Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum and its relationship with taxa of the Sacciolepis–Trichanthecium clade (Poaceae: Panicoideae: Paniceae) M. V. Nicola, M. A. Lizarazu & M. A. Scataglini Plant Systematics and Evolution ISSN 0378-2697 Volume 301 Number 9 Plant Syst Evol (2015) 301:2247-2260 DOI 10.1007/s00606-015-1227-9 1 23 Your article is protected by copyright and all rights are held exclusively by SpringerVerlag Wien. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Plant Syst Evol (2015) 301:2247–2260 DOI 10.1007/s00606-015-1227-9 ORIGINAL ARTICLE Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum and its relationship with taxa of the Sacciolepis– Trichanthecium clade (Poaceae: Panicoideae: Paniceae) M. V. Nicola1 • M. A. Lizarazu1 • M. A. Scataglini1 Received: 27 October 2014 / Accepted: 11 May 2015 / Published online: 24 May 2015 Ó Springer-Verlag Wien 2015 Abstract The new genus Kellochloa is proposed, on the basis of morphological and molecular characters, to include two North American species of Panicum s.l., previously classified in sect. Verrucosa: P. brachyanthum and P. verrucosum. Both species are annual, with decumbent culms branching divaricately at the lower nodes, and erect culms with terminal and axillary inflorescences. The spikelets are pilose, with lower glume 1/6 to 1/4 the length of the spikelet, upper glume and lower lemma subequal, 3–5nerved, the lower anthecium reduced to the lower lemma, and upper anthecium indurate, with bicellular microhairs and simple papillae evenly distributed all over the lemma and palea. Molecular phylogenetic studies, analyzing plastid ndhF and rpoA sequences, confirmed that these morphological characters are differential. The phylogenetic position and taxonomic features of the new genus are established and compared with Panicum s.str. and other taxa of the Sacciolepis–Trichanthecium clade. Full synonymies and descriptions, a distribution map, illustrations of both species, and a key are provided. Two new combinations are proposed. In addition, four African ungrouped species of Panicum s.l. were, for the first time, included in the phylogenetic analysis to analyze their relationship with the new genus and its positions in the Sacciolepis– Trichanthecium clade. Handling editor: Livia Wanntorp. & M. V. Nicola mnicola@darwin.edu.ar 1 Instituto de Botánica Darwinion, Labardén 200, Casilla de Correo 22, B1642HYD San Isidro, Buenos Aires, Argentina Keywords Kellochloa
Paniceae
Panicum
Phylogeny
Taxonomy
Verrucosa Introduction Panicum L., as traditionally circumscribed, was one of the largest genera of the Poaceae (Webster 1988). It included approximately 450 species distributed worldwide in different tropical and subtropical habitats, such as savannas, grasslands in dry or wet areas, streamsides, and forest edges, from sea level to approximately 2500 m (Zuloaga 1987). On the basis of inflorescence and spikelet characters, Hitchcock and Chase (1910) recognized two subgenera and 13 informal species groups of Panicum in North America. Zuloaga (1987) provided an infrageneric classification of the New World Panicum species, based on morphological characters, such as ornamentation of the upper anthecium, photosynthetic type, spikelet characters, and chromosome base number. Zuloaga (1987) recognized six New World subgenera within Panicum: Panicum, Agrostoides (Hitchc.) Zuloaga, Megathyrsus Pilg., Phanopyrum (Raf.) Pilg., Dichanthelium Hitchc. & Chase, and Steinchisma (Raf.) Zuloaga. Although the spikelets of Panicum, as traditionally circumscribed, are largely uniform, this feature contrasts with the variation present in several reproductive (including inflorescence type, nervation of glumes, and upper anthecium texture and ornamentation) and vegetative characters, together with the preferred habitat of the different species (Crins 1991). The infrageneric variation in vegetative characters is related to the presence of all known photosynthetic types found in grasses. Panicum included species with non-Kranz and Kranz physiology with all Kranz variations, i.e., NADPme, NAD-me, and PEP-ck subtypes (Brown 1977; 123 Author's personal copy 2248 Hattersley 1987; Ellis 1988). These photosynthetic types are correlated with particular anatomical characters, e.g., number of vascular bundles, and presence of specialized chloroplasts in the parenchymatic or mestomatic bundles (Brown 1977; Ellis 1977). Phylogenetic studies, based on morphological and molecular characters, have firmly demonstrated that Panicum in its traditional sense is not monophyletic (GómezMartı́nez and Culham 2000; Zuloaga et al. 2000; Duvall et al. 2001, 2003; Giussani et al. 2001; Aliscioni et al. 2003). These studies allowed new delimitations within the Paniceae, such as the recognition of four genera, previously treated by Zuloaga (1987) at subgeneric level: Dichanthelium (Hitchc. and Chase) Gould, Phanopyrum (Raf.) Nash, Steinchisma Raf., and Megathyrsus (Pilg.) B.K.Simon & S.W.L.Jacobs (Zuloaga et al. 1998, 2003; Aliscioni et al. 2003; Freckmann and Lelong 2003; Simon and Jacobs 2003; Barkworth 2004). In a phylogenetic study of Panicum based on the ndhF chloroplast gene, Aliscioni et al. (2003) restricted Panicum, in a strict sense, to the type subgenus, which was strongly supported as a monophyletic group. Hsu (1965), Brown (1977), and Zuloaga (1987), previously treated subgenus Panicum as a homogeneous group clearly distinguishable from other elements of the genus. Species of subgenus Panicum are C4, of the NAD-me subtype, and have a basic chromosome number of x = 9. Therefore, as Panicum is currently restricted to subg. Panicum, species treated by Zuloaga (1987) in subg. Phanopyrum, including among them section Verrucosa, need to be reevaluated and reclassified within the Paniceae. The group Verrucosa was established by Hitchcock and Chase (1910) who included two North American species, both with tuberculate spikelets: Panicum brachyanthum Steud. and P. verrucosum Muhl. Hitchcock and Chase (1910) characterized these species as being annuals, with divaricately branching culms, panicles lax and open, and spikelets hispid, with the fruit minutely papillose. Later, Hsu (1965) raised this group to a section of Panicum, and Zuloaga (1987) classified Panicum sect. Verrucosa in subg. Phanopyrum, and characterized the section as comprising annual plants with the panicles lax and diffuse, spikelets pilose, with a minute nerveless lower glume, upper glume and lower lemma subequal, 3–5-nerved, lower palea and lower flower absent, and upper anthecium longitudinally rugose, papillate and with bicellular microhairs. In the ndhF phylogeny of the Paniceae, Aliscioni et al. (2003) included one voucher of Panicum verrucosum, which appeared in a clade together with Sacciolepis indica (L.) Chase, Panicum parvifolium Lam., and Panicum schwackeanum Mez, the latter two species now included in the genus Trichanthecium Zuloaga & Morrone. Zuloaga et al. (2011) treated in Trichanthecium, on the basis of 123 M. V. Nicola et al. morphological and molecular (rpoA and ndhF sequences) characters, 38 American and African species of Panicum sects. Parvifolia and Verruculosa; the combined phylogenetic tree (Zuloaga et al. 2011) showed P. verrucosum grouped in an unresolved trichotomy with the genera Sacciolepis Nash and Trichanthecium, with P. trichanthum as the sister species of this trichotomy. Panicum species assigned to sections Ovalifolia and Monticola appeared as the sister group of the entire Sacciolepis–Trichanthecium clade. Finally, Morrone et al. (2012) corroborated the position of P. verrucosum, together with Sacciolepis, Trichanthecium, and species of sections Ovalifolia and Monticola, in subtribe B, an unnamed clade of Paniceae, still under revision. The purpose of the present contribution is to test the monophyly of sect. Verrucosa of Panicum s.l and to establish the position of this section within the Sacciolepis– Trichanthecium clade of the Paniceae, analyzing ndhF and rpoA sequence data and describing morphological and anatomical characters. Additionally, four ‘‘incertae sedis’’ African species of Panicum, presumably belonging to the Sacciolepis–Trichanthecium clade, were included in the phylogenetic analysis: P. aequinerve Nees, P. chionachne Mez, P. eickii Mez, and P. inaequilatum Stapf. These species were studied to test their position within the Sacciolepis–Trichanthecium clade and their hypothetical relationship with species of section Verrucosa. Materials and methods Molecular phylogenetic analysis Taxa selection Six new taxa were analyzed: two species assigned to sect. Verrucosa (Panicum brachyanthum and P. verrucosum) and four ‘‘incertae sedis’’ species of Panicum presumably belonging to the Sacciolepis–Trichanthecium clade: P. aequinerve, P. chionachne, P. eickii, and P. inaequilatum. We added rpoA and ndhF sequences obtained for these six taxa into the combined matrix of the Sacciolepis– Trichanthecium clade from Zuloaga et al. (2011). The aligned matrix was submitted to TreeBASE under the study number S16511. Details, GenBank accessions, and voucher information of taxa analyzed are shown in the ‘‘Appendix’’. DNA sequencing All six vouchers analyzed were from herbarium material. DNA extraction was conducted using the DNeasy Plant Mini kit (Quiagen). The complete ndhF gene was amplified using four pairs of primers specified by Olmstead and Author's personal copy Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum Sweere (1994): 5F-536R, 536F-972F, 972F-1666R, and 1666F-3R. The rpoA region amplified consisted of an approximately 1400 bp fragment containing the entire rpoA gene, the 30 -end of petD encoding subunit IV of the cytochrome b complex, the 30 -end of rps11 encoding ribosomal protein S11, and the two intergenic spacers IGS between rpoA and petD and between rpoA and rps11. Two pairs of primers were used: RPOA1-RPOA6 and RPOA5RPOA2, designed by Petersen and Seberg (1997). The PCR reactions were performed in 25 ll final volume with 50–100 ng of template DNA, 0.2 lM of each primer, 25 lM of dNTPs, 5 lM MgCl2, 19 buffer, and 1.5 units of Taq polymerase provided by Invitrogen (Brazil). The reaction conditions were: an initial period of denaturation at 94 °C for 5 min, followed by 35 cycles of denaturation at 94 °C for 30 s., annealing at 48 °C for 1 min, and extension at 72 °C for 1 min. 30 s., and a final extension at 72 °C for 6 min terminated the reactions. PCR products were run out on a 1 % TBE agarose gel and stained. Sequencing reactions were performed by Macrogen, Inc. (Seoul, Korea). To edit and manually align the sequences, we used the program BioEdit version 5.0.9 (Hall 1999). The sequences obtained were submitted to GenBank (KR232090–KR232100). Data analyses A maximum parsimony analysis was performed using TNT (Goloboff et al. 2008) with all characters equally weighted with respect to codon position and gaps scored as missing data. Searches were performed using 1000 random addition sequences (ras) followed by tree bisection–reconnection (TBR), saving 10 trees per ras. The shortest trees retained were then TBR swapped holding a maximum of 20,000 trees. A strict consensus tree was generated from the most parsimonious trees. To assess the relative support for clades, bootstrap analyses were performed using 10,000 replicates of the matrix, heuristic searches were done using 100 ras, holding 5 trees per ras and TBR swapping. A Bayesian inference analysis was also performed with BEAUti and BEAST 1.8.1 (Drummond et al. 2012). The appropriate model of nucleotide substitution for each partition was selected by the Akaike Information Criterion (AIC) implemented in jModelTest 2.1.4 (Darriba et al. 2012). The Bayesian analysis was conducted with settings as follows: GTR?I?G and TVM?I?G substitution models for ndhF and rpoA partitions, respectively, four gamma categories, empirical base frequencies, uncorrelated rate variation with lognormal distribution, random starting tree, a Yule process as tree prior, auto-optimization option for all operators except the GTR A-G substitution parameter deactivated for the rpoA partition to achieve a TVM model, and default values for all other settings. Two independent 2249 runs of 10 million generations were sampled every 1,000th generation. Convergence of the chain and effective sample size of the parameters (i.e. ESS [ 200) were checked in Tracer 1.6 (Rambaut et al. 2014).The two runs were combined with LogCombiner 1.8.1 (Drummond et al. 2012) after a burn-in of 25 % of the trees from each run. Posterior probabilities of branches were calculated from a maximum clade credibility tree obtained with TreeAnnotator 1.8.1 (Drummond et al. 2012) and edited in FigTree 1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/). Morphological and anatomical analyses Morphological characters were based on examination of herbarium collections and published accounts. Specimens belonging to the following herbaria were examined: MO, P, PH, SI, US, and WIS (acronyms after Thiers 2014, permanently updated). Micromorphological observations were based on herbarium material. For anatomical studies, the second leaf below the inflorescence was selected. Specimens compared were Tryon 4547 and Moore 49-698 of P. verrucosum and Dale 4728 and Moore 49-714 of P. brachyanthum. Crosssectional leaf anatomy was determined from hand-sectioned leaf blades of herbarium specimens rehydrated by boiling in water with soap and subsequently stored in 70 % alcohol. The materials were dehydrated in an ethanol series and embedded in Histoplast (Johansen 1940; Ruzin 1999) to obtain serial microtome sections, 10–20 lm thick. The slides were stained in Safranin-fast green (D’Ambrogio de Argüeso 1986; Ruzin 1999) and mounted in synthetic resin (Eukitt) for permanent slides. Freehand paradermal sections were taken from each leaf surface. Half of the transverse sections and all paradermal sections were bleached in diluted household bleach until the sections became transparent, after which they were rinsed three or four times with water, stained with safranin for 30 min (Metcalfe 1960), washed three times in water, and mounted gelatin–glycerin for temporary slides. The epidermis was stained in safranin. Anatomical descriptions were prepared using the terminology of Ellis (1976, 1979). The upper anthecia were selected and cleaned in xylene for 1.5 h with an ultrasonic cleaner (Cleanson, model CS 1106, Argentina). The material was air-dried, mounted, and coated with a gold–palladium (40–60 %) alloy by then observed using a Phillips XL 30 (Phillips, The Netherlands) Scanning Electron Microscope (SEM) at the Museo Bernardino Rivadavia (Zeiss, Germany). The histological sections were studied and photographed with a compound microscope Wild M20, equipped with Nikon DS-U2 digital camera, and picture processing software NIC-Elements, F-package 2.30. 123 Author's personal copy 2250 Results Molecular phylogeny The new sequences obtained for the six taxa analyzed were included in the combined ndhF–rpoA matrix of Zuloaga et al. (2011). The rpoA sequence of Panicum aequinerve could not be obtained. The combined matrix showed a total of 48 taxa and 3446 characters (2076 from ndhF and 1370 from rpoA data), being 258 parsimony-informative characters. Parsimony analysis of the combined matrix yielded 80 trees of 457 steps (CI = 68, RI = 84). The strict consensus tree was fully congruent with the tree obtained under Bayesian inference. The Bayesian tree is shown in Fig. 1 indicating Bayesian posterior probabilities (PP) and parsimony bootstrap support (BS). The two species assigned to section Verrucosa, Panicum brachyanthum and P. verrucosum, form a strongly supported monophyletic group (BS = 100, PP = 100). Five molecular synapomorphies (at positions 509, 1469, 1844, 2259, and 2323 of the combined matrix) support this section. Section Verrucosa appears with 100 % BS and 100 % PP as the sister group of the Sacciolepis–Trichanthecium clade; the latter including a 100 % supported clade formed by the four ‘‘incertae sedis’’ African species of Panicum (P. aequinerve, P. inaequilatum, P. chionachne, and P. eickii) Fig. 1 Phylogenetic tree from Bayesian analysis based on the combined plastid sequences (ndhF ? rpoA). Vouchers sequenced for this study are denoted by asterisks. Numbers above and below branches indicate Bayesian posterior probabilities and parsimony 123 M. V. Nicola et al. as the sister group of Trichanthecium. Panicum trichanthum appears as the sister species of the clade Verrucosa– Sacciolepis–Trichanthecium, while Panicum species of sections Ovalifolia and Monticola constitute the other clade of the subtribe B (sensu Morrone et al. 2012). Morphology Spikelets Both Panicum brachyanthum and P. verrucosum have glumes and lower lemma with a distinctive coverage of hairs all over the surface, which were not analyzed previously. Both species have modified hairs on the glumes and lower lemma as follows: bracts in P. brachyanthum are covered by tuberculate hairs, with macrohairs arising from a cushion base, formed by thickened and modified epidermal cells (Figs. 2d, e, 4a, b), while in P. verrucosum prickle hairs arise from a similar cushion base (Figs. 3d, e, 4c, d). The upper anthecium is indurate, with bicellular microhairs and simple papillae regularly distributed all over the surface in both species (Fig. 5c, d); P. verrucosum differs (Fig. 5a, b) by having thickened longitudinal and transverse walls (vs. eventually thickened on the margins of the upper lemma, otherwise smooth in P. brachyanthum). bootstrap values, respectively. Vertical bars correspond to principal clades as discussed in the text. The scale bar represents substitutions per site Author's personal copy Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum Fig. 2 Kellochloa brachyantha (Steud.) Lizarazu, Nicola & Scataglini. a Habit; b detail of ligule; c portion of a raceme; d spikelet ventral view; e spikelet, dorsal view; f upper anthecium, dorsal view; 2251 g upper anthecium, ventral view; h upper palea with lodicules and stamens; i caryopsis, embryo view; j caryopsis, hilum view; k caryopsis immature, hilum view (from Gould 12002) 123 Author's personal copy 2252 Fig. 3 Kellochloa verrucosa (Muhl.) Lizarazu, Nicola and Scataglini. a Habit; b detail of ligular region; c spikelet ventral views. d spikelet ventral view; e spikelet, dorsal view; f upper anthecium, 123 M. V. Nicola et al. dorsal view; g upper anthecium, ventral view; h upper palea with caryopsis; i caryopsis, embryo view; j caryopsis, hilum view (from Collins 114) Author's personal copy Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum 2253 Fig. 4 Scanning electron micrographs of the spikelet of Kellochloa brachyantha (a, b) and K. verrucosa (c, d). a Spikelet ventral view; b detail of the lower lemma with macrohairs, prickle hairs; c spikelet ventral view; d detail of the lower lemma with bicellular microhairs, prickle hairs. (a, b from Hatch 1074 and a–d from Brown 2698). Scale bars a 500 lm; b 200 lm; c 250 lm; d 100 lm Anatomy Panicum brachyanthum and P. verrucosum are C3 species, with non-Kranz anatomy of the PS (XYMS?) subtype (Hattersley and Watson 1976; Brown 1977; Ellis 1977) characterized by having a parenchymathous and a mestome sheath surrounding the vascular bundles and in contact with the metaxylem vessels. The mesophyll is distinguished by the presence of more than 5 chlorenchyma cells between consecutive vascular bundles. Leaf blade in transverse section Outline: broadly V-shaped, with slightly involute margins; leaf thickness 320–350 lm, arms of the lamina symmetrical. Ribs and furrows: slightly rounded adaxial ribs, abaxial ribs and furrows round, rib associated with first- and second-order vascular bundles. Keel: slightly rounded on the adaxial side and very developed on the abaxial side, 550–620 lm width in P. verrucosum (vs. 455–530 lm width. in P. brachyanthum), associated with colorless parenchyma and with vascular bundles. Vascular bundle arrangement: three or four second-order vascular bundles between contiguous first-order vascular bundles; all vascular bundles situated in the center of the blade. Vascular bundle structure: First-order vascular bundles circular in outline. Second-order vascular bundles circular in outline, with xylem and phloem tissue distinguishable. Vascular bundle sheath: non-Kranz, bundle sheaths are double with the outer sheath entire, without specialized chloroplasts; parenchyma bundle sheath of the first-order vascular bundles entire or with adaxial interruption of sclerenchyma girders, consisting of 13–18 rounded cells; parenchyma bundle sheath of the second-order vascular bundles entire, 123 Author's personal copy 2254 M. V. Nicola et al. Fig. 5 Scanning electron micrographs of upper anthecium of Kellochloa brachyantha (a, b) and K. verrucosa (c, d). a Upper anthecia ventral view; b detail of the upper palea, with simple papillae and bicellular microhairs; c upper anthecia ventral view; d detail of the upper palea with bicellular microhairs and simple papillae. (a, b from Hatch 1074 and c, d from Brown 2698). Scale bars a 500 lm; b, d, 100 lm; c 250 lm formed by 6–10 rounded cells. Sclerenchyma: small, adaxial and abaxial girders associated with the first- and second-order vascular bundles; fibers lignified, small, rounded sclerenchyma caps located in leaf margins. Mesophyll: chlorenchyma radiately arranged, 5 or more chlorenchyma cells between consecutive vascular bundles. Adaxial epidermal cells: bulliform cells fan-shaped, in restricted groups of 5–6 cells, epidermal cells small, and regular in outline. Abaxial epidermal cells: bulliform cells absent, cuticle thickened (Fig. 6a, b). Abaxial epidermis in surface view Zonation costal and intercostal zones distinguishable; costal zone formed by 4–6 rows of long cells; intercostal zone with 123 6–7 rows in P. verrucosum (vs. 7–9 rows in P. brachyanthum) of long cells. Intercostal cells elongated rectangularly, more than 3–5 times longer than wide in P. verrucosum (vs. 4–8 times longer than wide in P. brachyanthum); side walls parallel, end walls vertical, and anticlinal walls slightly thickened; rectangular cells with moderately undulated anticlinal walls. Stomata complex triangular, 1–2 rows of stomata in each intercostal zone, stomata 37.5–38.5 9 20–26 lm. Intercostal short cells absent or present, solitary, transversely elongated when present. Microhairs bicellular, finger-like, with the basal cell slightly longer than the distal cells. Macrohairs absent. Papillae absent. Prickles located in the costal zone, 54.5 9 18 lm, or absent. Silica bodies transversely elongated, intercostal silica bodies dumbbell-shaped in outline (Fig. 6c). Author's personal copy Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum 2255 Fig. 6 Leaf blade anatomy of Kellochloa verrucosa (a, b) and K. brachyantha (c, d). Transverse leaf section. a General aspect of the keel; b portion of the leaf blade showing first-, second-, and thirdorder vascular bundles. Abaxial epidermis. c Epidermal zonation with narrow intercostal zones; detail of stomata, with triangular subsidiary cells, rectangular long cells with moderately undulating anticlinal walls, bicellular microhairs, and short cells; silica bodies. Adaxial epidermis. d Detail of stomata, with triangular subsidiary cells, rectangular long cells with moderately undulating anticlinal walls, silica bodies, and short cells. (a, b from Tryon 4547 and c, d from Dale 4728). Scales bar a–d 100 lm Adaxial epidermis in surface view Section Verrucosa is distinguished from Sacciolepis by the following set of characters: panicle lax and open (vs. spiciform), spikelets biconvex (vs. gibbous), lower glume scale-like (vs. developed), lower flower and lower palea absent (vs. lower flower and lower palea present), and upper anthecium papillate with bicellular microhairs (vs. smooth, glabrous). Section Verrucosa differs also from Trichanthecium and the clade including ‘‘incertae sedis’’ African species of Panicum s.l., i.e., P. aequinerve, P. eickii, P. chionachne, and P. inaequilatum, by the presence of terminal and axillary inflorescences, spikelets with a scale-like, nerveless lower glume, and the lower palea absent (vs. inflorescences terminal, bearing spikelets with the lower glume 1/2 to 1/1 the length of the spikelet, with the lower palea present both in Trichanthecium and the former ‘‘incertae sedis’’ species mentioned). Panicum aequinerve, P. chionachne, P. eickii, and P. inaequilatum share a spikelet with the lower glume as long as the spikelet, 3–5(–7)-nerved, lower palea present, and upper anthecium smooth and glabrous, the latter Epidermal cells similar to the abaxial surface, except for the presence in the costal zones of a central band of rectangular cells, 2–4 cells wide (Fig. 6d). Discussion In the molecular analysis Panicum sect. Verrucosa was monophyletic and related to Sacciolepis, Trichanthecium, and ‘‘incertae sedis’’ species of Panicum s.l. of the Sacciolepis–Trichanthecium clade; therefore, they are distinct from of Panicum s.str. The species of sect. Verrucosa share being annual plants, with the culms divaricately branching at the base, with terminal and axillary inflorescences present, spikelets hispid, with the lower glume short and nerveless, lower palea and lower flower absent, and upper anthecium with bicellular microhairs and simple papillae evenly distributed. 123 Author's personal copy 2256 M. V. Nicola et al. character distinguishing these species from Trichanthecium, a genus with the upper anthecium with bicellular microhairs and simple papillae regularly distributed all over the upper lemma and palea. Species of sect. Verrucosa, together with P. aequinerve, P. chionachne, P. eickii, and P. inaequilatum, are unrelated to Panicum s.str. as defined by Aliscioni et al. (2003). Panicum, as presently circumscribed, includes species with membranous-ciliate or ciliate ligules, open and lax inflorescences, spikelets ellipsoid to long ellipsoid, with the lower glume 1/3 to 3/4 the length of the spikelet, lower palea present, and upper anthecium indurated, with simple or compound papillae at the top of the palea and without bicellular microhairs. In addition, all species of Panicum s.str. differ by C4 carbon fixation, by having the NAD-me subtype, and a basic chromosome number of x = 9. In agreement with Zuloaga et al. (2011), Panicum trichanthum, an American species distributed from Mexico to Argentina, appears as the sister species of the Sacciolepis–Trichanthecium clade. Species of sect. Verrucosa are distinguished from P. trichanthum by being annual, with both terminal and axillary inflorescences, spikelets pilose, with the lower palea absent (vs. plants perennial, with terminal inflorescences with spikelets glabrous, and a lower palea present in the latter species). A summary of characters distinguishing the new genus are presented in Table 1. Conclusions Our analysis allowed us to conclude that both species of Panicum sect. Verrucosa should be segregated from Panicum and considered as a new genus within tribe Paniceae. The taxonomic position of P. aequinerve, P. chionachne, P. eickii, and P. inaequilatum, and their final relationship and possible inclusion in Trichanthecium, should be confirmed with a detailed analysis of more related African species. A new contribution is in preparation to establish the taxonomic position of non-Kranz Panicum species included or related to the Sacciolepis–Trichanthecium clade to clarify the relationships within the entire subtribe. Key to distinguish Kellochloa from related taxa of the Sacciolepis–Trichanthecium clade 1. 10 . 2. 20 . Inflorescence spiciform with saccate spikelets, the upper glume gibbous. . .Sacciolepis Inflorescence open and lax, not spiciform; spikelets biconvex, not saccate, upper glume rounded. . .2 Lower glume 1/6 to 1/4 the length of the spikelet. . .3 Lower glume 1/2 to 1/1 the length of the spikelet. . .4 123 3. 30 . 4. 40 . Plants annual, with terminal and axyllary inflorescences, spikelets pilose, lower palea absent. United States. . .Kellochloa Plants perennial, with terminal inflorescences, spikelets glabrous, lower palea present. Mexico to Argentina. . .Panicum trichanthum Upper anthecium smooth, without bicellular microhairs and simple papillae. . .Panicum ‘‘African incertae sedis’’ species Upper anthecium with bicellular microhairs and simple papillae. . .Trichanthecium Taxonomic treatment Kellochloa Lizarazu, Nicola & Scataglini, gen. nov.— TYPE SPECIES: Panicum verrucosum Muhl. : Kellochloa verrucosa (Muhl.) Lizarazu, Nicola & Scataglini. = Panicum group Verrucosa Hitchc.and Chase., Contr. U.S. Natl. Herb. 15: 28, 126. 1910, nom. inval. = Panicum unranked Verrucosa Hitchc., N. Amer. Fl. 3(2): 200, 205. 1915. = Panicum sect. Verrucosa Hitchc. & Chase ex C.C. Hsu, J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 132. 1965. Annuals, with culms rooting and divaricately branching at the lower nodes, decumbent, then erect; nodes compressed, glabrous. Ligules membranous-ciliate; collar glabrous. Blades lanceolate to linear-lanceolate, glabrous, acuminate. Inflorescences open lax, multiflowered, exserted, peduncles cylindrical, smooth, and glabrous; terminal and axillary inflorescences present; main axis cylindrical or flattened, scaberulous; pulvini short-pilose or glabrous; first-order branches ascendent, divergent, alternate, axis of the branches triquetrous, scaberulous; pedicels solitary or paired, claviform. Spikelets ellipsoid to long ellipsoid, biconvex, pilose. Lower glume 1/6–1/4 the length of the spikelet, nerveless. Upper glume and lower lemma subequal, 3–5-nerved. Lower palea and flower absent. Upper anthecium ellipsoid, indurate, with bicellular microhairs and simple papillae evenly distributed all over the lemma and palea. Caryopsis obovoid to ellipsoid; hilum oblong to punctiform, embryo less than 1/2 the length of the caryopsis. Etymology: We are pleased to name this new genus after Dr. Elizabeth A. Kellogg, who has contributed significantly to the knowledge of grasses; also, Dr. Kellogg did a great and wonderful job helping so many young students of our institution. Key to the species 1. Blades lanceolate, flat; spikelets 1.8–2.1 mm long, glumes and lower lemma covered by tuberculate Author's personal copy Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum 2257 Table 1 Comparative morphological characters between Kellochloa and related taxa Kellochloa Trichanthecium Panicum s.str. Sacciolepis ‘‘Incertae sedis’’ African Panicum Panicum trichanthum Duration Annual Annual or perennial Annual or perennial Annual or perennial Annual or perennial Perennial Inflorescence Lax, open Lax, open Lax or contracted Contracted, spiciform Lax or contracted Lax, open Axillary inflorescences Present Absent, occasionally present Absent Absent Absent Absent Spikelet shape Not gibbous Not gibbous Not gibbous Gibbous Not gibbous Not gibbous Lower glume length 1/6 to  the length of the spikelet ‘ to 4/5 1/3 to 4/5 1/3 to ‘ 4/5 to 1/1 1/5 to  Lower palea Absent Present Present or absent Present Present Present Upper anthecium pilosity With bicellular microhairs With bicellular microhairs With macrohairs or glabrous Glabrous Glabrous Glabrous Upper anthecium ornamentation With simple papillae, smooth or rugose With simple papillae, smooth With simple or compound papillae, smooth Without simple papillae, smooth Smooth Smooth Photosynthetic pathway C3 C3 C4 C3 C3 C3 10 . prickle hairs, upper anthecium rugose. . .K. verrucosa Blades linear-lanceolate, involute; spikelets 3.2– 4.2 mm long, glumes and lower lemma covered by long tuberculate hairs; upper anthecium smooth.. . .K. brachyantha 1. Kellochloa brachyantha (Steud.) Lizarazu, Nicola & Scataglini, comb. nov. : Panicum brachyanthum Steud., Syn. Pl. Glumac. 1: 67. 1853.—TYPE: United States. Texas. Rusk Co.: in sabulosis sylvaticus, Vinzent 124 (holotype: P 00740934!; isotypes: US 80479!, fragment and photo ex P, W 18890237830!). Figure 2. = Panicum sparsiflorum Vasey, U.S. Dept. Agric. Bot. Div. Bull. 8: 36. 1889, nom. illeg. (Art. 53), non Döll, 1877.—TYPE: United States. Texas. San Bernardino, Oct 1839, J. L. Ridell 20 (lectotype, US 81288!, designated by Hitchcock & Chase, Contr. U.S. Natl. Herb. 15: 128. 1910; isolectotype, ISC 0000579!). Plants 30–90 cm tall; internodes 1–10 cm long; nodes pale. Sheaths 2–6 cm long, usually shorter than the internodes, the lower ones hirsute, with short papillose-pilose hairs, the upper ones glabrous, the margins membranous, ciliate. Ligules 0.3–0.5 mm long. Blades 4–14 cm long, 0.2–0.3 cm wide, linear-lanceolate, with involute margins, narrow at the base. Inflorescences 5–16 cm long, 4–10 cm wide; peduncles 7–25 cm long pedicels 2–13 mm long. Spikelets 3.2–4.2 mm long, 1.5–2 mm wide, long ellipsoid, green, glumes and lower lemma tuberculate, hispid, with stiff macrohairs arising from wartlike bases. Lower glume 0.6–0.8 mm long, 1/5–1/4 the length of the spikelet, obtuse or acute. Upper glume and lower lemma 5-nerved, acute. Upper anthecium 2.8–3.2 mm long, 1.4–1.6 mm wide, long ellipsoid, smooth or slightly rugose toward the margins of the lemma. Caryopsis ellipsoid, 2 mm long, 1.1 mm wide; hilum oblong, embryo less than 1/2 the length of the caryopsis. Phenology Flowering between August and October. Distribution and habitat Southeastern United States, in Arkansas, Louisiana, Mississippi, Oklahoma, and Texas (Fig. 7), growing in dry, sandy soils in open areas, woodland borders, and roadsides. Representative specimens examined United States. Arkansas. Benton, Chesney Prairie Natural Area, McKenzie et al. 2165 (MO); E of Strong, on roadside, high file for Ouachita R bridge, Moore 49-698 (SI). Florida. Roadbank beside Lapine Rd. 2 miles SW of jct. Of La. 34 and La. 3033, sec. 3, Dale 4728 (WIS). Louisiana. Lake Charles, Chase 69 (MO). Mississippi. Jones Co.: 1 mile northwest of Ellisville, at base of longleaf pine slope, common in ditch, McDaniel 3431 (MO). Oklahoma. Sapulpa, Indian Territory, Bush 1397 (MO). Texas. Nacogdoches Co.: about 1 mile east of Melrose, Correll 26242 (MO); 3.7 miles of the junction of Hwy. FM 1179 and FM 2038, NE of Bryan, Hatch 1074 (WIS); Trinity County, 5 miles northwest of Groveton, Gould 12002 (WIS). 123 Author's personal copy 2258 M. V. Nicola et al. Fig. 7 Map of North America showing the distribution of Kellochloa brachyantha and K. verrucosa 2. Kellochloa verrucosa (Muhl.) Lizarazu, Nicola & Scataglini, comb. nov. : Panicum verrucosum Muhl., Descr. Gram.: 113. 1817.—TYPE: Habitat in N. Caesarea, New Jersey, Delaware et Georgia, Muhlenberg 107, 6 (holotype, PH 00031497!; isotype, US, fragment and photo). Figure 3. = Panicum debile Elliott, Sketch Bot. S. Carolina 1: 129. 1816, nom. illeg. (Art. 53), non Desf., 1798.—TYPE: United States. South Carolina? (not located). – Panicum rugosum Bosc ex Spreng., Syst. Veg. 1: 314. 1825, pro syn. nom. nud., as a synonym of P. verrucosum Muhl. – Panicum umbraculum Bosc ex Spreng., Syst. Veg. 1: 314. 1825, pro syn. nom. nud., as a synonym of P. verrucosum Muhl. Plants 20–110 cm tall; internodes 1.5–7 cm long; nodes dark, compressed, glabrous. Sheaths 2–7.5 cm long, shorter or longer than the internodes, the margins ciliate. Ligules 0.2–0.5 mm long; collar brown. Blades 5–18 cm long, 0.2–0.8 cm wide, lanceolate, flat, rounded at the base. Inflorescences 7–22 cm long, 4–18 cm wide; peduncles 10–25 cm long; pedicels 1–6 mm long, scaberulous. Spikelets 1.8–2.1 mm long, 0.9–1 mm wide, ellipsoid, green or tinged with purple, glumes and lower lemma covered with prickle, tuberculate hairs. Lower glume 0.3–0.5 mm long, 1/6–1/4 the length of the spikelet, acute. Upper glume and lower lemma subequal, the upper glume shorter at maturity, 3–5-nerved, acute. Upper anthecium 1.7–2 mm 123 long, 0.8–1 mm wide, rugose, with thickened longitudinal and transverse walls. Caryopsis obovoid, 1.2–1.3 mm long, 0.7–0.8 mm wide; hilum punctiform, embryo 1/3 the length of the caryopsis. Phenology Flowering between August and October. Distribution and habitat Frequent in of eastern United States coasts, where it is present in Alabama, District of Columbia, Florida, Georgia, Louisiana, Maryland, Massachusetts, Mississippi, Missouri, New Jersey, North Carolina, Pennsylvania, Rhode Island, South Carolina, Texas, and Virginia; it can also be found in Indiana, Kentucky, and Missouri (Fig. 7); it grows in moist or wet sandy areas, occasionally can be found in open, drier woodlands. Representative specimens examined United States. Alabama. Fayette Co.: Tupelo swamp, east side of Fayette, Kral 48665 (MO); S of Bauxite, Moore 49-714 (SI). Florida. Franklin Co.: at gate to Ft. Gadsden State Park, 12 mi. W of route 65, 5.8 air mi. SSW of Sumatra, Anderson 10228 (MO). Georgia. Cook Co.: 3.3 mi. NW of Adel. Coastal Plain Province, Faircloth 4852 (MO). Indiana. Jasper Co.: Jasper-Pulaski State Game Preserve, 12 miles southeast of Thefft, Tryon & Tryon 4547 (MO); sloughs, Dune Park. Umbach 4600 (SI). Kentucky. Menifee Co.: McCaursey Ridge L.O., near Frenchberg, Reed 17496 (MO). Louisiana. Natchitoches Co.: Chopin, sandy ground, Palmer 8830 (MO). Maryland. Caroline Co.: Smithville, edge of Community Lake, Reed 68408 (MO). Massachusetts. Hampshire Co.: Northampton, King Street, Author's personal copy Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum along railroad, Ahles 87616 (MO); Fernald 8509 (WIS). Mississippi. Jackson Co.: 5 miles east of Ocean Springs, common on grassy slope near pine woods, McDaniel 3475 (MO). Missouri. Scott Co.: Unity Baptist Camp off of Rt. 77, c. 4 mi. NNE of Blodgett, McKenzie 1838 (MO). New Jersey. Lakewood, edge of bank, Drushel 8355 (MO). Rhode Island. Collins 114 (WIS).Texas. Harris Co., in Eisenhower Park below dam at Lake Houston, Brown 2680 (SI); in the Roy E. Larsen Sanctuary along Village Creek west of Silsbee, Brown 2698 (SI). Acknowledgments This work was supported by Consejo Nacional de Investigaciones Cientı́ficas y Técnicas (CONICET), Grant #11220100100207. We would like to express our deep gratitude to Fernando Zuloaga for his help, guidance, and his invaluable feedback on the manuscript. We also acknowledge Lone Aagesen for her valuable and careful suggestions on the manuscript and assistance with English editing. We thank as well Francisco Rojas and Marcelo Moreno for preparing the illustrations, and two anonymous reviewers for helpful comments on the manuscript. 2259 JF804841; T. brazzavillense Fay 5891 JF804880, JF804851; T. caaguazuense Anderson 35724 JF804875, JF804846; T. cyanescens Morrone 4772 JF804867, JF804837; T. dinklagei Jenik & Hall 1129 JF804866, JF804834; T. distichophyllum Longhi-Wagner 9664 JF804869, JF804840; T. gracilicaule Renvoize 2229 JF804864, JF804832; T. granuliferum Jansen-Jacobs 4064 JF804871, JF804842; T. machrisianum Viana 1727 JF804874, JF804845; T. margaritiferum Milne-Redhead 4530 JF804863, JF804831; T. micranthum Morrone 4770 JF804877, JF804848; T. natalense Kellogg 117 JF804879, JF804850; T. nervosum Morrone 4789 JF804876, JF804847; T. parvifolium Zuloaga s.n. AY188476, JF804835; T. polycomum Morrone 4763 JF804873, JF804844; T. pseudisachne Longhi-Wagner 9606 JF804868, JF804839; T. pyrularium Swallen 4936 JF804878, JF804849; T. rivale Morrone 4765 JF804872, JF804843; T. schwackeanum Morrone 115 AY188483, JF804838; T. tenellum Richards 9306 JF804865, JF804833; T. wettsteinii Zuloaga 6972 AY188497, JF804836. Appendix List of species used in the phylogenetic analysis including the six new vouchers, in bold, and vouchers from Zuloaga et al. (2011). Voucher information and GenBank accession numbers (ndhF, rpoA) are shown. Tribe Andropogoneae. Zea mays U21985, X07810. Tribe Paspaleae. Anthaenantiopsis rojasiana Zuloaga 6747 AY029620, JF804815; Echinochloa chacoensis Zuloaga 8573 EF218711, JF804820; E. cruspavonis Morrone 5369 EF218710, JF804819; Oplismenus burmanii Morrone 3625 EF218712, JF804821; Paspalum bertonii Zuloaga 7186 JF804854, JF804817; P. foliiforme Morrone 4669 JF804853, JF804816. Tribe Paniceae. Panicum aequinerve Kellogg 109 (MO) KR232095; P. bartlettii Alvarez 152 JF804882; P. brachyanthum Daniel et al. 25 (MO) KR232096, KR232090; P. brevifolium Gereau 5315 JF804860, JF804828; P. chionachne Wiehe 358 (US) KR232097, KR232091; P. eickii Robinson 5306 (US) KR232098, KR232092; P. heterostachyum Greenway 14150 JF804862, JF804830; P. hirtum Strudwick 4389 JF804861, JF804829; P. inaequilatum Phillips 61 (MO) KR232099, KR232093; P. millegrana Zuloaga 6766 AY029660, JF804852; P. sellowii Zuloaga 2123 AY188484, JF804822; P. trichanthum Morrone 5028 JF804858, JF804827; P. trichoides Zuloaga 7430 JF804859, JF804826; P. verrucosum Wheeler s.n. 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