Abstract
A phylogenetic survey of representatives from all New World and several Old World supraspecific groupings of Cleome, as well as from the closely related Podandrogyne and Polanisia, was conducted based on separate analysis of nuclear ribosomal ITS sequences and of morphological characters. Parsimony analysis of the molecular data recognized this group of cleomoid taxa as a strongly supported monophyletic lineage. Podandrogyne was imbedded within a highly supported Andinocleome clade, whereas Polanisia was placed as a member of a North American/Old World Cleome s. l. clade but with low support. The ITS data also indicated the sequential divergence of several basal Old World (sects. Cleome, Gymnogonia, Ranmanissa and Rutidosperma) and North American (subg. Physospermon, sect. Peritoma) lineages followed by more recent splittings of Central and South American lineages (the Andinocleome (sects. Pterosperma and Rimosperma) group, and sects. Melidiscus and Tarenaya). The morphological data showed extensive homoplasy and did not resolve the phylogeny of these cleomoids, although the cladistic analysis distinguished two poorly supported (subg. Eucleome and sect. Tarenaya) clades. Despite this, several sets of morphological and chromosomal secondary synapomorphies served to characterize the main sectional clades recovered in the molecular tree. Based on the strong support of the Cleome + Podandrogyne + Polanisia clade and the insufficient resolution and low support of the basal branches of this tree, and on the inherent homoplasy and unsatisfactory resolution of the morphological diagnostic traits used to characterize these taxa, a reunification of the three cleomoid genera under a large genus Cleome s. l. would be advisable. A biogeographical interpretation of our molecular phylogeny indicated and earlier origin of the ancestral Cleome lineages in the Old World, followed by colonization of North America and then a subsequent expansion towards central and South American with more recent secondary radiations in these subcontinents.
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Acknowledgments
We want to thank Hugh Iltis, Eric Schranz and Peter Stevens for their valuable comments and useful discussions on our phylogenetic study and for their critical review of our manuscript, Lupita Sánchez-Acebo (MO Bot. Gardens, USA) for providing us DNA accessions of Cleome and Polanisia, and D. Clark (COLO Herbarium, USA) and A. Ortega (University of Extremadura, Spain) for facilitating for us materials of C. serrulata and of C. violacea.
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Appendix
Appendix
Sources of taxa and materials used in the molecular (ITS code Genbank) and morphological study of Cleome and its close genera.
Cleome aculeata L. C. aculeata 1: Venezuela: Aragua: T. Ruiz 4973 (MY). DQ455780. C. aculeata 2: Venezuela: Trujillo: T. Ruiz y R. Villafañe 4989 (MY). C. aculeata 3: Bolivia: Santa Cruz: L. Sánchez 1117 (MO). DQ455781. Venezuela: Amazonas: Liesner 6844 (VEN). Venezuela: Amazonas: Stergios et al. 7998 (PORT). Venezuela: Amazonas: T.Ruiz 4008 (MY). Venezuela: Portuguesa: Aymard 96 (PORT). Venezuela: Portuguesa: Aymard 3131 (PORT). Venezuela: Portuguesa: Aymard y Ortega 1416 (PORT). Venezuela: Portuguesa: Aymard y Stergios 2572 (PORT). Venezuela: Monagas: Nee y Whalen 17174 (VEN ; WIS). Venezuela: Sucre: Cumana 867 (IRBR; VEN). Venezuela: Barinas: T. Ruiz 4311 (MY). Venezuela: Sucre: T. Ruiz y C.E. Benitez de Rojas 4589 (MY). Venezuela: Aragua: T. Ruiz y R. Villafañe 4776 (MY).
Cleome anomala Kunth. Venezuela: Táchira: T. Ruiz y L.Hernández 4980 (MY). DQ455782. Venezuela: Táchira: Bunting 2359 (MY). Venezuela: Táchira: Ruiz-Terán y Dugarte 15913 (MERF; MY). Venezuela: Táchira: T. Ruiz et al. 4711 (MY). Venezuela: Táchira: T. Ruiz et al. 4717 (MY).
Cleome arborea Kunth. C. Arborea 1: Venezuela: Mérida: T. Ruiz y L. Hernández 4981 (MY): DQ455783. C. arborea 2: Venezuela: Mérida: C.E. Benítez de Rojas 6371 (MY): DQ455784. Venezuela: Falcón: T. Ruiz y F. Rondón 3806 (MY). Venezuela: Falcón: T. Ruiz, F. Rondón y N. Mariño 4143 (MY). Venezuela: Mérida: A. Quintero 151 (MER). Venezuela: Mérida: J.G. Wessels Boer 1848 (MER). Venezuela: Mérida: A. Quintero et al. 1239 (MER). Venezuela: Mérida: Pannier 204 (MER; VEN). Venezuela: Mérida: T. Ruiz y R. Villafañe 4709 (MY). Venezuela: Mérida: C. Jeffrey, B. Trujillo y M. Condon 2214 (MY; VEN). Venezuela: Distrito Federal : B. Manara s/n (VEN). Venezuela: Distrito Federal: H. Pittier 9490 (VEN).
Cleome boliviensis H.H. Iltis. Bolivia: La Paz: L. Sánchez 1132 (MO): DQ455785.
Cleome briquetii Polhill. Tanzania: Kilimanjaro: J. Malangwa 285 (MO): DQ455786.
Cleome chapalaensis H.H. Iltis. México: Michoacán: H. H. Iltis et al. 832 (USZ) : DQ455800.
Cleome cordobensis Eichler ex Grisebach. Bolivia: Tarija: R. Ehrich 8 (LPB): DQ455787.
Cleome crenopetala DC. Brasil: Paraná: P. Dusen 7365 (MO): DQ455788.
Cleome diffusa Banks ex DC. Brasil: Bahia: R. Harley et al. 17276 (MO): DQ455789.
Cleome gynandra L. Venezuela: Aragua: T. Ruiz y L. Hernández 4974 (MY): DQ455790. Venezuela: Falcón: T. Ruiz y F. Rondón 3767 (MY). Venezuela: Falcón: T. Ruiz y C. Moreno 4084 (MY). Venezuela: Aragua: H. Rodríguez 954 (MY). Venezuela: Carabobo: B. Trujillo 15989 (MY). Venezuela: Nueva Esparta: T. Ruiz y C.E. Benítez de Rojas 4580 (MY). Venezuela: Sucre: A. Fernández 756 (PORT). Venezuela: Trujillo: M. Nee y S. Mori 4120 (VEN). Venezuela: Yaracuy: P. Martinez s/n (MY). Venezuela: Zulia: S. López Palacios 1806 (MER; MY). Venezuela: Carabobo: T. Ruiz y R. Villafañe 4707 (MY).
Cleome hassleriana Chodat. USA: St. Louis-Missouri: L. Sánchez s.n. (MO) : DQ455791.
Cleome lechleri Eichler. Bolivia: La Paz: L. Sánchez 1129 (MO): DQ455792. Venezuela: Táchira: Badillo et al. 7901 (MY).
Cleome lutea Hooker. AF137588.
Cleome microcarpa Ule. Brasil: Bahía: R. Harley 27228 (MO): DQ455793.
Cleome moritziana Klotzsch ex Eichler. Venezuela: Mérida: T. Ruiz y L. Hernández 4984 (MY): DQ455794. Venezuela: Aragua: Aristeguieta y Medina 2984 (VEN). Venezuela: Aragua: Steyermark y Liesner 121991 (VEN). Venezuela: Aragua: T. Ruiz y R. Villafañe 4703 (MY). Venezuela: Distrito Federal: L. Cárdenas 300 (MY). Venezuela: Mérida: Ruiz Terán 1632 (MER; MY). Venezuela: Mérida: Ruiz Terán 3939 (MER; MY). Venezuela: Mérida: Aymard y Ortega 1336 (MER; PORT). Venezuela: Miranda: R. Velasco 811 (MY). Venezuela: Trujillo: Aristeguieta y Medina 3665 (VEN). Venezuela: Trujillo: R. Rivero 1204 (PORT).
Cleome monophylla L. Senegal : Reserve de Bondia: A. Dniort 42 (MO): DQ455796.
Cleome multicaulis Sessé et Mociño ex DC. USA: Colorado: H. Iltis 4359: DQ455795.
Cleome paludosa Willdenow ex Eichler. Bolivia: Santa Cruz: L.Sánchez 1136 (MO): DQ455803.
Cleome parviflora Kunth. Bolivia: Santa Cruz: R. Guillen 5317: DQ455797. Venezuela: Apure: Steyermark et al. 101438 (VEN). Venezuela: Barinas: S. López Palacios 3125 (MERF). Venezuela: Delta Amacuro: Steyermark 93158 (VEN). Venezuela: Delta Amacuro: F.J. Breteler 3793 (VEN). Venezuela: Delta Amacuro: B. Trujillo et al. 17296 (MY). Venezuela: Zulia D. Díaz 30 (MY).
Cleome pernambucensis H.H. Iltis et Costa e Silva. Brasil: Pernambuco: Costa e Silva 1529 (MO): DQ455798.
Cleome pilosa Benth. Venezuela: Aragua: T. Ruiz 4720 (MY): DQ455799. Venezuela: Aragua: Badillo 3970 (MY). Venezuela: Aragua: T. Ruiz y C.E. Benítez de Rojas 4510 (MY). Venezuela: Distrito Federal: Aristeguieta 813 (VEN). Venezuela: Barinas: Oberwinkler 12824 (MER). Venezuela: Mérida: López-Palacios y Bautista 3476 (MER). Venezuela: Mérida: Aymard et al. 2055 (PORT). Venezuela: Mérida: Ruiz Terán y López-Figueira 631 (MERF; MY). Venezuela: Miranda: H. Pittier 11485 (VEN). Venezuela: Táchira: Badillo et al. 7805 (MY). Venezuela: Sucre: L. Cumana y P. Cabeza 2100 (IRBR).
Cleome rosea Vahl ex DC. Brasil: Río de Janeiro: Costa e Silva 1530 (MO): DQ4559801.
Cleome rutidosperma DC. Venezuela: Maracay T. Ruiz 4360 (MY): DQ455802. Francia: Guayana: B. Torke 217 (MO). Venezuela: Aragua: L. Cárdenas 3686 (MY). Venezuela: Anzoátegui L. Cumana 1434 (IRBR). Venezuela: Aragua: T. Ruiz 4991 (MY).
Cleome serrulata Pursh. USA: Colorado: D. Clark 1640 (COLO): DQ455804.
Cleome speciosa Rafinesque. Venezuela: Táchira: T. Ruiz y L. Hernández 4978 (MY): DQ455806. Venezuela: Táchira: M. Ramia 649 (VEN). Venezuela: Táchira: Baez 5 (VEN). Venezuela: Táchira: T. Ruiz y L. Hernández 4978 (MY). Venezuela: Táchira: Badillo et al. 7909 (MY). Venezuela: Táchira: Badillo et al. 7845 (MY). Venezuela: Táchira: Badillo et al. 7910 (MY). Venezuela: Portuguesa: Aymard et al. 4215 (PORT). Venezuela: Mérida: A. Quintero 1312 (MER). Venezuela: Mérida: Bernardi 3208 (MER).
Cleome spinosa Jacquin ssp. “spinosa”.Venezuela: Aragua: T. Ruiz 4702 (MY): DQ455807. Venezuela: Falcón: T. Ruiz y F. Rondón 3766 (MY). Venezuela: Falcón: T. Ruiz y F. Rondón 3709 (MY). Venezuela: Guárico: Aristeguieta y Agostini 6421 (MY). Venezuela: Barinas: Steyermark, Bunting y Blanco 102178 (VEN). Venezuela: Distrito Federal – Caracas: M. Nee y S. Mori 4023 (VEN). Venezuela: Bolívar: T. Ruiz y M. Ruiz 4706 (MY). Venezuela: Apure: M. Ramia y R. Montes 5301 (VEN). Venezuela: Aragua: G. Ferrari 418 (MY). Venezuela: Lara: G. Morillo y A. Pacheco 987 (VEN). Venezuela: Miranda: Bernardi 5884 (MER).
Cleome spinosa Jacquin ssp. “longicarpa” H.H. Iltis. Brasil: Pernambuco: Costa e Silva 1522 (MO): DQ4555808.
Cleome stenophylla Klotzsch ex Urban. Venezuela: Falcón: T. Ruiz y T. Ruiz 4122 (MY). Venezuela: Falcón: T. Ruiz y M. Ruiz 4110 (MY). Venezuela: Falcón: T. Ruiz y F. Rondón 4096 (MY). Venezuela: Falcón: T. Ruiz y R. Villafañe 4731 (MY). Venezuela: Carabobo: Trujillo y Sulbarán 16137 (MY). Venezuela: Nueva Esparta: C.E. Benítez de Rojas 1651 (MY). Venezuela: Zulia: G. Ferrari 357 (MY). Venezuela: Sucre: L. Cumana 2333 (MY). Venezuela: Zulia: Bunting, Aristeguieta y Heywood 5356 (VEN). Venezuela: Guárico: T. Ruiz y R. Villafañe 4987 (MY): DQ455814.
Cleome stylosa Eichler. Venezuela: Táchira: T. Ruiz y L. Hernández 4977 (MY): DQ455812. Venezuela: Táchira: T. Ruiz y L. Hernández 4976 (MY). Venezuela: Táchira: T. Ruiz y L. Hernández 4977 (MY). Venezuela: Mérida: Ricardi y Adamo 83 (MY; MERC). Venezuela: Mérida: Marcano-Berti, Valverde y Ramírez 982–089 (MER). Venezuela: Mérida: López-Palacios 1243 (MER).
Cleome titubans Spegazzini. Argentina: Buenos Aires: A. Krapovickas 2897 (MO): DQ455813.
Cleome torticarpa H.H. Iltis et Ruiz Zapata. Venezuela: Falcón: T. Ruiz y R. Villafañe 5011 (MY): DQ455810. Venezuela: Falcón: R. Wingfield 5879 (CORO). Venezuela: Falcón: T. Ruiz y T. Ruiz 4138 (MY). Venezuela: Falcón: T. Ruiz y T. Ruiz 4131 (MY). Venezuela: Falcón: T. Ruiz, R. Parra y N. Mariño 4057 (MY). Venezuela: Falcón: T. Ruiz y R. Villafañe 5011 (MY). Venezuela: Falcón: FF (HW, ES) 404 (CORO).
Cleome tucumanensis H.H. Iltis. Bolivia: Santa Cruz. L. Sánchez 1114 (USZ): DQ455811.
Cleome violacea L. C. violacea 1: Spain: Sevilla: El Ronquillo: A. Ortega Olivencia 7-4-06: DQ532098. C. Violacea 2: Spain: Sevilla: Guillena: A. Ortega Olivencia 7-4-06: DQ532099.
Cleome viridiflora Schreber. Venezuela: Barinas: Aristeguieta 2400 (VEN). Venezuela: Barinas: Barinitas: T. Ruiz y L. Hernández 4987 (MY): DQ455820. Venezuela: Sucre: Steyermark 62402 (VEN). Venezuela: Yaracuy: Diederichs 22 (VEN). Venezuela: Aragua: T. Ruiz 5010 (MY). México: Tabasco: Hubbuch sn. (MO): DQ455821. Botresearch (USA) Ind. Sem*82302 accno 61-135-9807: DQ455822.
Cleome viscosa L. Venezuela: Trujillo: T. Ruiz y R. Villafañe 4988 (MY): DQ455818. Venezuela: Portuguesa: T. Ruiz y L. Hernández 4963 (MY): DQ455819. Venezuela: Trujillo: T. Ruiz y R. Villafañe 4824 (MY). Venezuela: Portuguesa: T. Ruiz y C.E. Benítez de Rojas 4687 (MY). Venezuela: Aragua: T. Ruiz 4708 (MY). Venezuela: Trujillo: T. Ruiz y R. Villafañe 4988 (MY). Venezuela: Portuguesa: B. Stergios 6892 (PORT). Venezuela: Portuguesa: Aymard y Paredes 6219 (PORT). Venezuela: Portuguesa: Aymard y Stergios 2578 (PORT). Venezuela: Portuguesa: L. Cumana 2373 (IRBR). Venezuela: Guárico: M. Alagares s/n (MY).
Cleome werdermanni Ernst. Bolivia: Santa Cruz: L. Sánchez 1111a (MO): DQ455809.
Podandrogyne macrophylla (Turcz.) Woodson. Venezuela: Mérida: T. Ruiz y L. Hernández 4982 (MY): DQ455815.
Polanisia dodecandra (L.) DC. ssp. dodecandr a. USA: St. Louis-Missouri: P. Stevens s.n. (MO): DQ455816.
Polanisia dodecandra (L.) DC. ssp . trachysperma (Torr. et A. Gray) H.H. Iltis. Botresearch USA Ind. Sem.*82764 accno 67-4204-2077: DQ455817.
Arabidopsis thaliana (L.) Heynh. “columbia” ecotipo: Hall s.n. (WIS): AJ 232900.
Brassica nigra (L.) W.D.J. Koch. AF 128103.
Brassica rapa L. AF 128098.
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Inda, L.A., Torrecilla, P., Catalán, P. et al. Phylogeny of Cleome L. and its close relatives Podandrogyne Ducke and Polanisia Raf. (Cleomoideae, Cleomaceae) based on analysis of nuclear ITS sequences and morphology. Plant Syst Evol 274, 111–126 (2008). https://doi.org/10.1007/s00606-008-0026-y
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DOI: https://doi.org/10.1007/s00606-008-0026-y