PHYLOGENY AND ORIGINS OF HOLOPARASITISM IN OROBANCHACEAE 1

American Journal of Botany 100(5): 971–983, 2013 ; http://www.amjbot. org/ © 2013 Botanical Society of America Orobanchaceae Vent. (the broomrape family) comprise approximately 2060 species in 90 genera that are distributed across all continents and major islands with the exception of Antarctica. Narrow circumscriptions of the family included only nonphotosynthetic species (holoparasites) ( Ventenat, 1799 ; Beck, 1930 ), whereas broader circumscriptions have combined Orobanchaceae sensu stricto with parasitic members of von Wettstein’s (1891) rhinanthoid Scrophulariaceae ( Bellini, 1907 ), which is supported by morphological and anatomical character states ( Boeshore, 1920 ; Armstrong and Douglas, 1989 ). Phylogenetic analyses of nucleotide data support this broader circumscription, suggesting that holoparasitism has evolved multiple times within a wider group of photosynthetic parasites (hemiparasites), most of which were traditionally placed in Scrophulariaceae ( dePamphilis et al., 1997 ; Young et al., 1999 ; Wolfe et al., 2005 ; Bennett and Mathews, 2006 ). A few holoparasitic (e.g., species of Orobanche ) and hemiparasitic (e.g., species of Striga ) parasites are among the most serious of agricultural pests, a trait that has motivated substantial amounts of research into the interactions between host and parasite ( Press and Graves, 1995 ; Heide-Jørgensen and Kuijt, 1995 ; Heide-Jørgensen, 2008 ; Yoder and Scholes, 2010 ). Other members of the family are ecologically important due to direct impacts on community biomass and diversity, on plant–herbivore interactions, and on nutrient cycling ( Press and Phoenix, 2005 ). The impact is not always negative; in several cases, hemiparasitic Orobanchaceae have been shown to increase biodiversity and nutrient availability (reviewed in Press and Phoenix 2005 ). Because there are multiple transitions from hemito holoparasitism within the family, it serves as an excellent model to explore molecular evolutionary, genetic, and physiological changes that accompany the evolution of holoparasitism. Most recent studies suggest that Orobanchaceae are most closely related to Phrymaceae (including Mimulus and Phryma ), Paulowniaceae ( Paulownia ), and the genera Rehmannia and Mazus ( Xia et al., 2009 ). Previous phylogenetic studies have identifi ed the autotrophic genus, Lindenbergia , as the sister genus to all other Orobanchaceae ( Young et al., 1999 ; Bremer et al., 2001 ; Olmstead et al., 2001 ). The earliest molecular trees for Orobanchaceae in the broad sense provided limited insight into phylogenetic structure within the family, due partly to limited taxonomic sampling and partly to the limited information in the plastid loci that encode an intron maturase and a ribosomal protein subunit ( matK and rps2 , respectively) and in the nuclear ribosomal internal transcribed spacer region (ITS). The most extensive taxon sampling to date within Orobanchaceae used a low-copy nuclear locus, phytochrome A ( PHYA ), and 1 Manuscript received 27 August 2012; revision accepted 28 February 2013. The authors thank D. Boufford, A. Colwell, A. Miller, R. Nyffeler, R. Ree, G. Schneeweiss, R. Scotland, K. Steiner, D. Tank, J. Wood, and G. Yatskievych for tissue and/or DNA samples; Gaius Augustus, Benjamin Tseng, Daniel Sachs, Devon Castillo, Angelico Razon, Julia Berthet, Nidia Arguedas, Chris Randle, Jeff Morawetz, and members of the Wolfe laboratory group for laboratory assistance; and Dick Olmstead, Dave Tank, and one anonymous reviewer for helpful comments on the manuscript. 6 Author for correspondence (e-mail: smathews@oeb.harvard.edu)