Phylogeny and biogeography of the genus Hesperis (Brassicaceae, tribe Hesperideae) inferred from nuclear ribosomal DNA sequence data

Abstract

Despite its complicated taxonomy, the genus Hesperis has not yet been subjected to any detailed molecular phylogenetic study and little is known about its monophyly, origin and biogeographical history, as well as the evolution of morphological characters. Here, we present for the first time comprehensive molecular analyses (nuclear ribosomal ITS sequences) of approximately 40 Hesperis species which represent the full range of morphological variation and the entire geographic distribution area of the genus. Based on our results, monophyly of the genus Hesperis has been proved. Moreover, our phylogenetic analysis shows that almost all traditionally defined sections are not monophyletic. NeighborNet network analysis was performed in order to visualize conflicting phylogenetic signals. The split-graph corresponds to the major clades represented in the consensus tree and revealed a hybridization signal in the evolutionary history of only a single Hesperis species. Divergence time estimations indicate that the origin of Hesperis (7.66–19.9 Mya) coincides with the expansion of grasslands and the closure of the proto-Mediterranean Sea in the middle Miocene. Therefore, diversification within Hesperis was affected by global climate changes, substantial tectonic rearrangements and the expansion of open vegetation systems in the Miocene, all of which had a great impact on the speciation history of the Irano-Turanian flora and fauna. Furthermore, two new species from West of Iran are described and illustrated here. They are readily distinguished from their closely related species by morphological characters such as stem height, leaf shape, pedicel, sepal and fruit indumentum, petal size, stigma shape and seed characters.

This is a preview of subscription content, access via your institution.

Fig. 1

modified from world editable PowerPoint available at https://www.presentationmagazine.com/editable-maps

Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE T Automat Contr 19:716–723

    Article  Google Scholar 

  2. Al-Shehbaz IA (1984) The tribes of Cruciferae (Brassicaceae) in the southeastern United States. J Arnold Arbor 65:343–373

    Google Scholar 

  3. Al-Shehbaz IA (1988) The genera of Anchonieae (Hesperideae) (Cruciferae; Brassicaceae), in the southeastern United States. J Arnold Arbor 69:193–212

    Article  Google Scholar 

  4. Al-Shehbaz IA (2012) A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61:931–954

    Article  Google Scholar 

  5. Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Pl Syst Evol 259:89–120. https://doi.org/10.1007/s00606-006-0415-z

    Article  Google Scholar 

  6. Ansell SW, Schneider H, Pedersen N, Grundmann M, Russell SJ, Vogel JC (2007) Recombination diversifies chloroplast trnF pseudogenes in Arabidopsis lyrata. J Evol Biol 29:2400–2411. https://doi.org/10.1111/j.1420-9101.2007.01397.x

    CAS  Article  Google Scholar 

  7. Appel O, Al-Shehbaz IA (2003) Cruciferae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants, vol. 5. Springer, Berlin, pp 75–174

    Google Scholar 

  8. Aras S, Duran A, Yenilmez G, Duman DC (2009) Genetic relationships among some Hesperis L. (Brassicaceae) species from Turkey assessed by RAPD analysis. Afr J Biotechnol 8:3128–3134

    CAS  Google Scholar 

  9. Behrensmeyer AK, Damuth J, DiMichele W, Potts R, Sues HD, Wing S (1992) Terrestrial ecosystems through time. University of Chicago Press, Chicago

    Google Scholar 

  10. Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. Amer J Bot 93:607–619. https://doi.org/10.3732/ajb.93.4.607

    CAS  Article  Google Scholar 

  11. Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg EA (2008) Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: tribes and trichomes revisited. Amer J Bot 95:1307–1327

    CAS  Article  Google Scholar 

  12. Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci USA 107:18724–18728. https://doi.org/10.1073/pnas.0909766107

    Article  PubMed  PubMed Central  Google Scholar 

  13. Boissier E (1867) Flora orientalis, vol 1. https://doi.org/10.5962/bhl.title.20323

  14. Bortolussi N, Durand E, Blum M, François O (2006) apTreeshape: statistical analysis of phylogenetic tree shape. Bioinformatics 22:363–364. https://doi.org/10.1093/bioinformatics/bti798

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Bosch JA, Heo K, Sliwinski MK, Baum DA (2008) An exploration of LEAFY expression in independent evolutionary origins of rosette flowering in Brassicaceae. Amer J Bot 95:286–293

    Article  Google Scholar 

  16. Bowman JL (2006) Molecules and morphology: comparative developmental genetics of the Brassicaceae. Pl Syst Evol 259:199–215. https://doi.org/10.1007/s00606-006-0419-8

    CAS  Article  Google Scholar 

  17. Brochmann C (1992) Pollen and seed morphology of Nordic Draba (Brassicaceae): phylogenetic and ecological implications. Nordic J Bot 12:657–673

    Article  Google Scholar 

  18. Bryant D, Moulton V (2002) Neighbor net: an agglomerative method for the construction of planar phylogenetic networks. In: Guigó R, Gusfield D (eds) Algorithms in bioinformatics, WABI 2002, vol. LNCS 2452, pp 375–391

  19. Buckley CD (2012) Investigating cultural evolution using phylogenetic analysis: the origins and descent of the Southeast Asian tradition of warp Ikat weaving. PLoS ONE 7:e52064

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. Chazara O, Tixier-Boichard M, Morin V, Zoorob R, Bed’Hom B (2011) Organisation and diversity of the class II DM region of the chicken MHC. Molec Immunol 48:1263–1271

    CAS  Article  Google Scholar 

  21. Couvreur TLP, Franzke A, Al-Shehbaz IA, Bakker FT, Koch MA, Mummenhoff K (2010) Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Molec Biol Evol 27:55–71. https://doi.org/10.1093/molbev/msp202

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Crews TE, Blesh J, Culman SW, Hayes RC, Jensen ES, Mack MC, Peoples MB, Schipanski ME (2016) Going where no grains have gone before: From early to mid-succession. Agr Ecosyst Environm 223:223–238

    Article  Google Scholar 

  23. Crews TE, Rumsey B (2017) What agriculture can learn from native ecosystems in building soil organic matter: a review. Sustainability 9:578

    Article  CAS  Google Scholar 

  24. Cullen J (1965) Hesperis L. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands, vol. 1. Edinburgh University Press, Edinburgh, pp 452–460

    Google Scholar 

  25. Dariba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772. https://doi.org/10.1038/nmeth.2109

    CAS  Article  Google Scholar 

  26. Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H, Ali S, Yun DJ, Bressan RA, Zhu JK, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43:913–918

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Davis PH (1971) Distribution patterns in Anatolia with particular reference to endemism. In: Davis PH, Harper PC, Hedge IC (eds) Plant Life of south-west Asia. The Botanical Society of Edinburgh, Edinburgh, pp 15–27

    Google Scholar 

  28. Davis PH, Mill RR, Tan K (eds) (1988) Flora of Turkey and the East Aegean Islands, vol. 10. Edinburgh University Press, Edinburgh, pp 1–590

    Google Scholar 

  29. De Candolle AP (1821) Regni vegetabilis systema naturalle, vol. 2. Treuttel & Würtz, Paris

    Google Scholar 

  30. De Candolle AP (1824) Prodromus systematis naturalis Regni Vegetabilis, vol. 1. Treuttel & Würtz, Paris

    Google Scholar 

  31. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  32. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710. https://doi.org/10.1371/journal.pbio.0040088

    CAS  Article  Google Scholar 

  33. Duran A (2008) Two new species with pendulous fruits in Hesperis (Brassicaceae) from South Anatolia, Turkey. Novon 18:453–463. https://doi.org/10.3417/2006175

    Article  Google Scholar 

  34. Duran A (2009) Hesperis ozcelikii (Brassicaceae), a new species from Turkey. Ann Bot Fenn 46:577–584

    Article  Google Scholar 

  35. Duran A (2016) Hesperis L. A Taxonomic update of the Genus Hesperis in Turkey. In: Sanad SMK, Dašić P (eds) Proceedings of 5th international conference on agriculture, environment and biological sciences (ICAEBS-16), Thailand, Pattaya, pp 10–13. http://dx.doi.org/https://doi.org/10.17758/IAAST.A0416

  36. Duran A, Ocak A (2005) Hesperis turkmendaghensis (Sect. Hesperis) (Cruciferae/Brassicaceae), a new species from the Central Anatolia region, Turkey. Bot J Linn Soc 147:239–247. https://doi.org/10.1111/j.1095-8339.2005.00364.x

    Article  Google Scholar 

  37. Duran A, Ünal F, Pınar M (2003) The revision of the genus Hesperis L. in Turkey. TUBITAK Project Report (No: tbag 1748). Ankara, Turkey

  38. Dvořák F (1964) Some Remarks on Hesperis series Matronales in Caucasia and Transcaucasia. Phyton, Int J Exp Bot 11:93–101

    Google Scholar 

  39. Dvořák F (1966a) Hesperis luristanica Dvořák sp. nova. Ann Naturhist Mus Wien 69:29–33

    Google Scholar 

  40. Dvořák F (1966b) A contribution to the study of the evolution of Hesperis Series Matronales CVĚL. emend DVOŘÁK. Feddes Repert 73:94–99. https://doi.org/10.1002/fedr.19660730205

    Article  Google Scholar 

  41. Dvořák F (1966c) Hesperis pycnotricha Borb. et Deg. further diploid species of the Hesperis Section. Preslia 38:245–248

    Google Scholar 

  42. Dvořák F (1968) Hesperis L. In: Rechinger KH (ed) Flora Iranica, vol. 57. Akademische Druck-u, Verlagsanstalt, Graz, pp 266–274

  43. Dvořák F (1973) Infrageneric classification of Hesperis L. Feddes Repert 84:259–271. https://doi.org/10.1002/fedr.19730840402

    Article  Google Scholar 

  44. Dvořák F, Dadákova B (1976) The chromosome morphology of Hesperis matronalis subsp. matronalis and related diploid taxa. Folia Geobot Phytotax 11:313–326. https://doi.org/10.1007/BF02909479

    Article  Google Scholar 

  45. Eldridge T, Łangowski Ł, Stacey N, Jantzen F, Moubayidin L, Sicard A, Southam P, Kennaway R, Lenhard M, Coen ES, Østergaard L (2016) Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy. Development 143:3394–3406

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Erdtman G (1952) Pollen morphology and plant taxonomy. Angiosperms. Almqvist and Wiksell, Stockholm, pp 1–539

    Google Scholar 

  47. Eslami-Farouji A, Khodayari H, Assadi M, Özüdoğru B, Çetin Ö, Mummenhoff K, Bhattacharya S (2018a) Numerical taxonomy contributes to delimitation of Iranian and Turkish Hesperis L. (Brassicaceae) species. Phytotaxa 367:101–119. https://doi.org/10.11646/phytotaxa.367.2.1

    Article  Google Scholar 

  48. Eslami-Farouji A, Khodayari H, Assadi M (2018b) Taxonomic significance of pollen and seed micromorphology in the genus Hesperis L. (brassicaceae). Iran J Bot 24:91–104

    Google Scholar 

  49. Ezhova TA, Penin AA (2001) A new BRACTEA (BRA) gene controlling the formation of an intermediate bractless inflorescence in Arabidosis thaliana. Russ J Genet 37:772–775

    CAS  Article  Google Scholar 

  50. Faegri K, Iversen J (1975) Textbook of pollen analysis, vol. 3. Munksgaard, Copenhagen

    Google Scholar 

  51. Fournier E (1868) Monographie du genre Hesperis. Bull Soc Bot France 13:326–362

    Article  Google Scholar 

  52. Franzke A, German DA, Al-Shehbaz IA, Mummenhoff K (2009) Arabidopsis family ties: molecular phylogeny and age estimates in Brassicaceae. Taxon 58:425–437

    Article  Google Scholar 

  53. Franzke A, Koch MA, Couvreur TLP, Lysak MA, Mummenhoff K (2010) On the age of the mustard family (Brassicaceae). Nature 467:755

    Google Scholar 

  54. Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K (2011) Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Pl Sci 16:108–116. https://doi.org/10.1016/j.tplants.2010.11.005

    CAS  Article  Google Scholar 

  55. Franzke A, Koch MA, Mummenhoff K (2016) Turnip time travels: age estimates in Brassicaceae. Trends Pl Sci 21:554–561. https://doi.org/10.1016/j.tplants.2016.01.024

    CAS  Article  Google Scholar 

  56. German DA (2012) Taxonomical confusions in the Cruciferae of North and Central Asia. III. Hesperis flava and Hesperis rupestris. Turczaninowia 15:9–18

    Google Scholar 

  57. German DA, Al-Shehbaz IA (2018) A reconsideration of Pseudofortuynia and Tchihatchewia as synonyms of Sisymbrium and Hesperis, respectively (Brassicaceae). Phytotaxa 334:95–98. https://doi.org/10.11646/phytotaxa.334.1.17

    Article  Google Scholar 

  58. German DA, Friesten N, Neuffer B, Al-Shehbaz IA, Hurka H (2009) Contribution to ITS phylogeny of the Brassicaceae, with special reference to some Asian taxa. Pl Syst Evol 283:33–56. https://doi.org/10.1007/s00606-009-0213-5

    Article  Google Scholar 

  59. Glover JD, Culman SW, DuPont ST, Broussard W, Young L, Mangan ME, Mai JG, Crews TE, DeHaan LR, Buckley DH, Ferris H (2010) Harvested perennial grasslands provide ecological benchmarks for agricultural sustainability. Agr Ecosyst Environm 137:3–12

    Article  Google Scholar 

  60. Gök R, Sandvol E, Türkelli N, Seber D, Barazangi M (2003) Sn attenuation in the Anatolian and Iranian plateau and surrounding regions. Geophys Res Lett 30:8042

    Google Scholar 

  61. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    PubMed  Article  PubMed Central  Google Scholar 

  62. Guo YL, Bechsgaard JS, Slotte T, Neuffer B, Lascoux M, Weigel D, Schierup MH (2009) Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc Natl Acad Sci USA 106:5246–5251. https://doi.org/10.1073/pnas.0808012106

    Article  PubMed  PubMed Central  Google Scholar 

  63. Guo X, Liu J, Hao G, Zhang L, Mao K, Wang X, Zhang D, Ma T, Hu Q, Al-Shehbaz IA, Koch MA (2017) Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics 18:176. https://doi.org/10.1186/s12864-017-3555-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395. https://doi.org/10.1038/nature06877

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Harley MM (1992) The potential value of pollen morphology as an additional taxonomic character in subtribe Ociminae (Ocimeae, Nepetoideae, Labiatae). In: Harley RM, Reynolds T (eds) Advances in Labiatae science. Royal Botanic Gardens, Kew, pp 125–138

    Google Scholar 

  66. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  67. Harzhauser M, Piller WE (2007) Benchmark data of a changing sea—palaeogeography, palaeobiogeography and events in the Central Paratethys during the Miocene. Palaeogeogr Palaeoclimatol 253:8–31

    Article  Google Scholar 

  68. Hayek A (1911) Entwurf eines Cruciferen Systems auf phylogenetischer Grundlage. Beih Bot Centralbl 27:127–335

    Google Scholar 

  69. Hedge IC (1968) Pseudofortuynia Hedge. In: Rechinger KH (ed) Flora Iranica, vol. 57. Akademische Druck-u, Verlagsanstalt, Graz, pp 56–57

  70. Hedge IC (1976) A systematic and geographical survey of the old World cruciferae. In: Vaughn JG, MacLeod AJ, Jones BMG (eds) The biology and chemistry of the Cruciferae. Academic Press, London, pp 1–45

    Google Scholar 

  71. Hempel FD, Feldman LJ (1994) Bi-directional inflorescence development in Arabidopsis thaliana: Acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192:276–286

    Article  Google Scholar 

  72. Hloušková P, Mandáková T, Pouch M, Trávníček P, Lysak MA (2019) The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing. Ann Bot (Oxford) 124:103–120. https://doi.org/10.1093/aob/mcz036

    CAS  Article  Google Scholar 

  73. Hohmann N, Wolf EM, Lysak MA, Koch MA (2015) A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Pl Cell 27:2770–2784. https://doi.org/10.1105/tpc.15.00482

    CAS  Article  Google Scholar 

  74. Holmgren PK, Holmgren NH, Barnett LC (1990) Index Herbariorum, part 1: the Herbaria of the World. New York Botanical Garden for the International Association for Plant Taxonomy, New York

  75. Huang CH, Sun R, Hu Y, Zeng L, Zhang N, Cai L, Zhang Q, Koch MA, Al-Shehbaz IA, Edger PP, Pires JC, Tan DY, Zhong Y, Ma H (2016) Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Molec Biol Evol 33:394–412. https://doi.org/10.1093/molbev/msv226

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. Huang XC, German DA, Koch MA (2019) Temporal patterns of diversification in Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization events. Ann Bot (Oxford) 125:29–47. https://doi.org/10.1093/aob/mcz123

    CAS  Article  Google Scholar 

  77. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molec Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. IUCN (2016) The IUCN red list of threatened species. http://www.iucnredlist.org. Accessed 24 Sep 2016

  79. Janchen E (1942) Das system der Cruciferen. Österr Bot Zeit 91:1–28. https://doi.org/10.1007/BF01257342

    Article  Google Scholar 

  80. Kagale S, Robinson SJ, Nixon J, Xiao R, Huebert T, Condie J, Kessler D, Clarke WE, Edger PP, Links MG, Sharpe AG, Parkin IAP (2014) Polyploid evolution of the Brassicaceae during the Cenozoic era. Pl Cell 26:2777–2791

    CAS  Article  Google Scholar 

  81. Karl R, Koch MA (2013) A world-wide perspective on crucifer speciation and evolution: phylogenetics, biogeography and trait evolution in tribe Arabideae. Ann Bot (Oxford) 112:983–1001

    Article  Google Scholar 

  82. Katoh K, Firth MC (2012) Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics 28:3144–3146. https://doi.org/10.1093/bioinformatics/bts578

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  84. Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108

    CAS  Article  PubMed Central  Google Scholar 

  85. Kell DB (2011) Breeding crop plants with deep roots: Their role in sustainable carbon, nutrient and water sequestration. Ann Bot (Oxford) 108:407–418

    CAS  Article  Google Scholar 

  86. Kiefer M, Schmickl R, German DA, Mandáková T, Lysak MA, Al-Shehbaz IA, Franzke A, Mummenhoff K, Stamatakis A, Koch MA (2014) BrassiBase: introduction to a novel knowledge database on Brassicaceae evolution. Plant Cell Physiol 55(1–9):e3

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  87. Khosravi AR (2003) A reconsideration of Hesperis leucoclada Boiss. (Cruciferae). Iran J Bot 10:15–23

    Google Scholar 

  88. Khosravi AR, Mohsenzadeh S, Mummenhoff K (2009) Phylogenetic relationships of old world Brassicaceae from Iran based on nuclear ribosomal DNA sequences. Biochem Syst Ecol 37:106–115. https://doi.org/10.1016/j.bse.2009.01.010

    CAS  Article  Google Scholar 

  89. Koch MA, Kiefer M, German DA, Al-Shehbaz IA, Franzke A, Mummenhoff K, Schmickl R (2012) BrassiBase: Tools and biological resources to study characters and traits in the Brassicaceae–version 1.1. Taxon 61:1001–1009

    Article  Google Scholar 

  90. Koes RE, Verweij CW, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Pl Sci 5:236–242

    Article  CAS  Google Scholar 

  91. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Pl J 61:909–921. https://doi.org/10.1111/j.1365-313X.2009.04086.x

    CAS  Article  Google Scholar 

  92. Koul KK, Nagpal R, Raina SN (2000) Seed coat microsculpturing in Brassica and allied genera (subtribe Brassicinae, Raphaninae, Moricandiinae). Ann Bot (Oxford) 86:385–397

    Article  Google Scholar 

  93. Łangowski Ł, Stacey N, Østergaard L (2016) Diversification of fruit shape in the Brassicaceae family. Pl Reprod 29:149–163

    Article  CAS  Google Scholar 

  94. Long J, Barton MK (2000) Initiation of axillary and floral meristems in Arabidopsis. Developm Biol 218:341–353

    CAS  Article  Google Scholar 

  95. Manafzadeh S, Salvo, G, Conti E (2013) A tale of migrations from east to west: The Irano-Turanian floristic region as a source of Mediterranean xerophytes. J Biogeogr 1–14

  96. Manafzadeh S, Staedler YM, Conti E (2016) Visions of the past and dreams of the future in the Orient: the Irano-Turanian region from classical botany to evolutionary studies. Biol Rev Cambridge Philos Soc 92:1365–1388

    PubMed  Article  PubMed Central  Google Scholar 

  97. Mandáková T, Hloušková P, German DA, Lysak MA (2017) Monophyletic origin and evolution of the largest Crucifer genomes. Plant Physiol 174:2062–2071. https://doi.org/10.1104/pp.17.00457

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  98. Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  99. Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retrov 21:98–102

    CAS  Article  Google Scholar 

  100. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1

  101. Matzke NJ (2014) Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Syst Biol 63:951–970

    PubMed  Article  PubMed Central  Google Scholar 

  102. Meulenkamp JE, Sissingh W (2003) Tertiary palaeogeography and tectonostratigraphic evolution of the northern and southern Peri-Tethys platforms and the intermediate domains of the African-Eurasian convergent plate boundary zone. Palaeogeogr Palaeoclimatol 196:209–228

    Article  Google Scholar 

  103. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), New Orleans, LA, 14 Nov 2010, pp 1–8. https://doi.org/10.1109/gce.2010.5676129

  104. Mohammadin S, Peterse K, van de Kerke SJ, Chatrou LW, Dönmez AA, Mummenhoff K, Pires JC, Edger PP, Al-Shehbaz IA, Schranz ME (2017) Anatolian origins and diversification of Aethionema, the sister lineage of the core Brassicaceae. Amer J Bot 104:1042–1054

    Article  Google Scholar 

  105. Mummenhoff K, Polster A, Mühlhausen A, Theißen G (2009) Lepidium as a model system for studying the evolution of fruit development in Brassicaceae. J Exp Bot 60:1503–1513. https://doi.org/10.1093/jxb/ern304

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  106. Neill IC, Meliksetian K, Allen MB, Navasardyan G, Kuiper K (2015) Petrogenesis of mafic collision zone magmatism: the Armenian sector of the Turkish–Iranian Plateau. Chem Geol 403:24–41

    CAS  Article  Google Scholar 

  107. Nikolov LA (2019) Brassicaceae flowers: diversity amid uniformity J Exp Bot 3–13. doi:https://doi.org/10.1093/jxb/erz079

  108. Nikolov LA, Tsiantis M (2017) Using mustard genomes to explore the genetic basis of evolutionary change. Curr Opin Pl Biol 36:119–128

    CAS  Article  Google Scholar 

  109. Nikolov LA, Shushkov P, Nevado B, Gan X, Al-Shehbaz IA, Filatov D, Bailey CD, Tsiantis M (2019) Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytol 222:1638–1651. https://doi.org/10.1111/nph.15732

    Article  PubMed  PubMed Central  Google Scholar 

  110. Özüdoğru B, Akaydın G, Erik S, Al-Shehbaz IA, Mummenoff K (2015) Phylogeny, diversification, and biogeographic implications of the eastern Mediterranean endemic genus Ricotia (Brassicaceae). Taxon 64:727–740

    Article  Google Scholar 

  111. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  112. Penin AA (2008) Bract reduction in Cruciferae: possible genetic mechanisms and evolution. Wulfenia 15:63–73

    Google Scholar 

  113. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. https://doi.org/10.1080/10635150490522304

    Article  PubMed  PubMed Central  Google Scholar 

  114. Prantl K (1891) Cruciferae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien 3 (2). Engelmann, Leipzig, pp 145–206

    Google Scholar 

  115. Punt W, Hoen PP, Blackmore S, Nilsson S, Thomas A (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palyno 143:1–81

    Article  Google Scholar 

  116. Rabosky DL (2006) LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol Bioinform Online 2:247–250

    Article  Google Scholar 

  117. Rahman M, Khatun A, Liu L, Bj B (2018) Brassicacaeae mustards: traditional and agronomic uses in Australia and New Zealand. Molecules 23:231. https://doi.org/10.3390/molecules23010231

    CAS  Article  PubMed Central  Google Scholar 

  118. Rambaut A, Drummond AJ (2007) Tracer v1.4. Available at: http://beast.bio.ed.ac.uk/Tracer. Accessed 5 Aug 2011

  119. Reilinger RE, McClusky SC, Oral MB, King RW, Toksoz MN, Barka AA, Kinik I, Lenk O, Sanli I (1997) Global positioning system measurements of present-day crustal movements in the Arabia–Africa–Eurasia plate collision zone. J Geophys 102(B5):9983–9999. https://doi.org/10.1029/96JB03736

    Article  Google Scholar 

  120. Rollins RC (1993) The cruciferae of continental North America. Stanford University Press, Stanford

    Google Scholar 

  121. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  122. Schulz OE (1936) Cruciferae. In: Engler A, Prand K (eds) Die natürlkhen Pflanzenfamilien, Cruciferae, 17B. Engelmann, Leipzig, pp 227–658

    Google Scholar 

  123. Şengör AMC, Yilmaz Y (1981) Tethyan evolution of Turkey: A plate tectonic approach. Tectonophysics 75:181–241. https://doi.org/10.1016/0040-1951(81)90275-4

    Article  Google Scholar 

  124. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, de Pamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Amer J Bot 96:336–348

    Article  Google Scholar 

  125. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  126. Suchard MA, Rambaut A (2009) Many-core algorithms for statistical phylogenetics. Bioinformatics 25:1370–1376

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. Swofford DL (2001) PAUP* Phylogenetic analysis using parsimony and other methods, version 4.0b10 (software). Sinauer Associates, Sunderland

  128. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for the amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152

    CAS  Article  Google Scholar 

  129. Takhtajan A (1986) Floristic regions of the world. University of California Press, Berkeley

    Google Scholar 

  130. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molec Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  131. Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE, Hinchliff CE, Brown JW, Sessa EB, Harmon LJ (2015) Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol 207:454–467

    PubMed  Article  PubMed Central  Google Scholar 

  132. Toro-Núñez O, Al-Shehbaz IA, Mort ME (2014) Phylogenetic study with nuclear and chloroplast data and ecological niche reveals Atacama (Brassicaceae), a new monotypic genus endemic from the Andes of the Atacama Desert, Chile. Pl Syst Evol 301:1377–1396. https://doi.org/10.1007/s00606-014-1157-y

    Article  Google Scholar 

  133. Tzvelev NN (1959) The genus Hesperis in USSR. Notulae systematicae ex Herbario Instituti Botanici Nomine V.L Komarovii Akademiae Scientiarum URSS 19:114–155

    Google Scholar 

  134. Warwick SI, Mummenhoff K, Sauder CA, Koch MA, Al-Shehbaz IA (2010) Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Pl Syst Evol 285:209–232. https://doi.org/10.1007/s00606-010-0271-8

    CAS  Article  Google Scholar 

  135. Warwick SI, Sauder CA, Al-Shehbaz IA, Jacquemoud F (2007) Phylogenetic relationships in the tribes Anchonieae, Chorisporeae, Euclidieae, and Hesperideae (Brassicaceae) based on nuclear ribo-somal ITS DNA sequences. Ann Missouri Bot Gard 94:56–78. https://doi.org/10.3417/0026-6493(2007)94[56:PRITTA]2.0.CO;2

    Article  Google Scholar 

  136. Warwick SI, Al-Shehbaz AI, Sauder CA, Murray DF, Mummenhoff K (2004) Phylogeny of Smelowskia and related genera (Brassicaceae) based on nuclear ITS DNA and chloroplast trnL intron DNA sequences. Ann Missouri Bot Gard 91:99–123

    Google Scholar 

  137. Wessinger CA, Rausher MD (2012) Lessons from flower colour evolution on targets of selection. J Exp Bot 63:5741–5749

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  138. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky j, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1

  139. Yu Y, Harris AJ, Blair C, He X (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Molec Phylogenet Evol 87:46–49

    PubMed  Article  PubMed Central  Google Scholar 

  140. Yule GU (1925) A mathematical theory of evolution, based on the conclusions of Dr.J.C. Willis. Philos Trans Roy Soc London B Biol Sci 213:21–87

    Article  Google Scholar 

  141. Zhang X, Liu T, Li X, Duan M, Wang J, Qiu Y, Wang H, Song J, Shen D (2016) Interspecific hybridization, polyploidization, and backcross of Brassica oleracea var. alboglabra with B. rapa var. purpurea morphologically recapitulate the evolution of Brassica vegetables. Sci Rep 6:18618. https://doi.org/10.1038/srep18618

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  142. Zhao D, Tao J (2015) Recent advances on the development and regulation of flower color in ornamental plants. Frontiers Pl Sci 6:261

    Google Scholar 

Download references

Acknowledgements

This project was carried out at Hacettepe University by the first author (AEF) who wishes to express her special thanks to Hacettepe University for providing financial support and lab facilities. The authors thank the curators of the following institutions: the Research Institute of Forests and Rangelands (TARI), the Herbarium of Shiraz University (HSHU), the Hacettepe University Herbarium (HUB), the Konya Herbarium (KNYA), the Royal Botanic Gardens, Kew (K) & the Herbarium Russian Academy of Sciences- V. L. Komarov Botanical institute (LE) for providing herbarium materials. We also appreciate Dr. Sara Manafzadeh´s advice in selecting the appropriate method in biogeographical studies and Dr. Ihsan Al-Shehbaz for preparing Caucasian plant materials for phylogenetic study and his valuable recommendations. Special thanks go to Dr. Dmitry A. German for his valuable comments on the taxonomic part of the paper, and also special thanks to Prof. Dr. Ahmad Reza Khosravi for his great cooperation in the study of Sisymbrium leucocladum specimens in Shiraz University Herbarium. Furthermore, we thank Robabeh Farahdust, the artist from the Central Herbarium of Iran for preparing the sketches of the new species. Finally, we would like to express our deep gratitude to Lucille Schmieding for her generous support in language edition.

Funding

Hacettepe University provided financial support and laboratory facilities; Lorestan University financially supported the SEM studies.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hamed Khodayari.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Availability of data and material

All data are available in manuscript or as Online Resources.

Ethics approval

Ethical approval and responsibilities are compiled in this submission.

Consent to participate

All authors consent to participate in this manuscript.

Consent for publication

All authors consent for publication of this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Nora Walden.

Electronic supplementary material

Information on Electronic Supplementary Materials

Information on Electronic Supplementary Materials

Online Resource 1. GenBank accession numbers for the sequences (ITS + trnL-F region) used in phylogenetic study.

Online Resource 2. DNA sequence alignments of ITS dataset of Hesperis specimens for the current study in NEXUS format.

Online Resource 3. DNA sequence alignments of trnL-F dataset of Hesperis specimens for the current study in NEXUS format.

Online Resource 4. List of the character states used in the Ancestral Character State Reconstruction analysis.

Online Resource 5. Statistical output of ancestral area reconstruction analysis based on (A) Bayesian Binary MCMC (BBM) and (B) BioGeoBears (BayAreaLike) of the genus Hesperis.

Online Resource 6. Bayesian 50% majority rule consensus tree inferred from the trnL-F dataset.

Online Resource 7. Hesperis ilamica. a Plant, b flower, c petal (frontal view), d long stamen, e short stamen, f outer sepal, g inner sepal, h fruit, i fruit apex (drawing prepared from TARI, No. 102982).

Online Resource 8. Hesperis bakhtiarica. a Plant, b inlorescence, c flower, d outer sepal, e inner sepal, f long stamen, g short stamen, h petal (frontal view), i fruit apex (drawing prepared from TARI, No. 59927).

Online Resource 9. Hesperis ilamica, sp. nov. a Habitat, b–c, e flower, d stigma, f–g herbarium specimens including holotypus.

Online Resource 10. General view and habitat of Hesperis bakhtiarica, sp. nov. a–b, d Herbarium specimens including holotypus, c flower, e habitat.

Online Resource 11. The SEM micrographs of Iranian Hesperis new species. a–i Hesperis bakhtiarica: a fruit, b leaf, c–d petal (dorsal and ventral, respectively), e stem, f stigma, g pollen grain, h–i seed; j–r H. ilamica: j fruit, k leaf, l–m petal (dorsal and ventral, respectively), n stem, o stigma, p pollen grain, q–r seed.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Eslami-Farouji, A., Khodayari, H., Assadi, M. et al. Phylogeny and biogeography of the genus Hesperis (Brassicaceae, tribe Hesperideae) inferred from nuclear ribosomal DNA sequence data. Plant Syst Evol 307, 17 (2021). https://doi.org/10.1007/s00606-020-01727-y

Download citation

Keywords

  • Ancestral area reconstruction
  • Brassicaceae
  • Divergence time estimation
  • Hesperis
  • Irano-Turanian floristic region
  • Morphology