Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2026-06-30
Page range: 18-34
Abstract views: 0
PDF downloaded: 0

Puzzling parasitic plants: phylogenetics and classification of Santalales revisited

Department of Botany and Biodiversity Research; University of Vienna; Vienna; Austria
Hortus Botanicus; University of Technology; Delft; The Netherlands
Royal Botanic Gardens; Kew; Richmond; Surrey; UK
Hortus Botanicus; University of Technology; Delft; The Netherlands
Balanophoraceae Erythropalaceae hemiparasite holoparasite Olacaceae parasitic plants Santalaceae Strombosiaceae Eudicots

Abstract

Based on a previously published but realigned matrix for Santalales, we find many relationships that were weakly or unsupported in previous studies are here much better supported, providing a more robust foundation upon which to base Santalales classification. In the maximum likelihood analysis, we recovered the same basic relationships as in the previous studies, but with two major differences: i) Balanophoraceae in the broad sense are monophyletic and well supported as embedded in Santalaceae (rather than biphyletic and outside Santalaceae) and ii) most of the former Olacaceae form a moderately supported clade (rather than a weakly supported grade). In the parsimony analysis, the position of Balanophoraceae s.l. is not well supported (although their broader circumscription is). We outline three possible options for a classification of the order and propose a new familial and subfamilial classification for Santalales. This hopefully provides a stable, user-friendly taxonomic framework that is phylogenetically well supported and more consistent with historical usage than some recently proposed systems and provides taxa that can be more readily diagnosed morphologically. We recommend recognition of nine families (in phylogenetic sequence): Strombosiaceae, Erythropalaceae, Olacaceae, Opiliaceae, Santalaceae, Misodendraceae, Schoepfiaceae and Loranthaceae, plus an unresolved position for Balanophoraceae (including Mystropetalaceae), which we propose to exclude from Santalaceae until more evidence of their relationships to that family is available from nuclear genes. Four new subfamilies, Gaiadendroideae, Comandroideae, Nanodeoideae and Thesioideae, are proposed, and a new combination, Loranthus obtusifolius, is made.

References

  1. Anderson, B.M., Edlund, M., James, S.A., Lepschi, B.J., Nickrent, D.L., Sultan, A., Tate, J.A. & Petersen, G. (2025) Evolutionary relationships in Santalales inferred using target capture with Angiosperms353, focusing on Australasian Santalaceae sensu lato. Australian Systematic Botany 38: SB24026. https://doi.org/10.1071/sb24026
  2. APG III. (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Botanical Journal of the Linnaean Society 161: 105–121. https://doi.org/10.1111/j.1095-8339.2009.00996.x
  3. APG IV. (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1–20. https://doi.org/10.1111/boj.12385
  4. Barkman, T.J., McNeal, J.R., Lim, S.H., Coat, G., Croom, H.B., Young, N.D. & dePamphilis, C.W. (2007) Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evolutionary Biology 7: 248. https://doi.org/10.1186/1471-2148-7-248
  5. Bungard, R.A. (2004) Photosynthetic evolution in parasitic plants: insight from the chloroplast genome. BioEssays 26: 235–247. https://doi.org/10.1002/bies.10405
  6. Byng, J.W. (2014) The flowering plants handbook: a practical guide to families and genera of the world. Plant Gateway, Hertford, 628 pp.
  7. Chase, M.W., Soltis, D.E., Olmstead, R.G., Morgan, D., Les, D.H., Mishler, B.D., Duvall, M.R., Price, R.A., Hills, H.G., Qiu, Y.L., Kron, K.A., Rettig, J.H., Conti, E., Palmer, J.D., Manhart, J.R., Sytsma, K.J., Michaels, H.J., Kress, W.J., Karol, K.G., Clark, W.D., Hedren, M., Gaut, B.S., Jansen, R.K., Kim, K.J., Wimpee, C.F., Smith, J.F., Furnier, G.R., Strauss, S.H., Xiang, Q.Y., Plunkett, G.M., Soltis, P.S., Swensen, S.M., Williams, S.E., Gadek, P.A., Quinn, C.J., Eguiarte, L.E., Golenberg, E., Learn, G.H., Jr., Graham, S.W., Barrett, S.C.H., Dayanandan, S. & Albert, V.A. (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80 (3): 528–548, 550–580. https://doi.org/10.2307/2399846
  8. Christenhusz, M.J.M. & Byng, J.W. (2016) The number of known plant species in the world and its annual increase. Phytotaxa 261: 201–217. https://doi.org/10.11646/phytotaxa.261.3.1
  9. Christenhusz, M.J.M., Fay, M.F. & Chase, M.W. (2017) Plants of the World. Kew Publishing, Richmond, and University of Chicago Press, Chicago, 850 pp.
  10. Christenhusz, M.J., Fay, M.F., Clarkson, J.J., Gasson, P., Morales Can, J., Jimenez Barrios, J.B. & Chase, M.W. (2010) Petenaeaceae, a new angiosperm family in Huerteales with a distant relationship to Gerrardina (Gerrardinaceae). Botanical Journal of the Linnean Society 164: 16–25. https://doi.org/10.1111/j.1095-8339.2010.01074.x
  11. Christenhusz, M.J.M., Vorontsova, M.S., Fay, M.F. & Chase, M.W. (2015) Results from an online survey of family delimitation in angiosperms and ferns: recommendations to the Angiosperm Phylogeny Group for thorny problems in plant classification. Botanical Journal of the Linnean Society 178: 501–528. https://doi.org/10.1111/boj.12285
  12. Der, J.P. & Nickrent, D.L. (2008) A molecular phylogeny of Santalaceae (Santalales). Systematic Botany 33: 107–116. https://doi.org/10.1600/036364408783887438
  13. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113. https://doi.org/10.1186/1471-2105-5-113
  14. Fitch, W.M. (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Biology 20: 406–416. https://doi.org/10.1093/sysbio/20.4.406
  15. Gosline, G. & Malécot, V. (2011) A monograph of Octoknema (Octoknemaceae—Olacaceae s.l.). Kew Bulletin 66: 367–404. https://doi.org/10.1007/s12225-011-9293-9
  16. Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522. https://doi.org/10.1093/molbev/msx281
  17. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
  18. Kelchner, S.A. (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Annals of the Missouri Botanical Garden 87: 482–498. https://doi.org/10.2307/2666142
  19. Kuijt, J. & Hansen, B. (2015) The families and genera of vascular plants, vol. 12, (flowering plants: eudicots; Santalales, Balanophorales). Springer, Heidelberg. https://doi.org/10.1007/978-3-319-09296-6
  20. Malécot, V. & Nickrent, D.L. (2008) Molecular phylogenetic relationships of Olacaceae and related Santalales. Systematic Botany 33: 97–106. https://doi.org/10.1600/036364408783887384
  21. Malécot, V., Nickrent, D.L., Baas, P., Van den Oever, L. & Lobreau-Callen, D. (2004) A morphological cladistic analysis of Olacaceae. Systematic Botany 29: 569–586. https://doi.org/10.1600/0363644041744301
  22. Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
  23. Nickrent, D.L. (1997 and continuously updated) The parasitic plant connection. Available from: https://parasiticplants.siu.edu/ (accessed 25 April 2025)
  24. Nickrent, D.L. & García, M.A. (2015) Lacomucinaea, a new monotypic genus in Thesiaceae (Santalales). Phytotaxa 224: 173–184. https://doi.org/10.11646/phytotaxa.224.2.4
  25. Nickrent, D.L. & Malécot, V. (2001) A molecular phylogeny of Santalales. In: Fer, A., Thalouarn, P., Joel, D.M., Musselman, L.J., Parker, C. & Verkleij, J.A.C. (Eds.) 7th International Parasitic Weed Symposium: proceedings. Faculté des Sciences, Université de Nantes, Nantes, pp. 69–74.
  26. Nickrent, D.L., Anderson, F. & Kuijt, J. (2019) Inflorescence evolution in Santalales: integrating morphological characters and molecular phylogenetics. American Journal of Botany 106: 402–414. https://doi.org/10.1002/ajb2.1250
  27. Nickrent, D.L., Der, J.P. & Anderson, F.E. (2005) Discovery of the photosynthetic relatives of the “Maltese mushroom” Cynomorium. BMC Evolutionary Biology 5: 38. https://doi.org/10.1186/1471-2148-5-38
  28. Nickrent, D.L., Malécot, V., Vidal-Russell, R. & Der, J.P. (2010) A revised classification of Santalales. Taxon 59: 538–558. https://doi.org/10.1002/tax.592019
  29. 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
  30. Peng, Y., Chen, Z., Gong, X., Zhong, Y. & Shi, S. (2003) Phylogenetic position of Dipentodon sinicus: evidence from DNA sequences of chloroplast rbcL, nuclear ribosomal 18S, and mitochondria matR genes. Botanical Bulletin of Academia Sinica 44: 217–222.
  31. Philippe, H., Brinkmann, H., Lavrov, D.V., Littlewood, D.T., Manuel, M., Wörheide, G. & Baurain, D. (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 9: e1000602. https://doi.org/10.1371/journal.pbio.1000602
  32. POWO. (2025) Plants of the World online. Available from: https://powo.science.kew.org (accessed 18 February 2025)
  33. Su, H.J. & Hu, J.M. (2012) Rate heterogeneity in six protein-coding genes from the holoparasite Balanophora (Balanophoraceae) and other taxa of Santalales. Annals of Botany 110: 1137–1147. https://doi.org/10.1093/aob/mcs197
  34. Su, H.J., Hu, J.M., Anderson, F.A., Der, J.P. & Nickrent, D.L. (2015) Phylogenetic relationships of Santalales with insights into the origins of holoparasitic Balanophoraceae. Taxon 64: 491–506. https://doi.org/10.12705/643.2
  35. Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), 4.0 ed. Sinauer, Sunderland.
  36. Vidal-Russell, R. & Nickrent, D.L. (2007) A molecular phylogeny of the feathery mistletoe Misodendrum. Systematic Botany 32: 560–568. https://doi.org/10.1600/036364407782250643
  37. Vidal-Russell, R. & Nickrent, D.L. (2008a) The first mistletoes: origins of aerial parasitism in Santalales. Molecular Phylogenetics and Evolution 47: 523–537. https://doi.org/10.1016/j.ympev.2008.01.016
  38. Vidal-Russell, R. & Nickrent, D.L. (2008b) Evolutionary relationships in the showy mistletoe family (Loranthaceae). American Journal of Botany 95: 1015–1029.
  39. Wickham, H. (2016) ggplot2: Elegant graphics for data analysis. Springer, New York.
  40. Wilke, C.O. (2024) cowplot: Streamlined plot theme and plot annotations for ggplot2 (R package version 1.1.1).
  41. Worberg, A., Alford, M.H., Quandt, D. & Borsch, T. (2009) Huerteales sister to Brassicales plus Malvales, and newly circumscribed to include Dipentodon, Gerrardina, Huertea, Perrottetia, and Tapiscia. Taxon 58: 468–478. https://doi.org/10.1002/tax.582012
  42. Wurdack, K.J. & Davis, C.C. (2009) Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. American Journal of Botany 96: 1551–1570. https://doi.org/10.3732/ajb.0800207
  43. Xiang, Q.Y., Moody, M.L., Soltis, D.E., Fan, C.Z. & Soltis, P.S. (2002) Relationships within Cornales and circumscription of Cornaceae—matK and rbcL sequence data and effects of outgroups and long branches. Molecular Phylogenetics and Evolution 24: 35–57. https://doi.org/10.1016/s1055-7903(02)00267-1
  44. Yu, G., Smith, D.K., Zhu, H., Guan, Y. & Lam, T.T.Y. (2017) ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution 8: 28–36. https://doi.org/10.1111/2041-210x.12628
  45. Yu, G. (2022) Data integration, manipulation and visualization of phylogenetic trees (1st ed.). London, Chapman and Hall/CRC.
  46. Zuntini, A.R., Carruthers, T., Maurin, O., Bailey, P.C., Leempoel, K., Brewer, G.E., Epitawalage, N., Françoso, E., Gallego-Paramo, B., McGinnie, C., Negrão, R., Roy, S.R., Simpson, L., Romero, E.T., Barber, V.M.A., Botigué, L., Clarkson, J.J., Cowan, R.S., Dodsworth, S., Johnson, M.G., Kim, J.T., Pokorny, L., Wickett, N.J., Antar, G.M., DeBolt, L., Gutierrez, K., Hendriks, K.P., Hoewener, A., Hu, A.Q., Joyce, E.M., Kikuchi, I.A.B.S., Larridon, I., Larson, D.A., de Lírio, E.J., Liu, J.X., Malakasi, P., Przelomska, N.A.S., Shah, T., Viruel, J., Allnutt, T.R., Ameka, G.K., Andrew, R.L., Appelhans, M.S., Arista, M., Ariza, M.J., Arroyo, J., Arthan, W., Bachelier, J.B., Bailey, C.D., Barnes, H.F., Barrett, M.D., Barrett, R.L., Bayer, R.J., Bayly, M.J., Biffin, E., Biggs, N., Birch, J.L., Bogarín, D., Borosova, R., Bowles, A.M.C., Boyce, P.C., Bramley, G.L.C., Briggs, M., Broadhurst, L., Brown, G.K., Bruhl, J.J., Bruneau, A., Buerki, S., Burns, E., Byrne, M., Cable, S., Calladine, A., Callmander, M.W., Cano, A., Cantrill, D.J., Cardinal-McTeague, W.M., Carlsen, M.M., Carruthers, A.J.A., de Castro Mateo, A., Chase, M.W., Chatrou, L.W., Cheek, M., Chen, S.L., Christenhusz, M.J.M., Christin, P.A., Clements, M.A., Coffey, S.K., Conran, J.G., Cornejo, X., Couvreur, T.L.P., Cowie, I.D., Csiba, L., Darbyshire, I., Davidse, G., Davies, N.M.J., Davis, A.P., van Dijk, K.J., Downie, S.R., Duretto, M.F., Duvall, M.R., Edwards, S.L., Eggli, U., Erkens, R.H.J., Escudero, M., de la Estrella, M., Fabriani, F., Fay, M.F., Ferreira, P.de L., Ficinski, S.Z., Fowler, R.M., Frisby, S., Fu, L., Fulcher, T., Galbany-Casals, M., Gardner, E.M., German, D.A., Giaretta, A., Gibernau, M., Gillespie, L.J., González, C.C., Goyder, D.J., Graham, S.W., Grall, A., Green, L., Gunn, B.F., Gutiérrez, D.G., Hackel, J., Haevermans, T., Haigh, A., Hall, J.C., Hall, T., Harrison, M.J., Hatt, S.A., Hidalgo, O., Hodkinson, T.R., Holmes, G.D., Hopkins, H.C.F., Jackson, C.J., James, S.A., Jobson, R.W., Kaderet, G., Kahandawala, I.M., Kainulainen, K., Kato, M., Kellogg, E.A., King, G.J., Klejevskaja, B., Klitgaard, B.B., Klopper, R.R., Knapp, S., Koch, M.A., Leebens-Mack, J.H., Lens, F., Leon, C.J., Léveillé-Bourret, É., Lewis, G.P., Li, D.Z., Li, L., Liede-Schumann, S., Livshultz, T., Lorence, D., Lu, M., Lu-Irving, P., Luber, J., Lucas, E.J., Luján, M., Lum, M., Macfarlane, T.D., Magdalena, C., Mansano, V.F., Masters, L.E., Mayo, S.J., McColl, K., McDonnell, A.J., McDougall, A.E., McLay, T.G.B., McPherson, H., Meneses, R.I., Merckx, V.S.F.T., Michelangeli, F.A., Mitchell, J.D., Monro, A.K., Moore, M.J., Mueller, T.L., Mummenhoff, K., Munzinger, J., Muriel, P., Murphy, D.J., Nargar, K., Nauheimer, L., Nge, F.J., Nyffeler, R., Orejuela, A., Ortiz, E.M., Palazzesi, L., Peixoto, A.L., Pell, S.K., Pellicer, J., Penneys, D.S., Perez-Escobar, O.A., Persson, C., Pignal, M., Pillon, Y., Pirani, J.R., Plunkett, G.M., Powell, R.J., Prance, G.T., Puglisi, C., Qin, M., Rabeler, R.K., Rees, P.E.J., Renner, M., Roalson, E.H., Rodda, M., Rogers, Z.S., Rokni, S., Rutishauser, R., de Salas, M.F., Schaefer, H., Schley, R.J., Schmidt-Lebuhn, A.N., Shapcott, A., Al-Shehbaz, I., Shepherd, K.A., Simmons, M.P., Simões, A.O., Simões, A.R.G., Siros, M., Smidt, E.C., Smith, J.F., Snow, N., Soltis, D.E., Soltis, P.S., Soreng, R.J., Sothers, C.A., Starr, J.R., Stevens, P.F., Straub, S.C.K., Struwe, L., Taylor, J.M., Telford, I.R.H., Thornhill, A.H., Tooth, I., Trias-Blasi, A., Udovicic, F., Utteridge, T.M.A., Del Valle, J.C., Verboom, G.A., Vonow, H.P., Vorontsova, M.S., de Vos, J.M., Al-Wattar, N., Waycott, M., Welker, C.A.D., White, A.J., Wieringa, J.J., Williamson, L.T., Wilson, T.C., Wong, S.Y., Woods, L.A., Woods, R., Worboys, S., Xanthos, M., Yang, Y., Zhang, Y.X., Zhou, M.Y., Zmarzty, S., Zuloaga, F.O., Antonelli, A., Bellot, S., Crayn, D.M., Grace, O.M., Kersey, P.J., Leitch, I.J., Sauquet, H., Smith, S.A., Eiserhardt, W.L., Forest, F. & Baker, W.J. (2024) Phylogenomics and the rise of the angiosperms. Nature 629: 843–850. https://doi.org/10.1038/s41586-024-07324-0

How to Cite

Cauz-Santos, L.A., Byng, J.W., Chase, M.W. & Christenhusz, M.J.M. (2026) Puzzling parasitic plants: phylogenetics and classification of Santalales revisited. Phytotaxa 765 (1): 18–34. https://doi.org/10.11646/phytotaxa.765.1.2