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
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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;
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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
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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
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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
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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.
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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
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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
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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;
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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)
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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,
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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)
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Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum
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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,
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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
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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).
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Phylogenetic analysis and taxonomic position of section Verrucosa of Panicum
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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.
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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. AY188496; P. verrucosum Kral
48168 (MO) KR232100, KR232094; Sacciolepis angustissima Morrone 4319 JF804856, JF804824; S. indica
Bowen 3875 AY029677; S. myuros Longhi-Wagner 9390
JF804857, JF804825; S. vilvoides Zuloaga 6745 JF804854,
JF804823; Trichanthecium arctum Liesner 15757
JF804881; T. auricomum Longhi-Wagner 9637 JF804870,
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