of Parasitic Flowering Plants
The number of times parasitism has evolved in flowering plants (angiosperms) has long been debated. The closest
for a number of lineages have been known for some time: Cassytha
Lauraceae, Lennoaceae with Boraginaceae (or Ehretiaceae), Orobanchaceae with
in the traditional sense, and Cuscuta
For others, particularly the holoparasites in the traditionally
recognized families Hydnoraceae,
and Rafflesiaceae, placement among photosynthetic angiosperms
has been difficult. For this reason, traditional classifications
were often conflicted among different workers and even in different
treatments by the same worker. Relationships between parasitic and
nonparasitic angiosperms have
been greatly clarified through DNA sequencing and molecular
phylogenetic analyses, although not without some "bumps in the road."
One molecular evolutionary phenomenon that has made phylogenetic work
on the holoparasites less than straightforward has been horizontal gene
transfer, particularly of mitochondrial genes. This has generated
conflicts between gene trees derived from the different subcellular
genomes. A good example of this is the paper by Barkman et al. (2007)
who used molecular methods but could not given an exact number for the
origins of parasitism ("at least 11"). Currently, all clades of
parasitic plants have been placed on the global angiosperm phylogenetic
tree. As described below, parasitism has arisen independently
in angiosperms 12 times.
In terms of trophic modes, 9 lineages (clades, families) are composed
entirely of holoparasites (family names enclosed in solid line
rectangles). Only two lineages (Cassytha and Krameriaceae) contain just hemiparasites. In two families, Convolvulaceae (Cuscuta)
and Orobanchaceae, both hemi- and holoparasites be found (family
names enclosed in dashed line rectangles). Only the order
Santalales has more than one family of parasitic plants.
Click on the family names to go to those pages
the sole parasitic member of the large family Lauraceae, is
assigned to this family based on morphological and molecular data (Rohwer & Rudolph 2005).
Its superficial resemblance to Cuscuta is
an excellent example of convergent evolution.
were used to place Hydnoraceae with Aristolochiaceae s. lat. (Nickrent
et al. 2002), however, the exact topology of the component families of
this order (Aristolochiaceae, Hydnoraceae, Lactoridaceae, Piperaceae
and Saururaceae) was not determined. The analysis by Nickrent
(2005, IBC abstract) suggested Hydnoraceae was most closely
to Aristolochiaceae. This result was confirmed by more recent work (Naumann et al. 2013).
classified with Balanophoraceae, the family Cynomoriaceae has
been shown to be a component of Saxifragales (Nickrent
et al. 2005). For a more up-to-date and complete discussion of this finding, see the Supplement to Su et al. (2015) HERE. S. Renner (pers. com. 2015) has confirmed this result using NextGen sequencing.
The APG2 classification
considered Krameriaceae as an acceptable monophyletic alternative
to Zygophyllaceae. In APG3 the two families were considered
separate. This order is sister to the Fabid (previously Rosid I)
considered here in the strict sense (including Rafflesia,
Rhizanthes, and Sapria, i.e.,
clade") was placed with Malpighiales by Barkman et al. (2004)
using mitochondrial matR gene sequences. This position was confirmed
et al. (2004) using both nuclear SSU rDNA as well as
sequence data. Placement within the order shows that Rafflesiaceae is near Euphorbiaceae (Davis et al. 2007).
Traditionally placed in Rafflesiaceae, the "small-flowered
clade" is composed of Apodanthes, Berlinianche, and
Pilostyles. Mitochondrial matR and nuclear SSU rDNA
indicated either a relationship with Malvales or Cucurbitales (Nickrent
al. 2004). Additional sequencing and analyses indicated that this
family is part of Cucurbitales. That result was confirmed by Filipowicz & Renner (2010).
7. Cytinaceae. Traditionally placed in Rafflesiaceae, the"inflorescence
clade" is composed of Cytinus and Bdallophyton.
Mitochondrial matR and nuclear SSU rDNA both strongly support
a position for this family in Malvales (Nickrent
et al. 2004).
The analyses conducted
by Soltis et al. (2000) resolved the sandalwood order as monophyletic,
but this clade was part of a large polytomy among the core eudicots.
The number of taxa involved in that polytomy was quite high, involving
caryophyllids, rosids and asterids. A molecular analysis using complete
chloroplast genomes from over 80 angiosperms (Moore et al. 2010)
indicated that Santalales is sister to Caryophyllales and asterids (as shown in the above tree).
The number of families recognized for Santalales on this web site (20 total) follows Nickrent et al. (2010) and Su et al. (2015). Although the families segregated from Olacaceae s. lat. and recognized by Malécot & Nickrent (2008)
were for the most part accepted by APG III (2009), the segregate
families of Santalaceae s. lat. were not, despite the evidence
presented in Der & Nickrent (2008).
With regard to Santalaceae, Christenhusz et al. (2015)
said "... in the future perhaps expand this family to include the
majority of Santalales, apart from Balanophoraceae." From my
perspective, this tendency towards extreme lumping is excessive,
unjustified, and provides
no scientific advancement. Moreover, this rash statement was made in
the absence of information on the phylogenetic status of
Balanophoraceae s. lat. (see below).
The holoparasite family Balanophoraceae,
previously placed in its own order Balanophorales (Takhtajan
1997), has been shown from molecular evidence (Nickrent
et al. 2005)
to be related to Santalales. A detailed molecular phylogenetic analysis of
the entire order was reported in Su et al (2015) and in that study
Balanophoraceae was not monophyletic. Three genera, Dactylanthus, Hachettea, and Mystropetalon, emerged in a
separate clade and are therefore classified in a separate family Mystropetalaceae.
9. Mitrastemonaceae. Traditionally placed in Rafflesiaceae, this monogeneric family (Mitrastema) was shown to be
to Ericales by Barkman et al. (2004) using mitochondrial matR
gene sequences. This result is confirmed using nuclear SSU rDNA
and mitochondrial sequence data (Nickrent
et al. 2004).
name traditionally referred only to an assemblage of holoparasitic
taxa that were recognized to be related to the hemiparasites of
Scrophulariaceae. Modern circumscriptions of this group (see
Young et al. 1999, Olmstead et al. 2001) place all parasitic "scrophs"
in a monophyletic family Orobanchaceae along with the non-parasite Lindenbergia. Morphological and molecular
evidence clearly place this family in Lamiales.
parasitic genus of Convolvulaceae is Cuscuta that
been placed in its own family, Cuscutaceae. Analysis of sequence
data from four chloroplast gene regions resulted in Cuscuta
being nested within Convolvulaceae (Stefanovic et al. 2002),
thus the classification of APG III (2009) is supported.
have traditionally been placed in their own family, but APG III
lumped Lennoaceae with Boraginaceae, a family with which
they are clearly related as shown by both morphological and molecular
evidence. The genera Lennoa and Pholisma
were shown to be a component
of a monophyletic Ehretiaceae by Gottschling et al. (2014). More
recently, Luebert et al. (2016) provided a familial classification for
Boraginales and retained the family Lennoaceae, sister to Ehretiaceae.
APG III. 2009. An update of the Angiosperm Phylogeny Group
classification for the orders and families of flowering plants. Bot. J.
Linn. Soc. 161:105-121.
Barkman, T.J., Lim, S.-H., Mat Salleh, K., & Nais, J. 2004.
Mitochondrial DNA sequences reveal the photosynthetic relatives of
Rafflesia, the world's largest flower. Proc Natl Acad Sci U S A
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. B.M.C. Evol. Biol. 7:248.
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. Bot. J. Linn. Soc.
Davis, C.C., Latvis, M., Nickrent, D.L., Wurdack, K.J., & Baum,
D.A. 2007. Floral gigantism in Rafflesiaceae. Science 315:1812.
Der, J. P. and Nickrent, D. L. 2008. A molecular phylogeny of Santalaceae (Santalales). Syst. Bot. 33: 107-116.
Filipowicz, N., & Renner, S.S. 2010. The worldwide holoparasitic
Apodanthaceae confidently placed in the Cucurbitales by nuclear and
mitochondrial gene trees. BMC Evol. Biol. 10:48.
Gottschling, M., Luebert, F., Hilger, H.H., & Miller, J.S. 2014.
Molecular delimitations in the Ehretiaceae (Boraginales). Mol. Phylog.
Luebert, F. and 20 others. 2016. Familial classification of the Boraginales. Taxon 65(3): 502-522.
Malécot, V. and Nickrent, D. L. 2008. Molecular phylogenetic
relationships of Olacaceae and related Santalales. Syst. Bot. 33:
Moore, M.J., Soltis, P.S., Bell, C.D., Burleigh, J.G., & Soltis,
D.E. 2010. Phylogenetic analysis of 83 plastid genes further resolves
the early diversification of eudicots. Proc Natl Acad Sci U S A
Naumann, J., Salomo, K., Der, J.P., Wafula, E.K., Bolin, J.F., Maass,
E., Frenzke, L., Samain, M.-S., Neinhuis, C., dePamphilis, C.W., &
Wanke, S. 2013. Single-copy nuclear genes place haustorial Hydnoraceae
within Piperales and reveal a Cretaceous origin of multiple parasitic
angiosperm lineages. PLoS ONE 8:e79204.
Nickrent, D. L, A. Blarer, Y.-L. Qiu, R. Vidal-Russell, F. E. Anderson.
2004. Phylogenetic inference in Rafflesiales: the influence of rate
heterogeneity and horizontal gene transfer. BMC Evol. Biol. 4: 40.
Nickrent, D. L., A. Blarer, Y.-L. Qiu, D. E. Soltis, P. S. Soltis, and
M. Zanis. 2002. Molecular data place Hydnoraceae with Aristolochiaceae.
Amer. J. Bot. 89 (11): 1809-1817.
Nickrent, D.L., Der, J.P., & Anderson, F.E. 2005.
Discovery of the photosynthetic relatives of the "Maltese
mushroom" Cynomorium. BMC Evol. Biol. 5: 38.
Nickrent, D. L. V. Malécot, R. Vidal-Russell, and J. P. Der.
2010. A revised classification of Santalales. Taxon 59: 538-558.
Olmstead, R.G., dePamphilis, C.W., Wolfe, A.D., Young, N.D., Elisens,
W.J., & Reeves, P.J. 2001. Disintegration of the Scrophulariaceae.
Amer. J. Bot. 88:348-361.
Rohwer, J.G., & Rudolph, B. 2005. Jumping genera: the phylogenetic positions of Cassytha, Hypodaphnis, and Neocinnamomum (Lauraceae) based on different analyses of trnK intron sequences. Ann. Mo. Bot. Gard. 92:153-178.
Soltis, D.E., Soltis, P.S., Chase, M.W., Mort, M.E., Albach, D.C.,
Zanis, M., Savolainen, V., Hahn, W.H., Hoot, S.B., Fay, M.F., Axtell,
M., Swensen, S.M., Prance, L.M., Kress, W.J., Nixon, K.C., &
Farris, J.S. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL,
and atpB sequences. Bot. Jour. Linn. Soc. 133:381-461.
Stefanović, S., Krueger, L., & Olmstead, R.G. 2002. Monophyly of
the Convolvulaceae and circumscription of their major lineages based on
DNA sequences of multiple chloroplast loci. Amer. J. Bot. 89:1510-1522.
Su H.-J., J.-M. Hu, F. E. Anderson and D. L. Nickrent. 2015.
Phylogenetic relationships of Santalales with insights into the origins
of holoparasitic Balanophoraceae. Taxon 64(3): 491-506.
Takhtajan, A. 1997. Diversity and classification of flowering plants. Columbia University Press, New York, NY.
Young, N.D., Steiner, K.E., & dePamphilis, C.W. 1999. The evolution
of parasitism in Scrophulariaceae/ Orobanchaceae: Plastid gene
sequences refute an evolutionary transition series. Ann. Mo. Bot. Gard.
Last updated: 06-Dec-16 / dln