Down the Slippery Slope: Plastid Genome Evolution in Convolvulaceae

J Mol Evol (2005) 61:292–305 DOI: 10.1007/s00239-004-0267-5 Down the Slippery Slope: Plastid Genome Evolution in Convolvulaceae Sasˇ a Stefanovic´ ,1,2 Richard G. Olmstead1 1 Department of Biology, University of Washington, Box 355325, Seattle, WA 98195-5325, USA 2 Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario, L5L 1C6, Canada Received: 30 August 2004 / Accepted: 10 March 2005 [Reviewing Editor: Dr. Debashish Bhattacharya] Abstract. Cuscuta (dodder) is the only parasitic Key words: Convolvulaceae — Cuscuta — Parasitic genus found in Convolvulaceae (morning-glory fam- plants — Plastid genome — Genomic structural ily). We used long PCR approach to obtain large changes — Plastid evolution portions of plastid genome sequence from Cuscuta sandwichiana in order to determine the size, structure, gene content, and synteny in the plastid genome of this Cuscuta species belonging to the poorly investi- gated holoparasitic subgenus Grammica. These new Introduction sequences are compared with the tobacco chloroplast genome, and, where data are available, with corre- The plastid genome of land plants is highly conserved sponding regions from taxa in the other Cuscuta in size, structure, gene content, and synteny (Palmer subgenera. When all known plastid genome structural 1985, 1991; Palmer and Stein 1986; Downie et al. rearrangements in parasitic and nonparasitic Con- 1991, 1994; Downie and Palmer 1992). Any changes volvulaceae are considered in a molecular phyloge- may be important phylogenetic markers (Palmer netic framework, three categories of rearrangements 1985, 1990), but perhaps more importantly, they may in Cuscuta are revealed: plesiomorphic, autapomor- also be used to study molecular evolutionary and phic, and synapomorphic. Many of the changes in genetic processes involving the structure, function, Cuscuta, previously attributed to its parasitic mode of and evolution of the plant plastid genome (Palmer life, are better explained either as plesiomorphic 1985, 1990, 1991; dePamphilis and Palmer 1990). conditions within the family, i.e., conditions shared The morning-glory family, Convolvulaceae, is one with the rest of the Convolvulaceae, or, in most cases, of the few angiosperm families exhibiting substantial autapomorphies of particular Cuscuta taxa, not plastid genome rearrangement (Downie and Palmer shared with the rest of the species in the genus. The 1992). There is evidence from a small number of synapomorphic rearrangements are most likely to sampled species indicating structural differences in correlate with the parasitic lifestyle, because they the Convolvulaceae plastid DNA (ptDNA) relative represent changes found in Cuscuta exclusively. to other flowering plants. For example, the rpl2 gene However, it appears that most of the affected regions, is interrupted by an intron in most but not all an- belonging to all of these three categories, have prob- giosperms. Based on plastid genome sequences of ably no function (e.g., introns) or are of unknown diverse land plants, including one liverwort (Ohyama function (a number of open reading frames, the et al. 1986), one gymnosperm (Wakasugi et al. 1994), function of which, if any, has yet to be discovered). two basal angiosperms (Goremykin et al. 2003, 2004), five eudicots (Shinozaki et al. 1986a; Spielmann et al. 1988; Sato et al. 1999; Hupfer et al. 2000; Kato et al. Correspondence to: Sasˇ a Stefanovic´ ; email: sstefano@utm. 2000), and five monocots (Posno et al. 1986; utoronto.ca Hiratsuka et al. 1989; Maier et al. 1995; Ogihara et al. 293 2002; Stefanovic´ et al. 2004), it became evident that seedlings not attached to the host and in fruiting se- this intron was present in the common ancestor of pals and ovaries (Panda and Choudhury 1992; flowering plants (and probably land plants), but was Dawson et al. 1994). Thus, both holoparasitic and subsequently lost in some angiosperm lineages (e.g., hemiparasitic species occur in this genus. In holo- Spinacia oleracea; Zurawski et al. 1984; Sehmitz- parasites, found mostly in subgenera Cuscuta and Linneweber et al. 1999). In their large-scale filter Grammica, all carbohydrates are provided by the hybridization survey across angiosperms, Downie host. In herniparasites, confined predominantly to et al. (1991) reported at least six independent losses of subgenus Monogyna, carbohydrates supplied by hosts the rpl2 intron, including in the ancestor of two are supplemented, to a small extent, by the plantÕs representatives of green Convolvulaceae and one own photosynthesis (Hibberd et al. 1998). This Cuscuta species. Outside of Convolvulaceae, no other diversity of photosynthetic ability among Cuscuta member of the Asteridae was found to lack this in- species initiated several physiological studies of pho- tron. In another example, Downie and Palmer (1992) tosynthetic enzymes (Machado and Zetche 1990; van reported the loss of an open reading frame (ORF). der Kooij et al. 2000) and molecular evolution studies ycf1 (= ORF1244 in Nicotiana tabacum), of un- of the plastid genome (Haberhausen et al. 1992; known function, but common to plastid genomes of Bo¨ mmer et al. 1993; Haberhausen and Zetsche 1994; land plants in three nonparasitic Convolvulaceae and Krause et al. 2003). one Cuscuta species (as well as in Poaceae, Fabaceae, Even though the plastids of Cuscuta reflexa (sub- and some other families not closely related to Con- genus Monogyna) have no visible grana and the volvulaceae). Given the conserved nature and distri- number of thylakoids is highly reduced compared to bution of this ORF across the land plants, it is most normal plastids, Machado and Zetche (1990) showed parsimonious to conclude that ycf1 was lost several the presence of both chlorophyll a and b, detected times independently within angiosperms, similar to residual light- and CO2-dependent photosynthetic 14 the rpl2 intron. A third example is the atpB gene activity, and demonstrated incorporation of CO2 which, like rbcL, is very conserved in its length across into carbohydrates. In contrast, the plastids of all angiosperms (except at the very end of the gene). C. europaea (subgenus Cuscuta) lack both grana and However, in the two members of green Convolvula- thylakoids and appear to lack chlorophylls com- ceae for which sequences were known, an in-frame pletely. Consequently, neither ribulose-1,5-bisphos- deletion encoding two amino acids has been reported phate carboxylase-oxygenase (Rubisco) activity nor at the 5¢ end of this gene (Savolainen et al. 2000). light-dependent CO2 fixation could be detected Cuscuta, the only parasitic genus associated with (Machado and Zetche 1990). Further studies, focus- Convolvulaceae, has been the subject of more ing mainly on species of subgenus Grammica, dem- extensive molecular analyses than the rest of this onstrated that in most cases the rbcL gene, family (Machado and Zetche 1990; Haberhausen thylakoids, and chlorophylls are present, and low et al. 1992; Bo¨ mmer et al. 1993; Haberhausen and amounts of the large subunit of Rubisco could be Zetsche 1994; van der Kooij et al. 2000; Krause et al. detected immunologically (van der Kooij et al. 2000). 2003). Most major synoptic works on flowering However, two species from the same subgenus have plants (e.g., Cronquist 1988; Takhtajan 1997) accept been shown to lack thylakoids and chlorophylls, and Cuscuta at the family level, thus implying that it is neither the rbcL gene nor its protein product, Rub- only distantly related to other species in Convolvul- isco large subunit, could be detected (van der Kooij aceae, but recent phylogenetic results indicate it be- et al. 2000). longs within Convolvulaceae (Stefanovic´ et al. 2002; The ptDNA sequence of Cuscuta reflexa, a mem- Stefanovic´ and Olmstead 2004). Cytological, ana- ber of the predominantly hemiparasitic subgenus tomical, and morphological characters indicate the Monogyna, has been studied in most detail from a presence of three well-defined groups in Cuscuta and molecular evolutionary standpoint. Results indicate classification in three subgenera (Cuscuta, Grammica, that this species retains an affected, yet functional, and Monogyna) was proposed by Engelmann (1859; plastid genome (Haberhausen et al. 1992; Bo¨ mmer formalized by Yuncker 1932). Members of this genus et al. 1993; Haberhausen and Zetsche 1994). Epifagus are characterized by twining, slender, pale stems, with virginiana (Orobanchaceae, Lamiales) is the only reduced, scale-like leaves, no roots, and are attached parasitic plant species for which the entire plastid to the host by haustoria, therefore depending entirely genome has been mapped (dePamphilis and Palmer or almost entirely on their hosts to supply water and 1990) and subsequently sequenced (Wolfe et al. 1992). nutrients (Kuijt 1969; Dawson et al. 1994). Many In contrast to this holoparasitic species, which lacks Cuscuta species are characterized also by the reduced all photosynthetic and most putatively chlororespi- amounts or absence of chlorophylls (van der Kooij et ratory ndh genes (dePamphilis and Palmer 1990). al. 2000). However, some species produce significant C. reflexa retains most of the plastid genes generally amounts of chlorophylls, especially in the tips of found in autotrophic land plants, including both 294 those involved in photosynthesis and ‘‘house-keep- tionships among parasitic and autotrophic members ing’’ functions (Haberhausen et al. 1992). However, of the family is necessary. Convolvulaceae have been chlororespiratory (ndh) genes seem to be either al- the

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