Forum Letter A global database of C4 photosynthesis in grasses Introduction C3, C4 or Crassulacean acid metabolism (CAM) photosynthetic pathways represent a fundamental axis of trait variation in plants, with importance at scales from genome to biome. Knowing the distribution of these pathways among wild species is a crucial first step in understanding the patterns and processes of photosynthetic evolution and its role in ecological processes at large scales (e.g. changes in the composition of biomes under global change). C4 photosynthesis is most prevalent in the Poaceae (grasses), which account for about half of all C4 species (Sage et al., 1999a). Research on the evolution and ecology of these plants has undergone a renaissance during the last 7 yr, catalyzed by phylogenetic analyses showing multiple parallel C4 origins (e.g. Christin et al., 2007; Vicentini et al., 2008; GPWG II, 2012), insights into the distribution of C4 species and assembly of the C4 grassland biome (Edwards & Still, 2008; Edwards & Smith, 2010; Edwards et al., 2010), and efforts to introduce the C4 pathway into rice (Hibberd et al., 2008; von Caemmerer et al., 2012). C4 photosynthesis is an excellent model for investigating complex trait evolution, because of the broad knowledge base describing its biochemical basis, evolutionary history, and ecological interactions (Christin et al., 2010). Why do we need a C4 database? Investigations of the evolution and ecological significance of C4 photosynthesis are increasingly turning to large-scale comparisons of C3 and C4 species. These are straightforward for well-characterized common or model species. However, when comparisons are extended to include large numbers of nonmodel species, two important challenges arise. First, there are > 62 000 published scientific names for grasses corresponding to over 11 000 accepted species (Clayton et al., 2002b onwards), making an average of five synonyms for each accepted name. This leads to problems when linking data based on alternative names for the same species concept, and to redundancy in published data surveys, when values for synonyms are presented as independent data. Secondly, although there have been extensive previous surveys of the photosynthetic pathway spanning the diversity of wild species (Hattersley & Watson, 1992; Sage et al., 1999a), the rarity of most species means that this work is incomplete, and the synonymy problem makes it difficult to identify the gaps in these data. Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust Accounting for synonymy and spelling variants/mistakes has become one of the central challenges for the emerging fields of ecological and evolutionary informatics, in which data are synthesized across different sources on increasingly larger scales (Jones et al., 2006; Sidlauskas et al., 2009). In one infamous example, a 22.5 million record database of plant species occurrences and traits for the Americas contained more scientific names than there are thought to be plant species on Earth (Whitfield, 2011). However, this taxonomic impediment to data synthesis has been progressively broken down by a combination of new methodological developments for name matching (Patterson et al., 2010; Boyle et al., 2013; Chamberlain & Szocs, 2013; Kluyver & Osborne, 2013), and the compilation of nomenclatural databases by botanic gardens and natural history museums (e.g. The Plant List, 2010). Here, we showcase how such resources may be used to assemble and index databases of discrete traits for large numbers of species. Compilation and overview of the data Our database of C3 and C4 photosynthetic types in grasses is based principally on published anatomical and stable carbon isotope evidence. We followed previous authors in assuming that all species within each genus shared the same photosynthetic pathway, unless the evidence suggested otherwise. However, we also measured d13C for 99 species that had not previously been surveyed, including 96 species of Panicum s.l., Acostia gracilis, Lophopogon tridentatus and Thedachloa annua (Supporting Information, Table S1). We also obtained information on leaf anatomy and measured d13C to check previous unverified reports of a C3 species (Stipagrostis paradisea) in an otherwise C4 genus (Sage et al., 1999a), and a C4 subspecies (Chaetobromus dregeanus ssp. involucratus) in an otherwise C3 subfamily (Danthonioideae; Watson & Dallwitz, 1992 onwards). In both cases, our data contradicted previous reports, showing that the photosynthetic pathway of these taxa matches that of their close relatives; S. paradisea is C4 and C. dregeanus ssp. involucratus is C3 (Table 1). The photosynthetic pathways of Taeniorhachis repens, Veldkampia sagaingensis and 39 rare species of Panicum s.l. remain unclassified, because we were unable to take samples of type specimens from herbarium collections. Most of these species are endemics of Madagascar (26 species), and the remaining 13 species are endemics of a small number of countries in Africa and Southeast Asia, and oceanic islands (Table S2). This means that the database is complete for most countries of the world. Our approach has been to map the photosynthetic pathway data onto accepted species names in the Poaceae taxonomy of Clayton & Renvoize (1986) and Clayton et al. (2002b onwards), which is the most comprehensive treatment of accepted names and synonymy for grasses (see Methods S1 for full methodology). Coupling our New Phytologist (2014) 1 www.newphytologist.com 2 Forum New Phytologist Letter Table 1 Photosynthetic type for genera previously reported to include a mixture of C3, C4 and C3–C4 intermediate species Taxon 1. Alloteropsis A. angusta A. cimicina A. paniculata A. papillosa A. semialata ssp. semialata A. semialata ssp. eckloniana 2. Aristida A. longifolia Other Aristida species 3. Chaetobromus involucratus ssp. involucratus1 ssp. sericeus ssp. dregeanus 4. Dregeochloa D. calviniensis2 D. pumila 5. Eragrostis3 Eragrostis walteri4 Other Eragrostis species 6. Homolepis Homolepis aturensis5 Other Homolepis species 7. Neurachne N. alopecuroides N. annularis N. lanigera N. minor N. munroi N. queenslandica N. tenuifolia Paraneurachne muelleri6 8. Panicum s.l.3 252 species 169 species P. ruspolii 9. Steinchisma S. cupreum S. decipiens S. exiguiflorum S. hians S. laxum S. spathellosum S. stenophyllum 10. Stipagrostis S. paradisea7 Other Stipagrostis species 11. Streptostachys s.l.3 S. acuminata S. asperifolia5 S. lanciflora S. macrantha S. ramosa S. rigidifolia S. robusta Type References C4 C4 C4 C4 C4 C3 Metcalfe (1960), Ellis (1974), Hattersley et al. (1977), Watson & Dallwitz (1992 onwards) C3 C4 Cerros-Tlatilpa & Columbus (2009) Watson & Dallwitz (1992 onwards) C3 C3 C3 This study; H. P. Linder (pers. comm.) This study; H. P. Linder (pers. comm.) This study; H. P. Linder (pers. comm.) C3–C4(?) C3 Watson & Dallwitz (1992 onwards) C3 C4 Schulze et al. (1996); Ingram et al. (2011); Watson & Dallwitz (1992 onwards) C3–C4(?) C3 Christin et al. (2013); Watson & Dallwitz (1992 onwards) C3 C3 C3 C3–C4 C4 C3 C3 C4 Hattersley et al. (1982); Hattersley & Roksandic (1983); Christin et al. (2012) C3 C4 C3–C4(?) Various sources, including this study (see Table S4 for full details) C3–C4 C3–C4 C3–C4 C3–C4 C3 C3–C4 C3–C4 Brown (1977), Morgan & Brown (1979, 1980); Renvoize (1987); Watson & Dallwitz (1992 onwards) C4 C4 Renvoize (1986); this study Watson & Dallwitz (1992 onwards) C4 C3–C4(?) C3 C4 C4 C4 C3 Morrone & Zuloaga (1991); Watson & Dallwitz (1992 onwards); Filgueiras et al. (1993); De Olivera & Longhi-Wagner (2007); P.-A. Christin (pers. comm.) Taxonomy follows Clayton et al. (2002b onwards). 1 Anatomical (H. P. Linder, pers. comm.) and d13C evidence (Supporting Information Tables S1, S3) conflicts with a previous report that this subspecies is C4 (Watson & Dallwitz, 1992 onwards). 2 Anatomical evidence shows that in D. calviniensis most mesophyll cells are no more than one cell distant from bundle sheath cells, making it potentially a C3–C4 intermediate. 3 Genus known to be polyphyletic. 4 Note that a recent phylogenetic treatment (Ingram et al., 2011) places E. walterii outside the genus Eragrostis. However, its taxonomy has not yet been revised. 5 Anatomical evidence showing a concentration of chloroplasts within large bundle sheath cells suggests that this species is potentially a C3–C4 intermediate (Christin et al., 2013; P.-A. Christin, pers. comm.). 6 Phylogenetic analysis places the genus Paraneurachne nested within the genus Neurachne (Christin et al., 2012). 7 Anatomical (Renvoize, 1986) and d13C evidence (Tables S1, S3) conflicts with a previous report that this species is C3 (Sage et al., 1999a). New Phytologist (2014) www.newphytologist.com Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust New Phytologist dataset with this synonymy allows users to return the photosynthetic type for all except 46 (corresponding to 41 accepted species) of the 62 678 published scientific names (accepted names and synonyms) for grasses (Clayton et al., 2002b onwards). We have developed software tools to facilitate this task for users, which are detailed in the following. The database covers 99.6% of the 11 087 grass species. It shows that 42% of these species use the C4 photosynthetic pathway and 57% the C3 pathway (Table S3; Notes S1). Six genera (Alloteropsis, Aristida, Eragrostis, Neurachne, Panicum s.l., and Streptostachys s.l.) contain both C3 and C4 species (Tables 1,S4). Seven C3–C4 intermediate species (Table 1) are distributed between the genera Neurachne (one species) and Steinchisma (six species). Within the genus Panicum s.l., 169 species are C4, 250 are C3, and 41 remain unknown, with the photosynthetic type of Panicum ruspolii ambiguous on the basis of new d13C measurements (Tables S1, S2,S4; Notes S1). The latter species may be a previously unrecognized C3–C4 intermediate, but further work is required to test this hypothesis. A number of further potential C3–C4 intermediates have been identified on the basis of anatomical observations (Tables 1,S3), and also need to be investigated physiologically. These are Dregeochloa calviniensis (most mesophyll cells are no more than one cell distant from bundle sheath cells; Watson & Dallwitz, 1992 onwards), Homolepis aturensis and Streptostachys asperifolia (concentration of chloroplasts in large bundle sheath cells; Christin et al., 2013; P.-A. Christin, pers. comm.). In total there are therefore 11 putative C3–C4 intermediates in the grasses. Caveats A number of caveats are important when collating and using large trait databases of this kind. The assumption that all species within each genus share the same photosynthetic pathway is reasonable in most cases. However, significant and interesting exceptions, such as the C3 Aristida species in an otherwise C4 genus (Cerros-Tlatilpa & Columbus, 2009), raise the possibility of errors at the species level. Misclassification is most likely in lineages where multiple evolutionary transitions between photosynthetic pathways have occurred, especially in Paniceae and Paspaleae (Morrone et al., 2012). The polyphyly of many grass genera accentuates this problem, most acutely illustrated by Eragrostis walteri, which was previously considered to be a C3 species within a wholly C4 genus (Table 1). Recent phylogenetic work has demonstrated that this species is actually a member of the C3 Arundinoideae lineage and misplaced within Eragrostis (Ingram et al., 2011). The polyphyly of grass genera means that Tables 1, S3 and S4 should be interpreted with caution. While they do catalogue the known distribution of C4 photosynthesis among taxa, they do not necessarily provide information about its evolutionary history. However, ongoing phylogenetic work is steadily resolving the polyphyly issue, which is most acute in the genus Panicum. We have used the conservative circumscription of Panicum s.l. adopted in GrassBase (Clayton et al., 2002b onwards) and recently carried over to the World Checklist of Poaceae (Clayton et al., 2012 onwards) and The Plant List (The Plant List, 2010), because these Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust Letter Forum 3 online resources provide the most comprehensive, global list of accepted names and synonyms, and are regularly updated in the light of new publications. Using the software tools detailed in the following, it is straightforward to link the C3/C4 data listed for Panicum s.l. (see Table S4) to the new genus circumscriptions. The same applies to Streptostachys s.l. (Table 1). How to access the database Easy routes for users to access information are crucial determinants of the usefulness and usage of data. Our database may be accessed via three routes. The first is static, but the second and third will report updates to the database as we make them. First, simple tables list photosynthetic pathway by accepted scientific name, and may be accessed in the Supporting Information (Tables S3,S4). These require the user to first prepare a list of accepted species names according to the taxonomy of Clayton et al. (2002b onwards) for the taxa of interest. Secondly, the name-matching and data-linkage steps may be combined within the software package Taxonome (Kluyver & Osborne, 2013; http://taxonome.bitbucket.org; persistent URL http://purl.org/NET/taxonome). Taxonome links datasets using species names, handling both synonyms and spelling variants (including spelling mistakes). It deals rapidly with millions of names, and runs via either a simple Graphical User Interface (GUI) for basic functionality or python scripts for advanced users. A user first loads the Kew taxonomy and photosynthetic pathway database via a data file obtained from the Taxonome website. Custom lists comprising any published grass names may then be rapidly matched to this database, and outputted in CSV format. Thirdly, the photosynthetic pathway data are linked to the Kew taxonomy, together with morphological, phylogenetic, biogeographic and environmental data within the GrassPortal system (Osborne et al., 2011; www.grassportal.org). GrassPortal enables users to easily assemble large-scale, synthetic data products based on multiple original sources, and is accessed via an intuitive and simple GUI. Using this system, users are able to assemble a list of all grass species present in a particular geographic area, linked to photosynthetic pathway, growth form, and environmental niche data. Large-scale data synthesis By carrying out technically challenging bioinformatic steps of data processing and linkage, services like GrassPortal open up new possibilities for a broad biological community to explore large-scale synthetic data products. For example, linkage of the photosynthetic pathway dataset with species occurrence data (Clayton et al., 2002a) allows the distribution of C4 grass species to be mapped at the global scale (Fig. 1). This map improves the global coverage compared with previous data compilations, especially for Africa, South America and Southeast Asia (Sage et al., 1999b). It particularly highlights the prevalence of C4 photosynthesis among African grasses (Fig. 1a), and the importance of central-east Africa, India and northern Australia as hotspots of C4 grass species richness (Fig. 1b). The new dataset also facilitates large-scale New Phytologist (2014) www.newphytologist.com 4 Forum New Phytologist Letter (a) (b) Fig. 1 Global map of C4 grass species distributions. (a) Percentage of grass species within each mapping unit that uses the C4 pathway; (b) the species richness of C4 grasses in each mapping unit. The map shows species distributions at the Taxonomic Databases Working Group (TDWG) level 3 ‘botanical country’ scale, a biodiversity information standard corresponding largely to political countries, but with large countries subdivided into smaller mapping units (Brummitt et al., 2001). macroevolutionary analyses. For example, the Grass Phylogeny Working Group II (2012) used our data in phylogenetic analyses to discover multiple new C4 lineages, and to infer that evolutionary gains prevail over losses of this trait. Another recent study used our data in a macroevolutionary analysis to show an association between C4 photosynthesis and salt tolerance in grasses (Bromham & Bennett, 2014). The integration of our C4 pathway data with information on geographical distributions, environmental niche, and phylogenetic relationships promises important novel insights into the ecological significance and evolution of this complex physiological and anatomical trait. More generally, it offers biologists an example of how functional trait data may be used in large-scale synthesis and analysis to advance our understanding of the ecological and evolutionary processes acting on organisms. Acknowledgements We are grateful to Liliana Giussani and Pascal-Antoine Christin for their critical comments on the manuscript. This work builds on that of previous authors who have compiled comprehensive databases on grass leaf anatomy and photosynthetic type, including C. R. Metcalfe, Walter Brown, Roger Ellis, Paul Hattersley, Les Watson, and Rowan Sage, and owes a debt of gratitude to them. We thank Les Watson for his generosity in allowing us to use data from Grass Genera of the World (http:// delta-intkey.com/grass/), and the following for financially supporting this work: C.P.O. was supported by a Royal Society University Research Fellowship and NERC grant number NE/ I014322/1, A.S. by the European Union’s Erasmus scheme, T.A.K. by a University of Sheffield Postgraduate Studentship, New Phytologist (2014) www.newphytologist.com and V.V. by the GrassPortal project supported by the e-content programme of the JISC. The development of GrassPortal was funded by the JISC, with additional support from the University of Sheffield, the Royal Botanic Gardens, Kew, and KnowledgeNow Limited. We thank Peter Linder of the University of Zurich for information on the leaf anatomy of Danthonioid grasses, Tony Verboom (University of Cape Town) for material of Chaetobromus dregeanus for isotopic analysis, Marjorie Lundgren for her help in acquiring material and Heather Walker for running the analyses. We also thank the following herbaria and their staff for generous help with plant material for the isotope survey: Skye Coffey (Western Australian Herbarium), Olof Ryding (Botanisk Museum, Koebenhavus Universitet), Mats Thulin (Uppsala University), Brendan Lepschi (Australian National Herbarium), Bryan Simon (Queensland Herbarium), Lyn Fish (SANBI) and the Missouri Botanical Garden. Colin P. Osborne1*, Anna Salomaa1,2, Thomas A. Kluyver1, Vernon Visser1,3, Elizabeth A. Kellogg4, Osvaldo Morrone5, Maria S. Vorontsova6, W. Derek Clayton6 and David A. Simpson6 1 Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK; 2 Department of Biological and Environmental Science, University of Jyv€askyl€a, PO Box 35, Jyv€askyl€a 40500, Finland; 3 Centre for Invasion Biology, Department of Botany and Zoology, University of Stellenbosch, Natural Sciences Building, Private Bag X1, Matieland 7602, South Africa; 4 Donald Danforth Plant Science Center, 975 North Warson Road, Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust New Phytologist St Louis, MO 63132, USA; Instituto de Botanica Darwinion, Labarden 200, C.C. 22, B1642HYD, San Isidro, Buenos Aires, Argentina; 6 Herbarium, Library, Art and Archives, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK; (*Author for correspondence: tel +44 114 0146; email c.p.osborne@sheffield.ac.uk) 5 References Boyle B, Hopkins N, Lu Z, Garay JAR, Mozzherin D, Rees T, Matasci N, Narro ML, Piel WH, McKay SJ et al. 2013. The taxonomic names resolution service: an online tool for automated standardization of plant names. BMC Bioinformatics 14: 16. Bromham L, Bennett TH. 2014. Salt tolerance evolves more frequently in C4 grass lineages. Journal of Evolutionary Biology 27: 653–659. Brown WV. 1977. The Kranz syndrome and its subtypes in grass systematics. Memoirs of the Torrey Botanical Club 23: 1–97. Brummitt RK, Pando F, Hollis S, Brummitt NA. 2001. Plant taxonomic database standards no. 2. World geographical scheme for recording plant distributions, 2nd edn. Pittsburgh, PA, USA: Published for the International Working Group on Taxonomic Databases For Plant Sciences (TDWG) by the Hunt Institute for Botanical Documentation, Carnegie Mellon University. von Caemmerer S, Quick WP, Furbank RT. 2012. The development of C4 rice: current progress and future challenges. Science 336: 1671–1672. Cerros-Tlatilpa R, Columbus JT. 2009. C3 photosynthesis in Aristida longifolia: implication for photosynthetic diversification in Aristidoideae (Poaceae). American Journal of Botany 96: 1379–1387. Chamberlain S, Szocs E. 2013. taxize – taxonomic search and retrieval in R. F1000Research 2: 191. [WWW document] URL http://f1000research.com/ articles/2-191/v2 [accessed 28 May 2014]. Christin P-A, Freckleton RP, Osborne CP. 2010. Can phylogenetics identify C4 origins and reversals? Trends in Ecology and Evolution 25: 403–409. Christin P-A, Salamin N, Savolainen V, Duvall MR, Besnard G. 2007. C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Current Biology 17: 1241–1247. Christin P-A, Wallace MJ, Clayton H, Edwards EJ, Furbank RT, Hattersley PW, Sage RF, Macfarlane TD, Ludwig M. 2012. Multiple photosynthetic transitions, polyploidy, and lateral gene transfer in the grass subtribe Neurachninae. Journal of Experimental Botany 63: 6297–6308. Christin PA, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR, Garrison LM, Vorontsova MS, Edwards EJ. 2013. Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proceedings of the National Academy of Sciences, USA 110: 1381–1386. Clayton WD, Govaerts R, Harman KT, Williamson H, Vorontsova M. 2012 onwards. World checklist of Poaceae. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet. [WWW document] URL http://apps.kew.org/ wcsp/ [accessed 15 March 2012]; 11:30 GMT. Clayton WD, Renvoize SA. 1986. Genera Graminum. London, UK: HMSO. Clayton WD, Vorontsova MS, Harman KT, Williamson H. 2002a onwards. GrassBase – the online world grass flora. [WWW document] URL http://www.kew. org/data/grasses-db.html [accessed 25 September 2013]. Clayton WD, Vorontsova MS, Harman KT, Williamson H. 2002b onwards. GrassBase – the online world grass flora. Synonymy. [WWW document] URL http://www.kew.org/data/grasses-syn.html [accessed 25 September 2013]. De Olivera RP, Longhi-Wagner HM. 2007. New species of Streptostachys (Poaceae: Paniceae) from Brazil. Kew Bulletin 62: 493–497. Edwards EJ, Osborne CP, Str€omberg CAE, Smith SA, C4 Grasses Consortium. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328: 587–591. Edwards EJ, Smith SA. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. Proceedings of the National Academy of Sciences, USA 107: 2532– 2537. Edwards EJ, Still CJ. 2008. Climate, phylogeny and the ecological distribution of C4 grasses. Ecology Letters 11: 266–276. Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust Letter Forum 5 Ellis RP. 1974. The significance of the occurrence of both Kranz and non-Kranz leaf anatomy in the grass species Alloteropsis semialata. South African Journal of Science 70: 169–173. Filgueiras TS, Morrone O, Zuloaga FO. 1993. A new species of Streptostachys (Poaceae: Paniceae) from Brazil. Novon 3: 252–257. Grass Phylogeny Working Group II. 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytologist 193: 304–312. Hattersley PW, Roksandic Z. 1983. d13C values of C3 and C4 species of Australian Neurachne and its allies (Poaceae). Australian Journal of Botany 31: 317–321. Hattersley PW, Watson L. 1992. Diversification of photosynthesis. In: Chapman GP, ed. Grass evolution and domestication. New York, NY, USA: Cambridge University Press, 38–116. Hattersley PW, Watson L, Johnston CR. 1982. Remarkable leaf anatomical variations in Neurachne and its allies (Poaceae) in relation to C3 and C4 photosynthesis. Botanical Journal of the Linnean Society 84: 265–272. Hattersley PW, Watson L, Osmond CB. 1977. In situ immunofluorescent labelling of ribulose-1, 5-bisphosphate carboxylase in C3 and C4 plants. Australian Journal of Plant Physiology 4: 523–539. Hibberd JM, Sheehy JE, Langdale JA. 2008. Using C4 photosynthesis to increase the yield of rice – rationale and feasibility. Current Opinion in Plant Biology 11: 228–231. Ingram AL, Christin P-A, Osborne CP. 2011. Molecular phylogenies disprove an hypothesized C4 reversion in Eragrostis walteri (Poaceae: Chloridoideae). Annals of Botany 107: 321–325. Jones MB, Schildhauer MP, Reichman OJ, Bowers S. 2006. The new bioinformatics: integrating ecological data from the gene to the biosphere. Annual Review of Ecology, Evolution and Systematics 37: 519–544. Kluyver TA, Osborne CP. 2013. Taxonome: a software package for linking biological species data. Ecology and Evolution 3: 1262–1265. Metcalfe CR. 1960. Anatomy of the monocotyledons. I. Gramineae. Oxford, UK: Clarendon Press. Morgan JA, Brown RH. 1979. Photosynthesis in grass species differing in carbon dioxide fixation pathways. II. A search for species with intermediate gas exchange and anatomical characteristics. Plant Physiology 64: 257–262. Morgan JA, Brown RH. 1980. Photosynthesis in grass species differing in carbon dioxide fixation pathways. III. Oxygen response and enzyme activities of species in the laxa group of Panicum. Plant Physiology 65: 156–159. Morrone O, Aagesen L, Scataglini MA, Salariato DL, Denham SS, Chemisquy MA, Sede SM, Giussani LM, Kellogg EA, Zuloaga FO. 2012. Phylogeny of the Paniceae (Poaceae: Panicoideae): integrating plastid DNA sequences and morphology into a new classification. Cladistics 28: 333–356. Morrone O, Zuloaga F. 1991. Revision del genero Streptostachys (PoaceaePanicoideae), su posicion sistematica dentro de la tribu Paniceae. Annals of the Missouri Botanical Gardens 78: 359–376. Osborne CP, Visser V, Chapman S, Barker A, Freckleton RP, Salamin N, Simpson D, Uren V. 2011. GrassPortal: an online ecological and evolutionary data facility. [WWW document] URL www.grassportal.org [accessed 12 June 2013]. Patterson DJ, Cooper J, Kirk PM, Pyle RL, Remsen DP. 2010. Names are key to the new big biology. Trends in Ecology and Evolution 25: 686–691. Renvoize SA. 1986. A survey of leaf-blade anatomy in grasses: VIII. Arundinoideae. Kew Bulletin 41: 323–338. Renvoize SA. 1987. A survey of leaf-blade anatomy in grasses: XI. Paniceae. Kew Bulletin 42: 739–768. Sage RF, Li M, Monson RK. 1999a. The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK, eds. C4 plant biology. New York, NY, USA: Academic Press, 551–584. Sage RF, Wedin DA, Li M. 1999b. The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF, Monson RK, eds. C4 plant biology. New York, NY, USA: Academic Press, 313–373. Schulze ED, Ellis R, Schulze W, Trimborn P, Ziegler H. 1996. Diversity, metabolic types and δ13C carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia 106: 352–369. Sidlauskas B, Ganapathy G, Hazkani-Covo E, Jenkins KP, Lapp H, McCall LW, Price S, Scherle R, Spaeth PA, Kidd DM. 2009. Linking big: the continuing promise of evolutionary synthesis. Evolution 64: 871–880. New Phytologist (2014) www.newphytologist.com 6 Forum New Phytologist Letter The Plant List. 2010. Version 1. Published on the Internet. [WWW document] URL http://www.theplantlist.org/ [accessed 15 March 2012]. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA. 2008. The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biology 14: 2963–2977. Watson L, Dallwitz MJ. 1992 onwards. The grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. [WWW document] URL http://deltaintkey.com [accessed 11 February 2012]. Whitfield J. 2011. Species spellchecker fixes plant glitches. Online tool should weed out misspellings and duplications. Nature 474: 263. Supporting Information Additional supporting information may be found in the online version of this article. Methods S1 Full methodology used to compile and index the dataset. Notes S1 Full list of literature sources used to compile the dataset presented in Tables S3 and S4. Table S1 Herbarium specimens of grass species analyzed for stable carbon isotope ratio Table S2 Uncharacterized species with countries of occurrence and synonyms (Clayton et al., 2002a,b onwards) Table S3 Full genus-level dataset with numbers of species for each, and references for evidence Table S4 Full species-level dataset for the genus Panicum s.l., as circumscribed by Clayton et al. (2002b onwards), with the evidence and references used to ascribe photosynthetic type for each Please note: Wiley Blackwell are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Key words: C3 photosynthesis, C4 photosynthesis, comparative plant ecology, ecological informatics, evolutionary biology, grasses, Poaceae. www.newphytologist.com np-centraloice@lancaster.ac.uk np-usaoice@ornl.gov www.newphytologist.com New Phytologist (2014) www.newphytologist.com Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust