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Asteraceae) (Angiosperm Evolution/Molecular Systematics/Mutisieae/Barnadesiinae) ROBERT K

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Asteraceae) (Angiosperm Evolution/Molecular Systematics/Mutisieae/Barnadesiinae) ROBERT K Proc. NatI. Acad. Sci. USA Vol. 84, pp. 5818-5822, August 1987 Evolution A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae) (angiosperm evolution/molecular systematics/Mutisieae/Barnadesiinae) ROBERT K. JANSEN*t AND JEFFREY D. PALMER Department of Biology, University of Michigan, Ann Arbor, MI 48109 Communicated by Peter H. Raven, May 7, 1987 (receivedfor review February 10, 1987) ABSTRACT We determined the distribution of a chloro- Cronquist's (1, 4, 7) subfamilial classification for the Aster- plast DNA inversion among 80 species representing 16 tribes of aceae have been proposed in the last 12 years (8-10). the Asteraceae and 10 putatively related families. Filter hy- We are investigating chloroplast DNA (cpDNA) variation bridizations using cloned chloroplast DNA restriction frag- in the Asteraceae to resolve phylogenetic relationships at ments oflettuce and petunia revealed that this 22-kilobase-pair higher taxonomic levels. Our previous study (11) showed that inversion is shared by 57 genera, representing all tribes of the the 151-kilobase (kb) cpDNAs of two species in the family Asteraceae, but is absent from the subtribe Barnadesiinae of (Lactuca sativa and Barnadesia caryophylla) are colinear the tribe Mutisieae, as well as from all families allied to the throughout the genome, with the exception of a single 22-kb Asteraceae. The inversion thus defmes an ancient evolutionary inversion. The conservative organization of the chloroplast split within the family and suggests that the Barnadesiinae genome among land plants (12, 13) makes such rearrange- represents the most primitive lineage in the Asteraceae. These ments potentially valuable characters for phylogenetic stud- results also indicate that the tribe Mutisieae is not mono- ies. Here we report on the evolutionary direction of the phyletic, since any common ancestor to its four subtribes is also inversion in the Asteraceae by comparing the chloroplast shared by other tribes in the family. This is the most extensive genomes of Lactuca and Barnadesia with that of an out- survey of the systematic distribution of an organelle DNA group, Petunia hybrida (Solanaceae). We also examine the rearrangement and demonstrates the potential of such muta- distribution and phylogenetic significance of this rearrange- tions for resolving phylogenetic relationships at higher taxo- ment. nomic levels. MATERIALS AND METHODS The Asteraceae is one of the largest and economically most important families of flowering plants and consists of 12-17 cpDNAs were isolated by the sucrose gradient technique tribes, approximately 1100 genera, and 20,000 species (1). A (14). Where tissue amounts were limited, total DNA was combination of several specialized morphological character- isolated (15) and further purified by centrifugation in CsCl/ istics (e.g., capitula, highly reduced and modified flowers, ethidium bromide gradients. Restriction endonuclease diges- inferior ovaries, syngenesious anthers) strongly supports the tions, electrophoresis, transfer of DNA fragments from naturalness of the family. Cronquist (1) emphasized the agarose gels to Zetabind filters (AMF Cuono), and hybrid- distinctness of the Asteraceae by placing it in a monotypic izations were performed as described (11, 14). Recombinant order at the most advanced position within the subclass plasmids containing cpDNA fragments from Lactuca and Asteridae. In addition to its large size, the family has a Petunia were described previously (11, 16). cosmopolitan distribution and is highly diversified in its habitat preferences and life forms. This diversity includes RESULTS aquatics, herbs and shrubby trees in temperate, tropical, and Filter hybridizations using cloned restriction fragments (16) arid environments, and trees in tropical rain forests. Species from petunia (Petunia hybrida, Solanaceae) were performed ofAsteraceae are ofwide economic importance as vegetables to assess cpDNA genome arrangement in the Asteraceae. (lettuce, artichokes, endive), sources of oil (sunflower, saf- The petunia genome appears to have the ancestral cpDNA flower) and insecticides (pyrethrum), and garden ornamen- arrangement for angiosperms, since it is colinear with the tals (chrysanthemum, dahlia, marigold, and many others). genomes of a fern, a gymnosperm, and several diverse Although there is some controversy concerning its age (2, angiosperms (17-21). Barnadesia cpDNA is colinear with the 3), fossil evidence (4, 5) and biogeographical considerations petunia genome (Fig. 1) and therefore has the same gene (6) suggest that the Asteraceae originated in the middle to order as the ancestral angiosperm type. In contrast, lettuce upper Oligocene (30 million years ago) and subsequently (Lactuca sativa) cpDNA has a derived inversion in the large underwent rapid radiation. This rapid diversification has single copy region, as evidenced by the hybridization of posed special problems for understanding phylogenetic rela- nonadjacent petunia Pst I fragments of 9.0 and 15.3 kb to the tionships at higher taxonomic levels. Previous attempts (4, same two regions of the lettuce genome. For example, both 7-10) at constructing phylogenies have relied on comparative of these petunia probes hybridize to 7.5-kb Sac I-Sal I and anatomical, chromosomal, embryological, micromolecular, 6.7-kb Sac I lettuce restriction fragments (Fig. 1). Further- morphological, and palynological features. These studies more, the atpA through rpoB genes have an inverted order have been largely unsatisfactory because of the repeated and are transcribed in the opposite direction in lettuce parallel and convergent evolution of these characters. For relative to Barnadesia (Fig. 1; ref. 11). example, three major and highly divergent reformulations of Abbreviation: cpDNA, chloroplast DNA. The publication costs of this article were defrayed in part by page charge *Present address: Department of Ecology and Evolutionary Biology, payment. This article must therefore be hereby marked "advertisement" University of Connecticut, Storrs, CT 06268. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 5818 Downloaded by guest on October 1, 2021 Evolution: Jansen and Palmer Proc. Nati. Acad. Sci. USA 84 (1987) 5819 E E Bg S E E t " r9 .G '4 'd' aSZ, CI IQ mm * rn~~~~~ ~~~~~~~~~~~m~m ~~~~u co ~~~~~~~~~~~~~~~~ M mu mmTT m t T1ttIf NwIf I Lettuce -Dt1 X--.-L, :+lk+ Petunia 7.6 '4.6 19 2 4. 7614 9. 9. 15.3 13.1 8.0 1411 8.9 11.4 .IAI'- Q00) IMc "p 4 rn1 m m '4IR -I IN a IN on ------ *9U~~~4*4-~ g- ZC U;vUe QUrn Q Barnadesia Petunia FIG. 1. Physical maps showing the arrangement of homologous sequences in the petunia and either lettuce or Barnadesia chloroplast genomes. Numbers indicate fragment sizes in kb. Each of 15 petunia fragments was hybridized to filter blots containing Nsi I and Sac I fragments of cpDNA from lettuce and Barnadesia. The lettuce or Barnadesia fragments to which the probes hybridize are indicated by lines leading from the petunia fragments to the lettuce or Barnadesia fragments. The heavy black lines on each map indicate the inverted repeat and the arrows at far right show the orientation (i.e., direction of transcription) of mapped genes. The enlargements of the 7.5-kb Sac I-Sal I and 6.7-kb Sac I restriction fragments show the four inversion endpoint fragments used as probes. Arrows pointing at the EcoRl sites indicate the approximate locations of the inversion endpoints. Lettuce and Barnadesia restriction site and gene mapping data are from ref. 11 and petunia data are from ref. 16. Restriction sites shown: m, Nsi I; A, Pst I; *, Sac I; *, Sal I; Bg, Bgl 1I; E, EcoRI; S, Sal 1. Many additional taxa were surveyed for the inversion by in those genomes that contain the lettuce inversion. This performing filter hybridizations using cloned lettuce cpDNA situation is illustrated in Figs. 2 and 3, in which the two fragments that contain the inversion endpoints. The 7.5-kb inversion endpoint fragments from lettuce are hybridizing to Sac I-Sal I and 6.7-kb Sac I lettuce fragments were used as Sac I fragments of 14.7 and 17.0 kb in Vernonia. Similar hybridization probes against filter blots containing 12 restric- hybridization results are evident for Helianthus and Trixis tion enzyme digests of DNA from one species of each of 80 (Fig. 3), which are both members of the Asteraceae. In two genera representing 10 putatively allied families and 16 tribes contrast, in those genomes that are not rearranged, the Asteraceae 1). The 7.5-kb Sac I-Sal I and 6.7-kb lettuce probes will hybridize to two of the same restriction of (Table 6.7-kb Sac I probes will hybridize to different restriction fragments fragments. For example, the 7.5-kb Sac I-Sal I and Sac I lettuce probes both hybridize to Sac I fragments of 5.8 and 14.9 kb in Barnadesia (Figs. 2 and 3). The autoradi- ograms that of three related 5.8 _ t 14.9 (Fig. 3) reveal representatives tBarnadesia families, Cephalaria (Dipsacaceae), Pentas (Rubiaceae), and Scaevola (Goodeniaceae), also lack the 22-kb inversion. The results of the inversion survey for all 80 examined taxa are summarized in Table 1. The genome arrangements for 69 9Lettuce of these taxa have been confirmed by constructing complete restriction maps (R.K.J., H. Michaels, and J.D.P., unpub- lished data). The inversion is absent from all putatively allied 14.7 Vernonia families and, within the Asteraceae, from the subtribe Barnadesiinae of the tribe Mutisieae. All other examined members of the Asteraceae, including the three other sub- tribes in the Mutisieae, were found to have the inversion. The 80 genera surveyed represent the major evolutionary lineages within the 16 tribes of Asteraceae and 10 related families. We 7.5 6.7 JLettuce are confident that the selection of only one species from each genus is an adequate sampling because more extensive FIG. 2. Physical maps showing the arrangement of homologous studies of 60 species in Carthamus (R.
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