Orobanchoideae (VENT.) TERYOKHIN, Opredel. Sarazych. Flory SSSR 34. 1993; TAKHTAJAN, Flowering Plants ed. 2: 566. 2009
- Aeginetiaceae LIVERA,
- Aragoaceae D. DON,
- Buchneraceae LILJA,
- Cyclocheilaceae MARAIS,
- Euphrasiaceae MARTYNOV,
- Lindenbergiaceae DOWELD,
- Melampyraceae HOOKER & LINDLEY,
- Nesogenaceae MARAIS,
- Orobanchaceae L.
- Pedicularidaceae JUSSIEU,
- Phelypaeaceae HORANINOW,
- Rhinanthaceae VENTENAT
Description: - Most (hemi)parasitic herbs, many turn black on drying, (shrubs); stomata do not close; (mannitol), orobanchin +, little oxalate accumulation, 6- and/or 8-hydroxylated flavone glycosides 0; cork?; head of hair lacking vertical partitions; leaves spiral to opposite, often toothed to deeply lobed; inflorescence often racemose; (K ± free), C (tube development intermediate), abaxial lateral lobes outside others in bud [quincuncial], (otherwise); A (free from C - Eremitilla), 4, didynamous, (2), staminode 0 (1), anther thecae parallel or ± confluent sagittate to inverted U-shaped, (unequal or single: Castilejinae), often hairy, with tails or basal awns, (thecae unequal), pollen often starchy, commonly colpate with a retipilate surface, (polyporate), ([G 5]), (-1 ovule/carpel), placentation parietal, (placentae [2, bilobed] 4 [-6]), stigma clavate to capitate; integument (2-)4-12 cells across; (antipodal cells persistent); capsule loculicidal to septicidal; (seeds with elaiosomes); (cells of seed wings with reticulate thickenings on radial walls), exotestal cells variously thickened on the inner walls, (cells of other layers thickened and lignified); endosperm + (starchy; mannose-rich polysaccharides; 0), (embryo minute, undifferentiated; germination via germination tube); n = 7+. - Orobanchaceae are herbs, rarely shrubs, mostly with racemose inflorescences. In the flower, the abaxial lobes of the corolla are outside the others in bud. Nearly all members of the family have a holo- or hemiparasitic life-style. Some Plantaginaceae have similar corolla aestivation, but they are autotrophic.
Genera: - 96 genera/species 2127: Largest genera: Pedicularis (600-?800 - Mill 2001), Castilleja (160-200), Euphrasia (170-350), Orobanche (150), Buchnera (100), Bartsia (50), Agalinis (45), Rhinanthus (45), Alectra (40), Harveya (40), Sopubia (40). World wide, but especially N. (warm) temperate and Africa-Madagascar (map: from van Steenis & van Balgooy 1966; Hultén 1971; Meusel et al. 1978; Hong 1983).
Evolution: - Orobanchaceae may be some 50-40 million years old (Wolfe et al. 2005).
Euphrasia has a North Temperate distribution but is also circum-Pacific, i.e., it is basically bipolar; much dispersal seems to have been involved in attaining this range (Gussarova et al. 2008). Diversification within the large genus Castilleja is becoming better understood. There is a speciose West North American/Central/South American perennial clade - some 120 species - derived apparently quite recently from an annual ancestor; polyploidy is common in the perennials, but not in the annuals (Tank & Olmstead 2008, 2009). Annuals have dispersed more than once to South America (Tank & Olmstead 2009).
There has been diversification of agromyzid dipteran leaf miners on the hemiparasitic members of this clade (Winkler et al. 2009). Larvae of Nymphalidae-Melitaeini butterflies are commonly found here (also on Plantaginaceae, but not on Scrophulariaceae: Wahlberg 2001).
Holoparasites have evolved from hemiparasites more than once in this clade (dePamphilis et al. 1997; Nickrent et al. 1998; Young et al. 1999; Schneeweiss et al. 2004a; Bennett & Mathews 2006, etc.). Indeed, the hemiparasitic Harveya obtusifolia is well embedded in a holoparasitic clade of the genus; whether there has been reversion in habit, or several independent acquisitions of the holoparasitic habit in that part of the family alone is unclear (Morawetz & Randle 2009). Within the family there are several different types of haustoria, some forming a connection with xylem only, others with both xylem and phloem; nevertheless, haustoria may have but a single origin (Fischer 2004b for a summary). Stomata in this family seem to be perpetually open (Stewart & Press 1990; Smith & Stewart 1990), even in the apparently autotropic Lindenbergia, sister to most other Orobanchaceae; the situation in Rehmannia and relatives (see below) is unknown. Perpetually-open stomata are common in parasitic plants because they increase the transpiration flow in the parasite so faciltating movement of water, etc., from the host to the parasite.
Some Orobanchaceae, particularly the hemiparasitic taxa with chlorophyll, take up largely water, nitrogen, etc., from their hosts, others take up organic material as well; iridoid glucosides, pyrrolizidine and quinolizidine alkaloids, etc., may also move from host to parasite (e.g. Adler & Wink 2001; Hibberd & Jaeschke 2001; Shen et al. 2005 [also host selection]; Rasmussen et al. 2006 and references). Alder (2000, 2002, 2003) found a complex relationship between host and parasite, the the annual Castilleja indivisa. Association with Lupinus in particular led to a decrease in herbivores eating the parasite (sometimes), more visitors by pollinators, an increased seed set, etc., when compared with other hosts of the parasite. These effects were mediated by the movement both of alkaloids (?anti herbivore?) and nitrogenous compounds (increase in growth s.l.) from the lupin to the parasite. There may also be movement of material from parasite to host (Rank et al. 2004 for references). Indeed, some of the severe effects on the host caused by orobanchaceous parasites may be due in part by the release of the cytotoxic iridoid aglucone; the breakdown of the iridoid glucoside of the parasite is perhaps caused by the host's ß-glucosidases, themselves common because they are involved in the host's cyanogenic defence pathway (Rank et al. 2004). Recently, horizontal nuclear gene transfer between Sorghum or its relatives and Strica sopecies (but not Orobanche) has been demonstrated (Yoshida et al. 2010); the complexity of the relationships between host and parasite is likely to have been under-estimated. For other information on parasitism in Orobanchaceae, see Irving and Cameron (2009 and references).
Variation in floral morphology in Pedicularis is very great, some species having a corolla tube ca 10 cm long or more, and others having asymmetric flowers with an asymmetrical, proboscis-like extension of the upper lip, the two adaxial corolla members that form the galea. For comments on the floral evolution of the genus, see Ree (2005a). Pollen morphology - there is quite extensive variation - is linked with corolla morphology and pollinator type (Hong Wang et al. 2009a).
For myrmecochory of the seeds (Melampyrum, Pedicularis), see Lengyel et al. (2009, 2010).
For the evolution of genome size in the family, see Weiss-Schneewiess et al. (2005); genome size is reduced after polyploidization.
Economic Importance: - A number of Orobanchaceae, e.g. Striga and Alectra species of the tropical clade (see below), are very serious parasites primarily on legume and grain crops in warmer and drier areas and especially in sub-Saharan Africa, where they are still spreading. Striga affects ca 40% of the cereal producing areas there, causing average losses in yield of 30-90%, especially on poorer soils; a single plant of the parasite can produce up to 100,000 seeds which can remain viable for about 20 years (Scholes & Press 2008; see also Yoshida & Shirasu 2009; Irving & Cameron 2009); Alectra vogelii can cause the complete loss of legume crops it infects (Morawetz & Wolfe 2009).
Chemistry, Morphology, etc.: - Orobanchaceae have Orobanchin, a phenylpropanoid ester of caffeic acid, and silicic acid, and their iridoids are derived from the aucubin pathway (Thieret 1971; Rank et al. 2004); cf. Gesneriaceae. For seed fatty acids in Orobanche, see (Velasco et al. 2000). Fischer (2004b) notes that a collar-like base of the corolla tube persists after the rest has fallen off - is this a family character? Corolla aestivation is interesting in this clade. The abaxial-lateral pair of corolla lobes commonly envelops the adaxial-lateral lobes, while in Euphrasia and its relatives the abaxial lobe also envelops this latter pair of lobes - both forms of quincuncial aestivation; in a number of other Orobanchaceae, the abaxial lobe envelops all other lobes, i.e. ascending cochleate aestivation (Armstrong & Douglas 1989). For floral development, see Armstrong and Douglas (1989), Endress (1999). Greilhuber (1974) observed endomitotic polyploidization in the cells of the inner tapetum in some genera - but not in Pedicularis, Melampyrum, and Plantaginaceae.
The recently-described Eremitilla is very distinctive morphologically, i.a. the stamens are free from the corolla tube and the anther thecae are more or less embedded in the expanded filament apex Yatskievych & Jiménez, 2009.
For ovules of Cyclocheilon, etc., see Junell (1934), for embryology, see Tiagi (1963) and Arekal (1963), for seed morphology, see Musselman and Mann (1976), for pollen, see Minkin and Eshbaugh (1989) and Lu et al. (2007), for corolla aestivation, see Eichler (1875) and Armstrong and Douglas (1989), for floral development, see Canne-Hilliker (1987), for a general treatment, see Terekhin and Nikitcheva (1981) and Fischer (2004b: as Scrophulariaceae p. pte). Demissew (2004) provides a treatment of Cyclocheilaceae and Harley (2004) one of Nesogenaceae. See the Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008) for general information. Robert Mill caught a number of mistakes around here.
Phylogeny: - For the delimitation and composition of the family, see Young et al. (1999), Wolfe et al. (2005), Bennett and Mathews (2006), etc. Lindenbergia, perhaps sister to the rest of the family (e.g. Wolfe et al. 2005; Albach et al. 2009, but sampling limited) or linking more particularly with a small group of parasitic taxa (Bennett & Mathews 2006: support weak), is autotrophic (Hjertsen 1995). Lindenbergia has tricolporate pollen rather like that common in Lamiales, while the pollen of many other members is triporate and retipilate (Bennett & Mathews 2006). Other than that, a summary of relationships is [holoparasitic clade [Castilleja, Pedicularis, etc. [Euphrasia, Rhinanthus, etc. + tropical clade]]] (Bennett & Mathews 2006).
R. G. Olmstead (pers. comm.) notes that the inclusion in this clade of Nesogenes, Cyclocheilon and Asepalum - ex Cyclocheilaceae and Nesogenaceae and all poorly known - is likely (see also B. Bremer et al. 2002 for Cyclocheilon). There was strong support for Nesogenes (the only taxon of this group included) being sister to the shrubby Radamea (Bennett & Mathews 2006), and these two genera belonged to a strongly supported tropical clade relationships between whose members were then poorly known (Bennett & Mathews 2006). In a more comprehensive analysis, ex Cyclocheilaceae and Nesogenaceae are sister to this tropical clade of Orobanchaceae, within which there was some resolution (Morawetz & Randle 2009, esp. Morawetz et al. 2010); Nesogenes was sister to Graderia and in a clade that includes Strica (Morawetz et al. 2010).
These erstwhile Cyclocheilaceae and Nesogenaceae considerably increase the diversity of Orobanchaceae. Nesogenes has a verticillate inflorescence. Cyclocheilon and Asepalum, the two genera in Cyclocheilaceae, lack much in the way of a calyx but have large bracteoles enveloping the flower bud. They are also shrubs with red roots [?always]; the flowers are solitary, the calyx being at most a minute rim; A didynamous, pollen is 3-colpate, the exine being thickened near the apertures; the placentation is axile or parietal, with 1-5 apotropous ovules/carpel, endothelium?, the funicles are long and the stigma is lingulate. The fruit is a capsule or schizocarp; there is no endosperm (but present in Nesogenes? - Junell 1934). Although Harley (2004) notes similarities between the pollen of Cyclocheilaceae, Nesogenaceae (both have tricolpate pollen, that of Nesogenes is perhaps also pilate) and Orobanchaceae, nothing is known of the stomatal closure and parasitism - or lack of them - in these putative Orobanchaceae. There are other shrubby orobanchs, including Brandisia, an isolated genus of uncertain relationships (Bennet & Mathews 2006).
Rehmannia is a small genus of ca 6 species from China and Korea and the related Trianeophora includes two to three species from China. Oxelman (2005) found that Rehmannia linked very weakly with Phryma, Paulownia, Mazus and Lancea, as well as with genera of Orobanchaceae. In a restricted phylogenetic analysis, Rehmannia linked with Oreosolen (Albach et al. 2007), earlier placed in the Scrophulariaceae s. str. clade (Oxelman et al. 2005), but this may be a rooting problem; in a rather more extended analysis, Jensen et al. (2008b) found that Rehmannia was sister to Orobanchaceae. Albach et al. (2007) recorded the presence of iridoids in Rehmannia, although these are at best very uncommon in Gesneriaceae, and also at least some mannitol, a polyol not occuring in Scrophulariaceae s. str. but found i.a. in some Orobanchaceae, while in a more extended study Xia et al. (2009) placed both Rehmannia and Trianeophora in a strongly supported clade sister to Orobanchaceae (see also Albach et al. 2009), so they are provisionally included here. Rehmannia is not a hemiparasite and has a racemose inflorescence the flowers of which lack bracteoles and have quincuncial corolla aestivation in which the two abaxial-lateral lobes are outside the others, as is common in Orobanchaceae; Trianeophora has bracteoles, there may be a staminode, but floral aestivation is similar (Wang & Wang 2005). Phytochemistry links Triaenophora closely with Rehmannia but Oreosolen is unrelated, linking with Verbascum and relatives and forming a north temperate group in Scrophulariaceae (Jensen et al. 2008b); the first two genera also show more particular similarities with Orobanchaceae (Xia et al. 2009). Rehmannia has the 1:3 nodes and petioles with arcuate + wing bundles so common in Lamiales (pers. obs.).
For a phylogeny of Pedicularis, see Ree (2005), for that of Euphrasia, see Gussarova et al. (2008), for that of Orobanche, see Park et al. (2008), and for that of Castilleja, see Tank and Olmstead (2008, 2009). For further details of relationships, see dePamphilis (1995) and Olmstead and Reeves (1995). Tank et al. (2006) summarize ideas on relationships within the family.
Classification: - See Hjertsen (1995) for a monograph of Lindenbergia. Tank et al. (2009) provide a phylogenetic classification of Castillejinae.
Previous Relationships: - In the past, the argument has usually been over whether or not the holoparasitic Orobanchaceae s. str. were distinct from the Scrophulariaceae s.l., which then included hemiparasitic genera like Euphrasia and Pedicularis (e.g. Boeshore 1920). On the other hand, Rehmannia has often been linked with Titanotrichum and included in Gesneriaceae (Xia et al. 2009 for references).