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Phylogeny and Patterns of Floral Diversity in the Genus Piper (Piperaceae)

Authors:

Abstract

With ∼1000 species distributed pantropically, the genus Piper is one of the most diverse lineages among basal angiosperms. To rigorously address the evolution of Piper we use a phylogenetic analysis of sequences of the internal transcribed spacers (ITS) of nuclear ribosomal DNA based on a worldwide sample. Sequences from a total of 51 species of Piper were aligned to yield 257 phylogenetically informative sites. A single unrooted parsimony network suggested that taxa representing major geographic areas could potentially form three monophyletic groups: Asia, the South Pacific, and the Neotropics. The position of Pothomorphe was well supported among groups of New World taxa. Simultaneous phylogenetic analysis of an expanded alignment including outgroups suggested that taxa from the South Pacific and Asia formed a monophyletic group, provisionally supporting a single origin of dioecy. Within the Neotropical sister clade, resolution was high and strong bootstrap support confirmed the monophyly of several traditionally recognized infrageneric groups (e.g., Enckea [including Arctottonia], Ottonia, Radula, Macrostachys). In contrast, some of the species representing the highly polytypic subgroup Steffensia formed a clade corresponding to the previously recognized taxon Schilleria, while others were strongly associated with several of the more specialized groups of taxa. The distribution of putatively derived inflorescence and floral character states suggested that both umbellate and solitary axillary inflorescences have multiple origins. Reduction in anther number appears to be associated with highly packaged inflorescences or with larger anther primordia per flower, trends that are consistent with the suppression of later stages of androecial development.
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American Journal of Botany 88(4): 706–716. 2001.
P
HYLOGENY AND PATTERNS OF FLORAL DIVERSITY IN
THE GENUS
PIPER (P
IPERACEAE
)
1
M. A
LEJANDRA
J
ARAMILLO
2
AND
P
AUL
S. M
ANOS
Department of Botany, Duke University, Durham, North Carolina 27708-0338 USA
With ;1000 species distributed pantropically, the genus Piper is one of the most diverse lineages among basal angiosperms. To
rigorously address the evolution of Piper we use a phylogenetic analysis of sequences of the internal transcribed spacers (ITS) of
nuclear ribosomal DNA based on a worldwide sample. Sequences from a total of 51 species of Piper were aligned to yield 257
phylogenetically informative sites. A single unrooted parsimony network suggested that taxa representing major geographic areas could
potentially form three monophyletic groups: Asia, the South Pacific, and the Neotropics. The position of Pothomorphe was well
supported among groups of New World taxa. Simultaneous phylogenetic analysis of an expanded alignment including outgroups
suggested that taxa from the South Pacific and Asia formed a monophyletic group, provisionally supporting a single origin of dioecy.
Within the Neotropical sister clade, resolution was high and strong bootstrap support confirmed the monophyly of several traditionally
recognized infrageneric groups (e.g., Enckea [including Arctottonia], Ottonia, Radula, Macrostachys). In contrast, some of the species
representing the highly polytypic subgroup Steffensia formed a clade corresponding to the previously recognized taxon Schilleria,
while others were strongly associated with several of the more specialized groups of taxa. The distribution of putatively derived
inflorescence and floral character states suggested that both umbellate and solitary axillary inflorescences have multiple origins. Re-
duction in anther number appears to be associated with highly packaged inflorescences or with larger anther primordia per flower,
trends that are consistent with the suppression of later stages of androecial development.
Key words: flower evolution; inflorescence evolution; ITS sequences; Piper; Piperaceae.
The genus Piper includes .1000 species making it one of
the largest genera of basal angiosperms (Kubitzki, Rohwer,
and Brittrich, 1993; Soltis, Soltis, and Chase, 1999). One view
on the phylogenetic position of Piperaceae is among a diverse
assemblage of dicots termed ‘paleoherbs’ (Donoghue and
Doyle, 1989; Loconte and Stevenson, 1991), plants that resem-
ble monocots in certain vegetative features (e.g., adaxial pro-
phyll, scattered vascular bundles). More recently, the Pipera-
ceae and related families (e.g., Aristolochiaceae, Saururaceae,
Lactoridaceae) have been shown to form the sister group to
Winterales (Soltis, Soltis, and Chase, 1999; Qiu et al., 1999).
The high species diversity within Piper is unique among the
traditional Magnoliidae, providing a noteworthy example of
an increase in diversification rate at the base of the angio-
sperms (see Sanderson and Donoghue, 1994).
Piper species are distributed pantropically (Fig. 1) and take
the form of shrubs, herbs, and lianas common in the under-
story of lowland wet forests. The greatest diversity of Piper
species occurs in the American tropics (700 spp.), followed
by Southern Asia (300 spp.), where the economically impor-
tant species Piper nigrum L. (black pepper) and P. betle L.
1
Manuscript received 6 April 2000; revision accepted 20 June 2000.
The authors thank E. A. Zimmer, L. Prince, and R. Callejas for comments
in early versions of this manuscript; the National Tropical Botanical Gardens,
Fairchild Botanical Gardens, A. Filho-Oliveira, C. Castro, A. R. A. Gorts-van
Rijn, R. O. Gardner, and O. Vargas for plant material; the following institu-
tions and their staff for support during field work: Universidad de Antioquia
(Medellı´n, Colombia), Universidad Tecnolo´gica del Choco´ (Quibdo´, Colom-
bia), Fundacio´n Inguede´ (Bogota´, Colombia), Reserva del ´o N
˜
ambı´ (Alta-
quer, Colombia), Instituto de Ecologı´a (Xalapa, Me´xico), Philippines National
Herbarium (Manila, Philippines), Institute of Ecological and Biological Re-
sources (Hanoi, VietNam); and especially to Ricardo Callejas for determina-
tions and sharing his extensive knowledge on Piper. This work was partly
supported by the A. W. Mellon Foundation, the Tinker Foundation, the World
Wildlife Foundation, the Smithsonian Institution, the National Geographic So-
ciety (grant to R. Callejas), and the National Science Foundation (DEB 99-
72600).
2
Author for correspondence (e-mail: maj3@duke.edu, tel.: 919-660-7359).
(betel leaf) originated. Patterns of distribution of Piper species
vary from being locally endemic to widespread. There are sev-
eral species restricted to a specific center of diversity (e.g.,
Andes, Central America) and others occur throughout the Neo-
tropics or the Paleotropics. Piper is often a dominant element
in the understory of tropical forests and found to be one of
the five most speciose genera in select Neotropical forests
(Gentry, 1990). Not surprisingly, Piper species are of great
ecological importance and have been considered ‘key’ spe-
cies on the basis of their association with frugivorous bats
(Fleming, 1981, 1985; Bizerril and Raw, 1998).
Although the genus Piper is easy to recognize by a com-
bination of vegetative and reproductive characters, the appar-
ent uniformity of their diminutive flowers presents a signifi-
cant challenge to developing an infrageneric classification (Ta-
ble 1). The earliest classifications of Piperaceae emphasizing
Piper recognized between seven and 15 genera (Kunth, 1839;
Miquel, 1843–1844), within the current circumscription of the
genus. Five of these taxa continue to be accepted today: Piper,
Pothomorphe, Macropiper, Ottonia, and Zippelia (see Tebbs,
1993a). The most recent revision (DeCandolle, 1923) recog-
nized most of the same groupings, but at the sectional level.
These first monographs of Piper were based primarily on sta-
men number and position, carpel number, floral bract mor-
phology, inflorescence position, and leaf venation. After these
treatments three additional genera, Arctottonia (Trelease,
1930), Sarcorhachis (Trelease, 1927), and Trianaeopiper (Tre-
lease, 1928), were recognized from the Neotropics, and Pen-
ninervia was recognized from the Philippines at the sectional
level (Quisumbing, 1930). More recent taxonomic studies have
abandoned DeCandolle’s system citing the difficulty of eval-
uating floral characters from herbarium specimens (Trelease
and Yuncker, 1950; Burger, 1971). For example, Yuncker
(1973) recognized fewer segregates using inflorescence posi-
tion, a character he considered to be more conservative in its
variation. As a result, the infrageneric taxonomy of Piper is
April 2001] 707J
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ANOS
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HYLOGENETICS OF
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IPER
Fig. 1. Geographic distribution of the genus Piper. Species numbers are estimates for each of the centers of diversity of the group, thus regionally widespread
taxa may be represented more than once.
T
ABLE
1. Summary of the taxonomic history of Piper.
Kunth’s genera
(1839)
Miquel’s genera
(1843–1844)
DeCandolle’s
sections (1923)
Trelease and Yuncker
genera (1950)
Infrageneric
groups
Enckea
Chavica
Enckea
Macropiper
Macrostachys
a
Enckea
Macropiper
Arctottonia Arctottonia
Chavica
Enckea
Macropiper
Macrostachys
Ottonia
Piper
(Heckeria)
Steffensia
Schilleria
Ottonia
Piper
Pothomorphe
Radula
a
(Artanthe)
Ottonia
Eupiper
(Heckeria)
Sarcostemon
Steffensia
Ottonia
Piper
Pothomorphe
Trianaeopiper
Ottonia
Piper
Pothomorphe
Radula
Sarcostemon
Steffensia
Schilleria
Trianaeopiper
a
Described as sections within Artanthe (
5
Steffensia).
unsettled, and most local treatments have described species
without reference to subgeneric affiliation (Yuncker, 1953,
1972, 1973; Backer and Bakhuizen van der Brink, 1963; Bur-
ger, 1971; Steyermark, 1984; Chew, 1972; Howard, 1973; Liu
and Wang, 1975; Long, 1984; Green, 1994; Verdcourt, 1996;
Yongqian, Nianhe, and Gilbert, 1999).
To further develop our understanding of patterns of diver-
sification within Piper, the distribution of morphological
changes and/or combinations of character states needs to be
examined within a phylogenetic context. Floral variation in-
cludes the number and position of parts (e.g., 3–4 carpels and
1–10 stamens), relative size of filament and anther, and anther
aperture orientation. Additional variation occurs in the struc-
tures associated with flowers such as floral bracts and presence
or absence of pedicels. Flower structure in Piper appears to
be influenced by the packaging of flowers in the inflorescence.
Loosely arranged flowers have an unstable number of carpels
(varying between three and four), and tightly congested flow-
ers always have three. In a similar manner, loosely arranged
flowers have, in general, a higher number of stamens (e.g., P.
amalago has six stamens), while flowers in tightly congested
inflorescences may have as few as two (e.g., P. umbellatum).
Studies of flower ontogeny in Piper (Tucker, 1982; Callejas,
1986; Lei and Liang, 1998) have shown that the androecium
develops bilaterally with stamens initiated in pairs or individ-
uals (see Fig. 2). Stamen initiation begins with a lateral pair
followed by a single median anterior and then a single median
posterior (where they occur), whereas in species with six sta-
mens, the final pair is initiated in an anterior–lateral position.
Three or four carpels are initiated simultaneously from a gyn-
oecial ring (Tucker, 1982; Lei and Liang, 1998).
Flower presentation also may be correlated with differences
in pollination biology. The flowers of tightly congested inflo-
rescences often show a shift in anther dehiscence, from a lat-
eral slit towards an upwards or apical opening (Burger, 1971).
Pollen-collecting bees have been observed visiting the inflo-
rescences of certain Piper species (Semple, 1974; Marquis,
1988; Bornstein, 1989), and the tightly congested arrangement
may be advantageous since the bees can collect pollen from a
virtually seamless inflorescence surface. Inflorescence type in
Piper varies in position (axillary or terminal), length (from 2–
3 cm to 150 cm long), presentation (erect or pendulous), color
(cream to red), and number of spikes (single or umbellate; see
Fig. 2). Given the minute size of Piper flowers, changes in
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Fig. 2. Inflorescence morphology and associated flower structure. Names correspond to traditionally recognized groups within Piper. In each floral diagram,
circles are stamens, triangles are tricarpellate ovaries, and arching lines represent the subtending bract. The order of stamen initiation is indicated by numerical
sequence (Tucker, 1982; Jaramillo, unpublished data).
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ANOS
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IPER
floral structure may be evolutionarily less important than var-
iation in inflorescence type. It is likely that pollination and
dispersal biology have been influenced more by whole inflo-
rescence structure rather than individual flower structure
(Thies, Kalko, and Schnitzler, 1998).
The only previous cladistic analysis of Piper used morpho-
logical characters to suggest two major clades dividing Paleo-
tropical and Neotropical taxa into 25 subgenera with little res-
olution among them (Callejas, 1986). More recently a broader
morphological cladistic study of the Piperales including seg-
regates of Piper found support for two clades within Pipera-
ceae: Piper 1 Peperomia and Pothomorphe 1 Macropiper
(Tucker, Douglas, and Liang, 1993). Under this interpretation,
part of Piper is more closely related to Peperomia than to
other groups traditionally recognized within the genus. The
primary goal of this study is to develop a phylogenetic hy-
pothesis for Piper based on a broad sampling from throughout
its distribution using nucleotide data from the internal tran-
scribed spacer (ITS) of the nuclear ribosomal DNA. The ITS
region has been widely used for species level phylogenetic
analysis (Baldwin, 1993; Sang et al., 1994; Baldwin et al.,
1995; Kron and King, 1996; Manos, 1997) and preliminary
data indicate resolution within Piper is possible (Jaramillo and
Manos, 1998). The specific objectives were to: (1) identify
major clades within Piper, (2) reexamine previous classifica-
tions and the characters used to delimit traditionally recog-
nized taxa, (3) test the traditional taxonomic dichotomy be-
tween geographic regions within Piper, and (4) examine the
role of floral and inflorescence structure in the diversification
of Piper.
MATERIALS AND METHODS
Taxon sampling—Sixty-three accessions including 51 species of Piper rep-
resenting many of the subgenera recognized in the Neotropics and the Paleo-
tropics were examined. This study follows the proposal of Callejas (1986) to
consider all segregates of Piper as infrageneric groups (Table 1). At least four
species were sampled from nonmonotypic groups. For widely distributed spe-
cies, 2–3 plants were sampled from widespread localities to test for intraspe-
cific variation. Plant material was collected from naturally occurring popula-
tions, although a few species were cultivated in botanical gardens. A list of
species sampled, along with collection localities, vouchers, and accession
numbers is provided in Table 2. For members of segregate genera that do not
have a valid synonym within Piper, the most current classification was used
(e.g., Macropiper, Smith, 1975). For every species included, floral and inflo-
rescence structure was documented using field-collected material, and the con-
sistency of trait expression was verified in monographic treatments and her-
barium collections.
Potential outgroup taxa for this analysis included other genera of Pipera-
ceae, namely Peperomia and Sarcorhachis and two species of the family
Saururaceae (Houttuynia cordata and Saururus cernuus). Saururaceae is wide-
ly recognized as the sister family to Piperaceae in all recent global phyloge-
netic analyses (Chase et al., 1993; Qiu et al., 1999; Soltis, Soltis, and Chase,
1999) and macrosystematic taxonomic treatments (Cronquist, 1981; Takhta-
jan, 1997). The broader relationships within Piperaceae are not well estab-
lished and are currently the subject of DNA sequence-based investigations
(Jaramillo, unpublished data).
Total DNA was extracted from fresh or silica gel-dried leaves using the
23 CTAB (hexadecyl trimethyl ammonium bromide) method of Doyle and
Doyle (1987), or Dneasy Plant Mini kit (Qiagen Corporation, Valencia, Cal-
ifornia, USA). Amplification of the complete ITS region was done using one
of two pairs of primers ITS5-LS4R or LEU1-ITS4 (Baldwin, 1992; LEU1,
Baldwin, 1993). For all taxa the following sequencing primers were used:
ITS5, ITS4, ITS3, and ITS2 (Baldwin, 1992). Sequencing reactions were pre-
pared using the ABI Prism Dye Terminator Cycle Sequencing Reaction Kit,
according to the protocols provided by the manufacturer. Double-stranded
products were sequenced in all cases. Resulting sequences were assembled
using Sequencher (Gene Codes Corporation, Ann Arbor, Michigan, USA) and
deposited in GenBank (see Table 2 for accession numbers).
Sequence analysis—Sequences were aligned using CLUSTALX (Thomp-
son et al., 1997) and modified by visual inspection. Two different alignments
were used: Data Set 1 included only Piper species and Data Set 2 included
Piper species and the five outgroups. Because outgroup sequences were very
divergent from ingroup sequences, it was necessary to introduce additional
gaps to the alignment of Data Set 1. In particular, three sections of the align-
ment were ambiguous between Piper species and outgroups. Given that these
regions included several informative sites within Piper, the ambiguously
aligned bases that roughly correspond to these sites in outgroup sequences
were scored as missing. Phylogenetic analyses were performed with PAUP*
(Swofford, 1998) using the maximum parsimony algorithm with gaps treated
as missing data. Parsimony analyses were performed using heuristic searches
with 100 random addition replicates, TBR branch swapping, MULPARS,
steepest descent, and Goloboff fitness (k 5 2; Goloboff, 1997). Branches with
a minimum length of zero were collapsed using the ‘amb-’ option (Nixon
and Carpenter, 1996). Clade support was examined using 500 bootstrap rep-
licates (Felsenstein, 1985) and a complete heuristic search. Sequence distance
matrices also were calculated using PAUP*.
Because it is well known that moderate to high levels of sequence diver-
gence between ingroup and outgroup could potentially lead to spurious rooting
of the ingroup topology (e.g., Wheeler, 1990), the following options outlined
by Nixon and Carpenter (1996) were used: (1) examine unrooted trees derived
from analysis of Data Set 1; (2) use Lundberg rooting (Lundberg, 1972),
which derives a root for the unrooted tree by parsimoniously attaching out-
group states, read as ancestral states, to a particular network; and (3) examine
the rooted trees derived from analysis of Data Set 2 using various combina-
tions of potential outgroups. For Lundberg rooting, three outgroup taxa were
used (Peperomia, Sarcorhachis, and Saururus) to define ancestral states.
To explore flower and inflorescence evolution, select character states were
mapped onto a simplified phylogeny using MacClade (Maddison and Mad-
dison, 1992). The phylogeny conserved the topology obtained in the final
analysis and included taxa representing both unique and broadly representa-
tive combinations of character states.
RESULTS
Sequence variation and divergence—The alignment of
Data Set 1 included 51 taxa and 729 nucleotide sites distrib-
uted in the ITS region as follows: ITS1 5 244 bp (base pairs),
5.8S 5 166 bp, and ITS2 5 319 bp. A total of 257 (35.3%)
informative sites were included in the phylogenetic analysis of
Data Set 1 (ITS 1 5 98, 5.8S 5 14, ITS2 5 145). Sequence
divergence among Piper species ranged from 1.7% for sister
species P. archeri and P. spoliatum and 16.6% between Pa-
leotropical and Neotropical species P. celtidiforme and P.
amoenum. Intraspecific sequence variation was minimal in
comparisons among pantropically distributed species. For ex-
ample, sequence divergence among Piper umbellatum individ-
uals collected from Colombia, Brazil, and the Philippines was
0.04–0.06%. In general, intraspecific variation was always
lower than interspecific variation.
The alignment of Data Set 2 included all outgroup taxa and
773 nucleotide sites. A total of 332 (42.9%) informative sites
were included in the phylogenetic analysis. Sequence diver-
gence among the Piper species ranged from 3.8% for sister
species P. munchanum and P. augustum to 29.5% between
Paleotropical and Neotropical species P. bavinumP. ubatu-
bensis to .40% for outgroup–ingroup comparisons (Pepero-
mia elongata vs. P. amoenum).
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ABLE
2. Species examined for ITS variation. Vouchers are deposited in the Duke University Herbarium (DUKE) unless otherwise indicated.
Species Source
Voucher
a
or
GH accession
GenBank
accession
numbers
OUTGROUP
Houttuynia cordata Thunb. Cultivation, Duke University G. Houses Duke 86-180 AF 275211
Peperomia elongata HBK Depto. Antioquia, Colombia MAJ 108 AF 275213
Sarcorhachis naranjoana (CDC) Trel. La Selva Biological Station, Costa Rica OV s.n. AF 275210
S. sydowii Trel. Depto. Antioquia, Colombia MAJ 38 AF 275209
Saururus cernuus Thunb. Cultivation, Duke University G. H. Duke 86-174 AF 275212
INGROUP
Macropiper excelsum (Forst. f) Miq. Cultivation, Auckland Museum, New Zea-
land
ROG 8494 (AK) AF 275193
M. hooglandii Hutton & Green Cultivation Auckland Museum, New Zea-
land
ROG 8496 (AK) AF 275192
M. melchior Sykes Cultivation Auckland Museum, New Zea-
land
ROG 8495 (AK) AF 275191
Piper aduncum L. (VALLE) Depto. Valle, Colombia MAJ 76 AF 275157
P. aduncum L. (PHIL) Samar, Philippines MAJ 200 AF 275158
P. aduncum L. (LAV)
P. amalago L.
P. amoenum Yuncker
P. arborescens Roxb.
P. arboreum Aublet
P. archeri T. & Y.
P. arieianum CDC
P. augustum Rudge
P. auritum HBK
P. bartlingianum (Miq.) CDC
P. bavinum CDC
Edo. Minas Gerais, Brasil
Edo. Veracruz, Mexico
Depto. Choco´, Colombia
Prov. Albay, Philippines
Depto. Antioquia, Colombia
Depto. Antioquia, Colombia
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Guyana
Prov. Ha Tinh, VietNam
AFO 1253
MAJ 561
MAJ 116
MAJ 192
MAJ 112
MAJ 87
MAJ 69
MAJ 122
MAJ 63
RE 1267B
MAJ 392
AF 275159
AF 275186
AF 275160
AF 275202
AF 275180
AF 275178
AF 275163
AF 275165
AF 275175
AF 275183
AF 275199
P. betle L.
P. boehmeriaefolium Wall.
P. brevipedicellatum Bornstein
P. caninum Blume
P. cavendishioides T. & Y.
Cultivation, Duke University G. Houses
Prov. Ha Tinh, VietNam
Edo. Colima, Mexico
Prov. Surigao del Norte, Philippines
Lloro´, Choco´, Colombia
Duke 82-298
MAJ 235
MAJ 544
MAJ 218
MAJ 70
AF 275201
AF 275204
AF 275189
AF 275195
AF 275153
P. celtidiforme Opiz
P. cihuatlanense Bornstein
P. cinereum CDC
P. darienense CDC
P. decumanum L.
P. filistilum CDC
P. flagellicuspe T. & Y.
P. garagaranum CDC
P. hispidum Swartz
P. imperiale CDC
P. korthalsii Miq.
Prov. Lagunas, Philippines
Edo. Jalisco, Mexico
Depto. Choco´, Colombia
Depto. Antioquia, Colombia
Prov. Leyte, Philippines
Depto. Narin˜o, Colombia
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Prov. Quezo´n, Philippines
MAJ 171
MAJ 543
MAJ 66
MAJ 103
MAJ 210
MAJ 157
MAJ 65
MAJ 73
MAJ 53
MAJ 61
MAJ 184
AF 275205
AF 275187
AF 275190
AF 275181
AF 275203
AF 275155
AF 275154
AF 275162
AF 275156
AF 275176
AF 275208
P. methysticum Forst. f Cultivation, Nat. Trop. Bot. Garden
(NTBG)
NTBG-950585 AF 275194
P. michelianum CDC Edo. Jalisco, Mexico MAJ 537 AF 275188
P. multiplinervium CDC Depto. Choco´, Colombia MAJ 139 AF 275168
P. munchanum CDC Depto. Choco´, Colombia MAJ 120 AF 275164
P. nigrum L. (CULT) Cultivation, Duke University GH Duke94-006 AF 275197
P. nigrum L. (PHIL)
P. oxystachyum CDC
P. peltatum L. (AMAR)
P. peltatum L. (CHO)
P. peltatum L. (VIT)
Prov. Lagunas, Philippines
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Depto. Caldas, Colombia
MAJ 181
MAJ 140
MAJ 142
MAJ 45
JB sn
AF 275198
AF 275152
AF 275169
AF 275170
AF 275171
P. penninerve CDC Prov. Surigao del Norte, Philippines MAJ 213 AF 275206
P. pierrei CDC
P. pulchrum CDC
P. reticulatum L. (AMAR)
P. reticulatum L. (MED)
P. retrofractum Vahl
P. spoliatum T. & Y.
P. subpedale T. & Y.
P. ubatubensis Callejas
P. umbellatum L. (LAV)
Prov. Ha Tinh, VietNam
Depto. Antioquia, Colombia
Depto. Choco´, Colombia
Depto. Antioquia, Colombia
Prov. Ha Tinh, VietNam
Depto. Choco´, Colombia
Depto. Choco´, Colombia
Ed. Sa˜o Paulo, Brasil
Edo. Minas Gerais, Brasil
MAJ 394
MAJ 100
MAJ 128
MAJ 62
MAJ 395
MAJ 60
MAJ 57
CC 2
AFO 1251
AF 275200
AF 275177
AF 275184
AF 275185
AF 275196
AF 275179
AF 275161
AF 275182
AF 275172
P. umbellatum L. (CULT) Cultivation, Fairchild Botanical Garden 78-211B AF 275174
P. umbellatum L. (PHIL) Mindanao, Philippines MAJ 224 AF 275173
P. urdanetanum CDC Prov. Mindanao, Philippines MAJ 232 AF 275207
Trianaeopiper bullatum Cuatrec. Depto., Choco´, Colombia MAJ 55 AF 275167
T. confertinodum T. & Y. Depto. Choco´, Colombia MAJ 54 AF 275166
a
Collectors: AFO, A. F. de Oliveira; CC, C. Castro; MAJ, M. Alejandra Jaramillo; JB, J. Betancur; OV, Orlando Vargas; RE, R. Ek; ROG, R.
O. Gardner.
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IPER
Phylogenetic analysis—Parsimony analysis of Data Set 1
recovered one most parsimonious tree of 837 steps. The un-
rooted tree does not support the paraphyly of taxa representing
major geographical areas, thus as depicted these groups cor-
respond to three potentially monophyletic clades: Asia, the
South Pacific, and the Neotropics (Fig. 3). Within these clades
several well-supported subclades were found to correspond
with traditional subgeneric groupings: Enckea (including Arc-
tottonia), Ottonia, Radula, Pothomorphe (including P. auri-
tum), Macrostachys, Schilleria, Macropiper, and Penninervia.
Other taxa representing subgenera Trianaeopiper and Steffen-
sia are shown to be polyphyletic. The ITS data provided strong
bootstrap support (.85%) for the following clades: Asian,
South Pacific, Neotropical, Schilleria, Pothomorphe, Macros-
tachys, Radula, Macrostachys-Radula, Ottonia, Enckea, Ot-
tonia-Enckea, and Penninervia. Within the Neotropical clade,
species belonging to the broadly delimited subgenus Steffensia
were found to be intermixed with taxa corresponding to var-
ious subgenera of Piper. Species of the less speciose and more
narrowly defined subgenus Trianaeopiper also are widely
placed. In the South Pacific clade, species of the subgenus
Macropiper formed a monophyletic subclade sister to the cul-
tivated P. methysticum (kava-kava).
Rooting—The different approaches to root the tree pro-
duced similar results. Outgroup rooting placed the root on the
longest branch within Piper, between Neotropical and Paleo-
tropical taxa. Moving the root to depict (Asia 2 (Neotropics
1 South Pacific)) produced trees of equal length, whereas
trees specifying (South Pacific 2 (Neotropics 1 Asia)) were
only three steps longer. Lundberg rooting, using each of the
three outgroups (e.g., Peperomia elongata, Sarcorhachis nar-
anjoana, and Saururus cernuus) separately placed the root in
the same position as in unconstrained simultaneous analysis.
DISCUSSION
The phylogenetic hypothesis presented here suggests three
major clades within the Piper species sampled: Asia, the South
Pacific, and the Neotropics (Fig. 3). In contrast to the results
of Tucker, Douglas, and Liang (1993), we found support for
a broad concept of Piper, including the placement of Potho-
morphe among traditionally recognized groups of Neotropical
taxa. Our data independently support the morphological anal-
ysis of Callejas (1986) emphasizing the sharp distinction in
floral biology where Asian and South Pacific taxa are dioe-
cious, while all Neotropical taxa are bisexual. Given the dif-
ficulty in confidently resolving the relationships among the
three major clades, it is unclear whether dioecy is a synapo-
morphy for Asian and South Pacific Piper. Our findings also
demonstrate that the few pantropically distributed species of
Piper represent recent introductions. This is clear from the
strong association of samples of P. umbellatum and P. adun-
cum from the Philippines with their conspecifics from the Neo-
tropics. With respect to the pantropical distribution of the ge-
nus, phylogenetic evidence suggests a continuous ancestral
presence of Piper on the land areas of the Southern Hemi-
sphere, a result consistent with vicariance rather than dispersal.
One of the most controversial taxonomic issues within Piper
has been the appropriate rank at which to recognize infrage-
neric groups and closely related genera such as Macropiper
and Sarcorhachis (Miquel, 1843–1844; DeCandolle, 1923;
Trelease and Yuncker, 1950). Initial attempts to align ITS se-
quences among all potentially related taxa revealed patterns of
sequence divergence that may serve as a preliminary guide in
determining the phylogenetic limits of Piper. Using the cri-
terion of alignability, segregate genera such as Sarcorhachis
and Zippelia appear to be distantly related to Piper, whereas
Macropiper is more likely to represent a segregate within an
expanded concept of the genus. Further support for an ex-
panded phylogenetic circumscription of Piper will require a
broad phylogenetic survey of Piperales using placeholders
from the three groups resolved here (Jaramillo, unpublished
data). Nevertheless, provisional recognition of the three major
groups as subgenera within Piper establishes a working frame-
work to recognize additional subclades at the sectional level.
Neotropical clade—Our results resolve two major clades
and six well-supported subclades that correspond to many of
the traditionally recognized subgenera within Neotropical Pip-
er. The Enckea subclade was found to include species of the
subgenus Arctottonia (the pedicellate Piper species of Mexico;
Bornstein, 1989). Prior to the description of Arctottonia at the
genus level by Trelease (1930), species of this group were
included either in Enckea or Ottonia. Arctottonia species were
included in Enckea (Kunth, 1839) on the basis of reproductive
characters, such as number of stamens and carpels and floral
bract morphology, and in Ottonia (Presl, 1849) because ped-
icellate flowers occur in species of both groups. Enckea spe-
cies are shrubs distinguished by palmately veined leaves, in-
florescences with widely spaced bisexual flowers bearing four
stamens and three carpels, each subtended by a cucullate bract.
Molecular evidence confirms that Arctottonia is more closely
related to Enckea than to Ottonia, in agreement with vegeta-
tive morphology (e.g., leaf venation and growth habit) and
geographic distribution. Enckea and Arctottonia species are
found primarly in Central America, while Ottonia species oc-
cur mainly in the Atlantic Forest of Brazil (Trelease, 1930;
Callejas, 1986; Bornstein, 1989). Thus, traditional definitions
of Arctottonia and Enckea should be reconsidered.
Ottonia species are defined by pinnately veined leaves and
lax inflorescences with bisexual flowers bearing four stamens
and four carpels, each subtended by a cucullate bract. Al-
though the flowers of many Ottonia species are pedicellate, in
a considerable number of species flowers are sessile. An in-
teresting result is the close relationship of Enckea and Ottonia.
While Trelease (1930) had noted that Arctottonia was closer
to Enckea, he considered Ottonia to have more in common
with the generalized morphology of Steffensia species. Kunth
(1839), however, suggested that the only difference between
Ottonia and Enckea (as defined in his treatment) was the type
of leaf venation. Our results suggest that Trelease’s (1930) re-
liance on leaf venation differences among Neotropical Piper,
and in this particular example where Enckea has palmate veins
while Ottonia is pinnate, highlights one source of systematic
bias. As noted by Kunth (1839), Enckea and Ottonia present
the same floral morphology: flowers with generally four sta-
mens, three to four carpels, subtending cucullate bracts, and a
lax inflorescence.
Although both of these clades include taxa with pedicellate
flowers, it is premature to suggest the condition defines the
clade. In Ottonia, the pedicels are formed by zonal growth
below the gynoecium (Callejas, 1986), whereas pedicel for-
mation in Enckea is unstudied. Further studies of the devel-
opment of pedicellate flowers could clarify whether the loss
of pedicels in these taxa is derived. The evolution of pedicel-
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Fig. 3. Most parsimonious tree based on ITS sequence data. Length 5 837 steps; consistency index 5 0.52; retention index 5 0.792; G-fit 52184.841.
Branch lengths are drawn to scale. Percentage of 500 bootstrap replicates is given when higher than 50%. Branches with bootstraps higher than 85% are
indicated in boldface. * Steffensia, Trianaeopiper, n Sarcostemon, l Penninervia. See Table 2 for clarification of the abbreviations AMAR, CHO, CULT,
LAV, MED, PHIL.
April 2001] 713J
ARAMILLO AND
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ANOS
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IPER
late flowers may have been facilitated by the lax flower ar-
rangement within the inflorescence. Potential advantages of
pedicellate flowers cannot be assessed since little is known
about the pollination or dispersal ecology of these species. The
few studies that have observed pollination in species of sub-
genus Ottonia indicated that they are visited by generalist pol-
linators (e.g., flies, bees, and butterflies; De Figuereido and
Sazima, 2000), while only bees were observed visiting the
inflorescences of Arctottonia (Bornstein, 1989).
Species forming the Radula clade represent some of the
most commonly encountered of all Neotropical Piper. Most
species of Radula are shrubby and possess a generalized set
of features including thin, elliptic, membranaceous leaves with
unequal bases, and straight or curved inflorescences with tight-
ly congested flowers (but see Tebbs, 1993b). Radula were de-
scribed originally as a section of Steffensia (5 Artanthe; Mi-
quel, 1843–1844) and typically occurs in open areas or dis-
turbed habitats. Their widespread presence throughout the
Neotropics may be attributed to dispersal by bats along road-
sides. The sister group to Radula is Macrostachys, a small
group of species generally characterized as treelets with large,
lobulate leaves, and long pendulous inflorescences bearing
tightly congested flowers (but see Tebbs, 1989). These two
clades share tightly congested inflorescences, a characterfound
only in Neotropical species of Piper and probably related to
pollination by pollen-collecting bees (Burger, 1971).
The Pothomorphe clade includes P. auritum (subg. Steffen-
sia) in addition to the two species traditionally considered
within this group (e.g., P. umbellatum and P. peltatum). The
traditional concept of Pothomorphe recognized the presence
of umbellate axillary inflorescences as a defining feature.
Many authors have also noted that the inflorescence of Poth-
omorphe is a truncated axillary branch with reduced inter-
nodes and terminal inflorescences (Burger, 1971; Callejas,
1986; Tebbs, 1993b). Pothomorphe species are shrubs, with
palmately veined leaves borne on vaginated petioles. The flow-
ers are tightly congested in the inflorescence, each bearing two
stamens (four stamens in P. auritum) and three carpels that
are subtended by marginally ciliate hypopeltate bracts. Curi-
ously, species of Pothomorphe also occur in Asia and Africa.
Their presence in the Old World reflects recent introductions,
most likely by humans who used the plants in traditional med-
icines (Ehringhaus, 1997).
The results of this study do not support the monophyly of
all Steffensia sampled. Most species of Steffensia do form a
clade, but several others are associated with either Pothomorphe
or the Macrostachys 1 Radula clade (Fig. 3). Steffensia is the
largest group within Piper (;300 spp.), and its defining fea-
tures, such as the shrubby habit, plinerved to pinnately nerved
leaves, and flowers with four to five stamens and three carpels,
appear to represent many of the plesiomorphic states within
the genus. Miquel (1843–1844) described ten sections within
Steffensia based mainly on vegetative characters. The species
of Steffensia that form one of the clades resolved here have
lax inflorescences and correspond to species recognized within
the genus Schilleria (Kunth, 1839). Increased sampling is
needed across Miquel’s sections emphasizing the diversity in
the Atlantic Forest of Brazil, Amazonia, and the Caribbean.
The genus Trianaeopiper, endemic to the Choco´ Region of
northwestern South America and described by Trelease (1928)
for specimens with a single axillary inflorescence, appears to
be polyphyletic (Fig. 3). Comparative studies of the inflores-
cence structure in these species suggest differences in shape
and orientation, despite apparent similarities in position, as
well as variation in the packaging of flowers (Jaramillo and
Callejas, unpublished data). There may be multiple origins of
axillary inflorescences among the diverse lineages present in
the extremely wet forests of the Choco´.
South Pacific Islands clade—This small group includes
three species of the traditionally recognized genus Macropiper,
plus Piper methysticum, the source of kava-kava. Macropiper
are differentiated from the other species of Piper in having
axillary umbellate inflorescences, similar to those in Potho-
morphe, but with unisexual flowers. Recent reviews of the
taxonomy and morphology of Macropiper disagree on the in-
terpretation of the inflorescence. Smith (1975) suggested that
the inflorescence is truly axillary, whereas Gardner (1997) ar-
gued that it originated through reduction of axillary branches.
Recent studies of P. methysticum suggest a distant relation-
ship to Macropiper on the basis of its terminal inflorescence
and presence of kavalactones (Lebot and Le´vesque, 1989). Our
study suggests P. methysticum is related to Macropiper rather
than to other Asian species of Piper. To elucidate the phylo-
genetic relationships of South Pacific Piper and clarify the
origin of the unique inforescence type in Macropiper, greater
sampling is needed within the ;40 species of South Pacific
Piper.
The Asian clade—We included mainly samples from the
larger groups of Asian Piper and resolved four well-supported
subclades, but it is difficult to assign them to any traditionally
recognized groupings. Taxonomic treatments of Piper in Asia
have included from one to two broadly defined subgenera plus
a few small segregates. On the basis of floral bract morphol-
ogy, Miquel (1843–1844) defined two major groups within the
Asian species, Chavica (with hypopeltate bracts) and Piper
(with oblong bracts adnate to the rachis). DeCandolle (1923)
grouped all of these species regardless of bract morphology
into section Piper. The results from this study suggest that
bract type is not a good diagnostic character since the phylo-
genetic reconstruction shows that species with adnate bracts
(e.g., P. nigrum and P. korthalsii; see Fig. 3) are found in both
major clades of Asian Piper. The two species of section Pen-
ninervia sampled (P. celtidiforme and P. penninerve) form a
well-supported clade. These species are climbers, with pin-
nately nerved leaves and highly enlarged anther connectives.
Although there are other Asian species of Piper with pinnately
veined leaves, they are mostly shrubs and probably distantly
related to Penninervia. Piper korthalsii, the only member of
subgenus Sarcostemon, which is distinguished by having only
one stamen, formed the sister species to P. urdanetanum, a
species with three stamens. There are only two species of Pip-
er with a single stamen: P. korthalsii and the Neotropical P.
kegelii (‘‘subgenus’ Nematanthera). Assuming that the Neo-
tropical–Asian split holds throughout the genus, two origins
of this derived state are likely within Piper.
Floral and inflorescence evolution—Our developing phy-
logenetic hypothesis of Piper has confirmed the monophyly of
several traditionally recognized groups (e.g., Ottonia, Macro-
stachys, Macropiper), while indicating that other groups, such
as Steffensia and Trianaeopiper are polyphyletic. Interestingly,
taxa traditionally placed within Steffensia, the most general-
ized group of Piper with respect to flower morphology, form
the most basal lineages in each major clade of Neotropical
714 [Vol. 88A
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Fig. 4. Scenario for the evolutionary history of flower and inflorescence structure in the genus Piper. Simplified phylogeny is based on Fig. 3 to emphasize
flower and inflorescence diversity in selected lineages of Piper.*Steffensia, Trianaeopiper.
April 2001] 715J
ARAMILLO AND
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ANOS
—P
HYLOGENETICS OF
P
IPER
taxa. In the context of phylogeny, patterns of floral and inflo-
rescence evolution appear to generally support the derived sta-
tus of several of the traditionally recognized groups, in addi-
tion to suggesting multiple origins for certain specialized char-
acter states (Fig. 4). For example, the evolution of dioecy may
define Old World Piper, but we note that the unsampled Af-
rican species of Piper may be monoecious or dioecious, thus
potentially complicating the otherwise clean distinction be-
tween Old and New World taxa. A polyphyletic origin of Af-
rica Piper could be used to argue for long-distance dispersal,
while a shared history with Neotropical taxa would suggest an
independent origin of dioecy.
Inflorescence variation has been used to define taxa within
Piper, especially in combination with other characters, such as
in Pothomorphe where axillary umbellate inflorescences and
flowers with two stamens serve to distinguish these species.
The inflorescence in Piper is generally considered terminal,
with the solitary type most common and also found among
outgroup taxa. The presence of umbellate inflorescences in
Macropiper and Pothomorphe is best explained by conver-
gence (Fig. 4). Similarly, solitary axillary inflorescences have
been used to define the ;17 species described in Trianaeo-
piper; however, this trait also appears to have multiple origins
(Fig. 4). The precise nature of axillary inflorescences in Piper
remains poorly understood. Morphological studies have shown
that the axillary inflorescences in Macropiper and Pothomor-
phe represent axillary branches with reduced internodes (Bur-
ger, 1971; Gardner, 1997). Callejas (personal communication)
also suggested that the inflorescences in Trianaeopiper are de-
rived from reduced axillary branches.
There are several lines of evidence suggesting that the tight
packaging of floral primordia in developing inflorescences
may be associated with reduction in stamen number. Tucker
(1982) suggested that this general trend is probably a result of
spatial constraints leading to the suppression of later devel-
opmental sequences. Stamens in Piper are initiated succes-
sively by pairs or individuals (Fig. 2), thus flowers with fewer
stamens have lost pairs or single anthers that develop later in
species with higher numbers. Outgroups to Piper are consis-
tent in their expression of loosely packaged flowers with high-
er numbers of stamens. In Neotropical Piper, tightly congested
inflorescences have evolved numerous times and a general re-
duction to four stamens is apparent for most taxa, except for
Pothomorphe in which only the lateral pair develop (see Figs.
2 and 4). Although the unisexual flowers of Asian species have
one to three stamens, their inflorescences bear loosely arranged
flowers. In this case reduction of stamen number may be re-
lated to spatial constraints associated with larger stamen pri-
mordia. The larger stamens found in the Neotropical taxa Tri-
anaeopiper bullatum and P. filistilum also may explain why
their loosely arranged flowers possess only three stamens (see
Fig. 4).
The tendency of having tightly packaged flowers has been
associated with pollination by pollen-collecting bees (Burger,
1971). Studies comparing the pollination biology of species of
Piper with and without tightly congested inflorescences may
provide additional perspective on patterns of diversification
within the genus. A working hypothesis would state that Piper
species with tightly congested inflorescences have a more spe-
cialized guild of pollinators than Piper species with lax inflo-
rescences. One future goal is to use phylogeny as a tool to
design a sampling strategy for the comparative study of the
regulation of organ number and size that would be coupled
with field observations on pollinator diversity for the same set
of species. An integrative model for relating spatial constraints
to shifts in pollinators could begin to elucidate some of the
evolutionary forces responsible for the exceptional diversity
within Piper.
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... A detailed monographic study could throw more light on the distribution of Piper species in the Asiatic region that includes several biogeographic realms and biodiversity hotspots (Fig. 3). Jaramillo and Manos (2001) first attempted a molecular phylogenetic analysis on Piper based on 51 species and sequences from the internal transcribed spacer (ITS) of nuclear Clade. e. P. wightii f. ...
... Flowers of Piper species are small, open, bisexual or unisexual and arranged in spikes. Flower buds are often protected by bracts(Jaramillo & Manos, 2001). Spikes vary in their length, thickness, color and their positions (i.e., erect vs pendent). ...
... Spikes vary in their length, thickness, color and their positions (i.e., erect vs pendent). Due to similarity in morphological characters, sexual features were often used as a key reproductive trait to differentiate Neotropical and Paleotropical species(Faria Vieira & Rojas 2017;Jaramillo & Manos, 2001). Old-world Pipers are predominantly dioecious when compared to the Neotropical species, which are bisexual in nature. ...
Article
The genus Piper (Family Piperaceae), consisting of more than 2000 species worldwide, is one of the most speciose genera of flowering plants that belong to the broad category known as basal angiosperms. Piper is known for the several medicinally and economically important species that have been used throughout their native range. Interestingly, this genus is also one of the most taxonomically challenging genera among the angiosperms. The presence of taxonomically complex as well as ecologically and economically important species makes Piper an excellent study system to address the evolution of tropical biodiversity. Being an early-diverging angiosperm genus, understanding Piper systematics and divergence patterns holds vital clues to plant evolution in the tropics. However, research on this plant group is still in a nascent stage, with the primary focus being on its medicinal importance and natural product chemistry. Its distribution, natural history, ecology, evolution and systematics remain less explored. Lack of such knowledge will impede the ongoing conservation effort and may affect the sustainable utilization of this valuable plant resource. The Indian subcontinent is an important center of Piper diversity harboring ca. 100 species, including several economically and medicinally important species such as Black pepper. Piper species in India have a high potential for future utilization; however, their conservation status and needs have not been widely reviewed. Here, we review the taxonomy, ecology and evolution, of Piper species, the threats they face, and further discuss future research directions and suggest ways forward in conserving and effectively utilizing this important plant group in India.
... Piper represents an extraordinary diversification amongst early diverging angiosperms. It is a Pantropical group (Jaramillo and Manos 2001) and its highest diversity lies in the Neotropics (ca. 1800 species; fide Ulloa-Ulloa et al. 2018 onwards). ...
... We extracted DNA from all the new species (Table 1) using a CTAB method (Doyle and Doyle 1987). We amplified the nuclear ribosomal internal transcribed spacer (ITS) according to Jaramillo and Manos (2001) and aligned sequences using previous alignments as a guide (Jaramillo et al. 2008). First, we included the new sequences in our 900+ Piper ITS alignment, to determine the relationships of the new Piper species. ...
Article
Full-text available
We describe four new species of Piper from the Amazonian slopes of the northern Andes. Piper hoyoscardozii is distinguished from similar climbing species, P. dryadum and P. flagellicuspe, by its longer peduncles. The Amazonian species Piper indiwasii is distinguished from P. scutilimbum from Panama and northern Colombia by the narrowly spatulate leaf base extension. Piper nokaidoyitau is characterised by the presence of larger leaves and longer spikes than similar species, P. anonifolium and P. hostmannianum. Finally, P. velae is characterised by cordulate leaf bases in all nodes, petioles 0.8–1.5 cm long and pubescent fruits, which easily distinguish it from the related species, P. holdridgeanum.
... El género Piper es de gran relevancia en la familia piperaceae, ( Quijano-Abril et al., 2006) ya que contiene alrededor de 1,000 especies de interés medicinal (Torres-Pelayo et al., 2016). Estas se encuentran geográficamente en regiones tropicales y subtropicales del planeta ( Quijano-Abril et al., 2006;Standley & Steyermark, 1952), entre otras, Centroamérica, América del sur incluyendo la Amazonia central, (Jaramillo & Manos, 2001;Quijano-Abril et al., 2006), donde ha encontrado condiciones propicias para su distribución . ...
Article
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Guatemala is a country of great biological diversity,which has led natural product researchers to obtain results ofgreat interest and scientific relevance, mainly in pharmacologicalproperties; However, the molecular structure, conformations,and configurations of many secondary metabolites responsiblefor these properties are unknown. In this research, the objectivewas to isolate and elucidate the structure of a phenylpropanoidobtained from in the leaves of Piper patulum. e isolation wascarried out by liquid-liquid extractions and chromatographictechniques (Column Chromatography -CC-), obtaining .092 g.e elucidation was performed by mass spectroscopy, infraredspectroscopy -IR- and nuclear magnetic resonance experiments-NMR-, the data obtained indicates the corresponding (E)-1,3,5-trimethoxy-2- (prop-1-enyl) benzene. Subsequently, the phenylpropanoid presented antioxidant activity through thequalitative test with 2,2-diphenyl-1-picrylhydrazyl-DPPH
... The Piperaceae family has approximately eight genera and 3000 species [11]. The genus Piper is found in tropical and subtropical areas, and in America, there are approximately 700 species [12,13], with 324 species located in Peru [14,15]. This genus is an important source of essential oils and secondary metabolites, which have significant plant protection effects [16], including allelopathic/phytotoxic [14,17,18], antifungal [19,20], insecticidal, nematicidal, and antifeedant [10,21]. ...
Article
Full-text available
The chemical composition of essential oils (EOs) from ten Peruvian Piper species (Piper coruscans, Pc; P. tuberculatum, Pt; P. casapiense, Pcs; P. obliquum, Po; P. dumosum, Pd; P. anonifolium, Pa; P. reticulatum, Pr; P. soledadense, Ps; P. sancti-felicis, Psf and P. mituense, Pm) has been studied, along with their antifungal and phytotoxic activities. These EOs contained β-bisabolene/nerolidol (Pc), β-bisabolene/δ-cadinene/caryophyllene (Pt), caryophyllene oxide (Pcs), bicyclogermacrene/10-epi-Elemol (Po), bicyclogermacrene/germacrene-D/apiol (Pd), caryophyllene/germacrene-D (Pa), germacrene-D (Pr), limonene/apiol (Ps), apiol (Psf), and apiol/bicyclogermacrene (Pm) as major components, and some are described here for the first time (Ps, Pcs, Pm). A composition-based dendrogram of these Piper species showed four major groups (G1: Pc and Pt, G2: Pcs, Po, Pd, Pa, and Pr, G3: Ps, and G4: Psf and Pm). The spore germination effects (Aspergillus niger, Botrytis cinerea, and Alternaria alternate) and phytotoxicity (Lolium perenne and Lactuca sativa) of these EOs were studied. Most of these Piper essential oils showed important activity against phytopathogenic fungi (except G1), especially against B. cinerea. Similarly, most of the essential oils were phytotoxic against L. perenne (except G1), with P. sancti-felicis (G4), P. casapiense (G2), and P. reticulatum (G2) being the most effective. Caryophyllene oxide, β-caryophyllene, β-pinene, limonene, α-humulene, and apiol were evaluated against B. cinerea, with the most effective compounds being β-pinene, apiol, and limonene. This work demonstrates the species-dependent potential of essential oils from Peruvian Piper species as fungicidal and herbicidal agents.
... The American, Asian and South Pacific groups each appear to be monophyletic; the affinity of the African species is unclear. 10 For identification and classification of different taxa, rapid species identification techniques like DNA barcoding have been undertaken by different groups utilizing DNA regions from the mitochondrial, plastid and nuclear genomes. Traditional morphophenology methods to identify Piper species are mostly based on phenotypic characters, but morphological characteristics are subjected to be affected by developmental and environmental. ...
Article
Full-text available
The internal transcribed spacer (ITS) of nuclear ribosomal DNA is one of the most commonly used DNA markers in plant phylogenetic and DNA barcoding analyses and it has been recommended as a core plant DNA barcode. To compare and find out the genetic diversity difference, some individuals Peper were collected in different localities in Vietnam when using the ITS of nuclear ribosomal DNA. The ITS gene region from the nuclear genomes was tested for suitability as DNA barcoding regions of thirty-nine Peper individuals. Universal primers were used and sequenced products were analyzed using the Maximum Likelihood method and Tamura-Nei model in the MEGA X program. We did not observe high variability in intraspecific distance within the ITSu1-4 gene region between individuals ranging from 0.000 to 0.155. The size of the gene region has fluctuated from 667 to 685 bp between different individuals with the percentage (G + C) contained in the ITSu1-4 gene region which ranged from 54.776% to 60.805%, mean = 60.174%. The values of Fu's Fs, D, Fu and Li's D* and F* were negative as well (Fs =-0.209, D =-1.824; p < 0.05, D* =-1.205; not significant, p > 0.10 and F* =-1.699; not significant, 0.10 > p > 0.05) indicating an excess of recently derived haplotypes and suggesting that either population expansion or background selection has occurred. The value of Strobeck's S is high (S = 0.684). The results of evolutionary relationships of taxa obtained 3 groups with the highest value of Fst are shown in the pairs of groups II and III (Fst = 0.151) and the lowest is in groups II and I (Fst = 0.015). All of the new sequences have been deposited in GeneBank under the following accession numbers MZ636718 to MZ636756. This database is an important resource for researchers working on Species of Peper in Vietnam and also provides a tool to create ITSu1-4 databases for any given taxonomy.
... Molecular phylogenetic studies using nuclear ribosomal (nr) ITS DNA and plastid intron psbJ-petA, has been useful in examining the monophyly of Piper (Jaramillo and Manos, 2001;Jaramillo and Callejas, 2004a, b;Tepe et al., 2004;Jaramillo et al., 2008). So far, no study has examined the phylogenetic relationships of the Sri Lankan species of Piper, except for nrITS barcoding work (Jayarathna et al., 2016a). ...
Article
Full-text available
Applying restriction site-associated DNA sequencing (RADseq) and target capture for Piper species from species-rich South America and India, Southeast Asia, and Africa will highlight the origin and evolution of Sri Lankan endemics, P. zeylanicum, P. walkerii, and P. trineuron. Looking into the genetic diversity of cultivated P. nigrum from different agroclimatic regions and available germplasm in Sri Lanka using RADseq will give an overview of the existing genetic diversity of black pepper, which is economically important and needs genetic improvement. Variation in flower composition (male, female or bisexual) across the spikes and their shape is of major interest to evolutionary and pollination biologists and plant systematists. The 3D shape models of flowers obtained by computed tomography of the wild species of Piper from Sri Lanka and cultivated P. nigrum will play an important role in revising the taxonomy and understanding the pollination biology of the genus.
... Due to the number of Piper species in restinga areas, it is permissible to propose possible indications that they may present new physiological and morphological adaptation strategies for survival in this environment, making it interesting for a chemical study. [4][5][6][7][8][9][10][11][12] Piper species are recognized for showing ritualistic and medicinal usages, as well as aromatic plants rich in essential oils (EOs). Some of the species are medicinal recognized and of commercial importance, such as Piper nigrum L. (Black pepper), Piper methysticum Forst (Kava-kava) and P. hispidinervium C. DC. (Long pepper), while P. amalago L. (Aperta-ruão), P. mollicomum Kunth (Jaborandi-manso) and P. umbellatum L. (Capeba) are used in folk medicine. ...
... Nowadays, the phylogenetic position of Piper as well as of the Piperaceae family, is among the so-called "paleoherbs", a phylogenetically complex basal group of dicots (Loconte and Stevenson 1991;Chase et al. 2016), within the order Piperales (Jaramillo et al. 2008;Palchetti et al. 2018). Piperales are herbaceous or woody plants exhibiting quite primitive morpho-anatomical features (Isnard et al. 2012) Piper species can be described either as shrubs, or more frequently, as creepers and lianas in the equatorial regions (Jaramillo et al. 2001). Many Piper species present two circles of vascular bundles in the stem, sometimes called polystelic organization, considered as a synapomorphy of the Piperaceae family, except for genus Verhuellia (Isnard et al. 2012). ...
Article
Full-text available
This is the first contribution about the histochemistry of vegetative and reproductive aerial organs in the genus Piper L. Piper malgassicum accumulates alkaloids and terpenes in the epidermis and the underlying layers of parenchyma, both in the leaves, in the stems and in anthers. Some idioblasts appear to contain a large amount of secondary metabolites. The micro-anatomical analysis showed peculiar secretory structures both in the leaves, in the anthers and in the ovary. Several lipid aggregates, alkaloid droplets and calcium oxalate crystals were observed in leaves and stems, indicating their role in defence strategies, mechanical support, and pollinators attraction. In the anthers, we observed elaioplasts whose content suggest an alternative and indirect function in pollination and defence against micro-organisms. Besides, some lipid aggregates surrounded by microtubules, detected in the anthers, were recognized as lipotubuloids. The tapetum was of secretory type. Alkaloids and terpenes were widely distributed in the plant confirming the important biological role of this type of biomolecules and its functional range. In the anthers, terpene and polyphenol inclusions appeared particularly abundant in the epidermal layer, whereas calcium oxalate crystals were observed close to the ovule in the ovary at maturity.
... There are smaller groups of species from the South Paci c (about 40 species) and Africa (about 15 species). The American, Asian, and South Paci c groups each appear to be monophyletic; the a nity of the African species is unclear [5]. ...
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Background: The internal transcribed spacer (ITS) of nuclear ribosomal DNA is one of the most commonly used DNA markers in plant phylogenetic and DNA barcoding analyses, and it has been recommended as a core plant DNA barcode. To compare and find out the analysis genetic diversity difference some pepper individuals collected in different localities in Vietnam when using the ITS of nuclear ribosomal DNA. The ITS gene region from the nuclear genomes were tested for their suitability as DNA barcoding regions of thirty-nine pepper individuals. Universal primers were used, and sequenced products were analyzed using the Maximum Likelihood method and Tamura-Nei model in the MEGA X program. Results: We did not observe high variability in intraspecific distance within the ITSu1-4 gene region between individuals, ranged from 0.000 to 0.155 (mean = 0.033). The size of the gene region has fluctuated from 667 to 685 bp between different individuals with the percentage (G + C) contained in the ITSu1-4 gene region was ranged from 54.776% to 60.805%, mean = 60.174%. The values of Fu’s Fs, D, Fu and Li’s D* and F* were negative as well (Fs = -0.209, D = -1.824; P < 0.05, D* = -1.205; not significant, P > 0.10 and F* = -1.699; not significant, 0.10 > P > 0.05), indicating an excess of recently derived haplotypes and suggesting that either population expansion or background selection has occurred. The value Strobeck’s S the obtained between individuals in a population is high (S = 0.684). The results of evolutionary relationships of taxa obtained 3 groups with the highest value of Fst is shown in the pairs of groups II and III (Fst = 0.151), and the lowest is in groups II and I (Fst = 0.015). All of the new sequences have been deposited in GeneBank under the following accession numbers MZ636718 to MZ636756. Conclusions: This database is an important resource for researchers working on Species of pepper in Vietnam and also provides a tool to create ITSu1-4 databases for any given taxonomy.
Article
Maintaining floristic diversity in recognized biodiversity hotspots is a priority for ecosystem conservation. However, different taxonomical treatments often lead to over or underestimation of floristic diversity in species-rich groups, in particular in Tropical regions as Mesoamerica where floristic surveys are less detailed. Also, understanding the effects of climate changes on species distribution is an emerging question of conservation biology and ecological studies. Here, we used the species-rich genus Piper (Piperaceae) in Veracruz, as a model system to compare reported and actual species richness and to model their occurrence under a climate change scenario. We compared morphological characters of specimens preserved in three of the main Mexican herbaria and then applied new taxonomical treatments. We also used environmental niche models (ENMs) as implemented in Maxent to detect the effects of climate changes on species with different levels of habitat specificity and with specialized biotic interactions. We found that from a total of 108 Piper species reported in Veracruz, 80 were consistent to the new taxonomical treatments due to synonymy or misidentification. ENMs showed that the main determinants of Piper distribution are linked to temperature and precipitations depending on the species. Therefore, different species are likely to respond differently to climate changes. As expected, species with higher habitat specificity and species exhibiting specialized mutualisms are more likely to experience niche contractions. This study shows the importance of reconsidering species richness and of modelling species distribution including specialized ecological interactions as prerequisite for establishing conservation criteria.
Article
Phylogenetic relationships among nine of the 11 species of the endemic genus Dendroseris on the Juan Fernandez Islands were inferred from nucleotide sequences of the internal transcribed spacer regions (ITS) of the 18-26S nuclear ribosomal DNA. Sequences were determined for 15 populations of Dendroseris and one population for each of two outgroups from the genera Sonchus and Sventenia. Little length variation was detected in the ITS regions of Dendroseris, with ITS 1 253 or 254 bp long and ITS 2 224 or 225 bp. The sequence data provide strong support for the holophyly of Dendroseris despite the distinct morphological differences among the three subgenera. The molecular data also indicate that subg. Dendroseris and Phoenicoseris are holophyletic, but do not support holophyly of subg. Rea. The ITS sequences did not resolve relationships among subgenera, supporting the hypothesis of rapid adaptive radiation of Dendroseris on the islands. Relative rate tests indicate that rates of nucleotide substitutions in the ITS regions are not significantly different among the different lineages of Dendroseris following adaptive radiation. Comparisons of average pairwise sequence divergence of Dendroseris species in the ITS regions and chloroplast genome indicated that ITS sequences have evolved about 38 times faster than cpDNA in the genus. Rates of ITS sequence divergence of Dendroseris were estimated to be faster than (3.94 ± 0.10) × 10⁻⁹ per site per year, and likely (6.06 ±0.15) × 10⁻⁹ per site per year.
Article
Floral development in Piper was compared between four-staminate species (P. aduncum and P. marginatum) and six-staminate species (P. amalago). All Piper species have a syncarpous gynoecium composed of three or four carpels. The floral apex is initiated by a periclinal division in the subsurface layer in the axil of a bract 40-55 μm high; initiation of the bracts occurs separately and considerably earlier. The floral primordium widens and the first pair of stamens are initiated at either side. The median anterior stamen forms next, and the median posterior later. This sequence is common to all species studied. In the six-staminate P. amalago, the last two stamens form simultaneously in lateral-anterior positions. The stamens hence arise as pairs, and symmetry is bilateral or dorsiventral. The three or four carpels arise simultaneously; they are soon elevated on a gynoecial ring by growth of the receptacle below the level of attachment of the carpels to produce a syncarpous gynoecium. The floral apex lastly produces the solitary basal ovule and is used up in its formation.
Article
Phylogenetic patterns within Calycadenia were estimated from 18–26S nuclear ribosomal DNA sequences of the internal transcribed spacer (ITS) region in 19 representatives of all species in Calycadenia, including Osmadenia (C.) tenella, and in two outgroup species. In pairwise comparisons among the Calycadenia and Osmadenia sequences, divergence ranged from 0 to 11.2% of nucleotides in ITS 1 and from 0 to 8.6% in ITS 2. Of 62 nucleotide sites with potential phylogenetic information, 51.6% were in ITS 1, 46.8% were in ITS 2, and 1.6% were in the 5.8S subunit. A highly resolved, strict consensus tree from Wagner parsimony analysis of these data agrees well with morphological and cytological evidence. This tree suggests that: 1) the monotypic Osmadenia tenella is the sister-group to Calycadenia; 2) the base chromosome number in Calycadenia is n = 7, from which other numbers were derived; 3) species with multiple T-glands on cylindrical bracts and chromosome numbers of n = 5 or 6 (or 7 in C. oppositifolia) form a monophyletic group derived from an n = 7 species similar or identical in genomic structure to C. hooveri or C. villosa; 4) C. spicata (n = 4) is the product of an independent dysploid reduction from n = 7; 5) C. multiglandulosa and C. pauciflora, sensu Keck, are not monophyletic taxa; and 6) loss of chromosomal homology between Calycadenia species, as reflected by meiotic chromosomal association in hybrids, is positively correlated with time since evolutionary divergence. These results offer little evidence of homoplasy in chromosomal and phenotypic characters in Calycadenia and provide further support for the phylogenetic utility of plant ITS sequences.
Book
This volume - the first of this series dealing with angiosperms - comprises the treatments of 73 families, representing three major blocks of the dicotyledons: magnoliids, centrosperms, and hamamelids. These blocks are generally recognized as subclasses in modern textbooks and works of reference. We consider them a convenient means for structuring the hundreds of di­ cotyledon families, but are far from taking them at face value for biological, let alone mono­ phyletic entities. Angiosperm taxa above the rank of family are little consolidated, as is easily seen when comparing various modern classifications. Genera and families, in contrast, are comparatively stable units -and they are important in practical terms. The genus is the taxon most frequently recognized as a distinct entity even by the layman, and generic names provide the key to all in­ formation available about plants. The family is, as a rule, homogeneous enough to conve­ niently summarize biological information, yet comprehensive enough to avoid excessive re­ dundance. The emphasis in this series is, therefore, primarily on families and genera.
Article
The recently-developed statistical method known as the "bootstrap" can be used to place confidence intervals on phylogenies. It involves resampling points from one's own data, with replacement, to create a series of bootstrap samples of the same size as the original data. Each of these is analyzed, and the variation among the resulting estimates taken to indicate the size of the error involved in making estimates from the original data. In the case of phylogenies, it is argued that the proper method of resampling is to keep all of the original species while sampling characters with replacement, under the assumption that the characters have been independently drawn by the systematist and have evolved independently. Majority-rule consensus trees can be used to construct a phylogeny showing all of the inferred monophyletic groups that occurred in a majority of the bootstrap samples. If a group shows up 95% of the time or more, the evidence for it is taken to be statistically significant. Existing computer programs can be used to analyze different bootstrap samples by using weights on the characters, the weight of a character being how many times it was drawn in bootstrap sampling. When all characters are perfectly compatible, as envisioned by Hennig, bootstrap sampling becomes unnecessary; the bootstrap method would show significant evidence for a group if it is defined by three or more characters.