Contemplating the First Plantae Frederick W. Spiegel Science 335, 809 (2012); DOI: 10.1126/science.1218515
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PERSPECTIVES In essence, C–H bonds have emerged as a “new” functional group for organic synthesis: They can now be specifically targeted for reactivity in a synthetic sequence. Many challenges remain, however, including the development of chemoselective catalysts that can oxidize aliphatic C–H bonds in the presence of more electron-rich functional groups (such as olefins, aromatic rings, and nitrogen atoms); preparative catalysts for intermolecular aminations, alkylations, and halogenations; and catalysts that can override biases induced by the substrate itself. References
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7. R. H. Crabtree et al., J. Am. Chem. Soc. 101, 7738 (1979). 8. P. Bovicelli, P. Lupattelli, E. Mincione, T. Prencipe, R. Curci, J. Org. Chem. 57, 5052 (1992). 9. W. Adam, R. Curci, M. E. Gonzelez, R. Nunez, Mello, J. Am. Chem. Soc. 113, 7654 (1991). 10. M. P. Doyle, Q.-L. Zhou, A. B. Dyatkin, D. A. Ruppar, Tetrahedron Lett. 36, 7579 (1995). 11. D. F. Taber, R. E. Ruckle Jr., J. Am. Chem. Soc. 108, 7686 (1986). 12. C. G. Espino, J. Du Bois, Modern Rhodium-Catalyzed Organic Reactions (Wiley-VCH, Weinheim, Germany, 2005). 13. L. V. Desai, K. L. Hull, M. S. Sanford, J. Am. Chem. Soc. 126, 9542 (2004). 14. R. Giri et al., Angew. Chem. Int. Ed. 44, 2112 (2005). 15. M. S. Chen, M. C. White, Science 318, 783 (2007). 16. M. S. Chen, thesis, Harvard University (2009). 17. M. S. Chen, M. C. White, Science 327, 566 (2010). 18. N. D. Litvinas, B. H. Brodsky, J. Du Bois, Angew. Chem. Int. Ed. 48, 4513 (2009). 19. K. J. Fraunhoffer, D. A. Bachovchin, M. C. White, Org. Lett. 7, 223 (2005). 20. W. Liu, J. T. Groves, J. Am. Chem. Soc. 132, 12847 (2010). 21. T. Newhouse, P. S. Baran, Angew. Chem. Int. Ed. 50, 3362 (2011).
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rationales given for selectivities (sterics and electronics) made it difficult to see that such selectivity might be general. Newer methods have provided extraordinary examples of predictably selective aliphatic C–H oxidations in a wide range of complex-molecule settings. In the synthesis of the alkaloid tetrodotoxin, selective intramolecular 3° aliphatic C−H alkylation and amination reactions, made possible by newer Rh-acetamide catalysts, were used to install a section of the carbon skeleton and a key amine functionality (see the figure, panel G) (10, 12). The advent of Fe(PDP) catalysis enabled intermolecular aliphatic C–H oxidations to occur at both 3° and 2° sites in a wide range of complex terpenes (see the figure, panel H). Despite dense functionality, one equivalent of substrate could be used to afford preparatively useful amounts of monooxidized products (15–17).
10.1126/science.1207661
EVOLUTION
Contemplating the First Plantae
What characterized the first photosynthetic eukaryotes?
Frederick W. Spiegel
T
he cells of photosynthetic eukaryotes such as plants and algae contain organelles, called plastids or chloroplasts, responsible for photosynthesis. Plastids contain some DNA, a vestige of their origin from free-living cyanobacteria. On page 843 of this issue, Price et al. (1) use comparative genomics with the obscure algal protist, Cyanophora paradoxa, to propose a resolution to the question of how plastids have spread through the eukaryotes. By understanding the implications of their results, we may be able to picture the overall characteristics of the very first alga. In recent decades, it has become clear that photosynthetic eukaryotes rose through endosymbiosis (2, 3). In this process, a eukaryotic cell becomes inhabited by a photosynthetic cell. A complex set of events ensues, including transfer of genes from the colonizer’s genome to the host’s nuclear genome. This is followed by the evolution of mechanisms that allow proteins encoded by these transferred genes back into the colonizer so that it can still photosynthesize. The result is a chimeric organism in which the colonizer has become the plastid. If the colonizer was a cyanobacteDepartment of Biological Sciences, SCEN 601, 1 University of Arkansas, Fayetteville, AR 72701, USA. E-mail:
[email protected]
rium, the chimera is said to be the product of primary endosymbiosis. If the colonizer was a photosynthetic eukaryote, the chimera is the product of secondary or higher-order endosymbiosis (2, 3). Because of their complex genetic histories, the relationships among chimeric organisms can be difficult to interpret (3). It can also be challenging to infer relationships between photosynthetic eukaryotes and their closest relatives that never had plastids. Phylogenetic data suggest that all plastids in today’s photosynthetic eukaryotes can be traced back to just two different cyanobacterial colonizers (3). One of these colonizers led to the primary plastids in the photosynthetic amoeba Paulinella (3), but this is not the focus of Price et al., who investigate primary endosymbiotic events thought to have occurred more than a billion years ago. Today’s Glaucophyta (~13 species, including C. paradoxa), red algae (~6000 species), and green algae and land plants (over 300,000 species) all have primary plastids descended from one cyanobacterial ancestor (1, 2). All other eukaryotic algae have secondary or higher-order plastids derived from either red or green algae (1–3). The data have been equivocal as to how many times that cyanobacterium colonized eukaryotic hosts. According to the Plantae hypothesis, it entered only one protist; the resulting chi-
mera became the sole ancestor to the eukaryotic supergroup Plantae (or Archaeplastida), which contains the glaucophytes, red algae, and land plants and green algae. Alternative “non-Plantae” hypotheses suggest that the cyanobacterium that was ancestral to the plastids of glaucophytes, red algae, and land plants and green algae must have colonized different protists more than once (4-7). Acceptance of the Plantae hypothesis requires that Plantae be monophyletic and that it cannot include any secondarily photosynthetic algae or any primitively plastid-free eukaryotes. In other words, a well-supported phylogeny must show that only the glaucophytes, red algae, and land plants and green algae evolved from one chimeric ancestor. To test this hypothesis, Price et al. compare genomes from the most complete set of photosynthetic eukaryotes to date. They provide a number of independent lines of evidence, including data about genes that are independent of the plastids. All their data strongly support the Plantae hypothesis. The glaucophytes are the most speciespoor Plantae. Many phylogenies show them branching most basally in Plantae, that is, diverging before the separation of the reds and the greens (2). In such cases, we often have a careless tendency to think of the species-poor branch as “primitive” in all
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PERSPECTIVES
Anterior flagellum Kinetosomes/basal bodies
MLS/PPKS Nucleus
Host phagocytosing cyanobacterial ancestor of plastid Mitochondrion Microtubule bands
Hypothetical first alga in Plantae. After a phagocytic host was colonized by a cyanobacterium (inset), the chimeric first alga (shown in ventral view) probably had the following characters (5, 9–15): a nucleus, mitochondrion, flagella, and sex found in all major lineages of eukaryotes; a ventral groove supported by microtubule bands shared by Cyanophora, Excavata, SAR (Stramenopila, Alveolata, and Rhizaria), and Amoebozoa; a band of microtubules with a laminated structure at its proximal end (multilayered structure/parakinetosomal structure, abbreviated as MLS/PPKS) shared by these groups and streptophyte greens; and flattened vesicles underlying the plasma membrane shared by glaucophytes, SAR, and Hacrobia. Unique features of the first alga were the primary plastid and loss of phagocytosis.
bers of Plantae with those ity. It is nice that an obscure protist (her preshared with organisms in ferred term was protoctist) was so integral in Plastid other major eukaryotic lin- advancing the story of how plastids spread Flattened vesicles Microtubule bands eages (9-15), some of the through the eukaryotes. characteristics of the first Plasma membrane References alga can be postulated (see 1. D. C. Price et al., Science 335, 843 (2012). Posterior flagellum the figure). 2. P. J. Keeling, Am. J. Bot. 91, 1481 (2004). Some of the traits 3. C. X. Chan, J. Gross, H. S. Yoon, D. Bhattacharya, Plant Physiol. 155, 1552 (2011). inferred for the first Plan4. H. Nozaki et al., Mol. Biol. Evol. 24, 1592 (2007). tae (see the figure) may also 5. V. Hampl et al., Proc. Natl. Acad. Sci. U.S.A. 106, 3859 respects and the species-rich lineage as com- provide clues to the properties of eukaryotes (2009). 6. D. Baurain et al., Mol. Biol. Evol. 27, 1698 (2010). pletely “advanced.” However, all organisms in general 1 to 1.5 billion years ago. Careful 7. C. J. Howe et al., Phil. Trans. R. Soc. B. 363, 2675 (2008). are mosaics of inherited homologous char- examination of the literature on protist cells, 8. M. Sato et al., Planta 229, 781 (2009). acters. Some characters were derived after a combined with phylogenomic results such as 9. J. P. Mignot et al., J. Protozool. 16, 138 (1969). common ancestor had undergone speciation those of Price et al., may elucidate the evolu- 10. A. G. B. Simpson, A. J. Roger, Curr. Biol. 14, R693 and are unique to the lineage in which they tionary events in eukaryotes at all levels, from 11. (2004). S. M. Adl et al., J. Eukaryot. Microbiol. 52, 399 (2005). appear. Some characters were derived in the the molecular to the morphological. 12. F. W. Spiegel, Proc. Biol. Sci. 278, 2096 (2011). last common ancestor of the lineage and its Lynn Margulis, who championed the idea 13. F. W. Spiegel et al., Protoplasma 132, 115 (1986). sibling lineages and are unique to that set of that eukaryotic cells were chimeras of hosts 14. N. Okamoto et al., PLoS ONE 4, e7080 (2009). 15. F. Burki et al., PLoS ONE 2 (8), e790;10/1371/ lineages. Some characters, the most primi- and endosymbionts long before the hypothjournal.pone.0000790 (2007). tive set, were those that the common ances- esis was accepted, died on 22 November 16. M. Schaechter, Science 335, 302 (2012). tor inherited from its ancestors deeper in the 2011 (16). It is a shame that she missed out phylogeny and are shared widely. We need an on this most recent vindication of her tenac10.1126/science.1218515 independently derived phylogeny to be able to tell what category a homology falls into. Price et al. show unambiguously that C. paradoxa has both primitive and derived GEOCHEMISTRY genomic characters. Some are indicative of its membership in Glaucophyta to the exclusion of other Plantae. Others are indicative of its inclusion in Plantae to the exclusion of other eukaryotes. Finally, there are some that are indicative of being eukaryotic. Most important, Price et al. show that the plastids Adina Paytan of glaucophytes are not completely primitive with respect to the plastids of other Plantae Changes in the lithium isotope composition of seawater over the past 70 million years elucidate (8, 9). C. paradoxa is, as should be expected, the links between weathering and climate. a mosaic of characters. The authors also note that, despite the wealth of data at their disarth is sustained as a habitable planet varied through Earth’s history in response to posal, they could not resolve which of the through close interactions and feed- changes in global climate and tectonics (2, 3), three major lineages of Plantae branched backs among the lithosphere, hydro- making past records of seawater chemistry a basally with respect to the other two. Thus, sphere, atmosphere, and biosphere (1). These powerful archive for reconstructing how these the glaucophytes may not even have a posi- interactions occur through material and interactions and feedbacks changed over time. tion in the Plantae tree of life to allow them to energy transfer between Earth’s reservoirs, On page 818 of this issue, Misra and Froelich be considered “primitive.” referred to as global biogeochemical cycles, (4) report how the lithium isotopic composiPrice et al. do not discuss the appearance and result in chemical and physical changes tion of seawater (δ7LiSW), recorded in shells or life history of the original Plantae, but within each reservoir. Seawater chemistry has of tiny organisms living in the ocean, has their conclusion that Plantae is monophyletic changed over the past 70 million years. The allows us to do just that, because their data are results illustrate the tight interplay among the Earth and Planetary Sciences Department, University of independent of morphological and life cycle California, Santa Cruz, CA 95064, USA. E-mail: apaytan@ location of mountain belts, mountain erosion characters. By comparing features of mem- ucsc.edu processes, and climate.
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Ventral groove
Mountains, Weathering, and Climate
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