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The phylogenetic significance of the stem morpho-anatomy in the Hylocereeae (Cactoideae, Cactaceae)

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Abstract

The Hylocereeae is a monophyletic group in which eight genera are recognized based on molecular data. However, relationships between the genera remain partially resolved. In this study, combined analyses of molecular and structural characters for Hylocereeae were carried out with the aims of finding structural synapomorphies that support the genera and to resolve relationships between them. We studied sixty-nine species of the eight genera of Hylocereeae, as well as six Echinocereeae species as outgroup using light microscopy and scanning electron microscopy. Thirty-six morpho-anatomical characters were incorporated into a matrix and analyzed in combination with sequences of four chloroplast DNA regions. Phylogenetic analyses using maximum parsimony, maximum likelihood, and Bayesian inference yielded a robust phylogenetic hypothesis and showed morphological synapomorphies. Four of the genera (Acanthocereus, Aporocactus, Epiphyllum, and Kimnachia) have at least one structural synapomorphy. Disocactus and Pseudorhipsalis can be recognized by a combination of characters, while Selenicereus and Weberocereus cannot be recognized by any structural vegetative character. There are structural synapomorphies that allow recognizing relationships between genera. The cortical and vascular characters are as important as the epidermal traits, a condition that had not been reported for another group within Cactaceae.

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Acknowledgements

Thanks to the Graduate Program in Biological Sciences of the National Autonomous University of Mexico, to the National Council of Science and Technology (CONACyT, 450665), to Alicia Rojas for assistance in the lab, to Yolanda Morales for assistance in the living collection of the Botanical Garden, UNAM, to María Berenit Mendoza Garfias for assistance in SEM, and to Julio César Montero-Rojas for artwork. DMM-Q also thanks Thomas Borsch, Nils Köster, Juliane Bettig, Kim Govers, Robert Vogt, Christopher Neuenfeldt, and Gabriela Michaelis of the Botanic Garden and Botanical Museum Berlin for their support during his visit. The comments of two anonymous reviewers and the associated editor are highly appreciated.

Author information

DMM-Q and TT designed the work; DMM-Q performed observations and analyses; all authors reviewed analyses; DMM-Q and TT wrote the manuscript; all the authors have read and approved the manuscript.

Correspondence to Teresa Terrazas.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Electronic supplementary material

Appendices

Information on Electronic Supplementary Material

Online resource 1. List of characters and character states analyzed.

Online resource 2. Structural characters used in the matrix in the phylogenetic analyses.

Online resource 3. Majority-rule consensus tree of the Bayesian Inference analysis.

Online resource 4. Structural characters that support clades.

Appendix

List of taxa analyzed in this study, presented in alphabetical order following this format: Taxon Locality, Country: LIVING COLLECTION ACRONYM Accession and (HERBARIUM ACRONYM). Herbaria acronyms: B Herbarium Berolinense, CHAPA Colegio de Posgraduados, HNT The Huntington Library, Art Collections, and Botanical Gardens, INB Instituto Nacional de Biodiversidad, K Royal Botanic Gardens, MEXU Herbario Nacional de México, ZSS Sukkulenten-Sammlung Zürich. All INB and MEXU accessions are cultivated in the Living Collection of Botanical Garden of the Institute of Biology, UNAM.

Acanthocereus chiapensis Bravo. Chiapas, MX: JB-IBUNAM S. Arias 1021 (MEXU), JB-IBUNAM S. Arias 1183 (MEXU), JB-IBUNAM S. Arias 1664 (MEXU). Acanthocereus tetragonus (L.) Hummelinck. Oaxaca, MX: JB-IBUNAM S. Arias 2194 (MEXU). Veracruz, MX: JB-IBUNAM S. Arias 2166a (MEXU), JB-IBUNAM S. Arias 2166b (MEXU). Aporocactus flagelliformis (L.) Lem. Hidalgo, MX: JB-IBUNAM I. Rosas 03 (MEXU), JB-IBUNAM I. Rosas 23 (MEXU), JB-IBUNAM I. Rosas 25 (MEXU), JB-IBUNAM I. Rosas 29 (MEXU). Querétaro, MX: JB-IBUNAM I. Rosas 06 (MEXU), JB-IBUNAM I. Rosas 30 (MEXU), JB-IBUNAM I. Rosas 33 (MEXU). Veracruz, MX: JB-IBUNAM S. Arias 1235 (MEXU), JB-IBUNAM S. Arias 1237 (MEXU), JB-IBUNAM I. Rosas 22 (MEXU). Without locality data: JB-IBUNAM I. Rosas 01 (MEXU). Aporocactus martianus (Zucc.) Britton & Rose. Oaxaca, MX: JB-IBUNAM S. Arias 1230 (MEXU), JB-IBUNAM S. Arias 1246 (MEXU), JB-IBUNAM I. Rosas 15 (MEXU). Disocactus ackermannii (Haw.) Ralf Bauer. Oaxaca, MX: JB-IBUNAM M. Cruz 10 (MEXU), JB-IBUNAM M. Cruz 14 (MEXU). Disocactus anguliger (Lem.) M.Á.Cruz & S.Arias. Jalisco, MX: BGBM 046-15-07-40/001. Oaxaca, MX: BGBM 069-11-12-30/001. Without locality data: BGBM 014-26-74-80/001 (B 15229). Disocactus biformis (Lindl.) Lindl. Sololá, GT: BGBM 155-24-12-30/001 (ZSS 21337). Disocactus crenatus subsp. kimnachii (Bavo ex Kimnach) M.Á.Cruz & S.Arias. Chiapas, MX: JB-IBUNAM M. Cruz 23 (MEXU), BGBM 169-01-84-30/001 (B 26924). Oaxaca, MX: JB-IBUNAM M. Cruz 11 (MEXU). Disocactus eichlamii (Weing.) Britton & Rose. Escuintla, GT: BGBM 155-67-12-30/001. Disocactus macdougallii (Alexander) Barthlott. Chiapas, MX: BGBM 069-33-12-30/001 (ZSS 21400, 29520). Disocactus macranthus (Alexander) Kimnach & Hutchison. Veracruz, MX: JB-IBUNAM M. Cruz 07 (MEXU), JB-IBUNAM M. Cruz 08 (MEXU). Disocactus nelsonii (Britton & Rose) Linding. Chiapas, MX: BGBM 155-68-12-30/001. Disocactus nelsoniisubsp.hondurensis (Kimnach) Dowel. Comayagua, HN: BGBM 155-75-12-30/001 (HNT 1282a, b, c, 1285; ZSS 27902). Disocactus phyllanthoides (DC.) Barthlott. Puebla, MX: BGBM 155-94-12-30/001. Disocactus quezaltecus (Standl. & Steyerm.) Kimnach. Quezaltenango, GT: JB-IBUNAM M. Véliz 20054a (MEXU), JB-IBUNAM M. Véliz 20054b (MEXU), JB-IBUNAM M. Véliz 20054c (MEXU), BGBM 155-66-12-30/001 (ZSS 21369). Disocactus speciosus (Cav.) Barthlott. Jalisco, MX: JB-IBUNAM Y. Morales 01 (MEXU). Michoacán, MX: BGBM 155-19-12-30/001. Oaxaca, MX: JB-IBUNAM M. Cruz 16 (MEXU), BGBM 155-20-12-30/001. Disocactus speciosussubsp.cinnabarinus (Eichlam ex Weing.) Barthlott. San Marcos, GT: BGBM 156-20-12-30/001. Epiphyllum baueri Dorsch. Chocó, CO: BGBM 155-54-12-30/001 (K 000035667, 00005668, 000578667). Colón, PA: BGBM 155-63-12-30/001 (B 50240). Epiphyllum cartagense (F.A.C.Weber) Britton & Rose. San José, CR: BGBM 155-35-12-30/001. Bocas del Toro, PA: BGBM 156-34-12-30/001. Epiphyllum chrysocardium Alexander. Chiapas, MX: BGBM 014-74-74-83/001 (B 9420). Epiphyllum hookeri Haw. Veracruz, MX: JB-IBUNAM M. Cruz 03 (MEXU), JB-IBUNAM M. Cruz 04 (MEXU), JB-IBUNAM M. Cruz 05 (MEXU). Epiphyllum hookerisubsp.guatemalense (Britton & Rose) Ralf Bauer. San Marcos, GT: BGBM 155-52-12-30/001. Epiphyllum oxypetalum (DC.) Haw. Izabal, GT: BGBM 155-73-12-30/001. Chiapas, MX: JB-IBUNAM S. Arias 1656 (MEXU). Veracruz, MX: JB-IBUNAM G. Salazar 9280 (MEXU). Epiphyllum phyllanthus (L.) Haw. Magdalena, CO: BGBM 155-56-12-30/001 (ZSS 19797). SR: BGBM 177-19-10-60/001. Epiphyllum phyllanthussubsp.rubrocoronatum (Kimnach) Ralf Bauer. Chocó, CO: BGBM 155-85-12-30/001. Epiphyllum pumilum Britton & Rose. Chiapas, MX: JB-IBUNAM M. Cruz 17b (MEXU), BGBM 155-51-12-30/001 (ZSS 21396), BGBM 155-98-12-30/001. Veracruz, MX: JB-IBUNAM M. Cruz 06 (MEXU), BGBM 180-19-01-63/001 (B 45760). Epiphyllum thomasianum (K.Schum.) Britton & Rose. Chiapas, MX: BGBM 156-45-12-30/001. Without locality data: BGBM 059-59-74-80/001 (B 20196). Epiphyllum thomasianumsubsp.costaricense (F.A.C.Weber) Ralf Bauer. Magdalena, CO: BGBM 155-55-12-30/001. Kimnachia ramulosa (Salm-Dyck) S. Arias & N. Korotkova. EC: BGBM 153-08-92-43/001. Chiapas, MX: BGBM 055-23-06-40/001, BGBM 156-44-12-30/001. Kimnachia ramulosasubsp.jamaicensis (Britton & Harris) S.Arias & N.Korotkova. Cornwall, JM: BGBM 155-06-12-30/001 (ZSS 19803). Pseudorhipsalis acuminata Cufod. Limón, CR: BGBM 155-46-12-30/001 (ZSS 19801, 21362). Pseudorhipsalis alata (Sw.) Britton & Rose. Cockpit Country, JM: BGBM 155-25-12-30/001 (ZSS 22552). Pseudorhipsalis amazonicasubsp.panamensis (Britton & Rose) Ralf Bauer. Magdalena, CO: BGBM 155-60-12-30/001 (ZSS 21381). PA: BGBM 082-01-82-33/002. Pseudorhipsalis himanthoclada (Rol.-Goss.) Britton & Rose. San José, CR: BGBM 155-42-12-30/001 (HNT 1488; ZSS 21379). Selenicereus anthonyanus (Alexander) D.R.Hunt. Chiapas, MX: JB-IBUNAM MH S.N.a, JB-IBUNAM MH S.N.b. Without locality data: JB-IBUNAM S.N. Selenicereus atropilosus Kimnach. Jalisco, MX: JB-IBUNAM S. Arias 2216 (MEXU), JB-IBUNAM S. Arias 2217 (MEXU), JB-IBUNAM H. Arreola 1473. Selenicereus calcaratus (F.A.C.Weber) D.R.Hunt. Without locality data: BGBM 066-04-84-80/001. Selenicereus dorschianus Ralf Bauer. Jalisco, MX: JB-IBUNAM S. Arias 2219 (MEXU), JB-IBUNAM S. Arias 2220 (MEXU), JB-IBUNAM S. Arias 2221 (MEXU). Selenicereus extensus (Salm-Dyck ex DC.) Leuenberger. Atachi-Bakka Mountains, GF: BGBM 039-49-89-20/001 (B 33353, 43690). Cayenne, GF: BGBM 193-01-06-30/001. Selenicereus glaber (Eichlam) S.Arias & N.Korotkova. Ahuachapan, SV: BGBM 155-32-12-30/001 (ZSS 21352), BGBM 155-33-12-30/001. SV: GC3198. Suchitepéquez, GT: BGBM 155-10-12-30/001. Chiapas, MX: JB-IBUNAM H. Bravo 3180 (MEXU), JB-IBUNAM H. Bravo 5618 (MEXU). Selenicereus glabersubsp.mirandae (Bravo) S.Arias & N.Korotkova. Chiapas, MX: BGBM 155-40-12-30/001. Selenicereus grandiflorus (L.) Britton & Rose. Guantánamo, CU: BGBM 156-24-12-30/001. Chiapas, MX: JB-IBUNAM J. Meyrán 4030 (MEXU). Oaxaca, MX: JB-IBUNAM S. Arias, 2066 (MEXU). Veracruz, MX: JB-IBUNAM M. Rodríguez 06 (MEXU), JB-IBUNAM M. Rodríguez 10 (MEXU), JB-IBUNAM M. Rodríguez 11 (MEXU). Without locality data: JB-IBUNAM U. Guzmán 1365 (MEXU). Selenicereus grandiflorussubsp.donkelaarii (Salm-Dyck) Ralf Bauer. Campeche, MX: JB-IBUNAM U. Guzmán 986 (MEXU). Yucatán, MX: JB-IBUNAM S. Arias 1090 (MEXU), JB-IBUNAM U. Guzmán 990 (MEXU), JB-IBUNAM U. Guzmán 994 (MEXU). Selenicereus grandiflorussubsp.hondurensis (K.Schum. ex Weing.) Ralf Bauer. Izabal, GT: BGBM 155-26-12-30/001 (ZSS 21377). Selenicereus grandiflorussubsp.lautneri Ralf Bauer. Oaxaca, MX: BGBM 155-08-12-30/001. Selenicereus hamatus (Scheidw.) Britton & Rose. Veracruz, MX: JB-IBUNAM S. Arias 2171 (MEXU), JB-IBUNAM J. Rivera S.N. (MEXU), JB-IBUNAM M. Rodríguez 08 (MEXU), JB-IBUNAM G. Salazar 9308 (MEXU). Selenicereus inermis (Otto ex Pfeiff.) Britton & Rose. Guanacaste, CR: BGBM 155-15-12-30/001. Miranda, VE: BGBM 155-16-12-30/001. Sucre, VE: BGBM 155-07-12-30/001. Selenicereus inermissubsp.tricae (D.R.Hunt) Ralf Bauer. Cayo, BZ: BGBM 155-84-12-30/001. Veracruz, MX: BGBM 155-83-12-30/001. Selenicereus megalanthus (K. Schum. ex Vaupel) Moran. Amazonas, PE: BGBM 155-78-12-30/001. San Martín, PE: BGBM 155-79-12-30/001. Without locality data: BGBM 213-03-92-80 (B 31874). Selenicereus minutiflorus (Britton & Rose) D.R.Hunt. Without locality data: BGBM 175-02-81-80/001 (B 15053). Selenicereus monacanthus (Lem.) D.R.Hunt. Magdalena, CO: BGBM 155-58-12-30/001 (ZSS 22705). Chimborazo, EC: BGBM 156-30-12-30/001. Without locality data: BGBM 052-01-82-30/001 (B 31603). Selenicereus murrillii Britton & Rose. Colima, MX: BGBM 155-38-12-80/001 (ZSS 29368). Michoacán, MX: JB-IBUNAM H. Sánchez 4206 (MEXU). Selenicereus ocamponis (Salm-Dyck) D.R.Hunt. Michoacán, MX: M. García-Aguilar 34 (CHAPA), M. García-Aguilar 35 (CHAPA), M. García-Aguilar 36 (CHAPA). Without locality data: BGBM 155-23-12-80/001, BGBM 156-18-12-80/001, BGBM 258-07-93-80/001 (B 41127). Selenicereus pteranthus (Link ex A.Dietr.) Britton & Rose. Guantánamo, CU: BGBM 261-31-93-20/001 (B 34921). Holguín, CU: BGBM 155-17-12-30/001. Chiapas, MX: JB-IBUNAM U. Guzmán 945 (MEXU). Tamaulipas, MX: JB-IBUNAM L. G. 847 (MEXU). Without locality data: BGBM 014-95-74-80/001 (B 16496), BGBM 069-26-12-80/001. Selenicereus purpusii (Weing.) S.Arias & N.Korotkova. Guerrero, MX: M. García-Aguilar 32 (CHAPA). Nayarit, MX: M. García-Aguilar 21 (CHAPA), M. García-Aguilar 22 (CHAPA). Without locality data: BGBM 012-18-74-80/001 (B 12787a, b). Selenicereus setaceus (Salm-Dyck ex DC.) Werderm. Cerro Acahay, PY: BGBM 232-07-02-30/001 (B, 44115). Without locality data: BGBM 048-56-74-80/001 (B 15057), BGBM 069-32-12-80/001. Selenicereus spinulosus (DC.) Britton & Rose. Hidalgo, MX: JB-IBUNAM S. Arias 2231 (MEXU). Querétaro, MX: JB-IBUNAM S. Arias 1755 (MEXU), JB-IBUNAM J. Gozzy S.N. (MEXU), JB-IBUNAM D. Martínez 02 (MEXU). San Luis Potosí, MX: JB-IBUNAM J. Meyrán 97 (MEXU), JB-IBUNAM T. Terrazas 979 (MEXU). Tamaulipas, MX: JB-IBUNAM U. Guzmán 1121a (MEXU), JB-IBUNAM U. Guzmán 1121b (MEXU). Veracruz, MX: JB-IBUNAM M. Bárcenas 22 (MEXU), BGBM 266-02-94-30/001 (B 37937). Selenicereus stenopterus (F.A.C.Weber) D.R.Hunt. Limón, CR: BGBM 069-22-12-30/001 (B 49514). Selenicereus tonduzii (F.A.C.Weber) S.Arias & N.Korotkova. San José, CR: JB-IBUNAM B. Hammel 22487 (INB). Selenicereus triangularis (L.) D.R.Hunt. Pedernales, DO: BGBM 165-14-82-10/001. Without locality data: BGBM 014-96-74-80/001 (B 15049a, b). Selenicereus undatus (Haw.) D.R.Hunt. Chiapas, MX: M. García-Aguilar 17 (CHAPA). Michoacán, MX: M. García-Aguilar 20 (CHAPA). Without locality data: JB-IBUNAM C-10 (MEXU). Selenicereus vagans (K.Brandegee) Britton & Rose. Jalisco, MX: JB-IBUNAM N. Taylor 296 (MEXU). Nayarit, MX: JB-IBUNAM J. Blancas 111 (MEXU). Sinaloa, MX: JB-IBUNAM S. Arias 1832 (MEXU), JB-IBUNAM J. Meyrán 4137 (MEXU). Selenicereus validus S.Arias & U.Guzmán. Michoacán, MX: JB-IBUNAM H. Sánchez 4254a (MEXU), JB-IBUNAM H. Sánchez 4254b (MEXU). Weberocereus frohningiorum Ralf Bauer. CR: BGBM 155-76-12-60/001 (K 000100018; ZSS 19806). Weberocereus imitans (Kimnach & Hutchison) Buxb. San José, CR: JB-IBUNAM B. Hammel 26140 (INB), BGBM 156-21-12-30/001. Weberocereus rosei (Kimnach) Buxb. Chimborazo, EC: BGBM 155-49-12-30/001. Weberocereus trichophorus H.Johnson & Kimnach. Limón, CR: BGBM 069-27-12-80/001. Weberocereus tunilla (F.A.C.Weber) Britton & Rose. Cartago, CR: BGBM 271-02-82-20/001 (B 25043). Weberocereus tunillasubsp.biolleyi (F.A.C.Weber) Ralf Bauer. Alajuela, CR: BGBM 069-36-12-30/001.

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Martínez-Quezada, D.M., Arias, S., Korotkova, N. et al. The phylogenetic significance of the stem morpho-anatomy in the Hylocereeae (Cactoideae, Cactaceae). Plant Syst Evol 306, 8 (2020). https://doi.org/10.1007/s00606-020-01639-x

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Keywords

  • Combined phylogenetic analysis
  • Cortex
  • Epidermis
  • Mineral inclusions
  • Secondary xylem