P ERSPECTIVES narcotic properties are recorded for chemi- because reactions involving platinum were References and Notes cally unreactive N gas, giving rise to how Bartlett initiated his first xenon chem- 1. C. Sanloup et al., Science 310, 1174 (2005). 2 2. G.Wilson, The Life of the Honourable Henry Cavendish “l’ivresse des grandes profondeurs” (the istry experiments (5). Perhaps the capsules (Cavendish Society, London, 1851). “rapture of the deep”—the intoxication expe- are not completely innocent in the high- 3. W. Ramsay, The Gases of the Atmosphere, the History of Their Discovery (Macmillan, London, 1915). rienced by divers) (8). An early explanation pressure and high-temperature experi- 4. G. N. Lewis, J. Am. Chem. Soc. 38, 762 (1916). for xenon anesthesia was given by Pauling, ments, because they might act as reaction 5. N. Bartlett, Proc. Chem. Soc. 1962, 218 (June 1962). who suggested that clathrate hydrate struc- sites for xenon in addition to providing the 6. N. N. Greenwood, A. Earnshaw, Chemistry of the Elements (Pergamon, Oxford, 1984). tures encapsulating the rare gas atoms were host for platinum-silicon alloys formed dur- 7. N. P. Franks, R. Dickinson, S. L. de Sousa,A. C. Hall,W. R. formed near synapses, impeding interneu- ing the presumed silicate reduction reac- Lieb, Nature 396, 324 (1998). 8. J. Cousteau, The Silent World (Reprint Society, London, ronal transmission (9). Recent results suggest tions. However, even if that is the case, it 1953). a more interesting solution. The protein com- does not rule out the potential importance of 9. L. Pauling, Science 134, 15 (1961). plexes that form transmembrane ion pumps metal-silicate reactions involving xenon 10. P. Bennett, D. Elliott, The Physiology and Medicine of Diving (Saunders, New York, ed. 5, 2003). associated with neurotransmitters contain within Earth. These results could presage a 11. N. P. Franks,W. R. Lieb, Nature 300, 487 (1982). hydrophobic regions. It is thought that neutral new area in xenon solid-state chemistry 12. E.Anders,T. Owen, Science 198, 453 (1977). 13. A. P. Jephcoat, Nature 393, 355 (1998). species such as xenon and N2 might enter under high-pressure conditions, which 14. The author is supported by a Wolfson Royal Society these regions, especially at high pressure, and might be extended to other noble gases that Research Merit Award Fellowship. interfere with the neuronal process to result in have not yet been chemically awakened, if anesthesia and narcosis (10, 11). the conditions are made right. 10.1126/science.1121022 Highly oxidizing conditions are usually needed to activate xenon into true chemical PALEONTOLOGY reactivity and to form bonds with species such as oxygen. However, Sanloup et al. have used optical spectroscopy and synchrotron x- Dinosaurs Dined on Grass ray diffraction combined with chemical analysis to show that xenon can react with Dolores R. Piperno and Hans-Dieter Sues natural silicate materials, including SiO2, to form xenon oxide species under the high- rasses (family or Gramineae), have long depicted dinosaurs as grazing on pressure, high-temperature conditions found with about 10,000 extant species, are conifers, cycads, and ferns in landscapes in Earth’s crust (1). This is an important Gamong the largest and most ecologi- without grasses. The work of Prasad et al. result, because the noble gases form useful cally dominant families of flowering , (1) is the first unambiguous evidence that geochemical tracers. Formed by radioactive and today provide staple foods for much of the Poaceae originated and had already decay processes or encapsulated within deep humankind. Dinosaurs, the dominant mega- diversified during the Cretaceous. The Earth materials since the formation of the herbivores during most of the Mesozoic Era research shows that phytoliths, which planet, the “inert” gaseous elements are (65 to 251 million years ago), are similarly have become a major topic of study in thought to diffuse out from the mantle, core, one of the largest and best known groups of Quaternary research over the last 20 years and crust at well-defined rates. Xenon is par- organisms. However, the possible coevolution (4–8), can provide a formidable means for ticularly important in this regard. If it does of grasses and dinosaurs has never been reconstructing vegetation and animal diets undergo redox reactions and enter into chem- studied. Now, Prasad et al. (1) report on page for much earlier time periods when early ical combination with silicates and other 1177 of this issue their analysis of phy- angiosperms were diversifying. These oxides, this could explain the apparent toliths—microscopic pieces of silica remarkable results will force reconsidera- “xenon deficit” in the atmospheres of Earth formed in cells—in coprolites that the tion of many long-standing assumptions and Mars, remarked upon by geochronolo- authors attribute to titanosaurid sauropods about grass evolution, dinosaurian ecology, gists and geophysicists (12). If this is true for that lived in central India about 65 to 71 mil- and early plant-herbivore interactions. xenon, then perhaps it also occurs for the lion years ago. Their data indicate that those Scientists have long known that grasses radioactive rare gas, radon, that is formed by dinosaurs ate grasses. make distinctive kinds of phytoliths in the radioactive decay processes in crustal rocks. Part of the difficulty in studying the epidermis of their leaves and leaflike cover- The physical properties of xenon in deep question of dinosaur-grass coevolution ings that surround their flowers (9). More Earth environments are as strange as its pos- results from the poor quality of the fossil recent work has examined in greater detail sible chemical behavior. Jephcoat (13) has record for early grasses. The earliest phytolith characteristics from a large set of shown that under lower mantle and core con- unequivocal grass fossils date to the grasses comprising taxa representing the ditions, the melting point of xenon exceeds Paleocene-Eocene boundary, about 56 mil- entire range of diversification within the that of iron, as does its density. This means lion years ago (2, 3), well after the demise family, showing that discriminations at the that if xenon did not react chemically with of nonavian dinosaurs at the end of the subfamily, tribe, and levels are often mantle or core materials, it would fall as Cretaceous Period. Pollen and macrofossils possible (1, 4–8, 10). In addition, publica- “hail” toward the center of Earth, through of Poaceae are uncommon in sedimentary tion of a well-resolved consensus phy- the molten outer core. However, the results strata until the middle Miocene, about 11 to logeny of the Poaceae by the Grass Phy- of Sanloup et al. suggest that it can also react 16 million years ago, when the family is logeny Working Group (GPWG) (11) con- with silicates, oxidizing them to metallic thought to have undergone considerable siderably advances our overall understand- alloys or replacing silicon in mineral struc- evolutionary diversification and ecological ing of the evolutionary history of grasses tures. There might be new geochemical par- expansion (2). Thus, dioramas in museums and leads to improved interpretations of the titioning equilibria to be considered within early grass fossil record. For example, by the deep crust, mantle, and core, involving mapping the phytolith characters that dis- The authors are at the National Museum of Natural xenon physics and chemistry. History, Washington, DC 20560, USA. D. R. Piperno is criminate clades and subfamilies of extant It is of interest that Sanloup et al. carried also at the Smithsonian Tropical Research Institute, taxa onto this phylogenetic tree, we can out their experiments in platinum capsules, Balboa, Panama. E-mail: [email protected] infer how phytolith morphology changed at

1126 18 NOVEMBER 2005 VOL 310 SCIENCE www.sciencemag.org Published by AAAS P ERSPECTIVES GPWG Poaceae phylogeny Phytolith shapes Flagellaria Elegia Baloskion Joinvillea Anomochloa Streptochaeta Anomochlooideae Pharus Pharoideae Guaduella Eremitis Bambusoideae Pariana Lithachne Olyra Bambusoideae Buergersiochloa Pseudosasa Chusquea Streptogyna Incertae sedis Ehrharta Oryza Ehrhartoideae Leersia Ehrhartoideae Phaenosperma Anisopogon Ampelodesmos Stipa Nassella Piptatherum Brachypodium Avena Bromus Pooideae Triticum Diarrhena Melica Glyceria Lygeum Nardus Brachyelytrum Aristida Stipagrostis Aristidoideae Merxmuellera m. Aristidoideae Karroochloa Austrodanthonia Danthonia Amphipogon Arundo Molinia Phragmites Merxmuellera r. Centropodia Eragrostis Uniola Pappophorum Chloridoideae Zoysia Spartina Sporobolus Distichlis Eriachne Incertae sedis Thysanolaena Zeugites Centothecoideae Chasmanthium Gynerium Incertae sedis Danthoniopsis Panicum Pennisetum Panicoideae Miscanthus Zea Micraira Incertae sedis

Grass lineage. (Left) Phylogeny for grasses from GPWG (11). (Right) unlike those in the BEP clade. Phytoliths typical of the Aristidoideae, Examples of phytoliths from basalmost and later-diverging families of Panicoideae and Chloridoideae (PACCAD clade) are also shown. Phytolith grasses, showing that the earliest grasses probably contributed phytoliths images are from the work of the authors (4, 14). the origin of major clades and lineages (see (, rice relatives) in particular possess [see figure 2, a and b, of (1)] are confined to a the figure). many diverse bilobate, saddle- and cross- few extant genera of the ehrhartoidean tribe The most primitive grasses belong to the shaped phytoliths, and some are diagnostic of Oryzeae, and other reported phytoliths are family Anomochlooideae, represented by two each subfamily (see the figure). These also dif- probably from the Pooideae. Therefore, the extant genera from tropical America, fer substantially from the more simple, mirror- conclusion that a considerable amount of pre- Streptochaeta and Anomochloa. They make image kinds of phytoliths well described in Tertiary diversification occurred among the distinctive, oddly shaped kinds of phytoliths the large PACCAD (e.g., Panicoideae and Poaceae, leading to a much earlier emergence not found in other extant grasses. The Chloridoideae) clade of grasses (1, 4, 5, 8–10). and radiation of the major BEP clade than had Pharoideae, the next group to diverge, make In the dinosaur coprolites studied by been previously thought on the basis of fossil another type of unique phytolith. A notable Prasad et al., phytoliths indisputably derived and molecular clock data, is well supported. point is that bilobate, cross-shaped, and con- from grasses are common. It is noteworthy PACCAD-clade grasses may also have been ventional saddle-shaped phytoliths, the types that phytoliths diagnostic of the most basal present, but this finding is more ambiguous at long used by researchers to define grass silica grasses (those found in the modern genera the present time because of the possibility of deposition, appear to be absent from basal Anomochloa, Streptochaeta, and Pharus) are morphological overlap with basal Pooideae. grasses (1, 10). They apparently made their first absent, whereas types produced today in the These results also have considerable appearance in the later-diverging Puelioideae Puelioideae, Ehrhartoideae, and Bambu- importance for investigations of ancient plant- (producers of saddle-shaped phytoliths) and soideae were frequently encountered. herbivore interactions, a major field of study BEP (Bambusoideae/Ehrhartoideae/Pooideae) Moreover, the “vertical” bilobate and cross- because coevolutionary relationships that taxa. The Bambusoideae and Ehrhartoideae shaped phytoliths observed by Prasad et al. arise between plants and their herbivores have

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major, diverse effects on each group (12). The Phytoliths are common in an array of extant 2. B. F. Jacobs, J. D. Kingston, L. L. Jacobs, Ann. Mo. Bot. documentation by Prasad et al. of a range of basal angiosperms, , and Gard. 86, 590 (1999). 3. E.A. Kellogg, Plant Physiol. 125, 1198 (2001). poacean taxa in the Late Cretaceous of India eudicotyledons in addition to grasses and are 4. D. R. Piperno, Phytolith Analysis: An Archaeological makes the possibility real that titanosaurid among the few substances capable of inducing and Geological Perspective (Academic Press, San sauropods were not the only grass eaters of the morphological changes to animal mouthparts Diego, CA, 1988). 5. G. G. Fredlund, L.T.Tieszen, J. Biogeogr. 21, 321 (1994). era, and that coevolutionary interactions (14). It is believed that they constitute an 6. G. G. Fredlund, L.T.Tieszen, Quat. Res. 47, 206 (1997). between grasses and diverse vertebrate herbi- important type of mechanical plant defense 7. M. Blinnikov, A. Busacca, C. Whitlock, Palaeogeogr. vores may have greater antiquity than previ- against both insect and vertebrate herbivory Palaeoclimatol. Palaeoecol. 177, 77 (2002). 8. D. M. Pearsall, K. Chandler-Ezell, A. Chandler-Ezell, ously believed. For example, the enigmatic (14). By 65 million years ago, therefore, J. Archaeol. Sci. 30, 611 (2003). gondwanatherian mammals with their high- angiosperms may have experienced consider- 9. C. R. Metcalfe, Anatomy of the Monocotyledons. I. Gramineae (Oxford Univ. Press, London, 1960). crowned (hypsodont) cheek teeth could have able herbivore pressure such that some had 10. D. R. Piperno, D. M. Pearsall, Smithson. Contrib. Bot. eaten grasses (13). It has often been argued evolved simple, inexpensive mechanical 85, 1 (1998). that the intense consumption of vegetation defenses that involved impregnating their 11. Grass Phylogeny Working Group, Ann. Mo. Bot. Gard. 88, 373 (2001). by herd-forming herbivorous dinosaurs led to structures with silica. The new data provided 12. H.-D. Sues, Ed., Evolution of Herbivory in Terrestrial the diversification of angiosperms during the by Prasad et al. are certain to help resolve Vertebrates (Cambridge Univ. Press, Cambridge, 2000). Cretaceous (12). Prasad et al. identified the these and other important issues in Mesozoic 13. R. Pascual et al., J. Vertebr. Paleontol. 19, 373 (1999). 14. D. R. Piperno, Phytoliths: A Comprehensive Guide for silicified remains, including trichome phy- terrestrial ecology. Archaeologists and Paleoecologists (AltaMira, toliths, of a variety of nongrass angiosperms Lanham, MD, in press). References in the coprolites, providing direct evidence 1. V. Prasad, C. A. E. Strömberg, H. Alimohammadian, that the dinosaurs were generalist herbivores. A. Sahni, Science 310, 1177 (2005). 10.1126/science.1121020

GENETICS related proteins such as FEZ-1; postsynap- tic density–related proteins such as citron; Two Genes Link and nuclear proteins such as activating tran- scription factor 4 (12–14). DISC1 is critical for maintaining a complex containing Two Distinct Psychoses NUDEL and the microtubule-associated motor protein dynein at the centrosome. Akira Sawa and Solomon H. Snyder Mutations in DISC1, such as those that produce truncated forms of the protein, uring the past decade, the tools of whose chromosomal aberrations clearly prevent dynein-centrosome interaction in molecular genetics have begun to segregate with psychotic disturbance. This some schizophrenic patients (15). In addi- Dbear fruit in searches for selective includes both schizophrenia and affective tion, reduced expression of DISC1 in mice genes involved in the major psychotic ill- disorder, with direct involvement in at least disturbs proper neuronal migration nesses, schizophrenia and affective disor- two distinct pedigrees (5, 6). Furthermore, and arborization of dendritic neuronal der. The most direct evidence involves the linkage and association studies establish processes in the developing cerebral cortex gene DISC1 (disrupted in schizophrenia 1) DISC1 as a candidate susceptibility gene in (15). These findings have suggested that (1). On page 1187 of this issue (2), Millar et large populations of patients with schizo- localization of dynein to centrosomes al., who pioneered the discovery of DISC1 phrenia or affective disorder (4). The through DISC1 is critical for dynein signal- (3), now report a chromosomal transloca- intriguing relationship of DISC1 to both of ing that regulates the growth of neuronal tion in schizophrenia involving the gene these disorders, long thought to be distinct, processes and development of the cerebral encoding phosphodiesterase 4B, PDE4B. has been strengthened by a link to chromo- cortex. The DISC1 mutation found in the DISC1 binds PDE4B1, but an increase in some 1q42, the region of DISC1, for Scottish pedigree could lead to a truncation cellular cyclic adenosine monophosphate schizoaffective disorder. As the name of DISC1 at its carboxyl terminus and/or (cAMP) dissociates the proteins and acti- implies, this mental disorder shares the degradation of the protein. Failure to detect vates the phosphosdiesterase. This discov- characteristic of both cognitive and mood- the truncated DISC1 in lymphoblasts of a ery affords a molecular explanation of cog- related illnesses (7). few schizophrenics from the Scottish pedi- nitive and affective dysfunction and may How DISC1 influences mental function gree may also be attributed to variations in clarify the relationship between schizo- is beginning to be clarified. In schizo- DISC1 protein isoforms (see the second phrenia and affective illness, thus poten- phrenic patients, DISC1 variants are linked figure). Such isoforms could exhibit differ- tially leading to new therapeutic strategies. to specific neurocognitive impairments ences in their metabolism in the brain and Genetic linkage and association studies (8–11). A single-nucleotide polymorphism lymphoblasts as well as in the developing have implicated several candidate genes in in DISC1 that leads to an amino acid and adult brain (1, 16). Loss of DISC1 schizophrenia, including those encoding change (Ser704 → Cys) is associated with and/or actions of the truncated mutant neuregulin 1, dysbindin, and regulator of G schizophrenia and correlates with varia- DISC1 can cause dysfunctions that would protein signaling 4 (4). In contrast to these tions in hippocampal size and function dur- fit with substantial evidence that schizo- suggestive findings, DISC1 is the first gene ing cognitive tasks in normal subjects (8) as phrenia is a disorder of neural development well as cognitive variations in aged normal (17–19). The authors are in the Departments of Psychiatry and subjects (11). Millar et al. (2) now report a patient with Neuroscience and the Program in Cellular Molecular Cellular functions of DISC1 have been a chromosomal translocation involving the Medicine, and S. H. Snyder is also in the Department of revealed through the identification of vari- gene encoding PDE4 that leads to a 50% Pharmacology, Johns Hopkins University School of ous proteins that interact with it: micro- Medicine, 725 North Wolfe Street, Baltimore, MD reduction in expression of PDE4B1, one 21205, USA. E-mail: [email protected]; ssnyder@ tubule-centrosome–associated proteins subtype of PDE4B. They detect binding of jhmi.edu such as NUDEL (see the first figure); actin- PDE4B1 with DISC1 (see the second fig-

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