High developmental lability in the perianth of Inga (Fabales, Fabaceae): a Neotropical woody rosid with gamopetalous corolla

Abstract

Inga is a highly diverse Neotropical genus of Fabaceae with a rapid and recent diversification. Its flowers are actinomorphic with a wide variation in merism and size and length of perianth. Notwithstanding its species richness and economic importance, few floral ontogenetic studies have been carried out in this genus. Thus, we investigated perianth development and morphology of five Inga spp. using scanning electron and light microscopy. Perianth ontogeny is highly labile. Sepal and petal primordium number ranges from four to seven. The sequence of sepal initiation is generally reversed unidirectionally (from adaxial to abaxial side); petals are initiated simultaneously. The position of sepals and petals is variable among and within species. The sepal may be positioned adaxially, abaxially or slightly displaced in relation to the median sagittal plane. The median petal is positioned in the adaxial (I. congesta, I. grandis) or abaxial region (I. bella, I. hispida). Elongated petals touch each other apically through conspicuous papillae. Perianth development in Inga differs from that of other mimosoids. The early developmental stages show a wide variation. However, subsequent ontogenetic processes, known as equalization during intermediate stages, establish uniformity in the floral architecture, thus preventing possible functional disparities that could influence reproductive success.

Full text

High developmental lability in the perianth of Inga
(Fabales, Fabaceae): a Neotropical woody rosid with
gamopetalous corolla
JULIANA V. PAULINO
1,
*, VIDAL F. MANSANO
2
, GERHARD PRENNER
3
and
SIMONE P. TEIXEIRA
4
1
Departamento de Produtos Naturais e Alimentos, Faculdade de Farm 
acia, Centro de Ci^
encias da
Sa 
ude, Universidade Federal do Rio de Janeiro, Av Prof Paulo Rocco s/n –Bl A 2°andar sala 030,
Ilha do Fund~
ao, Rio de Janeiro, 21941902 RJ, Brazil
2
Instituto de Pesquisas Jardim Bot ^
anico do Rio de Janeiro, DIPEC Rua Pacheco Le ~
ao 915, Rio de
Janeiro, 22460-030 RJ, Brazil
3
Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK
4
Faculdade de Ci^
encias Farmac^
euticas de Ribeir ~
ao Preto, Universidade de S ~
ao Paulo (USP), Av. do
Caf
e s/n°, Ribeir~
ao Preto, 14040-903 SP, Brazil
Received 17 February 2016; revised 23 August 2016; accepted for publication 2 September 2016
Inga is a highly diverse Neotropical genus of Fabaceae with a rapid and recent diversification. Its flowers are
actinomorphic with a wide variation in merism and size and length of perianth. Notwithstanding its species
richness and economic importance, few floral ontogenetic studies have been carried out in this genus. Thus, we
investigated perianth development and morphology of five Inga spp. using scanning electron and light
microscopy. Perianth ontogeny is highly labile. Sepal and petal primordium number ranges from four to seven.
The sequence of sepal initiation is generally reversed unidirectionally (from adaxial to abaxial side); petals are
initiated simultaneously. The position of sepals and petals is variable among and within species. The sepal may
be positioned adaxially, abaxially or slightly displaced in relation to the median sagittal plane. The median petal
is positioned in the adaxial (I. congesta,I. grandis) or abaxial region (I. bella,I. hispida). Elongated petals touch
each other apically through conspicuous papillae. Perianth development in Inga differs from that of other
mimosoids. The early developmental stages show a wide variation. However, subsequent ontogenetic processes,
known as equalization during intermediate stages, establish uniformity in the floral architecture, thus preventing
possible functional disparities that could influence reproductive success. ©2016 The Linnean Society of London,
Botanical Journal of the Linnean Society, 2016
ADDITIONAL KEYWORDS: floral development – floral morphology – intraspecific diversity –
Leguminosae – merism – ontogeny.
INTRODUCTION
Inga Mill. is a Neotropical genus of Fabaceae tribe
Ingeae [Mimosoideae clade sensu LPWG (Legume
Phylogeny Working Group), 2013] with c. 380 species
distributed in 14 sections (Elias, 1981; Pennington,
1997; Richardson et al., 2001; The Plant List, 2013).
It is one of the ten most diverse genera of Fabaceae
(Lewis et al., 2005), the third largest family of
angiosperms with c. 24 000 species in c. 750 genera
(The Plant List, 2013). Some Inga spp. are used for
multi-purpose soil restoration, as agroforestry trees,
for their edible fruits, as shade for crops, for the pro-
duction of leaf mulch, for their nitrogen-fixing prop-
erties, as timber and firewood and for their
medicinal properties (L
eon, 1966; Garcia, 1998; Tre-
visol, 2002; Lewis et al., 2005).
Inga is considered a monophyletic genus, although
its infrageneric relationships remain poorly
*Corresponding author. E-mail: jvillelapaulino@pharma.ufrj.
br
1©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
Botanical Journal of the Linnean Society, 2016. With 7 figures

understood. It had a rapid and recent diversification
and probably originated between 14 and 2 Mya
(Richardson et al., 2001). This explosive speciation is
reflected in the morphological diversity found in the
genus, leading to many challenges in establishing
morphologically recognizable infrageneric groups
(Pennington, 1997; Richardson et al., 2001). Cytoge-
netic studies suggest that polyploidization is not rare
in Inga (Hanson, 1995; Okamoto, 1998; Figueiredo
et al., 2014) and may have influenced speciation in
the genus (Figueiredo et al., 2014).
Inga spp. are all woody plants (Richardson et al.,
2001) with actinomorphic flowers, but with a wide
variation in merism (i.e. a variable number of
organs in the same whorl: Specht & Bartlett, 2009;
Ronse De Craene, 2016), size and length of calyx,
corolla, stamens and carpels (Pennington, 1997;
Paulino et al., 2014). The calyx is gamosepalous,
with small lobes, varying from campanulate to
tubular or funnel-shaped. Despite being a member
of the rosids (APG IV, 2016), Inga has a gamopeta-
lous, tubular-shaped corolla with valvate lobes.
Petal colour is highly variable, including greenish
white [e.g. I. acuminata Benth., I. pilosula (Rich.)
J.F.Macbr.], greenish yellow (e.g. I. venusta Standl.,
I. vera Willd.) and pink or red [e.g. I. grazielae
(Vinha) T.D.Penn.]. Nevertheless, the androecium
with its numerous basally united stamens is the
attractive part of the flower (Endress, 1994). The
gynoecium is usually monocarpellate, but may have
two (e.g. I. congesta T.D.Penn., I. pleiogyna
T.D.Penn.: Pennington, 1997; Paulino et al., 2014)
to nine carpels (e.g. I. pluricarpellata T.D.Penn.,
I. aptera T.D.Penn.: Pennington, 1997). Among
Fabaceae, Inga has the highest number of species
with a polycarpellate gynoecium (Pennington, 1997;
Paulino et al., 2014), a feature that is generally
restricted in the family. The merism instability of
the gynoecium is most probably linked to the mer-
ism instability of the androecium and both are prob-
ably the result of floral meristem expansion
(Wanntorp et al., 2011; Paulino et al., 2014; Ronse
De Craene, 2016). Each carpel can house 12–32
ovules arranged in two rows. The number of ovules
per ovary is proportional to the flower size. Flowers
of Inga sections Bourgonia Benth. and Leptinga
Benth. are small with each ovary containing 10–16
ovules, whereas flowers of Inga section Longiflorae
(Benth.) T.D.Penn. are large with each ovary con-
taining 20–30 ovules (Pennington, 1997). Floral visi-
tors include bats, hummingbirds, moths, butterflies,
bees and ants (Koptur, 1984; Gonc
ßalves, Silva &
Candido, 2010); however, only moths, hummingbirds
and butterflies act as pollinators (Koptur, 1983,
1984; Piratelli, 1993; Kinoshita et al., 2006;
Gonc
ßalves et al., 2010).
A tubular corolla characterizes Inga and other
Mimosoideae; this character state is uncommon in
other legumes and in rosids in general (Polhill &
Raven, 1981; Barroso, 1991; Pennington, 1997; Lewis
et al., 2005).
The tubular perianth is ubiquitous in Inga with a
gamosepalous calyx and a gamopetalous corolla (Pen-
nington, 1997), but the number of organs forming
the tubular corolla and the sepal tube is variable,
which gives rise to several questions. What is the
ontogenetic basis for this variability? Does it reflect
an ontogenetic process (union or division) in the
early, intermediate or late stage of floral develop-
ment? Is gamopetaly the result of congenital or post-
genital fusion? Is it similar to patterns found in
other rosids [e.g. Galipea Aubl., Rutaceae (Pirani, El
Ottra & Menezes, 2010), Alsomitra macrocarpa
(Blume) M. Roem., Cucurbitaceae (Matthews & End-
ress, 2004)], indicating that gamopetaly is the result
of coherence of petals?
To date, there are few studies focusing on floral
ontogeny in Inga (Ram
ırez-Domenech & Tucker,
1990; Paulino et al., 2014). The aim of this study
was to compare the perianth development in five
Inga spp. placed in different taxonomic sections to
understand the ontogenetic pathways that give rise
to morphological similarities and intraspecific varia-
tion. These data are intended to expand our under-
standing of the floral architecture in this group.
MATERIAL AND METHODS
Five Inga spp. were sampled (Table 1): I. bella
M.Sousa, I. congesta,I. feuillei DC., I. grandis
T.D.Penn. and I. hispida Schott ex Benth (Figs 1, 2).
Garcia (1998) and Pennington (1997) were used for
identification of the specimens.
Buds in several developmental stages and anthetic
flowers were collected, fixed in FAA 50 (formalin–
acetic acid–alcohol; Johansen, 1940) or with Karnovs-
ky’s solution in 0.075 mol L
1
phosphate buffer (pH
7.2–7.4; Karnovsky, 1965) and dissected with the aid
of a Leica MZ 75 stereomicroscope. For organogra-
phy, flowers were analysed using a Leica MZ 75.
Organs from ten flowers were measured using a
ZAAS Precision Amatools digital caliper.
The surface analyses in a scanning electron micro-
scope were carried out after dehydration of the mate-
rials in an ethanol series (Tucker, 1993). Samples
were critical point dried in a Bal Tec CPD 030 or
Autosamdri-815B critical point dryer, mounted on
aluminium stubs with colloidal carbon or clear nail
polish, and covered with gold in a Bal Tec SCD 050
sputter coater or with platinum in an Emitech
K550a sputter coater. Observations and images were
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
2J. V. PAULINO ET AL.

obtained with Shimadzu SS-550 (FFCLRP/USP),
JEOL JSM 5200 (FMRP/USP), Hitachi S-4700-II
(Jodrell Laboratory, Royal Botanic Gardens, Kew,
UK), Zeiss IVO 50 (FMRP/USP) and Zeiss IVO 40
(JBRJ-RJ) scanning electron microscopes at 2, 15, 20
or 30 kV. The electron micrographs were processed
using Adobe Photoshop CS5.
For anatomical analyses in light microscopy, flow-
ers were fixed in FAA and stored in 70% ethanol.
Floral buds were prepared using standard methods
of wax embedding (Johansen, 1940) and serially sec-
tioned (4–6lm) using a rotary microtome. Sections
were stained with safranin and Alcian Blue (Gerlach,
1969), dehydrated in an ethanol series to 100% etha-
nol and transferred to Histoclear before being
mounted in D.P.X. medium. Photomicrographs were
taken with a Leica DM 4500B photomicroscope.
The terminology to describe ontogenetic processes
follows Tucker (1987) and Klitgaard (1999). The term
‘pre-anthesis’ refers to the bud immediately prior to
anthesis.
RESULTS
Organography and ontogenetic characters found for
the studied Inga spp. are summarized in Table 2.
ORGANOGRAPHY
The flowers are arranged in spikes, which are con-
gested in I. bella, moderately lax in I. congesta and
I. hispida and highly lax in I. grandis. Each flower
is subtended by an abaxial bract. No bracteoles are
present. The flowers are perfect, complete and radi-
ally symmetric (Figs 1, 2). The calyx is gamosepalous
Table 1. Voucher specimens of sampled species of Inga
Species Section Collection site and date Voucher
Inga bella M.Sousa Tetragonae (Pittier) T.D.Penn. Puerto Jimenez –Costa Rica,
January 2011
R Aguilar, 12746 and
13142 (SPFR)
I. congesta T.D.Penn. Affonsea (A.St.-Hil.) T.D.Penn. Niter
oi-RJ, July 2008 and 2010 J. V. Paulino et al., 2 and
J. V. Paulino et al., 3 (SPFR)
I. feuillei DC. Tetragonae (Pittier) T.D.Penn. cult. Botanic Garden Graz,
Austria, February 2000
G. Prenner, 140 (K)
I. grandis T.D.Penn. Grandiflorae T.D.Penn. Rio Branco-AC, June 2010 J. V. Paulino et al., 4,
J. V. Paulino et al.,
5and J. V. Paulino
et al., 6 (SPFR)
I. hispida
Schott ex Benth.
Vulpineae T.D.Penn. Santa Teresa-ES,
October 2008 and 2010
J. V. Paulino et al., 11 (SPFR)
Vouchers are housed in the herbaria of Universidade de Sao Paulo, Brazil (SPFR) and Royal Botanic Gardens, Kew, UK
(K).
Figure 1. Drawings of anthetic flowers of (A) Inga bella
and (B) I. grandis. Note the appendages at the base of
the flowers, the bracts from other flowers of the inflores-
cence, the gamosepalous calyx, the tubular corolla, the
polyandrous androecium and the three styles/stigmas.
(Drawings: Marcus Jos
e de Azevedo Falc~
ao Junior.)
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
DEVELOPMENT OF THE PERIANTH IN INGA 3

and has five to seven free lobes in I. congesta
(Fig. 3B, C), I. feuillei (Fig. 3D–F) and I. grandis
(Fig. 3H, I) and five or six free lobes in I. bella (see
Pennington, 1997) and I. hispida (Fig. 3K, L). It is
glabrous in I. bella and hairy on the abaxial surface
in I. congesta,I. feuillei,I. grandis and I. hispida.It
is greenish in I. bella and I. feuillei, yellow in I. con-
gesta, basally greenish with brown lobes in I. gran-
dis and brown in I. hispida.Itisc. 2.5 cm long in
I. bella,c. 1 cm long in I. congesta,I. hispida and
I. feuillei and c. 4 cm long in I. grandis. The corolla
is gamopetalous, i.e. the petals are basally united
and form a tube c. 5.0 cm long in I. bella,c. 2.0 cm
long in I. congesta and I. feuillei,c. 6.0 cm long in
I. grandis and c. 2.5 cm long in I. hispida. It is com-
posed of four or five petals in I. bella, five to seven
petals in I. congesta (Fig. 4A–C), I. feuillei (Fig. 4D–
F) and I. grandis (Fig. 4G–I), and five or six petals
in I. hispida (Fig. 4J–L). Petals are greenish in
I. bella,I. congesta,I. grandis and I. feuillei and
brownish on the abaxial surface and pink on the
adaxial surface in I. hispida. Petals are hairy on the
abaxial surface in I. bella,I. congesta,I. grandis and
I. feuillei. The ratios of the length of the united por-
tion of the corolla to the length of the united part of
the filaments are c. 0.8 in I.bella and I.grandis, 2.0
in I.congesta and 1.1 in I.hispida. The androecium
is polyandrous and the stamens are united forming a
staminal tube. In I. bella and I. grandis the staminal
tube is longer than the corolla tube, whereas in
I. congesta the staminal tube is shorter than the cor-
olla tube; in I. hispida the staminal and the corolla
tubes are approximately the same length. The gynoe-
cium is polycarpellate in I. bella,I. congesta,I. hisp-
ida and I. grandis and monocarpellate in I. feuillei.
The carpels are glabrous in I. bella and I. feuillei or
are covered by tector trichomes in I. congesta,
I. hispida and I. grandis.
Table 2. Perianth characters in Inga
Floral character I. bella I. congesta I. feuillei I. grandis I. hispida
Organography
Calyx colour Greenish Yellow Greenish Greenish
with brown
lobes
Brown
Corolla colour Slightly greenish Greenish Greenish Greenish ab (brown),
ad (pink)
Calyx size (cm) c. 2.5 c. 1c. 1c. 4c. 1
Corolla size (cm) c. 5c. 2c. 2c. 6c. 2.5
Early developmental stages
Number of sepal
primordia initiated
–5–75–75–75–6
Number of petal
primordia initiated
4–55–75–75–65–6
Order of sepal initiation ––ur ur ur
Median sepal position –ab ad/ab ab ad
Order of petal initiation –si si si si
Median petal position ab ab/ad ab/ad ad ab
Mid and late developmental stages
Size of the papillae
on the apical portion
of the petals (in bud) (lm)
120 100 –50 200
Stomata distribution
on perianth organs
Sepals Sepals, petals –Petals Sepals
Simple trichomes
on perianth
Petals (ab) Sepals (ab),
petals (ab)
Sepals (ab),
petals (ab)
Sepals (ab),
petals (ab)
Sepals (ab),
petals (ab)
Glandular trichomes
on perianth
Sepals (ab/ad),
petals (ab)
Sepals (ab),
petals (ab)
–Absent Sepals (ab),
petals (ab)
(–), missing information; (ab), abaxial; (ad), adaxial; (si), simultaneous; (ur), reversed unidirectional order.
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
4J. V. PAULINO ET AL.

ORGANOGENY
Floral development is synchronous in the inflores-
cences of I. bella,I. congesta,I. grandis and I. hisp-
ida. The development of floral organs only begins
after all floral meristems are formed on the inflores-
cence. Only I. feuillei shows an acropetal develop-
ment of meristems on the inflorescence. No material
was available for the early floral development of
I. bella, such as meristem shape and order of sepal
and petal initiation. The floral apex, formed in the
axil of a bract in all species, is circular in I. congesta
(Fig. 3A), I. feuillei and I. hispida (Fig. 3J) and ellip-
tical in I. grandis (Fig. 3G). The bract arises and
grows early so that it soon covers and protects the
floral meristem. No bracteoles are initiated. Whorls
are formed acropetally.
The sepals arise as individual primordia in
reversed unidirectional order, i.e. from the adaxial
to the abaxial side in I. grandis (Fig. 3H, I),
I. feuillei (Fig. 3D) and I. hispida (Fig. 3K, L). Even
though floral orientation and organ number vary
considerably, usually the median sepal is abaxial in
I. congesta (Fig. 3B) and I. grandis (Fig. 3H, I) and
adaxial in I. feuillei (Fig. 3D) and I. hispida
(Fig. 3K, L).
Petal primordia initiate after a long plastochrone,
during which the floral meristem is covered by the
enlarging sepals. The petal primordia generally
Figure 2. Drawings of anthetic flowers of (A) Inga hispida, (B) I. congesta and (C) I. feuillei. Note the appendages at
the base of the flowers, the bracts from other flowers of the inflorescence, the gamosepalous calyx, the tubular corolla,
the polyandrous androecium (A–C) and the two styles/stigmas (A, B). (Drawings: Marcus Jos
e de Azevedo Falc~
ao
Junior.)
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
DEVELOPMENT OF THE PERIANTH IN INGA 5

AB C
DE F
GH I
JK L
Figure 3. Scanning electron micrographs showing floral meristem and early sepal development of Inga spp. A–C, I. con-
gesta.D–F, I. feuillei.G–I, I. grandis.J–L, I. hispida. A, J, circular floral apex. G, elliptical floral apex. B, C, development
of sepals. D–F, development of sepals, showing the reversed unidirectional order of initiation, i.e. from the adaxial side to
the abaxial side. H–L, initiation of sepals in reversed unidirectional order. Note the variation in number of organs initiated:
five (B, D, H–L), six (F) and seven primordia (C, E). The abaxial side is at the bottom of all figures. Symbols: Br, bract; fm,
floral meristem; s, sepal. Scale bars: A, H =20 lm; B, C =10 lm; D =100 lm, E, F =200 lm; G =500 lm; I–L=50 lm.
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
6J. V. PAULINO ET AL.

AB C
DE F
GH I
JK L
Figure 4. Frontal view of early floral buds of Inga spp. with sepals removed. Petals initiate simultaneously. A–C,
I. congesta.D–F, I. feuillei.G–I, I. grandis.J–L, I. hispida. Note the variation in number of petals initiated: five (A, F,
H, J, K), six (E, G, I, L) and seven primordia (B–D). L, two primordia occupy a place that originally would have been
occupied by one primordium (arrow). The abaxial side is at the bottom of all figures. Symbols: Br, bract; p, petal; s,
sepal. Scale bars: A =20 lm; B =30 lm; C, L =100 lm; D–F=200 lm; G =10 lm, H–K=50 lm.
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
DEVELOPMENT OF THE PERIANTH IN INGA 7

alternate with the sepals. Petal initiation is gener-
ally simultaneous in all species studied, but the
number of initiated primordia is variable. The
number of petals ranges from four to seven. Five to
seven primordia are frequently found in I. congesta
(Fig. 4A–C) and I. feuillei (Fig. 4D–F) and five or six
AB C
DE F
GH I
JK L
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
8J. V. PAULINO ET AL.

in I. grandis (Fig. 4G–I) and I. hispida (Fig. 4J–L).
Following the variable position of the median sepal,
petal orientation also varies. A median petal is gen-
erally positioned on the adaxial region in I. congesta
(Fig. 4A–C) and I. grandis (Fig. 4G–I) and on the
abaxial side in I. bella and I. hispida (Fig. 4J–L).
When more than five petals are initiated, two pri-
mordia arise side by side occupying the space of one
primordium (Fig. 4L). Sometimes additional primor-
dia may arise with a delay. Sepals and petals may
arise slightly displaced in relation to the median
sagittal plane of the flower.
MID AND LATE STAGES OF FLORAL DEVELOPMENT
The young sepals become basally united and elongate
rapidly to form a tubular calyx with free lobes
(Fig. 5A, B, D, E, G–J). During the initial phase of
perianth elongation, the calyx exceeds the length of
other floral organs up to four times in I. bella (Fig. 5A,
B) and then the corolla elongates more than the
calyx during the final developmental stages,
exceeding it in length. The calyx opens the corolla
during pre-anthesis. In anthesis the calyx reaches
approximately half the length of the corolla in
I. bella,I. congesta,I feuillei and I. hispida and
about one-third of the corolla length in I. grandis.
Simple trichomes are generally formed at the
beginning of sepal elongation on the abaxial sur-
face in I. congesta (Fig. 5D–F), I. feuillei,I. grandis
(Fig. 5I) and I. hispida (Fig. 5K, L) and on both
surfaces in I. bella. Glandular trichomes are formed
during sepal elongation abaxially and adaxially in
I. bella (Fig. 5A–C) and on the abaxial side in
I. congesta (Fig. 5D, F) and I. hispida (Fig. 5L).
Stomata are found on the abaxial surface in
I. bella,I. congesta (Fig. 5F) and I. hispida
(Fig. 5K).
The petals elongate and display a valvate aestiva-
tion pattern (Figs 6A–C, G–J, 7A, B, H–K). When
the petals seal closing the bud, they touch apically
via conspicuous papillous cells distributed on the
adaxial surface of the apical region and intertwine
(Figs 6F–K, 7E, J, L, M). The petals unite post-geni-
tally at the base and form a tubular corolla with free
lobes (Figs 6D, F, J, 7D, K). Later, the petals exceed
the sepals in length, becoming the sole protective
structure of the reproductive organs in older floral
buds.
In later developmental stages, the abaxial side of
the petals is densely hairy. The indumentum is
composed of numerous long, simple trichomes in
I. congesta (Fig. 6G–L), I. feuillei (Fig. 7B, C),
I. grandis (Fig. 7D–F) and I. hispida (Fig. 7K, L).
These trichomes can be approximately six times
longer than the thickness of the petal blade in
I. grandis (Fig. 7F). Glandular trichomes can also
be formed on the abaxial surface of the petals in
I. bella (Fig. 6C, E), I. congesta (Fig. 6L) and
I. hispida (Fig. 7N). Stomata occur on the abaxial
petal surface in I. congesta (Fig. 6K, L) and
I. grandis (Fig. 7G).
DISCUSSION
WHAT ARE THE PLAUSIBLE EXPLANATIONS FOR THE MERISM
LABILITY AND OTHER VARIATIONS IN THE PERIANTH
DEVELOPMENT OF INGA?
Among the variable ontogenetic characters in Inga,
the lability in the merism in all floral whorls stands
out (present study; Paulino et al., 2014). This lability
is intraspecific, even among flowers in a single inflo-
rescence, and is interesting considering the trend in
Fabaceae and in all angiosperms towards fixed and
consistent organ numbers (Soltis et al., 2009; Specht
& Bartlett, 2009; Endress, 2011).
In Inga, the merism is determined in the earliest
developmental stages, when more than five perianth
primordia can arise in one whorl. The presence of
more than five perianth primordia is uncommon in
Fabaceae (Tucker, 2003a), even in Mimosoideae,
although a hexamerous calyx was recently reported
for Stryphnodendron adstringens (Mart.) Coville
Figure 5. Mid and late stages of sepal development of Inga spp. A–C, I. bella.D–F, I. congesta.G–I, I. grandis.
J–L, I. hispida. A, floral bud showing the sepals united at the base with free lobes. Note the trichomes on the
abaxial surface of the base of the calyx (circle). B, floral bud in lateral view with the calyx partially removed. Note
the glandular trichomes (arrows) on the sepals and petals. C, detail of two glandular trichomes on the abaxial
surface of the sepals. D, E, floral bud in late developmental stage. D, sepals united at the base with free distal
lobes. The calyx is densely hairy on the abaxial surface. E, bud with the calyx larger than the corolla. Calyx par-
tially removed. At this stage the sepals are much larger than the petals. F, the abaxial sepal surface in detail,
showing a glandular trichome and a stomatum (circle). G, bud with the calyx larger than the corolla. Calyx partially
removed. H–J, lateral view of the connate calyx at the base. I, abaxial surface of the sepals covered by trichomes.
K, detail of abaxial sepal surface, showing the stomata (arrowheads). L, glandular trichome in detail. Symbols: Br,
bract; p, petal; s, sepal. Scale bars: A, D, E =1 mm; B =2 mm; C, J =50 lm; F, K, L =10 lm; G, H =20 lm,
I=500 lm.
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
DEVELOPMENT OF THE PERIANTH IN INGA 9

(Pedersoli & Teixeira, 2016). In the present study,
we found that more than five primordia may be initi-
ated per perianth whorl. In this case all organ
primordia are initiated more closely together or two
primordia may arise side by side, occupying the
space of a single primordium.
AB C
DEF
GH I
JK L
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
10 J. V. PAULINO ET AL.

The merism lability in Inga is not only restricted
to the perianth. The androecium is the whorl with by
far the largest number of floral organs, ranging from
120 to 320 stamens per flower, which are formed
from a ring meristem. The ring meristem promotes
an increase in diameter of the meristem where the
stamen primordia will be initiated, thus providing
more space for the initiation of supernumerary sta-
men primordia in the floral meristem (Ram
ırez-
Domenech & Tucker, 1990; Prenner, 2011; Paulino
et al., 2014). The gynoecium of Inga also exhibits
variation in carpel number in some species, varying
between one and seven (Pennington, 1997; Paulino
et al., 2014). However, the additional carpels are
much less numerous than stamens, probably due to
the apical position of the carpels, which limits the
number of additional carpels and the size of the car-
pel meristem.
Merism lability, especially in the perianth, within
a species or individual is considered rare in Fabaceae
and has been recorded in only a few species from dis-
tinct clades: Acacia celastrifolia Benth., with four to
(rarely) five sepals (Prenner, 2011); Lecointea hatsch-
bachii R.C.Barneby, with four to six sepals and five
to seven petals (Mansano, Tucker & Tozzi, 2002);
Stryphnodendron adstringens, with five to six sepals
(Pedersoli & Teixeira, 2016); and Swartzia dipetala
Willd. ex Vogel, with three to four (rare) sepals and
corolla with one to (rarely) two petals (Paulino, Man-
sano & Teixeira, 2013). Our study, however, shows a
great lability in perianth merism in Inga (I. bella,
I. congesta,I. feuillei,I. grandis and I. hispida), in
which organ numbers not only vary between species,
but also within individuals.
The studied Inga spp. show an intraspecific diver-
sity of ontogenetic pathways, such as variation in
number, position and order of perianth initiation
(see Table 2), and variable number, position and
form of carpels during development (Paulino et al.,
2014). Intraspecific diversity of floral characters
related to its development, such as merism lability,
can also be found in Conostegia D.Don (Melastomat-
aceae; Wanntorp et al., 2011). Inga, a Neotropical
genus, has undergone a relatively recent and rapid
diversification and explosive speciation (between 13
and 2 Mya) (Richardson et al., 2001) and Conostegia
is a genus of Melastomataceae, a species-rich family,
with a greater diversification in the Neotropical
region (Renner, Clausing & Meyer, 2001). Although
Melastomataceae and Fabaceae are highly diverse
families (Renner et al., 2001; LPWG, 2013), merism
lability in the perianth is only reported for Conoste-
gia in Melastomataceae (Wanntorp et al., 2011), and
Inga (present study), Acacia Mill. (Prenner, 2011),
Lecointea Ducke (Mansano et al., 2002), Stryphn-
odendron Mart. (Pedersoli & Teixeira, 2016) and
Swartzia Screb. (Paulino et al., 2013) in Fabaceae.
Therefore, more comparative studies focusing on flo-
ral ontogeny will be useful in comprehending the
diversity of floral morphology in these groups.
Merism lability within families and genera is well
known and described in the literature (Ronse De
Craene, 2010). In contrast, variable organ numbers
in flowers of the same species and even in the same
individual are less common among core eudicots
(Ronse De Craene, 2016) than among early angios-
perms and early branching eudicots, such as Ranun-
culales (Specht & Bartlett, 2009; Endress, 2011). In
addition to several of Fabaceae (present study; Man-
sano et al., 2002; Pedersoli et al., 2010; Paulino
et al., 2013; Pedersoli & Teixeira, 2016), intraspecific
merism lability in all whorls has also been reported
for some species of Sapotaceae (K€
umpers et al.,
2016), Gentianaceae, Melanthiaceae (Ronse De
Craene, 2016) and species-rich families, including
Myrtaceae, Rosaceae, Euphorbiaceae (K€
umpers
et al., 2016) and Melastomataceae (Wanntorp et al.,
2011; A. P. S. Caetano, pers. comm.), most of which
have actinomorphic flowers (Ronse De Craene, 2010).
In addition, despite being rare in species with
whorled phyllotaxis, intraspecific merism lability
occurring in many cases within the same individual
is strongly associated with radially symmetric flow-
ers (Tucker, 1991; Mansano et al., 2002).
There is a clear trend towards pentamery in Faba-
ceae with zygomorphic flowers (Tucker, 1987; Ronse De
Craene, 2010). This becomes particularly evident in
Papilionoideae, in which the typical pentamerous
Figure 6. Mid and late stages of petal development of Inga spp. A–F, I. bella.G–L, I. congesta. A, B, floral bud, frontal
view, showing the valvate pattern of petal aestivation and variable orientation of the corolla (median petal abaxial in A
and adaxial in B). C, floral bud in lateral view, showing the union of the petals at the base (arrowhead). D, floral bud in
cross section. Note the true union of the petals. E, glandular trichome on the abaxial surface of the petal in detail (ar-
rowhead). F, detail of the inner surface (adaxial) at the apex, showing conspicuous papillae (arrow) that facilitate the
closing of the corolla (asterisks). G–I, floral bud in frontal view. Note the elongation of petals and the trichome formation
on the abaxial surface. J, floral bud in lateral view. Elongation of petals enclosing the floral bud. K, detail of the corolla
apex. Note the papillae (asterisks) and the stomata on the abaxial surface (circle). L, detail of the abaxial petal surface,
showing one glandular trichome (arrowhead) and stomata (circles). Symbols: A, androecium; Br, bract; c, carpel; ca,
calyx; co, corolla; p, petal; s, sepal. Scale bars: A =300 lm; B–D=500 lm; E =50 lm; F =400 lm; G–K=100 lm;
L=30 lm.
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
DEVELOPMENT OF THE PERIANTH IN INGA 11

papilionoid flowers evolved. In Mimosoideae some large
genera have actinomorphic flowers, e.g. Mimosa L.
with c. 700 species, Acacia s.l. with c. 1400 species and
Inga with c. 380 species (The Plant List, 2013); these
are exceptions in Fabales, in which rich genera usually
display zygomorphic flowering patterns (Bello, Haw-
kins & Rudall, 2007). Actinomorphic flowers are dis-
tributed in genera with few species, such as Gleditsia
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
12 J. V. PAULINO ET AL.

J.Clayton with c. 15 species and Gymnocladus Lam.
with c. five species in Caesalpinioideae s.l. (Tucker,
1991; Cardoso et al., 2013; The Plant List, 2013) and
Myrocarpus Allem. with c. 5 species, Dicraeopetalum
Harms with c. 3 species and Cadia Forssk. with c. 7 spe-
cies in Papilioinoideae (Cardoso et al., 2013; The Plant
List, 2013). Zygomorphy and strict pentamery are, on
the other hand, less frequent in Mimosoideae (Tucker,
1987; Ronse De Craene, 2010).
The increase of organ numbers can be associated
with the increased size of the floral meristem, such
as the presence of a ring meristem (Tucker, 2003a, b;
Paulino et al., 2013, 2014). Studies of Arabidopsis
thaliana (L.) Heynh. (Brassicaceae) target candidate
genes, which affect the regulation of floral meristem
size have shown that these genes are capable of
changing the number of floral organs (Soltis et al.,
2009; Specht & Bartlett, 2009; Pieper, Monniaux &
Hay, 2016). The CLV/WUS genetic module may
cause changes in meristem size and therefore shifts
in the number of floral organs. PAN and ETT genes
act in A. thaliana, affecting floral meristem identity
and the number of organs; pan mutants show a
switch from tetramery to pentamery (Soltis et al.,
2009). Based on quantitative trait locus analysis,
Pieper et al. (2016) showed that many genes of small
effect determine petal number in Cardamine hirsuta
Oeder (Brassicaceae).
Polyploidy events also may play a role in the vari-
ability of morphological and ontogenetic traits found
in the flowers of Inga spp. This can be a plausible
explanation if we observe the ploidy levels found so far
for Inga (Hanson, 1995; Figueiredo et al., 2014) and
take into account that polyploidy is considered one of
the main mechanisms of chromosome evolution driv-
ing new speciation events (Figueiredo et al., 2014).
Although ploidy has been studied in only a few species
so far, some polyploid species or populations have been
found which deviate from the basic chromosome num-
ber (n=13) (Hanson, 1995; Figueiredo et al., 2014):
2n=52 in I. capitata Desv., I. cylindrica (Vell.) Mart.,
I. fagifolia (L.) Willd. ex Benth., I. insignis Kunth,
I. laurina (Sw.) Willd. and I. luschnathiana Benth.
(Hanson, 1995; Okamoto, 1998; Figueiredo et al.,
2014) and 2n=104 in I. cayennensis SAgot ex Benth.
(Figueiredo et al., 2014).
It is noteworthy that there is also intraspecific vari-
ation in chromosome numbers, as in I.nga laurina
(2n=26 and 52), I. cayennensis (2n=26 and c. 104)
and I. cylindrica (2n=26 and 52) (Figueiredo et al.,
2014). Such variations seem to be rare (Figueiredo
et al., 2014), and the polyploid populations of I. lau-
rina are morphologically distinct. The extent that the
ploidy affects the morphology, especially traits con-
cerning the perianth merism lability in Inga,isan
important topic to be addressed in further studies.
WHAT ARE THE RELEVANT ASPECTS OF FLORAL
DEVELOPMENT AND MORPHOLOGY IN MIMOSOIDEAE?
The floral ontogeny in Mimosoideae differs from other
members of Fabaceae mainly in the position the organ
is initiated (Tucker, 2003a). However, our data show
that floral orientation of I. congesta and I. grandis
does not always follow the described pattern for Mimo-
soideae, in which, in general, a sepal is found in med-
ian adaxial position, as found in species of Acacia
(G
omez-Acevedo, Magall
on & Rico-Arce, 2007), Cal-
liandra Benth. (Prenner, 2004), Mimosa (Ram
ırez-
Domenech & Tucker, 1990), Neptunia Lour. (Tucker,
1988), Parkia R.Br. (Pedersoli & Teixeira, 2016), Pen-
taclethra Benth. and Stryphnodendron (our pers.
observ.) (Table 2). Additionally, the order of sepal ini-
tiation in I. feuillei,I. grandis and I. hispida (re-
versed unidirectional order) also differs from other
members of Mimosoideae studied thus far, in which
helical and simultaneous orders are most common
(Tucker, 1987; T. C. Barros, unpubl. data). Among
mimosoids, reversed unidirectional organ initiation
was also reported only in the sepal whorl of Lysiloma
vogelianum (Steud.) Stehl
e (Gemmeke, 1982) and Cal-
liandra angustifolia Spruce ex Benth. (Prenner,
2004). These conditions demonstrate the diversity of
traits linked to floral development in Inga, differing
Figure 7. Mid and late petal development of Inga spp. A–C, I. feuillei.D–G, I. grandis.H–N, I. hispida. A, B, floral
bud in frontal view. A, seven petal primordia. B, six petal primordia. Note one primordium initiated later (arrow). C,
median section through flower bud with valvate aestivation with the epidermis tightly closed at the inner tip (arrow-
head). D, petal elongation with post-genital union at the base (arrowhead). E, petals enclosing the bud. Two petals were
removed. Note the papillae at the tip of the petals that intertwine, closing the floral bud (asterisk). F, details of tri-
chomes on the abaxial petal surface. Note the thickness of the trichome layer. The trichome length (large double arrow)
is about six times larger than the thickness of the petal in cross section (short double arrow). G, detail of a stomatum on
the abaxial petal surface. H–K, floral bud in frontal view. H, five petals. I, six petals. Note the smaller petal, probably
initiated later. J, elongation of the petals. Note the formation of the papillae at the tip, which intertwine and enclose
the floral bud (asterisk). K, elongation of the petals. Note the region of the post-genital union (arrowhead). L, floral bud
in a later developmental stage with conspicuous papillae on the inner tips (square). M, detail of L. N, detail of the glan-
dular trichome on the abaxial surface of the petal (arrowhead). Symbols: c, carpel; p, petal; s, sepal; st, stamen. Scale
bars: A–C =200 lm; D, E, H–K=100 lm; F, L, M =500 lm; G, N =10 lm.
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
DEVELOPMENT OF THE PERIANTH IN INGA 13

from the established standard for closely related
groups (Ram
ırez-Domenech & Tucker, 1990). This
diversity might be related to the special conditions of
their evolutionary history (Richardson et al., 2001).
However, Mimosoideae requires additional ontoge-
netic and evolutionary studies to clarify whether
rapidly evolving genera always display shifts in floral
traits, such as organ position.
Specializations, such as the presence of papillae on
the adaxial tip of the petals and the glandular tri-
chomes on floral organs, are noteworthy. Glandular tri-
chomes are reported here for the first time in I. bella
(bract margins, abaxial and adaxial surface of the
sepals and abaxial surface of the petals) and I. congesta
and I. hispida (abaxial face of the sepals and petals).
Floral glandular trichomes with a similar distribution
had already been observed in Mimosa spp. (Leelavathi,
Prabhakar & Ramayya, 1984; Queiroz & Lewis, 1999;
Santos-Silva et al., 2013) and in Calliandra imbricata
E.R.Souza & L.P.Queiroz (Souza & Queiroz, 2004).
Considering the distribution of trichomes, they do not
seem to be related to the attraction of pollinators; in
addition, the attractive part of the flower is the showy
androecium (Endress, 1994). Also, the floral nectaries
found in Inga produce nectar as a food resource for
potential pollinators. Some studies have suggested
that floral glandular trichomes are related to protec-
tion against herbivory (Levin, 1973). Experimental
studies of the chemical composition of the exudate from
these trichomes might provide a better understanding
of their function.
The papillae on the adaxial and apical petal sur-
faces are important for an efficient closure of the flo-
ral bud as the petals overtop the sepals in mid
development and become the sole protective struc-
tures. Similar structures have been documented in
Acacia (G
omez-Acevedo et al., 2007; Prenner, 2011),
Calliandra angustifolia (Prenner, 2004), Neptunia
pubescens Benth. (Tucker, 1988), Mimosa (Ram
ırez-
Domenech & Tucker, 1990), Parkia multijuga
Benth., Stryphnodendron adstringens (Pedersoli &
Teixeira, 2016) and other mimosoid taxa (Ram
ırez-
Domenech & Tucker, 1990), indicating that the
mechanism of corolla closure by papillae or long uni-
cellular trichomes is a potential developmental trait
shared by species of Mimosoideae.
Contrary to what has been shown for other rosids
(see Pirani et al., 2010), the Inga spp. studied here
present gamopetalous corolla due to the post-genital
fusion of the petals at the base during their develop-
ment (the same pattern that is normally found among
asterids). The presence of a tubular corolla in Inga,
and many other genera of Mimosoideae, despite being
a rosid member (APG IV, 2016), raises questions about
which developmental processes lead to this floral trait.
Rosids members have, in general, flowers with
apopetalous corollas and gamopetaly in this group is
unusual (see Ronse De Craene, 2010; Endress, 2011).
Some rosids studied so far show gamopetaly as a
result of coherence of the petals instead of connation
(Matthews & Endress, 2004; Pirani et al., 2010), as
found in Inga spp. of the present study and in some
Acacia spp. (G
omez-Acevedo et al., 2007; Prenner,
2011). Acacia is the other species-rich genus closely
related to tribe Ingeae in Mimosoideae (LPWG
(Legume Phylogeny Working Group), 2013).
CONCLUSIONS AND OUTLOOK
Although some ontogenetic studies have been carried
out in the Mimosoideae clade (Gemmeke, 1982;
Tucker, 1988, 2003b; Ram
ırez-Domenech & Tucker,
1990; Prenner, 2004; Pedersoli & Teixeira, 2016)
highlighting some potential ontogenetic synapomor-
phies for the clade (Ram
ırez-Domenech & Tucker,
1990), these data should be expanded to establish
these patterns more accurately and to clarify the
existing variations.
It is noteworthy that in Inga, although the early
stages of development display a wide variation, there
are specializations in the intermediate stages, espe-
cially the fusion of the sepals and petals, which pro-
mote an ontogenetic process known as equalization
(Ram
ırez-Domenech & Tucker, 1990). This ensures
uniformity of the floral architecture in the later stages
and is important to enable the formation of morpholog-
ically similar flowers, avoiding possible functional dif-
ferences between them, which could influence the
reproductive success of the plants. Future analyses
that include the elucidation of the union levels, not
only in Inga but comparing many taxa of Mimosoideae,
are needed to clarify the evolution of gamopetaly in the
group, which is unusual among rosids. Such studies
would allow more accurate inferences regarding the
function of the ultimate ontogenetic requirement, i.e.
equalization, allowing standardization of floral archi-
tecture with the formation of the tubular corolla and
the acquisition of actinomorphic symmetry.
Inga is a good model for ontogenetic studies for
understanding the diversity of floral morphology. It
would be interesting to broaden the sample and
include additional data on chromosome number and
ploidy with the aim of corroborating the hypothesis
that polyploidy is one of the mechanisms responsible
for the diversification of this genus.
ACKNOWLEDGEMENTS
We thank Edim
arcio da Silva Campos (FCFRP/USP,
Brazil), Maria Dolores Seabra, Jos
e Augusto Maulin
©2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
14 J. V. PAULINO ET AL.

(FMRP/USP, Brazil), Rodrigo Ferreira Silva
(FFCLRP/USP, Brazil), Rog
erio da Costa Figueiredo,
Elaine Z
ozimo de Souza (Instituto de Pesquisas Jar-
dim Bot^
anico do Rio de Janeiro, Brazil) and Chris-
tina Prychid (Royal Botanic Gardens, Kew, UK) for
technical assistance; Ludovic Jean Charles Koll-
mann (Museu de Biologia Prof. Mello Leit~
ao, Bra-
zil), Reinaldo Aguillar (Los Charcos de Osa, Costa
Rica) and Herison Medeiros de Oliveira (Jardim
Bot^
anico do Rio de Janeiro, Brazil), who kindly pro-
vided help with the fieldwork and species identifica-
tion; Marcus Jos
e de Azevedo Falc~
ao Junior for the
scientific illustration of Figures 1 and 2; and Dewey
Litwiller (University of Saskatchewan, Saskatoon,
Saskatchewan, Canada) for review of the English
text. The first author thanks the PPG in Biologia
Comparada from S~
ao Paulo University (USP-
FFCLRP). This study was supported by FAPESP
(process number 2008/57487-0), CNPq (process num-
bers 142876/2008-9, 302204/2012-1, 312766/2009-2
and 309987/2012-1) and by the Bentham-Moxon
Trust, UK.
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