of the enigmatic matK maturase in chloroplast group IIA intron excision. Plant Direct, 4(3), 1–17. https://doi.org/10.1002/pld3.208
8. Barthet, M. M., Pierpont, C. L., & Tavernier, E. K. (2020). Unraveling the role of the enigmatic matK maturase in chloroplast group IIA intron excision. Plant Direct, 4(3), 1–17. https://doi.org/10.1002/pld3.208

9. Bioversity International. (2007). Descriptors for durian (Durio zibethinus Murr.). Bioversity International, Rome, Italy.
10. Bioversity International. (2007). Descriptors for durian (Durio zibethinus Murr.). Bioversity International, Rome, Italy.
11. Căprar, M., Copaci, C. M., Chende, D. M., Sicora, O., Şumălan, R., & Sicora, C. (2017). Evaluation of genetic diversity by DNA barcoding of local tomato populations from North-Western Romania. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 45(1), 276–279. https://doi.org/10.15835/nbha45110601
12. Căprar, M., Copaci, C. M., Chende, D. M., Sicora, O., Şumălan, R., & Sicora, C. (2017). Evaluation of genetic diversity by DNA barcoding of local tomato populations from North-Western Romania. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 45(1), 276–279. https://doi.org/10.15835/nbha45110601
13. Chen, J. R., & Shiau, Y. J. (2015). Application of internal transcribed spacers and maturase K markers for identifying Anoectochilus, Ludisia, and Ludochilus. Biologia Plantarum, 599(3), 485–490. https://doi.org/10.1007/s10535-015-0520-3
14. Chen, J. R., & Shiau, Y. J. (2015). Application of internal transcribed spacers and maturase K markers for identifying Anoectochilus, Ludisia, and Ludochilus. Biologia Plantarum, 599(3), 485–490. https://doi.org/10.1007/s10535-015-0520-3
15. Cheon, S. H., Jo, S., Kim, H. W., Kim, Y. K., Sohn, J. Y., & Kim, K. J. (2017). The complete plastome sequence of Durian, Durio zibethinus L. (Malvaceae). Mitochondrial DNA Part B: Resources, 2(2), 763–764. https://doi.org/10.1080/23802359.2017.1398615
16. Cheon, S. H., Jo, S., Kim, H. W., Kim, Y. K., Sohn, J. Y., & Kim, K. J. (2017). The complete plastome sequence of Durian, Durio zibethinus L. (Malvaceae). Mitochondrial DNA Part B: Resources, 2(2), 763–764. https://doi.org/10.1080/23802359.2017.1398615
17. Dkhar, J., & Pareek, A. (2014). What determines a leaf’s shape? EvoDevo, 5(1), 1–19. https://doi.org/10.1186/2041-9139-5-47
18. Dkhar, J., & Pareek, A. (2014). What determines a leaf’s shape? EvoDevo, 5(1), 1–19. https://doi.org/10.1186/2041-9139-5-47
19. Feng, J., Wang, Y., Yi, X., Yang, W., & He, X. (2016). Phenolics from durian exert pronounced NO inhibitory and antioxidant activities. Journal of Agricultural and Food Chemistry, 64(21), 4273–4279. https://doi.org/10.1021/acs.jafc.6b01580
20. Feng, J., Wang, Y., Yi, X., Yang, W., & He, X. (2016). Phenolics from durian exert pronounced NO inhibitory and antioxidant activities. Journal of Agricultural and Food Chemistry, 64(21), 4273–4279. https://doi.org/10.1021/acs.jafc.6b01580
21. Fernández-García, J. L. (2017). Phylogenetics for wildlife conservation. In: Phylogenetics (I. Y. Abdurakhmonov, ed), IntechOpen, London, UK.
22. Fernández-García, J. L. (2017). Phylogenetics for wildlife conservation. In: Phylogenetics (I. Y. Abdurakhmonov, ed), IntechOpen, London, UK.
23. Flint-Garcia, S. A. (2013). Genetics and consequences of crop domestication. Journal of Agricultural and Food Chemistry, 61(35), 8267–8276. https://doi.org/10.1021/jf305511d
24. Flint-Garcia, S. A. (2013). Genetics and consequences of crop domestication. Journal of Agricultural and Food Chemistry, 61(35), 8267–8276. https://doi.org/10.1021/jf305511d
25. Gao, Y., Yin, S., Wu, L., Dai, D., Wang, H., Liu, C., & Tang, L. (2017). Genetic diversity and structure of wild and cultivated Amorphophallus paeoniifolius populations in Southwestern China as revealed by RAD-seq. Scientific Reports, 7(1), 1-10. https://doi.org/10.1038/s41598-017-14738-6
26. Gao, Y., Yin, S., Wu, L., Dai, D., Wang, H., Liu, C., & Tang, L. (2017). Genetic diversity and structure of wild and cultivated Amorphophallus paeoniifolius populations in Southwestern China as revealed by RAD-seq. Scientific Reports, 7(1), 1-10. https://doi.org/10.1038/s41598-017-14738-6
27. Govindaraj, M., Vetriventhan, M., & Srinivasan, M. (2015). Importance of genetic diversity assessment in crop plants and its recent advances: An overview of its analytical perspectives. Genetics Research International, 2015, 1–14. https://doi.org/10.1155/2015/431487
28. Govindaraj, M., Vetriventhan, M., & Srinivasan, M. (2015). Importance of genetic diversity assessment in crop plants and its recent advances: An overview of its analytical perspectives. Genetics Research International, 2015, 1–14. https://doi.org/10.1155/2015/431487
29. Habib, S., Dang, V. C., Ickert-Bond, S. M., Zhang, J. L., Lu, L. M., Wen, J., & Chen, Z. D. (2017). Robust phylogeny of Tetrastigma (Vitaceae) based on ten plastid DNA regions: Implications for infrageneric classification and seed character evolution. Frontiers in Plant Science, 8(590), 1–16. https://doi.org/10.3389/fpls.2017.00590
30. Habib, S., Dang, V. C., Ickert-Bond, S. M., Zhang, J. L., Lu, L. M., Wen, J., & Chen, Z. D. (2017). Robust phylogeny of Tetrastigma (Vitaceae) based on ten plastid DNA regions: Implications for infrageneric classification and seed character evolution. Frontiers in Plant Science, 8(590), 1–16. https://doi.org/10.3389/fpls.2017.00590
31. Immanissa, S., Faizal, I., Salamah, A., Sari, I. A., & Susilo, A. W. (2020). Genetic variation in maturase K (matK) from cacao (Theobroma cacao L.) varieties in Indonesia. IOP Conference Series: Earth and Environmental Science, 481(1), 1–7. https://doi.org/10.1088/1755-1315/481/1/012026
32. Immanissa, S., Faizal, I., Salamah, A., Sari, I. A., & Susilo, A. W. (2020). Genetic variation in maturase K (matK) from cacao (Theobroma cacao L.) varieties in Indonesia. IOP Conference Series: Earth and Environmental Science, 481(1), 1–7. https://doi.org/10.1088/1755-1315/481/1/012026
33. IUCN. (2023). The IUCN red list of threatened species. Available in https://www.iucnredlist.org/search?query=durio&searchType=species (Accessed January 2023).
34. IUCN. (2023). The IUCN red list of threatened species. Available in https://www.iucnredlist.org/search?query=durio&searchType=species (Accessed January 2023).
35. Kar, P., Goyal, A.K., Sen, A (2015). Maturase K gene in plant DNA barcoding and phylogenetics. In Plant DNA Barcoding and Phylogenetics, Eds: Ajmal Ali, M., Gábor, G., Al-Hemaid, F., Lambert Academic Publishing, Germany.
36. Kar, P., Goyal, A.K., Sen, A (2015). Maturase K gene in plant DNA barcoding and phylogenetics. In Plant DNA Barcoding and Phylogenetics, Eds: Ajmal Ali, M., Gábor, G., Al-Hemaid, F., Lambert Academic Publishing, Germany.
37. Ke, X., Kang, H., & Tang, Y. (2022). Reduction in leaf size at higher altitudes across 39 broad-leaved herbaceous species on the northeastern Qinghai-Tibetan Plateau. Journal of Plant Ecology, 15(6), 1227–1240. https://doi.org/10.1093/jpe/rtac051
38. Ke, X., Kang, H., & Tang, Y. (2022). Reduction in leaf size at higher altitudes across 39 broad-leaved herbaceous species on the northeastern Qinghai-Tibetan Plateau. Journal of Plant Ecology, 15(6), 1227–1240. https://doi.org/10.1093/jpe/rtac051
39. Kovach, W. (1999). MVSP-A multivariate statistical Package for Windows, ver. 3.1. Kovach Computing Services.
40. Kovach, W. (1999). MVSP-A multivariate statistical Package for Windows, ver. 3.1. Kovach Computing Services.
41. Le, D. T., Zhang, Y. Q., Xu, Y., Guo, L. X., Ruan, Z. P., Burgess, K. S., & Ge, X. J. (2020). The utility of DNA barcodes to confirm the identification of palm collections in botanical gardens. PLoS One, 15, 1-14. https://doi.org/10.1371/journal.pone.0235569
42. Le, D. T., Zhang, Y. Q., Xu, Y., Guo, L. X., Ruan, Z. P., Burgess, K. S., & Ge, X. J. (2020). The utility of DNA barcodes to confirm the identification of palm collections in botanical gardens. PLoS One, 15, 1-14. https://doi.org/10.1371/journal.pone.0235569
43. Lee, S. C., Wang, C. H., Yen, C. E., & Chang, C. (2017). DNA barcode and identification of the varieties and provenances of Taiwan’s domestic and imported made teas using ribosomal internal transcribed spacer 2 sequences. Journal of Food and Drug Analysis, 25(2), 260–274. https://doi.org/10.1016/j.jfda.2016.06.008
44. Lee, S. C., Wang, C. H., Yen, C. E., & Chang, C. (2017). DNA barcode and identification of the varieties and provenances of Taiwan’s domestic and imported made teas using ribosomal internal transcribed spacer 2 sequences. Journal of Food and Drug Analysis, 25(2), 260–274. https://doi.org/10.1016/j.jfda.2016.06.008
45. Lemey, P., Salemi, M., & Vandamme, A. M. (2009). The phylogenetic handbook: A practical approach to phylogenetic analysis and hypothesis testing. Cambridge University Press, Cambridge, UK.
46. Lemey, P., Salemi, M., & Vandamme, A. M. (2009). The phylogenetic handbook: A practical approach to phylogenetic analysis and hypothesis testing. Cambridge University Press, Cambridge, UK.
47. Li, H. Q., Chen, J. Y., Wang, S., & Xiong, S. Z. (2012). Evaluation of six candidate DNA barcoding loci in Ficus (Moraceae) of China. Molecular Ecology Resources, 12(5), 783–790. https://doi.org/10.1111/j.1755-0998.2012.03147.x
48. Li, H. Q., Chen, J. Y., Wang, S., & Xiong, S. Z. (2012). Evaluation of six candidate DNA barcoding loci in Ficus (Moraceae) of China. Molecular Ecology Resources, 12(5), 783–790. https://doi.org/10.1111/j.1755-0998.2012.03147.x
49. Lloyd, M. M., Makukhov, A. D., & Pespeni, M. H. (2016). Loss of genetic diversity as a consequence of selection in response to high pCO2. Evolutionary Applications, 9(9), 1124–1132. https://doi.org/10.1111/eva.12404
50. Lloyd, M. M., Makukhov, A. D., & Pespeni, M. H. (2016). Loss of genetic diversity as a consequence of selection in response to high pCO2. Evolutionary Applications, 9(9), 1124–1132. https://doi.org/10.1111/eva.12404
51. Luan, S., Chiang, T. Y., & Gong, X. (2006). High genetic diversity vs. low genetic differentiation in Nouelia insignis (Asteraceae), a narrowly distributed and endemic species in China, revealed by ISSR fingerprinting. Annals of Botany, 98(3), 583–589. https://doi.org/10.1093/aob/mcl129
52. Luan, S., Chiang, T. Y., & Gong, X. (2006). High genetic diversity vs. low genetic differentiation in Nouelia insignis (Asteraceae), a narrowly distributed and endemic species in China, revealed by ISSR fingerprinting. Annals of Botany, 98(3), 583–589. https://doi.org/10.1093/aob/mcl129
53. Mursyidin, D. H. (2023). Phenotypic diversity of super local durian (Durio zibethinus Murr.) varieties from South Kalimantan,Indonesia: A case study. Yuzuncu Yil University Journal of Agricultural Sciences, 33(2), 259-268. https://doi.org/10.29133/yyutbd.1249017
54. Mursyidin, D. H. (2023). Phenotypic diversity of super local durian (Durio zibethinus Murr.) varieties from South Kalimantan,Indonesia: A case study. Yuzuncu Yil University Journal of Agricultural Sciences, 33(2), 259-268. https://doi.org/10.29133/yyutbd.1249017
55. Mursyidin, D. H., & Daryono, B. S. (2016). Genetic diversity of local durian (Durio zibethinus Murr.) cultivars of South Kalimantan’s province based on RAPD markers. AIP Conference Proceedings, 1755, 040008-1-040008–7. https://doi.org/10.1063/1.4958483
56. Mursyidin, D. H., & Daryono, B. S. (2016). Genetic diversity of local durian (Durio zibethinus Murr.) cultivars of South Kalimantan’s province based on RAPD markers. AIP Conference Proceedings, 1755, 040008-1-040008–7. https://doi.org/10.1063/1.4958483
57. Mursyidin, D. H., Nazari, Y. A., Badruzsaufari, & Masmitra, M. R. D. (2021). DNA barcoding of the tidal swamp rice (Oryza sativa) landraces from South Kalimantan, Indonesia. Biodiversitas Journal of Biological Diversity, 22(4), 1593–1599. https://doi.org/10.13057/biodiv/d220401
58. Mursyidin, D. H., Nazari, Y. A., Badruzsaufari, & Masmitra, M. R. D. (2021). DNA barcoding of the tidal swamp rice (Oryza sativa) landraces from South Kalimantan, Indonesia. Biodiversitas Journal of Biological Diversity, 22(4), 1593–1599. https://doi.org/10.13057/biodiv/d220401
59. Mursyidin, D. H., Nazari, Y. A., & Daryono, B. S. (2017). Tidal swamp rice cultivars of South Kalimantan Province, Indonesia: A case study of diversity and local culture. Biodiversitas Journal of Biological Diversity, 18(1), 427–432. https://doi.org/10.13057/biodiv/d180156
60. Mursyidin, D. H., Nazari, Y. A., & Daryono, B. S. (2017). Tidal swamp rice cultivars of South Kalimantan Province, Indonesia: A case study of diversity and local culture. Biodiversitas Journal of Biological Diversity, 18(1), 427–432. https://doi.org/10.13057/biodiv/d180156
61. Mustafa, K. M., Ewadh, M. J., Al-Shuhaib, M. B. S., & Hasan, H. G. (2018). The in silico prediction of the chloroplast maturase k gene polymorphism in several barley varieties. Agriculture, 64(1), 3–16. https://doi.org/10.2478/agri-2018-0001
62. Mustafa, K. M., Ewadh, M. J., Al-Shuhaib, M. B. S., & Hasan, H. G. (2018). The in silico prediction of the chloroplast maturase k gene polymorphism in several barley varieties. Agriculture, 64(1), 3–16. https://doi.org/10.2478/agri-2018-0001
63. Nei, M., & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases (molecular evolution/mitochondrial DNA/nucleotide diversity). PNAS, 76(10), 5269–5273.
64. Nei, M., & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases (molecular evolution/mitochondrial DNA/nucleotide diversity). PNAS, 76(10), 5269–5273.
65. Rizaty, M. A. (2021). National production of durian [Produksi durian nasional]. Available in https://databoks.katadata.co.id/datapublish/2021/06/23/produksi-durian-di-indonesia-menurun-pada-2020 (Accessed September 2022).
66. Rizaty, M. A. (2021). National production of durian [Produksi durian nasional]. Available in https://databoks.katadata.co.id/datapublish/2021/06/23/produksi-durian-di-indonesia-menurun-pada-2020 (Accessed September 2022).
67. Santoso, P. J., Indriyani, N. L. P., Istianto, M., Pancoro, A., & Aryantha, I. N. P. (2017). Phylogeny of Indonesian durian (Durio sp.) germplasm based on polymorphism of ITS-nrDNA sequences. Acta Horticulturae, 1186(), 35–41. https://doi.org/10.17660/ActaHortic.2017.1186.5
68. Santoso, P. J., Indriyani, N. L. P., Istianto, M., Pancoro, A., & Aryantha, I. N. P. (2017). Phylogeny of Indonesian durian (Durio sp.) germplasm based on polymorphism of ITS-nrDNA sequences. Acta Horticulturae, 1186(), 35–41. https://doi.org/10.17660/ActaHortic.2017.1186.5
69. Slobodian, V., & Pastana, M. N. L. (2020). Monophyletic. In: Encyclopedia of Animal Cognition and Behavior, Springer International Publishing, Cham, Switzerland.
70. Slobodian, V., & Pastana, M. N. L. (2020). Monophyletic. In: Encyclopedia of Animal Cognition and Behavior, Springer International Publishing, Cham, Switzerland.
71. Stoltzfus, A., & Norris, R. W. (2016). On the causes of evolutionary transition:transversion bias. Molecular Biology and Evolution, 33(3), 595–602. https://doi.org/10.1093/molbev/msv274
72. Stoltzfus, A., & Norris, R. W. (2016). On the causes of evolutionary transition:transversion bias. Molecular Biology and Evolution, 33(3), 595–602. https://doi.org/10.1093/molbev/msv274
73. Suriani, C., Prasetya, E., Harsono, T., Manurung, J., Prakasa, H., Handayani, D., Jannah, M., & Rachmawati, Y. (2021). DNA barcoding of andaliman (Zanthoxylum acanthopodium DC) from North Sumatra province of Indonesia using maturase K gene. Tropical Life Sciences Research, 32(2), 15–28. https://doi.org/10.21315/tlsr2021.32.2.2
74. Suriani, C., Prasetya, E., Harsono, T., Manurung, J., Prakasa, H., Handayani, D., Jannah, M., & Rachmawati, Y. (2021). DNA barcoding of andaliman (Zanthoxylum acanthopodium DC) from North Sumatra province of Indonesia using maturase K gene. Tropical Life Sciences Research, 32(2), 15–28. https://doi.org/10.21315/tlsr2021.32.2.2
75. Swarup, S., Cargill, E. J., Crosby, K., Flagel, L., Kniskern, J., & Glenn, K. C. (2021). Genetic diversity is indispensable for plant breeding to improve crops. Crop Science, 61(2), 839–852. https://doi.org/10.1002/csc2.20377
76. Swarup, S., Cargill, E. J., Crosby, K., Flagel, L., Kniskern, J., & Glenn, K. C. (2021). Genetic diversity is indispensable for plant breeding to improve crops. Crop Science, 61(2), 839–852. https://doi.org/10.1002/csc2.20377
77. Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120
78. Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120
79. Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2002). Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, 00(1), 2.3.1-2.3.22. https://doi.org/10.1002/0471250953.bi0203s00
80. Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2002). Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, 00(1), 2.3.1-2.3.22. https://doi.org/10.1002/0471250953.bi0203s00
81. Tosh, J., James, K., Rumsey, F., Crookshank, A., Dyer, R., & Hopkins, D. (2016). Is DNA barcoding child’s play? Science education and the utility of DNA barcoding for the discrimination of UK tree species. Botanical Journal of the Linnean Society, 181, 711–722.
82. Tosh, J., James, K., Rumsey, F., Crookshank, A., Dyer, R., & Hopkins, D. (2016). Is DNA barcoding child’s play? Science education and the utility of DNA barcoding for the discrimination of UK tree species. Botanical Journal of the Linnean Society, 181, 711–722.
83. Tsukaya, H. (2017). Leaf shape diversity with an emphasis on leaf contour variation, developmental background, and adaptation. Seminars in Cell and Developmental Biology, 79, 48–57. https://doi.org/10.1016/j.semcdb.2017.11.035
84. Tsukaya, H. (2017). Leaf shape diversity with an emphasis on leaf contour variation, developmental background, and adaptation. Seminars in Cell and Developmental Biology, 79, 48–57. https://doi.org/10.1016/j.semcdb.2017.11.035
85. Turner-Hissong, S. D., Mabry, M. E., Beissinger, T. M., Ross-Ibarra, J., & Pires, J. C. (2020). Evolutionary insights into plant breeding. Current Opinion in Plant Biology, 54, 93–100. https://doi.org/10.1016/j.pbi.2020.03.003
86. Turner-Hissong, S. D., Mabry, M. E., Beissinger, T. M., Ross-Ibarra, J., & Pires, J. C. (2020). Evolutionary insights into plant breeding. Current Opinion in Plant Biology, 54, 93–100. https://doi.org/10.1016/j.pbi.2020.03.003
87. Uji, T. (2005). Keanekaragaman jenis dan sumber plasma nutfah Durio (Durio spp.) di Indonesia. Buletin Plasma Nutfah, 11(1), 28–33.
88. Uji, T. (2005). Keanekaragaman jenis dan sumber plasma nutfah Durio (Durio spp.) di Indonesia. Buletin Plasma Nutfah, 11(1), 28–33.
89. van Huylenbroeck, J. (2018). Handbook of Plant Breeding: Ornamental crops. Springer International Publishing AG, Cham, Switzerland.
90. van Huylenbroeck, J. (2018). Handbook of Plant Breeding: Ornamental crops. Springer International Publishing AG, Cham, Switzerland.
91. Wilberg, E. W. (2015). What’s in an outgroup? the impact of outgroup choice on the phylogenetic position of Thalattosuchia (Crocodylomorpha) and the origin of Crocodyliformes. Systematic Biology, 64(4), 621–637. https://doi.org/10.1093/sysbio/syv020
92. Wilberg, E. W. (2015). What’s in an outgroup? the impact of outgroup choice on the phylogenetic position of Thalattosuchia (Crocodylomorpha) and the origin of Crocodyliformes. Systematic Biology, 64(4), 621–637. https://doi.org/10.1093/sysbio/syv020
93. Wilcove, D. S., Giam, X., Edwards, D. P., Fisher, B., & Koh, L. P. (2013). Navjot’s nightmare revisited: Logging, agriculture, and biodiversity in Southeast Asia. Trends in Ecology and Evolution, 28(9), 531–540. https://doi.org/10.1016/j.tree.2013.04.005
94. Wilcove, D. S., Giam, X., Edwards, D. P., Fisher, B., & Koh, L. P. (2013). Navjot’s nightmare revisited: Logging, agriculture, and biodiversity in Southeast Asia. Trends in Ecology and Evolution, 28(9), 531–540. https://doi.org/10.1016/j.tree.2013.04.005
95. Wintle, B. A., Kujala, H., Whitehead, A., Cameron, A., Veloz, S., Kukkala, A., Moilanen, A., Gordon, A., Lentini, P. E., Cadenhead, N. C. R., & Bekessy, S. A. (2019). Global synthesis of conservation studies reveals the importance of small habitat patches for biodiversity. Proceedings of the National Academy of Sciences, 116(3), 909–914. https://doi.org/ 10.1073/pnas.1813051115
96. Wintle, B. A., Kujala, H., Whitehead, A., Cameron, A., Veloz, S., Kukkala, A., Moilanen, A., Gordon, A., Lentini, P. E., Cadenhead, N. C. R., & Bekessy, S. A. (2019). Global synthesis of conservation studies reveals the importance of small habitat patches for biodiversity. Proceedings of the National Academy of Sciences, 116(3), 909–914. https://doi.org/ 10.1073/pnas.1813051115
97. Wu, F., Ma, S., Zhou, J., Han, C., Hu, R., Yang, X., Nie, G., & Zhang, X. (2021). Genetic diversity and population structure analysis in a large collection of white clover (Trifolium repens L.) germplasm worldwide. PeerJ, 9, 1–17. https://doi.org/10.7717/peerj.11325
98. Wu, F., Ma, S., Zhou, J., Han, C., Hu, R., Yang, X., Nie, G., & Zhang, X. (2021). Genetic diversity and population structure analysis in a large collection of white clover (Trifolium repens L.) germplasm worldwide. PeerJ, 9, 1–17. https://doi.org/10.7717/peerj.11325
99. Zumajo-Cardona, C., Vasco, A., & Ambrose, B. A. (2019). The evolution of the KANADI gene family and leaf development in lycophytes and ferns. Plants, 8(9), 1–11. https://doi.org/10.3390/plants8090313
100. Zumajo-Cardona, C., Vasco, A., & Ambrose, B. A. (2019). The evolution of the KANADI gene family and leaf development in lycophytes and ferns. Plants, 8(9), 1–11. https://doi.org/10.3390/plants8090313