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(Tageteae, Asteraceae), a C4 Genus of the Neotropics

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(Tageteae, Asteraceae), a C4 Genus of the Neotropics 6 LUNDELLIA DECEMBER, 2016 MOLECULAR PHYLOGENY OF PECTIS (TAGETEAE,ASTERACEAE), A C4 GENUS OF THE NEOTROPICS, AND ITS SISTER GENUS POROPHYLLUM Debra R. Hansen,1 Robert K. Jansen,1 Rowan F. Sage,2 Jose´ Luis Villasen˜or,3 and Beryl B. Simpson1 1Department of Integrative Biology, The University of Texas at Austin, 205 West 24th Street, Austin, Texas 78712, USA, email: [email protected] 2Department of Ecology & Evolutionary Biology, University of Toronto, 25 Willcocks Street, Room 3055, Toronto, Ontario, Canada M5S 3B2 3Departamento de Bota´nica, Instituto de Biologı´a, Universidad Nacional Auto´noma de Me´xico, Apartado Postal 70-233, 04510 Me´xico, D.F. Mexico Abstract: Pectis is a genus of 690 xeric adapted New World species. Previous molecular phylogenetic studies showed Pectis closely related to Porophyllum, and one analysis resolved Porophyllum species nested within Pectis. Some Pectis species are known to use C4 photosynthesis. Here we investigate the phylogeny of Pectis and Porophyllum, examine the ploidy levels and geographical distribution of Pectis species in light of its phylogeny, and infer the origin and extent of C4 photosynthesis in both genera. Chloroplast and ITS data from 78 Pectis and 22 Porophyllum species were used to test the monophyly of Pectis and its previously described sections. Carbon isotope data were obtained to infer the photosynthetic pathway of 80 species, and the results mapped on the inferred phylogenies to determine the timing and pattern of evolution of the C4 pathway. The ITS dataset supports a monophyletic Pectis sister to a monophyletic Porophyllum, while the chloroplast dataset places two Porophyllum species sister to a combined Pectis+Porophyllum clade. Five well-supported lineages are recovered in 13 Pectis. All Pectis sampled have L C values consistent with C4 photosynthesis, and all 13 Porophyllum species sampled have L C values consistent with C3 photosynthesis. We conclude that Pectis is monophyletic but only two of its recognized sections are monophyletic. Porophyllum is monophyletic but its sections are not. Porophyllum amplexicaule and Pr. scoparium should be treated as members of a new genus. The switch to the C4 pathway in Pectis happened in the late Miocene, probably in north/ central Mexico, at or after the divergence of Pectis and Porophyllum. This location and timing is consistent with the evolution of C4 photosynthesis in other North American eudicot lineages, suggesting similar environmental conditions may underlie the switch to C4 photosynthesis. Keywords: Asteraceae, C4 photosynthesis, Pectis, Pectidinae, Porophyllum, Tageteae. Pectis L. is the largest genus in the recently been naturalized in Taiwan (Jung marigold tribe (Pectidinae: Tageteae: Aster- et al., 2011). Pectis is distinguished from the aceae), and comprises about 90 annual and other Tageteae by its combination of simple, perennial species (Keil, 2006) adapted to opposite leaves with pairs of bristles at their warm, arid regions of the New World. bases; phyllaries that are each adnate to, and Species are found in deserts, thorn scrub, subtend the base of, a ray floret (often falling coastal plains, savannas, and openings in as a single unit at maturity) and very short seasonally dry tropical forests and oak-pine and often densely papillose style branches. woodlands. Pectis is most diverse in Mexico Most Pectis species have noticeable oil glands and the Caribbean, but its species range on their phyllaries and on the margins or from Wyoming and Nebraska in the U.S. to undersides of their leaves, a character they southern Brazil and northern Argentina. share with other genera in Tageteae subtribe Two species are endemic to the Galapagos, Pectidinae. The oil of Pectis species often has one is introduced in Hawaii, and one has a strong medicinal, spicy, or lemony scent, LUNDELLIA 19:6–38. 2016 Lundellia lund-19-00-02.3d 16/11/16 20:02:10 6 NUMBER 19 HANSEN ET AL.: PECTIS AND POROPHYLLUM PHYLOGENY AND C4 PHOTOSYNTHESIS 7 and various Pectis species have traditional (Cassini, 1819) along with other former culinary or medicinal uses (Asprey & Heliantheae genera with leaves and phylla- Thornton, 1953; Bye, 1996). A few species ries bearing glands. Based on molecular and have a distasteful odor likened to that of morphological similarities, Panero (2007) stinkbugs, leading to the common name included Tageteae in his Heliantheae Alli- “cinchweed.” Pectis angustifolia has a high ance, placing the traditional Tageteae genera, thimole content (Albers, 1942), and Pectis including Pectis and Porophyllum Guett., papposa has been suggested as a potential into subtribe Pectidinae. source of commercial food and beverage The most extensive taxonomic treat- flavoring because of its high cumaldehyde ments of Pectis are by Gray (1849, 1852, and carvone content (Bradley & Haagen- 1884, 1888), Fernald (1897), and Keil (1975, Smit, 1949). Phototoxic, antibacterial, and 1977a, 1978). Gray described six subgeneric antifungal properties of Pectis oil have been divisions within Pectis based largely on reported (Downum et al., 1985; Downum & differences in pappus elements (1849, Rodriquez, 1986; Downum et al., 1989; da 1852). By 1883 Gray recognized just three Silva et al., 2005; Soares et al., 2009). Pectis is sections, Pt. sect. Eupectis, Pt. sect. Pecto- noteworthy because some species previously thrix, and Pt. sect. Pectidium. In 1897 surveyed were shown to use C4 photosyn- Fernald elevated the sections to subgenera, thesis, a photosynthetic pathway that confers and used pappus characters to assign 34 enhanced efficiency in conditions of high North American species to five subgenera: heat and high light intensity (Sage et al., Eupectis, Heteropectis, Pectothrix, Pectidopsis 2011). C4 photosynthesis is uncommon in (resurrected from Gray 1852) and Pectidium. eudicots, and especially rare in the Aster- Fernald’s treatment remains the most com- aceae, in which just 0.3% of the genera use plete revision to date. the C4 pathway (Kellogg, 1999). In the mid-70s, Keil revised four of the The goals of the present study were to Pectis subgenera. For Pectis subg. Hetero- clarify the relationship between Pectis and pectis (1975) and Pectidium (5 Pt. sect. Porophyllum, test the monophyly of pre- Pectis, Keil, 1978) he followed Fernald’s viously described generic subdivisions, and treatment of the species (two species in each determine the age, origin, and extent of the section) but reduced the subgenera to evolution of C4 photosynthesis in Pectis.We sections. Although various workers used primarily focused on the phylogeny of Pectis, pappus characters to segregate Pectis into but sampled deeply in Porophyllum to different genera (Lessing, 1830; de Candolle, confirm the relationship between the two 1836) or divide it into sections or subgenera genera. Using a greatly expanded sample of (Gray, 1849, 1884; Fernald, 1897), these 78 Pectis and 22 Porophyllum species and characters can be variable, even within varieties, we provide the first molecular populations. In 1977, Keil dismantled sub- evidence for relationships within the genera, genera Pectothrix and Pectidopsis, using some and suggest direction regarding sectional species from each (as well as a few pre- organization for both Pectis and Porophyl- viously-unassigned taxa) to form a redefined lum. We also present carbon isotope values Pt. sect. Pectothrix. Keil included species in for 62 Pectis and 18 Porophyllum species and Pt. sect. Pectothrix based on a combination varieties, the first comprehensive survey of of characters – position of foliar glands, photosynthetic pathway for both genera. shape of capitula, number of ray and disc TAXONOMY. Linnaeus included two florets, and corolla pubescence. In spite of species of Caribbean Pectis (Pt. ciliaris L. these significant revisions, fewer than half of and Pt. linifolia L.) when describing the Pectis species have been assigned to sectional genus in 1759. Pectis was included in the rank, and no treatment has covered the full original circumscription of tribe Tageteae geographic range of the genus. Lundellia lund-19-00-02.3d 16/11/16 20:02:11 7 8 LUNDELLIA DECEMBER, 2016 Porophyllum is a genus of about 25 CHROMOSOME NUMBERS IN PECTIS AND species of annual herbs and perennial shrubs POROPHYLLUM. The base chromosome num- (or subshrubs) found from the southwestern ber for Pectis is x 5 12 (Keil, 1977). Of the United States to southern Brazil, including 54 Pectis species and varieties for which the Caribbean islands. Some are arid- chromosomes have been counted, 39 (72%) adapted but, unlike Pectis, many species of are diploid and 15 are polyploid (Appendix Porophyllum occur in mesic areas. Like S2 in Supplemental Data with the online Pectis, they have prominent oil glands on version of this article). Eight species are their leaves and phyllaries but in Porophyl- tetraploid, two of which (Pt. longipes and Pt. lum the scent is usually described as strong repens) have been reported as having diploid and unpleasant. The genus differs from individuals as well. Six Pectis are hexaploid, others in the Tageteae by its combination among them Pt. saturejoides, which has also of well-developed leaves, discoid heads, and been reported as diploid. Pectis ericifolia is a pappus entirely of bristles. In the most the only octoploid reported in the genus. recent treatment of the genus, Johnson Most Porophyllum species have a base num- (1969) placed Porophyllum species into Pr. ber of x 5 12, but five species (Pr. sect. Hunteria Moc. & Sesse´ (DC.) and Pr. lanceolatum, Pr. macrocephalum, Pr. puncta- sect. Porophyllum based primarily on leaf tum, Pr. ruderale and Pr. viridiflorum) have characters and habitat. Species of Pr. sect. been counted as x 5 11. Of these, Pr. Hunteria have thick leaves that are sessile to punctatum and Pr. ruderale have also been short-petioled, with narrow blades and are reported with x 5 12 counts. Of the 14 distributed in arid or semi-arid Mexico and Porophyllum species for which the ploidy the southwestern U.S. Species of Pr. sect. level is known, nine are diploids, four are Porophyllum have thin, petioled leaves that tetraploid and Pr.
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