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Article

The Coexistence of Bicellular and Tricellular Pollen Might Be the Third Type of Pollen Cell Number: Evidence from Annonaceae

by
Yangying Gan
1,
Qi Zhang
2,
Chunfen Xiao
3 and
Jingyao Ping
4,*
1
Institute of Agricultural Economics and Information, Guangdong Academy of Agricultural Sciences/Key Laboratory of Urban Agriculture in South China, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China
2
The Agro-Biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
3
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna 666303, China
4
College of Life Sciences, Sun Yet-Sen University, Guangzhou 510275, China
*
Author to whom correspondence should be addressed.
Biology 2025, 14(5), 562; https://doi.org/10.3390/biology14050562
Submission received: 7 April 2025 / Revised: 10 May 2025 / Accepted: 12 May 2025 / Published: 17 May 2025
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Simple Summary

Anther is thought to release either bicellular or tricellular pollen when mature. In the present work, we found that 16 species from 10 genera of Annonaceae shed both bicellular and tricellular pollen. This is the first time that so many species with both types of pollen has been observed in the same family. Combined with reports from other families, the plants that were known to shed both types of pollen included 15 families, 40 genera, and 52 species. Our results indicate that the coexistence of bicellular and tricellular pollen might be the third type of pollen cell number. And the systematic relationship among them is needed to be reanalyzed.

Abstract

Anther is thought to release either bicellular or tricellular pollen when mature. Though a few species had been found to shed both bicellular and tricellular pollen, due to their low frequency, they had been overlooked as special cases of bicellular or tricellular pollen in previous phylogenetic studies. In the present work, the pollen cytologies of 89 species from 26 genera of Annonaceae were observed using the overall transparency method and paraffin sectioning method. The results show that 73 species from 25 genera distribute bicellular pollen, while 16 species from 10 genera shed both bicellular and tricellular pollen. This is the first time that so many species with both types of pollen has been observed in the same family. Combined with reports from other families, the plants that were known to shed both types of pollen included 15 families, 40 genera, and 52 species. Our results indicate that the coexistence of bicellular and tricellular pollen might be the third type of pollen cell number. And the systematic relationship among them is needed to be reanalyzed.

1. Introduction

Most angiosperms contain only one vegetative cell and one reproductive cell in their pollen before dispersal, known as bicellular pollen. About 30% of angiosperms complete the second cell division before dispersal, forming two reproductive cells and one vegetative cell, known as tricellular pollen [1]. There has long been controversy regarding the systematic evolution of pollen cell numbers. Early researchers believed that bicellular pollen was primitive and that the evolution from bicellular to tricellular pollen was irreversible [2,3]. Based on these claims, Webster and Rupert proposed the “Schürhoff–Brewbaker Law” [4]. However, subsequent research has suggested that the evolution from bicellular to tricellular pollen is reversible, and is skeptical of the primitive trait [1]. Additionally, in all previous systematic analyses on pollen cell numbers, only bicellular and tricellular pollen were taken into consideration. Although a few species had been found to shed both types of pollen [5,6,7], due to their low frequency, they had been considered as special cases and excluded from samples [1,3]. But, over time, more and more species with both kinds of pollen have been discovered [8,9,10,11,12,13,14,15,16].
Annonaceae was reported to be bicellulate by Brewbaker [3], but the coexistence of bicellular and tricellular pollen has been found in anthers of Annona cherimola Mill. and Mitrephora macclurei [6,9]. According to previous reports, Annonaceae has great diversity in terms of pollen size, shape, polarity, symmetry, dispersal unit, number/position/shape of germination aperture, ornamentation, and tectal and infratectal characters [17,18,19,20]. As a large family, comprising 107 genera and c.2400 species [21], it may also be diverse in terms of pollen cell number. But, until now, only nine species from six genera are known to have bicellular pollen [1,3,22,23,24,25], and two species from two genera are known to have both types of pollen [6,9,26]. Among the other undetected species, will there be more abundant discoveries (more taxa with both types of pollen, or even tricellular pollen)? With these questions and expectations, we have observed the pollen cell numbers of most of the Annonaceae plants currently distributed or introduced in China. The results may enrich our botanical understanding of pollen cell numbers and provide more evidence for systematic evolution research.

2. Materials and Methods

2.1. Materials

Fully mature flowers from 89 species across 26 genera of Annonaceae were collected from 2019 to 2021, taking about 5–10 flowers per plant and 5–10 anthers per flower annually for 2–3 consecutive years. The sampling species information includes the location, introduction number, and specimen number. The introduction number is available on the official website of the three botanical gardens (Xishuangbanna Tropical Botanical Garden: https://www.xtbg.ac.cn/ (accessed on 15 March 2024); Wuhan Botanical Garden: http://www.whiob.ac.cn/ (accessed on 18 March 2024); South China Botanical Garden: https://www.scbg.ac.cn/ (accessed on 20 March 2024)). The specimen number is available on the official website of the National Plant Specimen Resource Center of China (http://www.nsii.org.cn (accessed on 22 March 2024)) or the Chinese Virtual Herbarium (https://www.cvh.ac.cn/ (accessed on 25 March 2024)). All materials were fixed in formalin acetic alcohol (FAA: 70% alcohol, formaldehyde, and glacial acetic acid in a ratio of 90:5:5).

2.2. Methods

The pollen cell numbers were observed either by the overall transparency method described by Fu et al. [27] or the paraffin sectioning method described by Gan and Xu [9]. The proportion of anthers with both types of pollen in the sample anthers was also calculated.
Overall transparency method: All pollen was peeled off from mature anthers under a dissecting microscope to create a pollen suspension. The suspension was then subjected to hydrochloric acid hydrolysis, hematoxylin staining, gradient alcohol dehydration (30%, 50%, 70%, 90%, 95%, 100%) and transparent treatment with methyl salicylate, followed by DAPI staining, and placed on a glass slide dripped with clove oil for sealing. Fluorescence microscopy was used for observation and photography.
Paraffin sectioning method: For 64 species that the overall transparency method was not applicable, the paraffin sectioning method described by Gan and Xu [9] was applied instead. FAA-fixed anthers were subjected to ethanol gradient dehydration, xylene transparency, safranin-fixed green staining, paraffin embedding, and sectioning for 9 μm. A Leica DFC550 optical microscope (Leica Microsystem, Wetzlar, Germany) was used for observation and photography.

3. Results

Through the observation of 89 species from 26 genera of Annonaceae, we found that 16 species from 10 genera disperse both types of pollen (Figure 1, Figure 2 and Figure 3, Table 1), while 73 species from 25 genera shed bicellular pollen (Figure 4, Figure 5, Figure 6 and Figure 7, Table 1). Among the 16 species that disperse both types of pollen, 12 of them had more than half of anthers that contain both types of pollen, and for others such as Uvaria grandiflora Roxb, Uvaria calamistrata Hance, Mitrephora wangii Hu and Artabotrys hexapetalus (L. f.) Bhandar, 20–30% of sample anthers generally had both types of pollen. Our findings increase the number of known plants in Annonaceae that disperse both types of pollen from 2 genera and 2 species to 10 genera and 17 species (Table 2), However, pure tricellular pollen has not yet been detected in this family. In this study, we also observed both types of pollen (Figure 2Q) in the anthers of Annona cherimola Mill., confirming the research report of Lora et al. [26]. Additionally, we once again observed both types of pollen within the same pollen unit (Figure 2I–L), supporting the report by Gan and Xu [9].
According to the molecular phylogenetic tree of the Annonaceae family constructed by Guo et al. [21], we found that species with both types of pollen are mostly distributed in the relatively evolved tribes, including Annoneae, Uvariaeae (Annonoideae), and Miliuseae (Malmeoideae) (Figure 8). No samples containing both types of pollen were found in the more primitive subfamilies, such as Anaxagoreoideae and Ambavioideae.

4. Discussion

4.1. The Coexistence of Bicellular and Tricellular Pollen May Be More Prevalent in Angiosperms than We Thought

Grayum [5] and Lora et al. [6] reported that the coexistence of bicellular and tricellular pollen occurs transiently prior to dispersal, often with an imbalanced ratio of the two pollen types. If samples are collected prematurely, this mixed population may be misinterpreted as exclusively bicellular pollen. Similarly, incomplete sampling could lead to misclassification as either purely bicellular or tricellular pollen. Such errors have historically caused taxonomic inconsistencies. For example, Calla palustris was described as tricellular by Dudley [41] but bicellular by Brewbaker [3]; subsequent detailed analysis by Grayum [5] revealed that ~5% of pollen completed the second mitotic division prior to dispersal, confirming mixed development. Similarly, while Annonaceae was initially classified as bicellular [3], Rosell et al. [42] identified tricellular pollen in Annona cherimola. later corroborated by Lora et al. [6], who observed both pollen types 9–10 h before anther dehiscence. To mitigate sampling bias, our study exclusively used fully matured flowers at the point of pollen dispersal. We confirmed mixed bicellular and tricellular pollen in Mitrephora maingayi Hook. f. et Thoms [9] and 16 additional species across 10 genera within Annonaceae. This suggests that strict developmental staging of floral material is critical, and we hypothesize that broader sampling with rigorous temporal controls may reveal this phenomenon to be more widespread in angiosperms than currently acknowledged.

4.2. Is the Coexistence of Bicellular and Tricellular Pollen a Special Case or the Third Type?

Previous systematic analysis on pollen cell numbers has treated mixed populations as anomalies of either bicellular or tricellular pollen, often excluding them from samples [1,4,43]. However, within Annonaceae, 17 of 90 species (~19%) and 10 of 30 genera (~33%) exhibit this trait [1,3,22,23,24,25]. Notably, the ratio of bicellular and tricellular pollen is not always imbalanced. A high percentage of both pollen types have been observed in six species of Araceae [5]. Lora et al. [6] reported a mixed population of bicellular (49%) and tricellular (51%) pollen in Annona cherimola Mill. In our study, some anthers contained up to 40% tricellular pollen. In these cases, distinguishing whether this represents a variant of bicellular or tricellular pollen becomes challenging. Thus, at least within Annonaceae, it may be reasonable to take the coexistence of bicellular and tricellular as the third type except for bicellular and tricellular pollen.
In recent years, the discovery of anthers containing both types of pollen has continued to increase in other families, such as the Arundinaria simonii f.albostriatus and Shibataea chinensis Nakai [36], the Bambusa textilis [14], Sasaella kogasensis ‘Aureostriatus’ [11], Bambusa multiplex [8], Pseudosasa viridula [12], Menstruocalamus sichuanensis [36] and Phyllostachys edulis (Carrière) J. Houzeau [16] from Poaceae, the Swertia bimaculata [31] and Tripterospermum chinense (Migo) Harry Sm. [32] from Gentianaceae, the Limonium from Plumbaginaceae [35], which were previously reported as tricellular [3,44]. Similarly, Conyza canadensis (L.) C ronq [29] from Asteraceae, Michelia figo (Lour.) Spreng from Magnoliaceae [15], Coptis deltoidea C. Y. Cheng et Hsiao [37] and Adonis amurensis Regel et Radde [10] from Ranunculaceae, Viola tricolor L. from Violaceae [10], Diphylleia sinensis H. L. Li [30] and Leontice incerta Pall. [12] from Berberidaceae, Solanum japonense Nakai and Solanum septemlobum Bunge from Solanaceae [39], were previously reported as bicellular [1,3]. Additionally, there is also Hemerocallis from Asphodelaceae [28], which had not been reported before. Table 2 lists all the reports of plants shedding both types of pollen. These findings support the idea of treating the coexistence of both types of pollen as the third type of pollen cell number.

4.3. Which Is Primitive and How It Evolved?

The systematic study of pollen cell numbers has been developed and controversial for over a century. Schürhoff [45] firstly observed that most plant families produce either bicellular or tricellular pollen. Schnarf [46,47,48] and Brewbaker [3] further noted that taxa with bicellular pollen were predominantly basal within the phylogenetic tree. Webster and Rupert [4] proposed the “Schiirhoff-Brewbaker Law”, which claims that bicellular pollen was primitive in the angiosperms as a whole and that the evolution process from bicellular to tricellular pollen was irreversible. However, this hypothesis was challenged by Gardner [34], who identified tricellular pollen in Lauraceae (a primitive group), and Webster et al. [49], who found tricellular pollen in early-diverging Euphorbieae. Williams et al. [1] analyzed 2511 species and modeled trait evolution using time-calibrated phylogenines, revealing reversible transitions between bicellular and tricellular states, as well as differential diversification rates between the two lineages. Although they questioned the likelihood of a tricellular origin, they could not conclusively determine the ancestral state.
Interestingly, gymnosperms exhibit varying mitotic divisions during pollen maturation, releasing pollen at different male gametophyte developmental stages [50]. However, previous systematic studies on angiosperms pollen have only considered strictly bicellular and tricellular forms, often disregarding mixed cases as anomalies. If the coexistence of both types of pollen are taken into account, where should it be located? From the limited known results (Table 2), the coexistence of both types of pollen are found in primitive families such as Lauraceae, Magnoliaceae, Annonaceae, and relatively advanced families such as Asteraceae, Gentianaceae and Violaceae. However, in Annonaceae, the coexistence of both types of pollen are mostly distributed in relatively advanced tribes such as Annoneae, Uvariaeae (Annonoideae), and Miliuseae (Malmeoideae) (Figure 8). Lora et al. [6] indicated that the coexistence of both types of pollen may have stronger adaptability than bicellular and tricellular pollen because the environmental conditions of pollen after dispersal are unpredictable, and the combined type of pollen could increase the chance of fertilization. Thus, the coexistence of both types of pollen may be advanced.
Franchi et al. [51] proposed that pollen, like seeds, may undergo developmental arrest (DA) under unfavorable conditions. DA in pollen refers to the phenomenon where the development of pollen slows or temporarily halts before reaching full maturity. This process typically occurs at the bicellular stage, during which the pollen consists of one vegetative cell and one generative cell that has not yet divided into two sperm cells, such as drought conditions Furthermore, DA can occur at any stage of pollen development; it might manifest as bicellular pollen when arrested at the bicellular stage, as either type of pollen when halted during the transition from bicellular to tricellular stage, or as tricellular pollen when environment conditions are favorable and no DA takes place. DA in pollen is strongly associated with the acquisition of desiccation tolerance (DT), which extends pollen viability during air travel [52]. Williams and Brown [53] found a close relationship between the number of pollen cells and pollen water content, revealing that most tricellular pollen exhibited a relatively high water content, whereas bicellular pollen showed comparatively low water content. From the perspective of DA, bicellular pollen appears to represent an evolutionary adaptation from aquatic to terrestrial plants. Additionally, the retrogradation of tricellular pollen observed by Williams et al. [1] may have resulted from a loss of dehydration tolerance during subsequent evolutionary processes.

5. Conclusions

In the present study, we identified 16 species from 10 genera of Annonaceae that shed both types of pollen. Including reports from other families, approximately 15 families, 40 genera, and 52 species are known to produce both types of pollen. The coexistence of bicellular and tricellular pollen might be the third type of pollen cell number. And the systematic relationship among them is needed to be reanalyzed.

Author Contributions

Conceptualization, Y.G.; methodology, Y.G., J.P. and Q.Z.; software, Q.Z.; validation, C.X.; formal analysis, Y.G. and J.P.; investigation, Y.G. and J.P.; resources, Q.Z. and C.X.; data curation, Y.G.; writing—original draft preparation, Y.G.; writing—review and editing, J.P.; visualization, Q.Z.; supervision, Y.G.; project administration, Y.G.; funding acquisition, Y.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Sciences Foundation of China (grant number 31800184) and the “Jinying Star” Talent Project of Guangdong Academy of Agricultural Sciences (grant number R2023PY-JX021).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed at the corresponding author.

Acknowledgments

The authors thank Peng Caixia, Chen Ling and Xue Bine, Liao Jingping, Wen bin, Lai Han and Deng Xingmin for their assistance with material collection.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Mixed developmental stages of Annonaceae pollen before anther release (I). (A–D) The bicellular (A,C,D left) and tricellular (B,D right) pollen of Uvaria grandiflora Roxb; (E–H) the bicellular (G) and tricellular (E,F,H) pollen of Uvaria kurzii (King) P. T. Li; (I–L) the bicellular (I–K) and tricellular (L) pollen of Artabotrys hexapetalus (L. f.) Bhandar; (M–P) the bicellular (N right, P) and tricellular (M,N left,O) pollen of Artabotrys hongkongensis Hance. Scale bar = 50 μm. Arrows show cell nucleus.
Figure 1. Mixed developmental stages of Annonaceae pollen before anther release (I). (A–D) The bicellular (A,C,D left) and tricellular (B,D right) pollen of Uvaria grandiflora Roxb; (E–H) the bicellular (G) and tricellular (E,F,H) pollen of Uvaria kurzii (King) P. T. Li; (I–L) the bicellular (I–K) and tricellular (L) pollen of Artabotrys hexapetalus (L. f.) Bhandar; (M–P) the bicellular (N right, P) and tricellular (M,N left,O) pollen of Artabotrys hongkongensis Hance. Scale bar = 50 μm. Arrows show cell nucleus.
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Biology 14 00562 g002
Figure 2. Mixed developmental stages of Annonaceae pollen before anther release (II). (A–D) The bicellular (C left,D right) and tricellular (A,B,C right,D right) pollen of Artabotrys pachypetalus B. Xue & Junhao Chen; (E–H) the bicellular (E) and tricellular (F–H) pollen of Goniothalamus calvicarpus Craib; (I–L) the bicellular (I,J down,K,L) and tricellular (J up) pollen of Goniothalamus gardneri Hook. f. et Thoms; (M–P) the bicellular (N right, O) and tricellular (M,N left,P) pollen of Fissisfigma polyanthum Hook. f. et Thoms; (Q) the tricellular pollen of Annona cherimola Mill; (R,S) the bicellular (R) and tricellular (S) pollen of Uvaria calamistrata Hance. Scale bar = 50 μm. Arrows show cell nucleus.
Figure 2. Mixed developmental stages of Annonaceae pollen before anther release (II). (A–D) The bicellular (C left,D right) and tricellular (A,B,C right,D right) pollen of Artabotrys pachypetalus B. Xue & Junhao Chen; (E–H) the bicellular (E) and tricellular (F–H) pollen of Goniothalamus calvicarpus Craib; (I–L) the bicellular (I,J down,K,L) and tricellular (J up) pollen of Goniothalamus gardneri Hook. f. et Thoms; (M–P) the bicellular (N right, O) and tricellular (M,N left,P) pollen of Fissisfigma polyanthum Hook. f. et Thoms; (Q) the tricellular pollen of Annona cherimola Mill; (R,S) the bicellular (R) and tricellular (S) pollen of Uvaria calamistrata Hance. Scale bar = 50 μm. Arrows show cell nucleus.
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Biology 14 00562 g003
Figure 3. Mixed developmental stages of Annonaceae pollen before anther release (III). (A–D) The bicellular (A up,B down,C,D) and tricellular (A down,B up) pollen of Mitrephora wangii Hu; (E–H) the bicellular (F,G) and tricellular (E,H) pollen of Meiogyne oligocarpa B. Xue & Y. H. Ta; (I,J) the bicellular (J up) and tricellular (I,J down) pollen of Dasymaschalon rostratum Merr. & Chun; (K,L) the bicellular (K) and tricellular (L) pollen of Orophea laui Leonardía & Kessler; (M–P) the tricellular (M right,N) and bicellular (O,P) pollen of Polyalthia cheliensis Hu; (Q–T) the tricellular (Q,R) and bicellular (S,T) pollen of Goniothalamus chinensis Merr. et Chun. Scale bar = 50 μm. Arrows show cell nucleus.
Figure 3. Mixed developmental stages of Annonaceae pollen before anther release (III). (A–D) The bicellular (A up,B down,C,D) and tricellular (A down,B up) pollen of Mitrephora wangii Hu; (E–H) the bicellular (F,G) and tricellular (E,H) pollen of Meiogyne oligocarpa B. Xue & Y. H. Ta; (I,J) the bicellular (J up) and tricellular (I,J down) pollen of Dasymaschalon rostratum Merr. & Chun; (K,L) the bicellular (K) and tricellular (L) pollen of Orophea laui Leonardía & Kessler; (M–P) the tricellular (M right,N) and bicellular (O,P) pollen of Polyalthia cheliensis Hu; (Q–T) the tricellular (Q,R) and bicellular (S,T) pollen of Goniothalamus chinensis Merr. et Chun. Scale bar = 50 μm. Arrows show cell nucleus.
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Biology 14 00562 g004
Figure 4. Bicellular pollen of Annonaceae shortly before anther dehiscence. (I). (A) Desmos chinensis Lour; (B) Desmos dumosus (roxb.) saff; (C) Desmos yunnanensis (Hu) P. T. Li; (D) Dasymaschalon trichophorum Merr; (E) Desymaschalon filipes (Ridl.) Ridl.Ban; (F) Dasymaschalon macrocalyx Finet & Gagnep; (G) Polyalthia suberosa (Roxburgh) Thwaites; (H) Polyalthia verrucipes C. Y. Wu ex P. T. Li; (I) Polyalthia laui Merrill; (J) Polyalthia chinensis S. K. Wu & P. T. L; (K) Polyalthia yingjiangensis Y. H. Tan & B. Xue; (L) Polyalthia obliqua Hook.f. & Thomson; (M) Polyalthia longifolia (Sonn.) Thwaites; (N) Hubera cerasoides (Roxb.) Benth.et Hook.f.ex Bedd; (O) Cananga odorata (Lamarck) J. D. Hooker & Thomson; (P) Cananga odorata var. fruticosa (Craib) J.Sinclair; (Q) Alphonsea monogyna Merrill & Chun, (R) Alphonsea mollis Dunn; (S) Alphonsea glandulosa Y.H. Tan & B. Xue; (T) Alphonsea ventricosa (Roxb.) Hook.f.&Thomson. Scale bar = 50 μm.
Figure 4. Bicellular pollen of Annonaceae shortly before anther dehiscence. (I). (A) Desmos chinensis Lour; (B) Desmos dumosus (roxb.) saff; (C) Desmos yunnanensis (Hu) P. T. Li; (D) Dasymaschalon trichophorum Merr; (E) Desymaschalon filipes (Ridl.) Ridl.Ban; (F) Dasymaschalon macrocalyx Finet & Gagnep; (G) Polyalthia suberosa (Roxburgh) Thwaites; (H) Polyalthia verrucipes C. Y. Wu ex P. T. Li; (I) Polyalthia laui Merrill; (J) Polyalthia chinensis S. K. Wu & P. T. L; (K) Polyalthia yingjiangensis Y. H. Tan & B. Xue; (L) Polyalthia obliqua Hook.f. & Thomson; (M) Polyalthia longifolia (Sonn.) Thwaites; (N) Hubera cerasoides (Roxb.) Benth.et Hook.f.ex Bedd; (O) Cananga odorata (Lamarck) J. D. Hooker & Thomson; (P) Cananga odorata var. fruticosa (Craib) J.Sinclair; (Q) Alphonsea monogyna Merrill & Chun, (R) Alphonsea mollis Dunn; (S) Alphonsea glandulosa Y.H. Tan & B. Xue; (T) Alphonsea ventricosa (Roxb.) Hook.f.&Thomson. Scale bar = 50 μm.
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Figure 5. Bicellular pollen of Annonaceae shortly before anther dehiscence. (II). (A) Annona squamosa Linn; (B) Annona muricata Linnaeus; (C) Annona montana Macf; (D) Annona reticulata L; (E) Annona glabra Linn; (F) Mitrephora thorelii Pierre; (G,H) Mitrephora teysmannii Scheff; (I) Mitrephora sirikitiae Weeras; (J,K) Pseuduvaria trimera (Craib) Y. C. F. Su & R. M. K. Saunders; (L) Artabotrys hainanensis R. E. Fries; (M) Artabotrys pilosis Merrill & Chun; (N,O) Trivalvaria costata (J. D. Hooker & Thomson) I. M. Turner; (P) Trivalvaria carnosa (Teijsm. & Binn.) Scheff; (Q) Uvaria yunnanensis Hu; (R) Marsypopetalum littorale (Bl.) B. Xue & R. M. K; (S) Chieniodendron hainanense (Merr.) Tsiang et P. T. Li; (T) Cleistopholis glauca Pierre ex Engl. & Diels. Scale bar = 50 μm.
Figure 5. Bicellular pollen of Annonaceae shortly before anther dehiscence. (II). (A) Annona squamosa Linn; (B) Annona muricata Linnaeus; (C) Annona montana Macf; (D) Annona reticulata L; (E) Annona glabra Linn; (F) Mitrephora thorelii Pierre; (G,H) Mitrephora teysmannii Scheff; (I) Mitrephora sirikitiae Weeras; (J,K) Pseuduvaria trimera (Craib) Y. C. F. Su & R. M. K. Saunders; (L) Artabotrys hainanensis R. E. Fries; (M) Artabotrys pilosis Merrill & Chun; (N,O) Trivalvaria costata (J. D. Hooker & Thomson) I. M. Turner; (P) Trivalvaria carnosa (Teijsm. & Binn.) Scheff; (Q) Uvaria yunnanensis Hu; (R) Marsypopetalum littorale (Bl.) B. Xue & R. M. K; (S) Chieniodendron hainanense (Merr.) Tsiang et P. T. Li; (T) Cleistopholis glauca Pierre ex Engl. & Diels. Scale bar = 50 μm.
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Figure 6. Bicellular pollen of Annonaceae shortly before anther dehiscence. (III). (A) Uvaria macrophylla Roxb; (B) Uvaria tokinensis Finet et Gagnep; (C) Uvaria tonkinensis var. subglabra Melodorum; (D) Uvaria kweichowensis P. T. Li; (E) Uvaria grandiflora var.flava (Teijsm. & Binn.) Scheff; (F) Uvaria rufa Bl; (G) Goniothalamus saccopetaloides Y.H. Tan & Bin Yang; (H) Uvaria boniana Finet et Gagnep; (I) Goniothalamus howii Merrill & Chun; (J) Goniothalamus donnaiensis Finet et Gagnep; (K) Goniothalamus cheliensis Hu; (L) Goniothalamus leiocarpus (W. T. Wang) P. T. Li; (M) Fissistigma acuminatissimum Merrill; (N) Fissistigma polyanthoides (Aug. DC.) Merr; (O) Fissistigma glaucescens (Hance) Merrill; (P) Fissistigma wallichii (Hook. f. et Thoms.) Merr; (Q) Fissistigma bracteolatum Chatt; (R) Fissistigma maclurei Merr; (S) Fissistigma uonicum (Dunn) Merr; (T) Fissistigma thorelii (Pierre ex Finet&Gagnep.) Merr. Scale bar = 50 μm.
Figure 6. Bicellular pollen of Annonaceae shortly before anther dehiscence. (III). (A) Uvaria macrophylla Roxb; (B) Uvaria tokinensis Finet et Gagnep; (C) Uvaria tonkinensis var. subglabra Melodorum; (D) Uvaria kweichowensis P. T. Li; (E) Uvaria grandiflora var.flava (Teijsm. & Binn.) Scheff; (F) Uvaria rufa Bl; (G) Goniothalamus saccopetaloides Y.H. Tan & Bin Yang; (H) Uvaria boniana Finet et Gagnep; (I) Goniothalamus howii Merrill & Chun; (J) Goniothalamus donnaiensis Finet et Gagnep; (K) Goniothalamus cheliensis Hu; (L) Goniothalamus leiocarpus (W. T. Wang) P. T. Li; (M) Fissistigma acuminatissimum Merrill; (N) Fissistigma polyanthoides (Aug. DC.) Merr; (O) Fissistigma glaucescens (Hance) Merrill; (P) Fissistigma wallichii (Hook. f. et Thoms.) Merr; (Q) Fissistigma bracteolatum Chatt; (R) Fissistigma maclurei Merr; (S) Fissistigma uonicum (Dunn) Merr; (T) Fissistigma thorelii (Pierre ex Finet&Gagnep.) Merr. Scale bar = 50 μm.
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Figure 7. Bicellular pollen of Annonaceae shortly before anther dehiscence. (IV). (A,B) Orophea hainanensis Merr; (C) Orophea hirsuta King; (D) Anaxagorea luzonensis A. Gray; (E) Anaxagorea javanica Blume; (F) Miliusa chunii W. T. Wan; (G) Miliusa horsfieldii (Bennett) Pierre; (H,I) Miliusa sinensis Finet et Gagnep; (J) Miliusa chantaburiana Damthongdee & Chaowasku; (K) Miliusa glochidioides Hand.-Mazz; (L) Miliusa bannaensis X.L. Hou; (M) Melodorum fruticosum Lour; (N) Melodorum siamense (Scheff.) Bân; (O,Q) Asimina triloba Dunal; (P) Disepalum plagioneurum (Diels) D. M. Johnson; (R) Popowia pisocarpa (Bl.) Endl. in Walp. Rep; (S) Rollinia mucosa (Jacquin) Baillon. Scale bar = 50 μm.
Figure 7. Bicellular pollen of Annonaceae shortly before anther dehiscence. (IV). (A,B) Orophea hainanensis Merr; (C) Orophea hirsuta King; (D) Anaxagorea luzonensis A. Gray; (E) Anaxagorea javanica Blume; (F) Miliusa chunii W. T. Wan; (G) Miliusa horsfieldii (Bennett) Pierre; (H,I) Miliusa sinensis Finet et Gagnep; (J) Miliusa chantaburiana Damthongdee & Chaowasku; (K) Miliusa glochidioides Hand.-Mazz; (L) Miliusa bannaensis X.L. Hou; (M) Melodorum fruticosum Lour; (N) Melodorum siamense (Scheff.) Bân; (O,Q) Asimina triloba Dunal; (P) Disepalum plagioneurum (Diels) D. M. Johnson; (R) Popowia pisocarpa (Bl.) Endl. in Walp. Rep; (S) Rollinia mucosa (Jacquin) Baillon. Scale bar = 50 μm.
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Figure 8. The phylogenetic relationships of sampled species at the genus level. Species with both types of pollen are black and marked with *; others are species with binucleate pollen. The phylogenetic tree referenced Guo et al. [21].
Figure 8. The phylogenetic relationships of sampled species at the genus level. Species with both types of pollen are black and marked with *; others are species with binucleate pollen. The phylogenetic tree referenced Guo et al. [21].
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Table 1. List of investigated species with provenance, voucher number and corresponding figure plate.
Table 1. List of investigated species with provenance, voucher number and corresponding figure plate.
No.TaxonProvenance aVoucherFigures
1Desmos chinensis Lour.SCBGxx060308, 20081072, xx271155Figure 4A
2Desmos dumosus (roxb.)saff.XTBG00012542, C06009, 273677Figure 4B
3Desmos yunnanensis (Hu) P. T. LiXTBG275056, 258389Figure 4C
4Dasymaschalon trichophorum Merr.SCBG20011172, 19975026, 19970018Figure 4D
5Dasymaschalon filipes (Ridl.) Ridl.BanXTBG1320030093, 0020220650Figure 4E
6Dasymaschalon rostratum Merr. & Chun *XTBG0020023226, 0020020479Figure 3I,J
7Dasymaschalon macrocalyx Finet & Gagnep.XTBG1320030078, 0020022105Figure 4F
8Polyalthia suberosa (Roxburgh) ThwaitesSCBG20010982, 20070804, 20140665Figure 4G
9Polyalthia cheliensis Hu *XTBG0020081058, 0020100741Figure 3M–P
10Polyalthia verrucipes C. Y. Wu ex P. T. LiXTBG0020031897(2)Figure 4H
11Polyalthia laui MerrillSCBGxx240010, xx320026Figure 4I
12Polyalthia chinensis S. K. Wu & P. T. LiXTBG0020023088, 0020150274Figure 4J
13Polyalthia yingjiangensis Y. H. Tan and B. XueXTBG0020021384(3)Figure 4K
14Polyalthia obliqua Hook.f. & ThomsonXTBG0020013801(3)Figure 4L
15Polyalthia longifolia (Sonn.) ThwaitesSCBGxx271140, 20055086Figure 4M
16Hubera cerasoides (Roxb.) Benth.et Hook.f.ex Bedd.SCBG20031137(3)Figure 4N
17Annona squamosa Linn.XTBG0020071074(3)Figure 5A
18Annona muricata LinnaeusSCBG19940242, 20070500Figure 5B
19Annona montana MacfXTBG0019600558A, 2019940014Figure 5C
20Annona reticulata L.XTBG0320140001, 275081Figure 5D
21Annona glabra Linn.SCBGxx080063, xx080276, xx080383Figure 5E
22Annona cherimola Mill. *XTBG1520060007(3)Figure 2Q
23Cananga odorata (Lamarck) J. D. Hooker & ThomsonSCBG20090663, 20140876, xx120033Figure 4O
24Cananga odorata var. fruticosa (Craib) J.SinclairSCBG20040790(3)Figure 4P
25Mitrephora thorelii PierreSCBG20030719(3)Figure 5F
26Mitrephora wangii Hu *XTBG0020022041, 256509, 0019780252Figure 3A–D
27Mitrephora teysmannii ScheffSCBG20042613(3)Figure 5G,H
28Mitrephora sirikitiae WeerasXTBG3820130137(3)Figure 5I
29Pseuduvaria trimera (Craib) YCF Su & RMK. SaundersXTBG0019880077, 274490, 3020020011Figure 5J,K
30Alphonsea monogyna Merrill & ChunSCBG20011014(3)Figure 4Q
31Alphonsea mollis DunnXTBG0020040356, 0020150149, 286072Figure 4R
32Alphonsea glandulosa Y.H. Tan & B. XueXTBG0019750173(3)Figure 4S
33Alphonsea ventricosa (Roxb.) Hook.f.&ThomsonXTBG0019970165(3)Figure 4T
34Artabotrys hexapetalus (L. f.) Bhanda *XTBG0020040193, 0020090146Figure 1I–L
35Artabotrys hainanensis R. E. FriesSCBG20012148(3)Figure 5L
36Artabotrys pilosis Merrill & ChunSCBG00012542(3)Figure 5M
37Artabotrys hongkongensis Hance *SCBG20011052(3)Figure 1M–P
38Artabotrys pachypetalus B.Xue & Junhao Chen *SCBG00028772(3)Figure 2A–D
39Trivalvaria costata (J. D. Hooker & Thomson) I. M. TurnerSCBGxx110217(3)Figure 5N,O
40Trivalvaria carnosa (Teijsm. & Binn.) ScheffXTBG1320010126(3)Figure 5P
41Uvaria macrophylla RoxbXTBG0020023255, 287484, 0020090148Figure 6A
42Uvaria grandiflora Roxb *XTBG3820021106(3)Figure 1A–D
43Uvaria calamistrata Hance *XTBG0020201075(3)Figure 2R,S
44Uvaria tokinensis Finet et GagnepXTBG3820020732(3)Figure 6B
45Uvaria tonkinensis var. subglabra MelodorumSCBG20030552(3)Figure 6C
46Uvaria kweichowensis P. T. LiSCBG20031112(3)Figure 6D
47Uvaria kurzii (King) P. T. Li *SCBG042778(3)Figure 1E–H
48Uvaria boniana Finet et GagnepSCBG00044133(3)Figure 6H
49Uvaria grandiflora var. flava (Teijsm. & Binn.) ScheffXTBG3820130135(3)Figure 6E
50Uvaria rufa BlXTBG284407(3)Figure 6F
51Uvaria yunnanensis HuXTBG0020070685(3)Figure 5Q
52Marsypopetalum littorale (Bl.) B. Xue & R. M. K.XTBG0020012213(3)Figure 5R
53Goniothalamus chinensis Merr. et Chun *XTBG3020021381, 0020162454Figure 3Q–T
54Goniothalamus calvicarpus Craib *SCBG20042665, 284928, 275874Figure 2E–H
55Goniothalamus gardneri Hook. f. et Thoms *SCBG20113045(3)Figure 2I–L
56Goniothalamus saccopetaloides Y.H. Tan and Bin YangXTBG3020020407(2)Figure 6G
57Goniothalamus cheliensis HuXTBG3020050005, C30121, 274125Figure 6K
58Goniothalamus leiocarpus (W. T. Wang) P. T. LiXTBG0020013790(2)Figure 6L
59Goniothalamus howii Merrill & ChunXTBG0020021240(2)Figure 6I
60Goniothalamus donnaiensis Finet et GagnepLMNRAU072086 bFigure 6J
61Fissistigma wallichii (Hook. f. et Thoms.) MerrXTBG0020070161, 0020100719Figure 6P
62Fissistigma glaucescens (Hance) MerrillSCBGXX271312(2)Figure 6O
63Fissistigma polyanthum Hook. f. et Thoms *SCBG20050538(2)Figure 2M–P
64Fissistigma polyanthoides (Aug. DC.) Merr.XTBG0020011877, 275869, 275870Figure 6N
65Fissistigma acuminatissimum MerrillXTBG285650(2)Figure 6M
66Fissistigma bracteolatum ChattXTBG374189, 274189, 277352Figure 6Q
67Fissistigma maclurei MerrXTBG0020080638, 286008, 286009Figure 6R
68Fissistigma uonicum (Dunn) MerrNMNR0078738 bFigure 6S
69Fissistigma thorelii (Pierre ex Finet&Gagnep.) MerrXTBG0020020480, 0020031109Figure 6T
70Meiogyne oligocarpa B. Xue & Y. H. Tan *XTBG0020013864(2)Figure 3E–H
71Chieniodendron hainanense (Merr.) Tsiang et P. T. LiSCBG19980193(2)Figure 5S
72Cleistopholis glauca Pierre ex Engl. & DielsXTBG3119800151(2)Figure 5T
73Orophea hainanensis MerrSCBG20011196(3)Figure 7A,B
74Orophea laui Leonardía & Kessler *XTBG275549, 287159Figure 3K,L
75Orophea hirsuta KingSCBG20011196(2)Figure 7C
76Anaxagorea luzonensis A. GrayDMNR1020170057(2)Figure 7D
77Anaxagorea javanica BlumeXTBG3820021060, 0020200920Figure 7E
78Miliusa chunii W. T. WanXTBG0019970179(2)Figure 7F
79Miliusa horsfieldii (Bennett) PierreSCBG20051897(2)Figure 7G
80Miliusa sinensis Finet et GagnepSCBG011047(2)Figure 7H,I
81Miliusa chantaburiana Damthongdee & ChaowaskuXTBG0020210589(2)Figure 7J
82Miliusa glochidioides Hand.-Mazz.SCBG20113642(2)Figure 7K
83Miliusa bannaensis X.L. HouXTBG0020060634(2)Figure 7L
84Melodorum fruticosum LourXTBG3820021019(2)Figure 7M
85Melodorum siamense (Scheff.) BânXTBG3820021101(2)Figure 7N
86Disepalum plagioneurum (Diels) D. M. JohnsonDMNR01187407 bFigure 7P
87Popowia pisocarpa (Bl.) Endl. in Walp. RepDMNR0079742 bFigure 7R
88Asimina triloba Dunal.WBG20177223(2)Figure 7O,Q
89Rollinia mucosa (Jacquin) BaillonSCBGAU080617 bFigure 7S
Taxoxon with “*” have both types of pollen; others are binucleate. a SCBG (South China Botanical Garden, Chinese Academy of Sciences), XTBG (Xishuangbanna Tropical Botanical Garden of Chinese Academy of Sciences), WBG (Wuhan Botanical Garden Chinese Academy of Sciences), DMNR (Diaoluo Mountain Nature Reserve, Hainan, China), NMNR (Nankun Mountain Nature Reserve, Huizhou, China), LMNR (Longgang Nature Reserve, Guangxi, China). b The voucher column lists the introduction number or specimen number of material used in this study. The numbers in parentheses indicate the number of plants.
Table 2. Taxon known to have both bicellular and tricellular pollen.
Table 2. Taxon known to have both bicellular and tricellular pollen.
No.FamilyTaxon% of Anthers with Both Types of PollenReferences
1AnnonaceaeUvaria grandiflora Roxb23.2% (±3%)Present paper
2AnnonaceaeUvaria kurzii (King) P. T. Li55.0% (±5%)Present paper
3AnnonaceaeUvaria calamistrata Hance33.3% (±5%)Present paper
4AnnonaceaeAnnona cherimola Mill53.0% (±3%)Present paper; [6]
5AnnonaceaeMitrephora wangii Hu33.3% (±5%)Present paper
6AnnonaceaeMitrephora maingayi Hook. f. et Thoms33.3% (±5%)[9]
7AnnonaceaeArtabotrys hexapetalus (L. f.) Bhandar25.0% (±5%)Present paper
8AnnonaceaeArtabotrys hongkongensis Hance55.6% (±5%)Present paper
9AnnonaceaeArtabotrys pachypetalus B.Xue & Junhao50.0% (±3%)Present paper
10AnnonaceaeGoniothalamus calvicarpus Craib54.5% (±5%)Present paper
11AnnonaceaeGoniothalamus gardneri Hook. f. et Thoms52.5% (±3%)Present paper
12AnnonaceaeGoniothalamus chinensis Merr. et Chun53.5% (±5%)Present paper
13AnnonaceaeFissistigma polyanthum Hook. f. et Thoms53.0% (±3%)Present paper
14AnnonaceaeDasymaschalon rostratum Merr. & Chun50.0% (±2%)Present paper
15AnnonaceaeMeiogyne oligocarpa B. Xue & Y. H. Tan51.0% (±2%)Present paper
16AnnonaceaeOrophea laui Leonardía & Kessler53.0% (±5%)Present paper
17AnnonaceaePolyalthia cheliensis Hu52.5% (±5%)Present paper
18AraceaeCalla palustris——[5]
19AraceaeRhodospatha forgetii——[5]
20AraceaeAnubias afzelii——[5]
21AraceaeDieffenbachia maculata——[5]
22AraceaeXanthosoma pilosum——[5]
23AraceaeChlorospatha castula——[5]
24AraceaeAlocasia cuprea——[5]
25AsphodelaceaeHemerocallis sp.——[28]
26AsteraceaeConyza canadensis (L.) C ronq——[29]
27BerberidaceaeLeontice incerta Pall.——[13]
28BerberidaceaeDiphylleia sinensis H. L. Li——[30]
29EuphorbiaceaeBeyeria leschenaultii——[4]
30GentianaceaeSwertia bimaculata——[31]
31GentianaceaeTripterospermum chinense (Migo) Harry Sm.——[32]
32LauraceaeLaurelia novae-zelandiae A. Cunn——[33]
33LauraceaeBeilschmiedia tara——[34]
34LauraceaeBeilschmiedia taw——[34]
35MagnoliaceaeMichelia figo (Lour.) Spreng.——[15]
36PlumbaginaceaeLimonium sp.——[35]
37PoaceaeBambusa textilis——[14]
38PoaceaeShibataea chinensis——[36]
39PoaceaeArundinaria simonii f. albostriatus——[36]
40PoaceaePseudosasa viridula——[12]
41PoaceaeMenstruocalamus sichuanensis——[36]
42PoaceaeBambusa multiplex——[8]
43PoaceaeSasaella kogasensis ‘Aureostriatus’——[11]
44PoaceaePhyllostachys edulis (Carrière) J. Houzeau——[16]
45RanunculaceaeAdonis amurensis Regel et Radde.——[10]
46RanunculaceaeCoptis deltoidea C. Y. Cheng et Hsiao——[37]
47SaxifragaceaeSaxifraga pseudohirculus——[7]
48SaxifragaceaeSaxifraga caveana——[7]
49SolanaceaeSolanum phureja——[38]
50SolanaceaeSolanum japonense Nakai——[39]
51SolanaceaeSolanum septemlobum Bunge——[39]
52ViolaceaeViola tricolor L.——[40]
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MDPI and ACS Style

Gan, Y.; Zhang, Q.; Xiao, C.; Ping, J. The Coexistence of Bicellular and Tricellular Pollen Might Be the Third Type of Pollen Cell Number: Evidence from Annonaceae. Biology 2025, 14, 562. https://doi.org/10.3390/biology14050562

AMA Style

Gan Y, Zhang Q, Xiao C, Ping J. The Coexistence of Bicellular and Tricellular Pollen Might Be the Third Type of Pollen Cell Number: Evidence from Annonaceae. Biology. 2025; 14(5):562. https://doi.org/10.3390/biology14050562

Chicago/Turabian Style

Gan, Yangying, Qi Zhang, Chunfen Xiao, and Jingyao Ping. 2025. "The Coexistence of Bicellular and Tricellular Pollen Might Be the Third Type of Pollen Cell Number: Evidence from Annonaceae" Biology 14, no. 5: 562. https://doi.org/10.3390/biology14050562

APA Style

Gan, Y., Zhang, Q., Xiao, C., & Ping, J. (2025). The Coexistence of Bicellular and Tricellular Pollen Might Be the Third Type of Pollen Cell Number: Evidence from Annonaceae. Biology, 14(5), 562. https://doi.org/10.3390/biology14050562

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