Comparative gynoecium anatomy in Paullinieae (Paulliniodae, Sapindaceae): taxonomic implicationsAbstract
Supertribe Paulliniodae (Sapindaceae) includes Athyaneae, Bridgesieae, Thouinieae and Paullinieae tribes. Paullinieae is considered the most recent tribe within Sapindaceae and comprises six genera, namely Thinouia, Lophostigma, Cardiospermum, Paullinia, Serjania and Urvillea. Species of these genera occur in the Semideciduous Seasonal Forest of Paraná, Brazil, which is currently represented only by forest fragments. Studies of gynoecium structure in Sapindaceae are referenced in the literature, but there is a clear knowledge gap in Paullinieae/Paulliniodae. In the present study, the gynoecia of ten species belonging to Paullinieae genera were morphoanatomically investigated, and compared with the gynoecia of Allophylus edulis and Diatenopteryx sorbifolia. Both species are trees and belong to the tribes Thouinieae and Athyaneae, respectively. The main purpose of this study was to ascertain the usefulness of gynoecium in characterizing and separating species within the tribe. Gynoecium samples were obtained from the herbarium of the State University of Maringá and from forest remnants in Paraná, Brazil. The samples were processed for analysis under a light microscope, according to standard techniques in plant anatomy. Paullinieae/Paulliniodae gynoecia consist of a trifid or bifid stigma, style, and superior ovary, generally with one anatropous, campylotropous, or hemitropous ovule per carpel locule, with axile placentation. Gynoecium characters that may have taxonomic value at the species level in Paullinieae/Paulliniodae include placental structure, the presence and shape of the gynophore, ovary shape, and the presence of locular trichomes.
Keywords:
androgynophore; gynophore; locular hairs; ovule; placentation; pollen tube transmitting tract
Resumo
A supertribo Paulliniodae (Sapindaceae) inclui as tribos Athyaneae, Bridgesieae, Thouinieae e Paullinieae. Paullinieae é considerada a mais recente tribo dentro de Sapindaceae e consiste em seis gêneros, a saber Thinouia, Lophostigma, Cardiospermum, Paullinia, Serjania and Urvillea. Espécies destes gêneros ocorrem em Floresta Sazonal Semidecídua no Paraná, Brasil, que atualmente é representada somente por fragmentos florestais. Estudos da estrutura do gineceu em Sapindaceae são referidos na literatura, mas há clara lacuna no conhecimento de Paullinieae/Paulliniodae. No presente estudo, os gineceus de dez espécies pertencentes aos gêneros de Paullinieae foram morfoanatomicamente investigados e comparados com os gineceus de espécies de Allophylus edulis e Diatenopteryx sorbifolia. Ambas espécies são arbóreas e pertencem às tribos Thouinieae e Athyaneae, respectivamente. O principal objetivo desse estudo foi verificar a utilidade do gineceu na caracterização e separação de espécies da tribo. Amostras dos gineceus foram obtidos no herbário da Universidade Estadual de Maringá e de remanescentes florestais do Paraná, Brasil. As amostras foram processadas para análise em microscópio de luz, de acordo com técnicas usuais de anatomia vegetal. Os gineceus de Paullinieae/Paulliniodae consistem em estigma bífido ou trífido, estilete e ovário súpero, geralmente com um óvulo anátropo, campilótropo ou hemítropo por lóculo carpelar, com placentação axial. Os caracteres dos gineceus que podem ter valor taxonômico em nível de espécie de Paullinieae/Paulliniodae são a estrutura da placenta, presença e forma do ginóforo, forma do ovário e presença de tricomas loculares.
Palavras-chave:
androginóforo; ginóforo; tricomas loculares; óvulo; placentação; tecido transmissor
1. Introduction
The Sapindaceae family encompasses approximately 1900 species and 141 genera, primarily distributed in tropical and subtropical regions, with a smaller representation in temperate zones (Acevedo-Rodríguez et al., 2017; Buerki et al., 2021). In Brazil, the family is represented by 35 genera and 443 species, including 193 endemic species (Flora e Funga do Brasil, 2026). Based on molecular phylogenetic analysis, Acevedo-Rodríguez et al. (2017) proposed the supertribe Paulliniodae within Sapindaceae, which comprises the tribes Athyaneae, Bridgesieae, Thouinieae, and Paullinieae. These tribes share structural characters of the flower, inflorescence and leaf blade (Urdampilleta et al., 2025). According to Acevedo-Rodríguez et al. (2017), this supertribe is characterized by zygomorphic flowers, thyrses with lateral cincinni, corollas with four petals, and alternate leaves with a well-developed distal leaflet. Within this supertribe, these authors include several genera, such as Paullinia L., Cardiospermum L., Urvillea Kunth, Serjania Mill., Thinouia Planch. & Triana, Allophylus L., and Diatenopteryx Radlk.
The Paullinieae, considered the most recent tribe within Sapindaceae, is circumscribed to include six genera: Thinouia, Lophostigma Radlk., Cardiospermum, Paullinia, Serjania, and Urvillea (Acevedo-Rodríguez et al., 2017; Urdampilleta et al., 2025). These genera are climbers or climber-derived with stipulate leaves and a pair of inflorescence tendrils (Buerki et al., 2021). Paullinieae comprises approximately 509 species, with the majority distributed across the tropical and subtropical regions of the American continent (Acevedo-Rodríguez et al., 2017; Ferrucci and Steinmann, 2019). Lophostigma is the only genus not found in Brazil (Faria et al., 2022). Brazil hosts a significant number of taxa: 8 species (5 endemic) of Cardiospermum; 102 species (40 endemic) of Paullinia; 121 species (64 endemic) of Serjania; 12 species (5 endemic) of Thinouia; and 16 species (11 endemic) of Urvillea (Flora e Funga do Brasil, 2026). These species are particularly found in the Semideciduous Seasonal Forest of Paraná, Brazil, an ecosystem currently represented solely by fragmented forest areas (Rosado et al., 2022). Specifically, in the northern region of Paraná, the tribe Paullinieae includes 2 species of Cardiospermum, 4 of Paullinia, 12 of Serjania, 2 of Thinouia, and 2 of Urvillea (Rosado et al., 2022).
Sapindaceae flowers are considered functionally staminate or pistillate. In the latter, the gynoecium is morphologically syncarpous, and the pistil is more developed than the stamens (Rosado et al., 2022). According to Endress (1994), most syncarpous gynoecia have a common pollen tube transmitting tract (PTTT), specifically within the symplicate region, where the surfaces of all carpels communicate. Carr and Carr (1961) term this common zone of carpels the compitum, a structure that allows pollen tubes to cross between carpels. A gynoecium possessing a compitum is reported as eu-syncarpous, carrying significant physiological and evolutionary implications (Carr and Carr, 1961).
The gynoecium is a complex and complicated floral organ that yields an enormous diversity of morphological, structural, and histological characters that can be useful in the taxonomy and phylogeny of different angiosperm taxa (Endress, 1994, 2015; Endress and Igersheim, 2000). A review of the gynoecium in Sapindales, particularly in Sapindaceae, revealed that gynoecium features can provide taxonomic relationships and show relevant structural variations within the order or family (El Ottra et al., 2022).
A survey of studies on the gynoecium of Sapindaceae, especially in Paullinieae, has shown data that are still insufficient for characterizing and relating the different taxa within the family or tribe. Weckerle and Rutishauser (2005) structurally analyzed the gynoecium of nine Paullinieae species, emphasizing the development of the pollen tube transmitting tract (PTTT) and the synascidiate and symplicate zones of the ovary. In a review of the gynoecium of Sapindales, El Ottra et al. (2022) reported that information on different carpel zones is scarce and scattered within Sapindaceae, especially considering the family's high diversity. These authors further noted that PTTT features are well-described for some Sapindaceae members, particularly for Averrhoidium Baill. (subfamily Dodonaeoideae) and Koelreuteria J. Agardh (subfamily Sapindoideae). The ovary structure of Paullinieae species, particularly concerning ontogenetic studies of fruits, has been reported by Souza (2006), Weckerle and Rutishauser (2005) and Tanaka et al. (2014). In this last publication, the authors describe the development of adaxial meristem in the inner epidermis of the ovaries of Serjania communis Cambess. and Urvillea ulmacea Kunth.
For this study, we selected species from the Paullinieae tribe, specifically the climbing genera Cardiospermum, Paullinia, Serjania, Thinouia, and Urvillea. Additionally, we analyzed the species Allophylus edulis (A.St.-Hil. et al.) Hieron. ex Niederl. and Diatenopteryx sorbifolia Radlk., which belong to the same supertribe Paulliniodae (tribes Thouinieae and Athyaneae, respectively), but with arboreal habit. The primary objective was a morphoanatomical investigation of their gynoecia. We comparatively analyzed the gynoecium's structural characters to support taxonomic insights within the tribe.
2. Material and Methods
2.1. Plant material
Flowers and flower buds were obtained from vouchers from the Herbarium of the State University of Maringá (HUEM), Paraná, Brazil (Table 1). In the case of Serjania species, the plant material was collected from specimens of forest remnants, located in Maringá, Paraná, Brazil (Table 1). Two pistillate flowers per species were analyzed.
Species of Paulliniodae that were selected for study, including information on Brazilian collection sites and herbarium registration (vouchers) (HUEM=Herbário da Universidade Estadual de Maringá, Brasil).
2.2. Rehydration of herbarium material
In the case of material obtained from an herbarium, it was previously rehydrated. For hydration, the material was separated into pots with enough boiling water to cover the material. After, the material was kept at room temperature. In sequence, the material was placed in NOH and left for 2 hours. Then, the material was washed in water until it lost its color (about 10 times). Finally, the material was subjected to the ethyl series of 10%, 30%, 50% and 70%, remaining 1 hour in each alcohol (Smith and Smith, 1942, modified).
2.3. Light microscope analysis
Flower buds and flowers that were collected and rehydrated were fixed in glutaraldehyde and then preserved in 70% alcohol (Souza et al., 2016). Subsequently, the samples were subjected to the ethyl alcohol series and embedded in Leica historesin (glicolmetacrilato) (Guerrits, 1991).The material was sectioned on a rotatory microtome with 5 to 7 μm thickness. The sections were spread over glass slides containing water on a hot plate (40°C). After drying, the material was stained with 0.05% aqueous Toluidine Blue in acetate buffer (pH 4.7) (O’Brien et al., 1964). Light microscope photographs were taken with a Leica EZ4D digital camera and subsequently processed using the software Leica Application Suite LAS EZ (ver. 3.1.0, Leica Microsystems (Switzerland) Limited).
2.4. Terminology
The terminology used for gynoecium analysis was based on Endress (1994). For the ovule classification, Fahn (1990) and Endress (2011) were consulted.
3. Results and Discussion
3.1. Gynoecium morphology
The stigma is trifid or bifid (Figure 1A,B) (Table 2), and it exhibits papillae on the adaxial surface of each branch, occasionally extending to the edge (e.g., in Cardiospermum halicacabum) (Figure 1A). A bifurcate stigmatic branch, as observed in Serjania meridionalis, may also be present. The stigmatic portion of all analyzed species constitutes the apocarpous zone of the gynoecium, which appears to be a common characteristic among the Paullinieae species studied to date (El Ottra et al., 2022).
Stigma and style structure of Cardiospermum halicacabum (A,C), Diatenopteryx sorbifolia (B,E), Alophyllus edulis (D) and Urvillea ulmacea (F), in cross-sections. (A,B) Trifid and bifid stigmas; (C) Pentagonal style with three vascular bundles; (D) Pentagonal style with four vascular bundles; (E) Rounded style with four vascular bundles; (F) Triangular style with three larger outer vascular bundles and six inner smaller vascular bundles. (ct=stylar canal lined with the pollen tube transmitting tract (PTTT); sb=stigma branch; vb=vascular bundle). Scale bars: 150 µm (C), 200µm (A-E).
The style exhibits a variable outline or shape in cross-section (Figure 1CD) (Table 2). It comprises a hairy or glabrous epidermis, parenchyma—where the subepidermal cell layer may contain secretory structures—and a varying number of collateral vascular bundles depending on the species (Figure 1CD) (Table 2). The style of all species possesses a single canal lined with the pollen tube transmitting tract (PTTT) (Figure 1CD), which itself displays a variable number of cell layers (Table 2). The stylar canal (Figure 1CD) also shows a variable shape across the different species (Table 2).
The style vasculature of the investigated species consists of three or more vascular bundles (Figure 1CF) (Table 2). Three vascular bundles (Figure 1C) were found in the style of both Cardiospermum species, while Thinouia species exhibited six bundles in the style. Paullinia meliifolia has a variable number of bundles along the style. Within Serjania, the number of vascular bundles can be an interesting character to separate the three species: Serjania fuscifolia has six bundles, while the other two species have several bundles arranged in two rings in the style, Serjania meriodionalis with three bundles forming the outer ring and Serjania tripleuria showing several bundles in the outer circle. Both Urvillea species have similar vascularization, with several vascular bundles, the larger outer bundles and smaller inner bundles (Figure 1F).
It must be pointed out here that the style venation pattern in Paulliniodeae deserves some attention. In a classic publication on floral anatomy, Carlquist (1969) reports that the 3-veined condition is based on physiological correlations, in which the two ventral veins are typically related to the supply of ovules, and the dorsal vein typically supplies the stigma. On the other hand, Souza et al. (2003), in an analysis of the vascularization pattern of Pilocarpus pennatifolius Lem. (Rutaceae), state that the style vascularization is carried out by the ventral vascular bundles. Our floral analysis of Paulliniodeae showed that the style vascularization is variable and complex. The styles of Allophylus, Cardiospermum, Diatenopteryx, and Urvillea species are vascularized by branching of the ventral carpel bundles. In the case of Paullinia, Serjania, and Thinouia species, the styles have vascularization via branches of both the ventral and dorsal bundles. It is important to note that the way these bundles are organized varies among all species and warrants further detailed study of floral vascularization.
The ovary is superior (hypogynous flower) in the studied species, typically comprising two to three carpels and two to three locules (Figure 2AE) (Table 3). The ovary's outline or shape in cross-section varies among species (Figure 2AE) (Table 3). All locules are uniovulate, and placentation is axile (Figure 2AF), with variability placenta’s position along the septum (Table 3). Ovules were found in the base (Figure 2F), the lower third (Figure 2G), and at the middle portion of the septum (Figure 2H) (Table 3).
Gynoecium structure of Allophylus edulis (A), Diatenopteryx sorbifolia (B), Thinouia mucronata (C), Thinouia ventricosa (D,F), Cardiospermum halicacabum (E), Urvillea ulmacea (G) and Urvillea laevis (H), in cross-sections (A,B,D,E) and longitudinal sections (C,F-H)))). (A,E) Ovary tricarpellary, trilocular, with axile placentation (note the narrow expansion of the dorsal region of each carpel in figure E); (B) Ovary bicarpellary, bilocular, with axile placentation; (C) Detail of ovary wall tissues; (D) Ovary tricarpellary, but with a locule limited by two carpels; (F) Gynoecium with ovary evidencing locular trichomes (white arrows) and basal axile placentation; (G,H) Gynoecia exhibiting ovules in the lower third and middle portion of the septum, respectively. (im=parenchymatous inner mesophyll; lc=locule limited by two carpels; oe=outer epidermis; om=parenchymatous outer mesophyll; pt=PTTT; se=septum; tm=tissue originating from adaxial meristem). Scale bars: 50µm (C), 100µm (A), 200µm (B), 300µm (D-F), 400µm (G,H).
Comparative structural characters of gynophore/androgynophore, ovary and PTTT of Paullinieae/Paulliniodae species.
The gynoecium of Thinouia ventricosa deserves some attention. It is superior, syncarpous, and tricarpellate like other species of the genus (Oliveira, 2022), but one of its carpels delimits its own locule, while the other two carpels share a common locule (Figure 2D). Oliveira (2022) reports an extensive review and phylogenetic relationships on the Neotropical genus Thinouia, but makes no reference to the number of ovary locules. The author also includes in his work the entire detailed description of Thinouia ventricosa, without any allusion to the number of ovary locules. Our record of a tricarpellate and bilocular ovary in Thinouia ventricosa should therefore not be considered definitive, requiring analysis of a larger number of floral samples.
The ovary wall (Figure 2C) (Table 3) consists of a single layered, hairy or glabrous outer epidermis. The common outer epidermal cells (Figure 2C) exhibit variable shapes in cross-section, including square, rectangular, pentagonal or slightly prismatic ones. The cuticle or cuticular layer is generally thin. Trichomes may be glandular or non-glandular. The mesophyll (Figure 2C) is parenchymatous, and can be homogeneous or display two regions of parenchymatous tissue (Table 3).
On the ventral or adaxial surface of the ovary wall, there’s tissue with cells that are more or less aligned (Figure 2C), indicating the activity of an adaxial or ventral meristem established during pre-anthesis. Evidence from cross sections of the ovaries suggests this meristem may originate from the subepidermal layer of the mesophyll and the inner epidermis.
The adaxial or ventral meristem commonly originates from the ovary wall giving rise to capsule and schizocarp fruits typical of Paullinieae species. This meristem can originate from meristematic activity within either the inner epidermis or the subepidermal layer of the ovary's mesophyll. Tanaka et al. (2014) investigated the pericarp ontogeny of Serjania communis and Urvillea ulmacea, reporting the presence of an adaxial meristem in the ovaries of these species, which specifically originates from the inner epidermis.
Examination of the ovary wall's inner surface (locule) revealed the presence of hairs on the inner epidermis or septum (locular hairs) (Figure 2F) in both species of Cardiospermum species, Serjania fuscifolia, Thinouia ventricosa and in both Urvillea species (Table 3). Souza (2006) observed trichomes on the ovary wall/endocarp of Fabaceae species, suggesting, according to Kaniewski (1968) that these structures can help maintain moisture within the locule, where ovules and developing seeds are found. Weckerle and Rutishauser (2005) reported the occurrence of unicellular hairs in Paullinia clavigera Schltdl. and multicellular glandular hairs in Urvillea ulmacea. Based on a study of fruit in the araceous Acer pseudoplatanus L. by Kaniewski and Wazynska (1970), these authors propose that these hairs maintain moisture supply in the locules.
In syncarpous gynoecia of Paullinieae species, the pollen tube transmitting tract (PTTT) is common in the zone between the upper region of the style and the placenta in the ovary. This region, specifically the symplicate region according to Endress (1994), varies in height within the ovary across the studied species. The zone beneath the symplicate region is termed the synascidiate zone, where the PTTTs diverge for each carpel or placenta (Figure 2A) (Endress, 1994).
The symplicate region characterizes what Carr and Carr’s (1961) defined as the compitum, in which pollen tubes can cross between carpels. These authors classify taxa possessing a compitum in the gynoecium as eu-syncarpous. Consequently, all investigated Paullinieae species are eu-syncarpous. El Ottra et al. (2022) report that current research in Paullinieae indicates that the gynoecium is syncarpous, with only the stigma representing the apocarpous region. Furthermore, Weckerle and Rutishauser (2005) suggest a possible asymplicate zone in the stigmatic region in Urvillea ulmacea, Paullinia alata G. Don, Paullinia pachycarpa Benth. and Paullinia aff. caloptera Radlk.
Androgynophore and gynophore (Figure 3AF) were observed in both Cardiospermum species, Diatenopteryx sorbifolia, Paullinia meliifolia, Serjania meridionalis, Serjania tripleura, and Urvillea species (Table 3). Serjania fuscifolia and Thinouia species exhibited only a gynophore (Table 3), while Allophylus edulis gynoecium was devoid of both androgynophore and gynophore (Table 3). In evaluating the presence of androgynophore, it is necessary to emphasize that this floral structure is distinguished in Paullinia meliifolia, Serjania tripleura, and Urvillea species only through serial cross-sections.
Structure of the androgynophore and gynophore of Urvillea ulmacea (A-C) and Diatenopteryx sorbifolia (D-F), in longitudinal (A,D) and cross-sections (B,C,E,F). (A,D) Flowers evidencing the gynoecia with androgynophore and gynophore; (B,E) Gynophores surrounded by filaments; (C,F) Androgynophore with fused and free filaments. (an=androgynophore; fi=filament; gy=gynophore). Scale bars: 100µm (B-F), 150µm (A,D).
The gynophore has a different outline or shape in cross-section (Figure 3B,E) among the studied species. It comprises a hairy or glabrous epidermis, parenchymatous tissue, and a variable number of vascular bundles (Figure 3B,E). An androgynophore (Figure 3A,D) has been described in species of Cardiospermum, Paullinia and Urvillea (sensuEl Ottra et al., 2022). Solís et al. (2017) reported a gynophore for several species of Paullinieae, including Houssayanthus incanus (Radlk.) Ferrucci, Paullinia elegans Cambess., Serjania meridionalis and Lophostigma plumosum Radlk., though they did not provide a structural description.
The Paullinieae ovules investigated in this study are anatropous, campylotropous, or hemianatropous (Figure 4AC) (Table 3). They are bitegmic and crassinucelate, featuring a short funiculus and both integuments with 3 or more cell layers (Figure 4C). Corner (1976) reported anatropous or campylotropous ovules for Sapindaceae, while Weckerle and Rutishauser (2005) classified the ovules as campylotropous for some Paullinieae species. Acevedo-Rodríguez et al. (2010) indicated the anatropous, campylotropous, and hemitropous ovule types for Sapindaceae.
Structure and types of ovules of Cardiospermum halicacabum (A), Paullinia meliifolia (B), and Diatenopteryx sorbifolia (C), in longitudinal sections. (A) Campylotropous ovule; (B) Hemianatropous ovule; (C) Anatropous ovule. (es=embryonary sac; fu=funicle; ii=inner integument; mi=micropyle; nu=nucellus; oi=outer integument). Scale bars: 200µm.
The hemianatropous ovule (Figure 4B), according to Fahn's terminology (1990), was observed in Paullinia and Thinouia species (Table 3). This type of ovule does not appear to be recorded for Sapindaceae, but it is important to emphasize that Shamrov (2018) considers hemianatrapous as a subtype of hemitropous. It must be pointed out here that there is ample variation in the ovule terminology (Shamrov, 2018), and the ovule morphology can be different according to the development of the gynoecium. For instance, Corner (1976) indicated anatropous ovules for Allophylus L. species before fertilization and campylotropous ovules in the post-fertilization phase.
The characterization of the short funicle (Figure 4) in Paullinieae was a topic of discussion for Weckerle and Rutishauser (2005). These authors noted that there appears to be no clear distinction between the funicle and the placenta. They suggested the ovule-bearing structure in Sapindaceae could also be interpreted as a placental protuberance with a very short funicle at its apex. However, Weckerle and Rutishauser (2005) ultimately preferred to term this entire structure the short funicle. Our anatomical analysis of the short funicle indeed revealed the need for more detailed study of this structure in Paullinieae.
3.2. Structural features of taxonomic value and evolutionary considerations on the gynoecium of Paullinieae
Tables 2and 3 present comparative structural features of the gynoecium of 10 species of Paullinieae, and Allophylus edulis (tribe Thouinieae) and Diatenopteryx sorbifolia (tribe Athyaneae) from Paulliniodae. It highlights characteristics potentially useful for species differentiation, such as placental position within the septum, the presence and shape of the gynophore, the ovary's overall shape, number and arrangement of vascular bundles of the style, and the presence of locular hairs appear to hold significant taxonomic value within these taxa.
Weckerle and Rutishauser (2005) considered fruit characters more crucial for distinguishing genera and species within Paullinieae, as they found vegetative and floral characters less effective in for this purpose. Nevertheless, these authors did indicate some gynoecium features that could be taxonomically important at the species level, including, PTTT structure, ovary vascular patterns, hairs of the outer and inner epidermis and obturator.
It must be pointed out here that the gynoecium features of species belonging to the same genus are similar, though occasionally some distinctive features may stand out. For instance, in the case of Cardiospermum species, no features of taxonomic value were identified. On the other hand, among the three Serjania species investigated, Serjania fuscifolia exhibited some distinctive characters when compared to the other two species. Specifically, Serjania fuscifolia uniquely possesses a bifurcated stigmatic branch, lack of androgynophore, style with six vascular bundles surrounding the stylar canal, a homogeneous mesophyll, and it displays fewer PTTT cell layers (Tables 2 and 3).
Both species of Thinouia can be distinguished by several traits: the position of the placenta in the septum, number of locules in the ovary (two in T. ventricosa versus three in T. mucronata), the presence of locular trichomes in T. ventricosa, the ovule type (anatropous in Thinouia ventricosa and hemianatropous in Thinouia mucronata), and by the PTTT being massive in Thinouia mucronata (Table 3). In the case of Urvillea species, the gynoecium is structurally similar, but in Urvillea ulmacea, in addition to campylotropous ovules, the hemianatropous type was found (Table 3).
When comparing Paullinieae species (from the genera Cardiospermum, Paullinia, Serjania, Thinouia and Urvillea) with the Paulliniodae species (from the genera Allophylus and Diatenopteryx), we observed that the gynoecium characters are remarkedly similar (Tables 2 and 3). However, two specific characteristics warrant attention: the presence of two carpels in the gynoecium of D. sorbifolia and the absence of gynophore in A. edulis.
The androgynophore proved very difficult to visualize morphologically in the studied Paullinieae species; therefore, its identification relied on serial anatomical sections. According to El Ottra et al. (2022), it isn't a widespread structure in the order Sapindales, and these authors suggest that it’s likely a homoplastic and derived feature within the order.
Conversely, the gynophore is a common structure in the gynoecium of Sapindales, but of low occurrence in Sapindaceae (El Ottra et al., 2022). The authors considered for some families of Sapindales (not for Sapindaceae), based on literature, that the gynophore may also be a homoplastic and derived feature.
Acevedo-Rodríguez et al. (2017) confirmed the monophyly of Paullinieae, which comprises Cardiospermum, Lophostigma, Paullinia, Serjania, Thinouia, and Urvillea. This forms one of four successively nested clades within the greater supertribe Paulliniodae. Chery et al. (2019) considered Paullinia as a monophyletic genus sister to Cardiospermum, which together are sister to Serjania + Urvillea. Typically, Paullinieae species have one median ovule per carpel (Weckerle and Rutishauser, 2005). However, our gynoecium analysis of Paullinieae revealed that Thinouia was the only genus exhibiting species with an ovule in a bicarpellary locule. Within Sapindoideae, which belongs to the supertribe Paulliniodae, the presence of one or two ovules per carpel was considered by Buerki et al. (2021) as a synapomorphy in the subfamily.
Weckerle and Rutishauser (2005) reported no clear distinction between placenta and funicle, suggesting the ovule-bearing structure in Sapindaceae might be interpreted as either a placental protuberance or a funicle. Indeed, our analysis of the 12 species revealed the difficulty in clearly separating the placental portion from the funicle, particularly in species where the ovule is located basally within the septum (Table 3).
Puri's (1952) review of placentation in Angiosperms discusses the nature of placentation as axial, carpellary, or mixed. Based on this review, it appears that Paullinieae includes species with an essentially carpellary placentation (species with a placenta in the middle region, lower third, or basal of the septum). In Sapindaceae, middle placentation is considered the most common, with basal and apical types being the least frequent (Acevedo-Rodríguez et al., 2010).
The structural characters of the gynoecium analyzed here deserve some consideration within the phylogenetic study of the supertribe Paullinoidae reported by Acevedo-Rodríguez et al. (2017). For the authors, the tribe Athyaneae containing the genera Athyana and Diatenopteryx was considered basal in the supertribe, and in our study only Diatenopteryx sorbifolia exhibited a bicarpellary gynoecium with bifid stigma. Within Paullinieae, the authors have established that Thinouia is a basal clade, where we find the only tricarpellary and bilocular species (Thinouia ventricosa), successively followed by Lophostigma and the most inclusive clade, which is defined as a polytomy uniting Serjania, Paullinia, Urvillea, and Cardiospermum. All investigated species of this last clade have basically similar gynoecium (Tables 2 and 3).
In conclusion, our findings indicate that several gynoecium features hold taxonomic value at the species level within Paullinieae. These include the placental position in the septum, the presence and shape of the gynophore, the ovary's morphology, and the presence of locular hairs. The synapormophic character of one ovule per locule, considered by Buerki et al. (2021) for the clades corresponding to the Paulinniodae supertribe, was confirmed for all taxa analyzed. Future research could productively explore features such as indument type and gynoecium vascularization to further clarify the taxonomy of Paullinieae.
Acknowledgements
We thank CAPES (Higher Education Personnel Improvement Coordination, Brazil) and CNPq (National Council of Scientific and Technological Development, Brazil) for the support granted to the accomplishment of this study. Special thanks are due to PGB/UEM (Graduate Program in Comparative Biology, State University of Maringá), and herbarium of the State University of Maringá for authorizing the collection of botanical material.
Data Availability Statement
Research data is only available upon request.
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Editor:
Takako Matsumura Tundisi
