Abstract

Mature pollen grains of 295 angiosperm species were screened by epifluorescence microscopy for a marker that denotes the mode of cytoplasmic inheritance. We used the DNA fluorochrome DAPI (4′,6-diamidino-2-phenylindole) for pollen cell staining. The presence or absence of fluorescence of cytoplasmic DNA in the generative cell or sperm cells was examined in each species. The species examined represented 254 genera and 98 families, and 40 of these families had not been previously studied in this regard. The cytoplasmic DNA of the generative cell or sperm cells did not fluoresce in 81% of the species examined, from 83% of the genera and 87% of the families examined, indicating the potential for maternal cytoplasmic inheritance in these species. In contrast, the male reproductive cells of 19% of the species, from 17% of the genera and 26% of the families examined, displayed fluorescence of the cytoplasmic DNA, indicating the potential for biparental cytoplasmic inheritance in these species. The results revealed the potential for biparental cytoplasmic inheritance in several species in which the inheritance mode was previously unknown, including plants in the Bignoniaceae, Cornaceae, Cruciferae (Brassicaceae), Cyperaceae, Dipsacaceae, Hydrocharitaceae, Papaveraceae, Portulacaceae, Tiliaceae, Valerianaceae, and Zingiberaceae. Electron microscopy revealed that the sperm cells of Portulaca grandiflora contain both plastid and mitochondrial DNA. However, in the generative cells of Musella lasiocarpa, the mitochondria contain DNA, but the plastids do not. These data provide a foundation for further studies of cytoplasmic inheritance in angiosperms.

(Received May 9, 2003; Accepted July 22, 2003)

Introduction

At the beginning of the twentieth century, maternal and biparental transmission of leaf color in angiosperms were reported (Correns 1909, Baur 1909). These non-Mendelian phenomena, termed cytoplasmic inheritance, have been studied in the intervening years (Sears 1980, Hagemann and Schröder 1989, Kuroiwa 1991, Mogensen 1996). However, despite decades of research, the modes of cytoplasmic inheritance in angiosperms have been determined for only about 60 genera (Tilney-Bassett 1978, Smith 1988), and cytological examination to determine the mode of inheritance has been applied to only about 100 genera of flowering plants (Whatley 1982, Nagata et al. 1999). Plants whose patterns of cytoplasmic inheritance are known constitute the minority among all of the angiosperms, which number approximately 200,000 species in 10,000 genera and 300–400 families. By contrast, the development of molecular techniques has stimulated the application of plastid genome and mitochondrial genome studies on population genetics, systematics, and organismal evolution. However, many such studies routinely assume maternal cytoplasmic inheritance due to a lack of available information (Mogensen 1996). Therefore, the overall distribution of cytoplasmic inheritance patterns in angiosperms requires further investigation.

The method traditionally used for the cytological examination of cytoplasmic inheritance is electron microscopy. However, this method is inappropriate for the study of large numbers of species. Miyamura et al. (1987) used DAPI-staining fluorescence microscopy to study 16 species whose cytoplasmic inheritance patterns were known. The results demonstrated that cytoplasmic DNA is present in the generative cells or sperm cells of plants known to display biparental or paternal inheritance, but it is not present in species known to display maternal inheritance. Since this method allows rapid screening of large numbers of male reproductive cells, it is suitable for the examination of a large range of angiosperm species. Using the same method, Corriveau and Coleman (1988) examined 235 species within 80 families to determine their patterns of cytoplasmic inheritance. They found that biparental plastid inheritance occurs in about 14% of the genera and 19% of the families examined.

In the present study, we determined the potential for cytoplasmic inheritance in 295 additional flowering plants by detecting the presence or absence of cytoplasmic DNA in the generative cells or sperm cells of mature pollen. Our examination extended to 98 families, of which 40 had not been previously studied in this regard. Of the species examined, 81%, representing 83% of the genera and 87% of the families studied, displayed maternal inheritance, and the remaining 19% of the species, in 17% of the genera and 26% of the families examined, showed a potential for biparental inheritance. The results of the present study should contribute to a better understanding of the systematic distribution of cytoplasmic inheritance in angiosperms.

Results

Cytoplasmic DNA in generative cells and sperm cells

When mature pollen grains were squashed in buffer containing DAPI and glutaraldehyde and examined with an epifluorescence microscope, nuclear DNA and cytoplasmic DNA aggregates in the pollen cells were visible. In species with the potential for biparental cytoplasmic inheritance, the fluorescence of cytoplasmic DNA aggregates was clearly associated with the generative cell or sperm cells (Fig. 1a). In contrast, in species that display maternal inheritance, no fluorescence was detectable (Fig. 1b). The presence or absence of the fluorescence corresponded to species with the potential for biparental or maternal cytoplasmic inheritance, respectively. This trait was therefore used as a criterion in our screening of species for modes of cytoplasmic inheritance.

Distribution of maternal and biparental cytoplasmic inheritance

The generative cells or sperm cells of 295 species representing 254 genera in 98 families were examined. The results are summarized in Tables 1 and 2.

Maternal inheritance, the dominant mode of cytoplasmic inheritance in angiosperms, was detected in 238 species from 87 families. Cytoplasmic DNA was not detectable in the male reproductive cells of these species. Within the families containing species identified as displaying maternal inheritance, a single mode of maternal inheritance appeared in 72 families, including the two largest angiosperm families, the Orchidaceae (four species) and the Compositae (15 species in 14 genera).

Cytoplasmic DNA was detected in the male reproductive cells of 57 species, comprising 43 genera of 25 families, indicating the potential for biparental inheritance in these species. Within the families containing species identified as displaying potential for biparental cytoplasmic inheritance, the potential for both maternal and biparental inheritance appeared in 14 families, including the Aizoaceae, Araceae, Bignoniaceae, Caprifoliaceae, Cornaceae, Cruciferae, Leguminosae, Liliaceae, Musaceae, Oleaceae, Papaveraceae, Portulacaceae, Solanaceae, and Zingiberaceae. Species with a single mode of biparental inheritance appeared in 11 families, including the Actinidiaceae (one species), Cactaceae (one species), Campanulaceae (four species in two genera), Cyperaceae (one species), Dipsacaceae (three species in three genera), Hydrocharitaceae (one species), Linaceae (two species in one genera), Plumbaginaceae (one species), Tiliaceae (two species in two genera), Turneraceae (one species), and Valerianaceae (three species in two genera). An unusual case was Jasminum polyanthum in the Oleaceae, which had dual features. Fluorescence of the cytoplasmic DNA was detected in the sperm cells of about 50% of the pollen grains, implying that the species is intermediate between biparental and maternal inheritance.

Although most genera were determined to have the same mode of cytoplasmic inheritance, interspecies variation appeared in three genera. In Portulaca (Portulacaceae), cytoplasmic DNA was detected in the sperm cells of P. grandiflora but not in P. oleracea, suggesting that the two species have different modes of cytoplasmic inheritance. Similar cases of intrageneric variation were found in Mesembryanthemum (Aizoaceae) and Syringa (Oleaceae).

Identification of plastid and mitochondrial DNA in male reproductive cells

The fluorescent spots of cytoplasmic DNA that appear in the generative or sperm cells can be emitted from either plastid DNA or mitochondrial DNA. In some cases, dimorphic fluorescent spots indicated that the male reproductive cells contained both plastid and mitochondrial DNA. However, in most species identified by us as having potential for biparental inheritance, it was impossible to discriminate between plastid and mitochondrial DNA aggregates with epifluorescence microscopy, since the fluorescent spots derived from this DNA had similar features (see examples in Fig. 2). In these cases, the fluorescence derived from plastid and mitochondrial DNA needed to be distinguished in order to determine whether the plastids or mitochondria have the potential for biparental inheritance.

Electron microscopy of the sperm cells of P. grandiflora (Portulacaceae) indicated that the cells contained both plastids and mitochondria (Fig. 3c). In addition, Immunogold electron microscopy revealed that anti-DNA gold particles localized to both of the organelles (Fig. 3b). These results suggest that the fluorescent spots in the sperm cells (as shown in Fig. 3a) must have been derived from both plastid and mitochondrial DNA, and therefore both the plastids and the mitochondria of P. grandiflora have the potential for biparental inheritance.

A similar examination was performed for Musella lasiocarpa (Musaceae). In plants of this species, there was a large ratio of cytoplasm to nucleus in the generative cell, which contained a large number of mitochondria but few plastids (Fig. 4a). In the case of M. lasiocarpa, however, clusters of gold particles were localized on the mitochondria but not on the plastids (Fig. 4c–f). These results showed that the fluorescent spots in the generative cell shown in Fig. 4b resulted only from mitochondrial DNA and provided evidence for the biparental inheritance of mitochondria and maternal inheritance of plastids in this species.

Discussion

The sexual crossing test is a traditional tool that gives an exact result for determining the mode of cytoplasmic inheritance. However, since the cytoplasmic phenotype mutants that are useful for crossing tests are exceedingly scarce, application of the method has been limited to about 60 angiosperm genera in crops and ornamental species (Tilney-Bassett 1978, Whatley 1982, Smith 1988, Reboud and Zeyl 1994). For the same reason, the use of molecular techniques such as restriction fragment length polymorphism is limited. This is why cytoplasmic inheritance has been less well studied in wild plants than in cultivated species. To investigate a broader range of angiosperms, we used fluorescence microscopy to detect the presence or absence of cytoplasmic DNA in the male reproductive cells and determine the potential mode of cytoplasmic inheritance. The method allows rapid, large-scale screening of plants for the potential for different modes of cytoplasmic inheritance, with reliable results (Miyamura et al. 1987, Corriveau and Coleman 1988). In this study, cytoplasmic DNA was observed in the male reproductive cells of Actinidia deliciosa, Zantedeschia aethiopica, and Turnera ulmifolia, which were previously reported to display biparental plastid inheritance (Yao et al. 1994, Testolin and Cipriani 1997, Shore and Triassi 1998). This result may be thought as a positive control for the method. Based on the results of previous studies and this one, we conclude that the fluorescence of cytoplasmic DNA in male reproductive cells can be used as a reliable marker for our purposes.

Using fluorescence microscopy, Corriveau and Coleman (1988) examined 235 species of angiosperms representing 80 families. The results are important for understanding the distribution of different modes of cytoplasmic inheritance in angiosperms. We determined the potential for cytoplasmic inheritance in 295 additional angiosperm species using a strategy similar to that of Corriveau and Coleman (1988). The examination included 98 families, of which 40 had not been previously studied in this regard. Our results show that 81% of the species studied, in 83% of the genera and 87% of the families examined, display maternal inheritance, and 19% of the species studied, in 17% of the genera and 26% of the families examined, show a potential for biparental inheritance. These rates are similar to those determined by Corriveau and Coleman (1988), who found that approximately 80% of angiosperm species display maternal cytoplasmic inheritance. Furthermore, we discovered the potential for biparental inheritance in the Bignoniaceae, Cornaceae, Cruciferae (Brassicaceae), Cyperaceae, Dipsacaceae, Hydrocharitaceae, Papaveraceae, Portulacaceae, Tiliaceae, Valerianaceae, and Zingiberaceae. Biparental inheritance has not been reported previously in these families, which are distributed in quite distant orders. Four genera (seven species) in the Caprifoliaceae and all species studied in the Dipsacaceae and Valerianaceae have the potential for biparental inheritance in Dipsacales. Species with the potential for biparental inheritance were found in the Aizoaceae and Portulacaceae in the Aizoales. The distribution of families with biparental inheritance among the distant taxons examined in this study is consistent with the results of previous studies. Our results, therefore, support the suggestion that cytoplasmic inheritance evolved independently many times in response to different selective pressures (Sears 1980, Birky 1995).

An analysis of our results showed that the presence or absence of cytoplasmic DNA in male reproductive cells could be used as a trait for systematic studies. For example, cytoplasmic DNA was detected in Corydalis and Dicentra but not in other genera of the Papaveraceae. This result agrees with the suggestion of Lidén that Corydalis and Dicentra should be reclassified from the Papaveraceae to the new family Fumariaceae (Lidén 1993). In the Caprifoliaceae, four genera (Abelia, Linnaea, Lonicera and Weigela) showed a potential for biparental cytoplasmic inheritance, and two genera (Sambucus and Viburnum) displayed maternal cytoplasmic inheritance. These results coincide with Wilkinson’s opinion that Sambucus and Viburnum (biparental genera) should be grouped into one lineage and others (maternal genera) should be grouped into another lineage (Wilkinson 1949). In addition, we detected cytoplasmic DNA in the generative cells of Swida walteri (Cornaceae), also called Cornus walteri. However, no cytoplasmic DNA was detected in the generative cells of Cornus florida (Corriveau and Coleman 1988) or Cornus officinalis. These results provide evidence for the establishment of Swida walteri as a species.

Cytoplasmic inheritance includes the inheritance of both the plastid and the mitochondrial genomes. Recent studies have indicated that inheritance of these organelle genomes is controlled in different ways (Nagata et al. 1999, Sodmergen et al. 2002). Therefore, it will be necessary to determine whether the fluorescence in male reproductive cells following DAPI staining is derived from plastid or mitochondrial DNA. We have applied electron and immunoelectron microscopy for this purpose, as described previously (Sodmergen et al. 1997, Sodmergen et al. 1998, Zhang and Sodmergen 2003). The results show that both plastids and mitochondria of P. grandiflora have the potential for biparental inheritance, and that mitochondria, but not plastids, of M. lasiocarpa appear to result from biparental inheritance. A similar examination of the male reproductive cells of other species, using fluorescence of cytoplasmic DNA after DAPI staining, is underway.

Since the strategy used in this study was similar to that of Corriveau and Coleman (1988), our examination did not initially include the genera that were examined in their study. However, during the examination, several conflicts appeared. In the Limonium, Astragalus, Trifolium, Vicia, Campsis, Linum, and Zingiber genera, fluorescence of cytoplasmic DNA appeared in the generative or sperm cells in our study, but was not detected in these cells by Corriveau and Coleman (1988). In Campsis radicans, treatment of the cells with ethanol and glacial acetic acid as described by Corriveau and Coleman (1988) degraded the fluorescence. Therefore, the discrepancies may be due to differences in the methods used or intrageneric variation. For these genera, further confirmation of the mode of inheritance is required.

Materials and Methods

Mature pollen grains were collected from plants at sites in Beijing and Yunnan. The majority of the experimental materials were obtained from plants collected in three botanical gardens: Beijing Botanical Garden, Institute of Botany, Chinese Academy of Sciences; Kunming Botanical Garden, Kunming, Yunnan; and Xishuangbanna Botanical Garden, Menglun, Yunnan. Pollen were sampled and examined from April to August.

Epifluorescence microscopy of cytoplasmic DNA was performed according to the method of Kuroiwa and Suzuki (1980). In brief, pollen grains were collected on a glass slide and immersed in a drop of 3% glutaraldehyde and 1 µg ml–1 DAPI in Tan buffer (Nemoto et al. 1988). The pollen grains were covered with a cover slip, then squashed by pressing the cover slip against the slide. The samples were examined after 10 min with an Olympus BH-2 epifluorescence microscope.

Electron microscopy of pollen cells was performed using routine methods. For DNA Immunogold electron microscopy, pollen grains were fixed with 3% glutaraldehyde in cacodylate buffer (pH 7.4) and embedded in LR White resin. The sections were labeled using the method of Johnson and Rosenbaum (1990). A mouse monoclonal antibody that recognizes single- and double-stranded DNA (Boehringer Mannheim, Germany) and a goat anti-mouse IgM antibody conjugated to 10-nm colloidal gold (British BioCell International, U.K.) were used for the detection. Sections were examined with a JOEL JEM-1010 electron microscope.

We routinely performed a DNase test to confirm the free localization of the Immunogold on the sample sections pretreated with DNase (data not shown).

Acknowledgments

This research was supported by the National Science Fund for Distinguished Young Scholars of China (No. 30025004) and the State Key Basic Research and Development Plan of China (No. G1999011700). Many thanks are due to Prof. J.C. Chen (Institute of Botany, Chinese Academy of Sciences, Beijing) and Dr. T.G. Gao (Institute of Botany, Chinese Academy of Sciences, Kunming) for their assistance in collecting and identifying the materials.

1

Corresponding author: E-mail, sodmergn@bio.pku.edu.cn; Fax, +86-10-62751526.

Fig. 1 DAPI-stained epifluorescence microphotographs showing squashed pollen grains of (a) Actinidia deliciosa, a species that displays biparental plastid inheritance, and (b) Sophora japonica f. pendula, a species that displays maternal cytoplasmic inheritance. Arrows indicate the fluorescent spots of cytoplasmic DNA. GN, generative nucleus; VN, vegetative nucleus, W, pollen wall. Bar = 5 µm.

Fig. 1 DAPI-stained epifluorescence microphotographs showing squashed pollen grains of (a) Actinidia deliciosa, a species that displays biparental plastid inheritance, and (b) Sophora japonica f. pendula, a species that displays maternal cytoplasmic inheritance. Arrows indicate the fluorescent spots of cytoplasmic DNA. GN, generative nucleus; VN, vegetative nucleus, W, pollen wall. Bar = 5 µm.

Fig. 2 DAPI-stained epifluorescence microphotograph showing the male reproductive cells squashed from pollen grains of (a) Weigela florida, (b) Syringa pekinensis, (c) Codonopsis lanceolata, (d) Incarvillea sp., (e) Corydalis bungeana, (f) Musa coccinea, (g) Carex baccans, (h) Zingiber purpureum, (i) Trifolium repens, and (j) Vicia bungei. Note the fluorescent spots in the cells. GN, generative nucleus; SN, sperm nucleus; VN, vegetative nucleus. Bar = 10 µm.

Fig. 2 DAPI-stained epifluorescence microphotograph showing the male reproductive cells squashed from pollen grains of (a) Weigela florida, (b) Syringa pekinensis, (c) Codonopsis lanceolata, (d) Incarvillea sp., (e) Corydalis bungeana, (f) Musa coccinea, (g) Carex baccans, (h) Zingiber purpureum, (i) Trifolium repens, and (j) Vicia bungei. Note the fluorescent spots in the cells. GN, generative nucleus; SN, sperm nucleus; VN, vegetative nucleus. Bar = 10 µm.

Fig. 3 DAPI-stained epifluorescence (a), electron (b) and immunoelectron (c) microphotographs showing sperm cells of Portulaca grandiflora. (a) Cytoplasmic DNA in the sperm cells emitted similar epifluorescent spots (arrow). (b) The cell contained both plastids and mitochondria. (c) Gold particles appeared on both of the organelles. M, mitochondrion; P, plastid; SN, sperm nucleus. Bars = 10 µm (a), 0.5 µm (b, c).

Fig. 3 DAPI-stained epifluorescence (a), electron (b) and immunoelectron (c) microphotographs showing sperm cells of Portulaca grandiflora. (a) Cytoplasmic DNA in the sperm cells emitted similar epifluorescent spots (arrow). (b) The cell contained both plastids and mitochondria. (c) Gold particles appeared on both of the organelles. M, mitochondrion; P, plastid; SN, sperm nucleus. Bars = 10 µm (a), 0.5 µm (b, c).

Fig. 4 Electron (a), DAPI-stained epifluorescence (b) and immunoelectron (c–f) microphotographs showing generative cells of Musella lasiocarpa. (a) Numerous mitochondria but few plastids were seen in the cell. (b) Fluorescence of cytoplasmic DNA was evident. (c–f) Gold particles appeared in clusters on mitochondria. (d, e, f) Serial sections through a plastid were sparsely labeled with gold particles. GN, generative nucleus; M, mitochondrion; P, plastid. Bars = 0.5 µm (a, d–f), 5 µm (b) and 1 µm (c).

Fig. 4 Electron (a), DAPI-stained epifluorescence (b) and immunoelectron (c–f) microphotographs showing generative cells of Musella lasiocarpa. (a) Numerous mitochondria but few plastids were seen in the cell. (b) Fluorescence of cytoplasmic DNA was evident. (c–f) Gold particles appeared in clusters on mitochondria. (d, e, f) Serial sections through a plastid were sparsely labeled with gold particles. GN, generative nucleus; M, mitochondrion; P, plastid. Bars = 0.5 µm (a, d–f), 5 µm (b) and 1 µm (c).

Table 1

The mode of cytoplasmic inheritance of 295 plant species determined using epifluorescence microscopy to reveal the presence or absence of cytoplasmic DNA in the generative or sperm cells

TaxonMode aPollen b
Acanthaceae
 Adhatoda vasicaM2
Thunbergia grandifloraM2
Actinidiaceae
 Actinidia deliciosaB2
Aizoaceae
 Mesembryanthemum cordifoliumM3
Mesembryanthemum spectabileB3
Alismataceae
 Sagittaria subulataM3
Amaranthaceae
 Amaranthus lividusM3
Amaranthus tricolarM3
Amaryllidaceae
 Crinum aciaticumM2
Crinum amabileM2
 Lycoris aureaM2
Apocynaceae
 Allemanda catharticaM2/3
Allemanda neriifoliaM2
 Apocynum venetumM2
Catharanthus roseusM2
 Rauvolfia verticillataM2
Thevetia peruvianaM2
Araceae
 Pinellia ternataM2
Zantedeschia aethiopica B3
Asclepiadaceae
 Cynanchum thesioidesM2
Berberidaceae
 Nandina domesticaM2
Bigoniaceae
 Begonia argyrostigmaM2
Bigononiaceae
 Catalpa bungeiM2
Catalpa speciosaM2
 Campsis radicansB2
Incarvillea sp.B2
Bixaceae
 Bixa orellanaM2
Boraginaceae
 Cynoglossum amabileM2/3
Bromeliaceae
 Anans sp.M2
Buxaceae
 Buxus sinicaM2
Cactaceae
 Pereskia aculeataB3
Calycanthaceae
 Chimonanthus praecoxM2
Campanulaceae
 Adenophora divaricataB2
Adenophora paniculataB2
 Codonopsis lanceolataB2
Codonopsis pliosulaB2
Cannabinaceae
 Cannabis sativaM2
Cannaceae
 Canna indicaM2
Caprifoliaceae
 Abelia bifloraB3
Abelia chinensisB/M3
 Kolkwitzia amabiliaB3
Lonicera maackiiB3
 Lonicera pekinensisB3
Lonicera X TellmannianaM3
 Viburnum sargentiiM2
Weigela floridaB3
Caryophyllaceae
 Arenaria fridericaM3
Dianthus fragransM3
 Lychnis fulgensM3
Silene fortuneiM3
Ceratophyllaceae
 Ceratophyllum demersumM3
Commelinaceae
 Commelina communisM2
Compsitae
 Adenocaulon himalaicumM3
Anaphalis sinicaM3
 Aster sp.M3
Atractylodes lanceaM2
 Bidens bipinnataM2
Bupleurum chinenseM3
 Doellingeria scabraM2
Eupatorium japonicumM3
 Senecio rowleyanusM3
Galinsogo parvifloraM3
 Hemistepta lyrataM3
Ligularia lapathifoliaM3
 Ligularia intermediaM3
Myripnois dioicaM3
 Syneilesis aconitifoliaM2
Cornaceae
 Swida walteri (=Cornus walteri)B2
Cornus officinalis (= Macrocarpium officinalis)M2
Crassulaceae
 Rhodiola roseaM2
Sedum aizoonM2
Cruciferae
 Arabis pendulaM3
Hesperis trichosepalaB3
Matthiola incanaM3
 Nasturtium officinaleM2
Orychophragmus violaceusM3
 Rorippa indicaM3
Cyperaceae
 Carex baccansB3
Dioscoreaceae
 Dioscorea nipponicaM2
Dipsacaceae
 Dipsacus asperoidesB3
Morina nepalensisB3
 Scabiosa tschiliensisB3
Ebenaceae
 Diospyros lotusM3
Eucommiaceae
Eucommia ulmoidesM2
Euphorbiaceae
 Euphobia miliiM2
Leptopus chinensisM2
 Securinega suffruticosaM2
Gentianaceae
 Halenia corniculataM3
Nymphoides peltatumM3
Gesneriaceae
 Lysionotus paucilorusM2
Saintpaulia ionanthaM2
 Sinnigia speciosaM2
Graminaceae
 Melica scabrosaM3
Hamamelidaceae
 Loropetalum chinensis var. rubrumM2
Hippocastansceae
 Aesculus chinensisM2
Hydrocharitaceae
 Ottelia acuminata var. crispaB2
Hypoxidaceae
 Cucurligo capitullataM2
Iridaceae
 Belamcanda chinensisM2
Freesia refractaM2
Juglandaceae
 Juglans cathayansisM2
Labiatae
 Agastache rugosaM3
Ajuga lupulinaM2
 Clerodendranthus spicatusM2
Dracocephalum rupstreM3
Mentha haplocalyx var. piperascensM2
Phlomis jeholensisM2
 Salvia japonicaM3
Salvia miltiorrthizaM3
 Scutellaris baicalensisM2/3
Veronica linariaefoliaM2/3
Leguminosae
 Astragalus dahuricusB2
Astragalus strictusB2
 Bauhnie feberiM3
Caesalpinia pulcherrimaM2
 Caesalpinia sappanM2
Calliandra suriniaceaeM3
 Campylotropis macrocarpaM2/3
Cassia surattensisM2
 Colutea arborescensB2
Erythrina variegataM2
 Glycyrrhiza pallidifloraB2
Lespedeza davuricaM3
 Mimosa pudicaM2
Phyllodium pulchellumM2
 Sophora flavescensM2
Sophora japonica f. pendulaM2
 Trifolium repensB2
Vicia bungeiB2
 Vicia fabaB2
Vicia giganteaB2
 Vicia pseudorobusB2
Vicia unijugaB2
Liliaceae
 Allium odorumM2
Allium victorialisM2
 Aloe sp.M2
Asparagus cochinchinensisM2
 Diuranthera majorB2
Gagea sp.M2
 Lloydia ixiolirioidesB3
Ornithogalum caudatumM2
 Ophiopogon japonicusM2
Polygonatum odoratumM2
 Zephyranthes grandifloraM2
Linaceae
 Linum stelleroidesB3
Linum usitatissmumB3
Loganiaceae
 Buddleja yunnanensisM2
Lythraceae
 Lagerstroemia indicaM2
Lythrum salicariaM2
Malpighiaceae
 Malpighia glavcaM2
Malvaceae
 Malva sp.M2
Melastomataceae
 Osbeckia opiparaM2
Menispermaceae
 Stephania epigaeaM2
Moraceae
 Broussonetia papyriferaM2
Ficus elasticaM3
 Humulus scandensM2
Musaceae
 Heliconia aurantiacaM2
Heliconia pendulaM2
 Musa coccineaB2
Musa sapientumB2
 Musella lasiocarpaB2
Myrtaceae
 Callistemon rigidusM2
Syzygium cuminiM2
Nymphaeaceae
 Nelumbo nuciferaM2
Nymphaea tuberosaM2
Oleaceae
 Chionanthus retususM2
Fontanesia fortuneiM3
 Fraxinus excelsior var. aureaM2
Jasminum polyanthumB/M3
 Syringa oblataM2
Syringa pekinensisB2
Onagraceae
 Circaea quadrisulcataM2
Fuchsia hybridaM2
Orchidaceae
 Arundina graminifoliaM2
Calanthe discolorM2
 Liparis yunnanensisM2
Spiranthes lanceM2
Oxalidaceae
 Oxalis oreganaM2
Palmae
 Archontophoeni alexanandraeM2
Papaveraceae
 Chelidonium majusM2
Corydalis bungeanaB2
 Dicentra spectabilisB2
Hepecoum leptocarpumM2
 Macleaya cordataM2
Papver rhoeasM2
Phrymaceae
 Phryma leptostachyaM3
Phytolacaceae
 Rivina humilisM3
Plumbaginaceae
 Limonium sinuatumB3
Polemoniaceae
 Phlox subulataM2
Polygalaceae
 Polygala arillataM3
Polygala sibiricaM3
 Polygala tenuifoliaM3
Polygonaceae
 Fagopyrum esculentumM3
 Polygonum amplexicaule var. sinensisM2
 Polygonum senticosumM3
Polygonum suffultumM3
 Rheum offcinaleM3
Portulacaceae
 Portulaca grandifloraB3
Portulaca oleraceaM3
 Talinum patensM3
Pontederiaceae
 Eichhornia crassipesM2
Primulaceae
 Cyclamen persicumM2
Lysimachia barystachysM2
 Lysimachia clethroidesM2
Primula secundifloraM2
 Primula sikkimensisM2
Punicaceae
 Punica granatumM2
Ranuncalaceae
Aconitum alboviolaceumM2
 Anemone cathayensisM2
Anemone rivularis var. flore-minoreM2
 Clematis hexapetalaM2
Paeonia lactifloraM2
 Ranunculus japonicaM2
Thalictrum aquilegifoliumM2
 Trollius chinensisM2
Rhamnaceae
 Rhamnus floridaM2
Rosaceae
 Agrimonia pilosaM2
Chaenomeles speciosaM2
 Chamaerhodos erectaM2
Dontostemon dentatusM3
 Erysimum bungeiM3
Geum aleppicumM2
 Kerria japonicaM2
Malus hallianaM2
 Potentilla discolarM2
Rosa xanthinaM2
 Sanguisorba officinalisM2
Spiraea fritchianaM2
 Spiraea sahcifoliaM2
Sorbaria sorbifoliaM2
 Taihangia rupestrisM2
Rubiaceae
 Galium aparineM2
Gardenia jasminoidesM2
 Hamelia patensM2
Hymenodictyon flaccidumM2
 Ixora yunnanensisM2
Mussaenda erythrophyllaM2
 Mycetia gracilisM2
Serissa japonicaM2
Rutaceae
 Fortunella margaritaM2
Micromelum paniculataM2/3
Salicaceae
 Populus tomentosaM2
Salix babylonicaM2
 Salix gracilistyla M2
Sapindaceae
 Koelreuteria paniculataM2
Saururaceae
 Saururus chinensisM2
Saxifragaceae
 Astilbe chinensisM2
Deutzia grandifloraM2
Ribes fasciculatumM2
Scrophulariaceae
 Calceolaria crenatiflora M2
Digitalis purpureaM2
 Paulownia tomentosaM2
Pedicularis likiangensisM2
 Pedicularis siphonanthaM2
Pedicularis striataM2
 Rehmannia glutinosaM2
Verbascum thapsusM2
 Veronica didymaM
Veronica linariaefoliaM2/3
Simaroubaceae
 Ailanthus altissimaM2
Solanaceae
 Brunfelsia latifoliaB2
Datura sp.M2
 Lycium chinenseM2
Solanum nigrumM2
Sterculiaceae
 Firmiana simplexM2
Sterculia nobilisM2
Taccaceae
 Tacca chantrieriM2
Thymelaeaceae
 Daphne sp.M3
Tiliaceae
 Grewia bilobia var. parvifoliaB3
Tilia tuanB3
Trapaceae
 Trapa bispinosaM3
Turneraceae
 Turnera ulmifoliaB3
Umbelliferae
 Heracleum moellendorffiiM3
Saposhnikovia divaricataM3
 Sphallerocarpus gracilisM3
Urticaceae
 Pilea paperomioidesM3
Urtica angustifoliaM2
Valerianaceae
 Patrinia heterophyllaB3
Patrinia scabiosaefoliaB3
 Valeriana officinalisB3
Verbenaceae
 Callicarpa arboreaM2
Clerodendron thomsonaeM2
 Clerodendron trichotomumM2
Stachytarpheta jamaicensisM3
 Tectona grandisM3
Verbena trifoliaM2
 Vitex negunda var. heterophyllaM2
Zingiberaceae
 Costus lacerusM2
Curcuma domesticaM2/3
 Etlingera erythrophyllaM2
Globba barthriB2
 Globba racemosaB2
Hedychium spicatumM2
 Zingiber purpureumB2
Zingiber zerumbetB2
Zygophyllaceae
 Tribulus terrestrisM3
TaxonMode aPollen b
Acanthaceae
 Adhatoda vasicaM2
Thunbergia grandifloraM2
Actinidiaceae
 Actinidia deliciosaB2
Aizoaceae
 Mesembryanthemum cordifoliumM3
Mesembryanthemum spectabileB3
Alismataceae
 Sagittaria subulataM3
Amaranthaceae
 Amaranthus lividusM3
Amaranthus tricolarM3
Amaryllidaceae
 Crinum aciaticumM2
Crinum amabileM2
 Lycoris aureaM2
Apocynaceae
 Allemanda catharticaM2/3
Allemanda neriifoliaM2
 Apocynum venetumM2
Catharanthus roseusM2
 Rauvolfia verticillataM2
Thevetia peruvianaM2
Araceae
 Pinellia ternataM2
Zantedeschia aethiopica B3
Asclepiadaceae
 Cynanchum thesioidesM2
Berberidaceae
 Nandina domesticaM2
Bigoniaceae
 Begonia argyrostigmaM2
Bigononiaceae
 Catalpa bungeiM2
Catalpa speciosaM2
 Campsis radicansB2
Incarvillea sp.B2
Bixaceae
 Bixa orellanaM2
Boraginaceae
 Cynoglossum amabileM2/3
Bromeliaceae
 Anans sp.M2
Buxaceae
 Buxus sinicaM2
Cactaceae
 Pereskia aculeataB3
Calycanthaceae
 Chimonanthus praecoxM2
Campanulaceae
 Adenophora divaricataB2
Adenophora paniculataB2
 Codonopsis lanceolataB2
Codonopsis pliosulaB2
Cannabinaceae
 Cannabis sativaM2
Cannaceae
 Canna indicaM2
Caprifoliaceae
 Abelia bifloraB3
Abelia chinensisB/M3
 Kolkwitzia amabiliaB3
Lonicera maackiiB3
 Lonicera pekinensisB3
Lonicera X TellmannianaM3
 Viburnum sargentiiM2
Weigela floridaB3
Caryophyllaceae
 Arenaria fridericaM3
Dianthus fragransM3
 Lychnis fulgensM3
Silene fortuneiM3
Ceratophyllaceae
 Ceratophyllum demersumM3
Commelinaceae
 Commelina communisM2
Compsitae
 Adenocaulon himalaicumM3
Anaphalis sinicaM3
 Aster sp.M3
Atractylodes lanceaM2
 Bidens bipinnataM2
Bupleurum chinenseM3
 Doellingeria scabraM2
Eupatorium japonicumM3
 Senecio rowleyanusM3
Galinsogo parvifloraM3
 Hemistepta lyrataM3
Ligularia lapathifoliaM3
 Ligularia intermediaM3
Myripnois dioicaM3
 Syneilesis aconitifoliaM2
Cornaceae
 Swida walteri (=Cornus walteri)B2
Cornus officinalis (= Macrocarpium officinalis)M2
Crassulaceae
 Rhodiola roseaM2
Sedum aizoonM2
Cruciferae
 Arabis pendulaM3
Hesperis trichosepalaB3
Matthiola incanaM3
 Nasturtium officinaleM2
Orychophragmus violaceusM3
 Rorippa indicaM3
Cyperaceae
 Carex baccansB3
Dioscoreaceae
 Dioscorea nipponicaM2
Dipsacaceae
 Dipsacus asperoidesB3
Morina nepalensisB3
 Scabiosa tschiliensisB3
Ebenaceae
 Diospyros lotusM3
Eucommiaceae
Eucommia ulmoidesM2
Euphorbiaceae
 Euphobia miliiM2
Leptopus chinensisM2
 Securinega suffruticosaM2
Gentianaceae
 Halenia corniculataM3
Nymphoides peltatumM3
Gesneriaceae
 Lysionotus paucilorusM2
Saintpaulia ionanthaM2
 Sinnigia speciosaM2
Graminaceae
 Melica scabrosaM3
Hamamelidaceae
 Loropetalum chinensis var. rubrumM2
Hippocastansceae
 Aesculus chinensisM2
Hydrocharitaceae
 Ottelia acuminata var. crispaB2
Hypoxidaceae
 Cucurligo capitullataM2
Iridaceae
 Belamcanda chinensisM2
Freesia refractaM2
Juglandaceae
 Juglans cathayansisM2
Labiatae
 Agastache rugosaM3
Ajuga lupulinaM2
 Clerodendranthus spicatusM2
Dracocephalum rupstreM3
Mentha haplocalyx var. piperascensM2
Phlomis jeholensisM2
 Salvia japonicaM3
Salvia miltiorrthizaM3
 Scutellaris baicalensisM2/3
Veronica linariaefoliaM2/3
Leguminosae
 Astragalus dahuricusB2
Astragalus strictusB2
 Bauhnie feberiM3
Caesalpinia pulcherrimaM2
 Caesalpinia sappanM2
Calliandra suriniaceaeM3
 Campylotropis macrocarpaM2/3
Cassia surattensisM2
 Colutea arborescensB2
Erythrina variegataM2
 Glycyrrhiza pallidifloraB2
Lespedeza davuricaM3
 Mimosa pudicaM2
Phyllodium pulchellumM2
 Sophora flavescensM2
Sophora japonica f. pendulaM2
 Trifolium repensB2
Vicia bungeiB2
 Vicia fabaB2
Vicia giganteaB2
 Vicia pseudorobusB2
Vicia unijugaB2
Liliaceae
 Allium odorumM2
Allium victorialisM2
 Aloe sp.M2
Asparagus cochinchinensisM2
 Diuranthera majorB2
Gagea sp.M2
 Lloydia ixiolirioidesB3
Ornithogalum caudatumM2
 Ophiopogon japonicusM2
Polygonatum odoratumM2
 Zephyranthes grandifloraM2
Linaceae
 Linum stelleroidesB3
Linum usitatissmumB3
Loganiaceae
 Buddleja yunnanensisM2
Lythraceae
 Lagerstroemia indicaM2
Lythrum salicariaM2
Malpighiaceae
 Malpighia glavcaM2
Malvaceae
 Malva sp.M2
Melastomataceae
 Osbeckia opiparaM2
Menispermaceae
 Stephania epigaeaM2
Moraceae
 Broussonetia papyriferaM2
Ficus elasticaM3
 Humulus scandensM2
Musaceae
 Heliconia aurantiacaM2
Heliconia pendulaM2
 Musa coccineaB2
Musa sapientumB2
 Musella lasiocarpaB2
Myrtaceae
 Callistemon rigidusM2
Syzygium cuminiM2
Nymphaeaceae
 Nelumbo nuciferaM2
Nymphaea tuberosaM2
Oleaceae
 Chionanthus retususM2
Fontanesia fortuneiM3
 Fraxinus excelsior var. aureaM2
Jasminum polyanthumB/M3
 Syringa oblataM2
Syringa pekinensisB2
Onagraceae
 Circaea quadrisulcataM2
Fuchsia hybridaM2
Orchidaceae
 Arundina graminifoliaM2
Calanthe discolorM2
 Liparis yunnanensisM2
Spiranthes lanceM2
Oxalidaceae
 Oxalis oreganaM2
Palmae
 Archontophoeni alexanandraeM2
Papaveraceae
 Chelidonium majusM2
Corydalis bungeanaB2
 Dicentra spectabilisB2
Hepecoum leptocarpumM2
 Macleaya cordataM2
Papver rhoeasM2
Phrymaceae
 Phryma leptostachyaM3
Phytolacaceae
 Rivina humilisM3
Plumbaginaceae
 Limonium sinuatumB3
Polemoniaceae
 Phlox subulataM2
Polygalaceae
 Polygala arillataM3
Polygala sibiricaM3
 Polygala tenuifoliaM3
Polygonaceae
 Fagopyrum esculentumM3
 Polygonum amplexicaule var. sinensisM2
 Polygonum senticosumM3
Polygonum suffultumM3
 Rheum offcinaleM3
Portulacaceae
 Portulaca grandifloraB3
Portulaca oleraceaM3
 Talinum patensM3
Pontederiaceae
 Eichhornia crassipesM2
Primulaceae
 Cyclamen persicumM2
Lysimachia barystachysM2
 Lysimachia clethroidesM2
Primula secundifloraM2
 Primula sikkimensisM2
Punicaceae
 Punica granatumM2
Ranuncalaceae
Aconitum alboviolaceumM2
 Anemone cathayensisM2
Anemone rivularis var. flore-minoreM2
 Clematis hexapetalaM2
Paeonia lactifloraM2
 Ranunculus japonicaM2
Thalictrum aquilegifoliumM2
 Trollius chinensisM2
Rhamnaceae
 Rhamnus floridaM2
Rosaceae
 Agrimonia pilosaM2
Chaenomeles speciosaM2
 Chamaerhodos erectaM2
Dontostemon dentatusM3
 Erysimum bungeiM3
Geum aleppicumM2
 Kerria japonicaM2
Malus hallianaM2
 Potentilla discolarM2
Rosa xanthinaM2
 Sanguisorba officinalisM2
Spiraea fritchianaM2
 Spiraea sahcifoliaM2
Sorbaria sorbifoliaM2
 Taihangia rupestrisM2
Rubiaceae
 Galium aparineM2
Gardenia jasminoidesM2
 Hamelia patensM2
Hymenodictyon flaccidumM2
 Ixora yunnanensisM2
Mussaenda erythrophyllaM2
 Mycetia gracilisM2
Serissa japonicaM2
Rutaceae
 Fortunella margaritaM2
Micromelum paniculataM2/3
Salicaceae
 Populus tomentosaM2
Salix babylonicaM2
 Salix gracilistyla M2
Sapindaceae
 Koelreuteria paniculataM2
Saururaceae
 Saururus chinensisM2
Saxifragaceae
 Astilbe chinensisM2
Deutzia grandifloraM2
Ribes fasciculatumM2
Scrophulariaceae
 Calceolaria crenatiflora M2
Digitalis purpureaM2
 Paulownia tomentosaM2
Pedicularis likiangensisM2
 Pedicularis siphonanthaM2
Pedicularis striataM2
 Rehmannia glutinosaM2
Verbascum thapsusM2
 Veronica didymaM
Veronica linariaefoliaM2/3
Simaroubaceae
 Ailanthus altissimaM2
Solanaceae
 Brunfelsia latifoliaB2
Datura sp.M2
 Lycium chinenseM2
Solanum nigrumM2
Sterculiaceae
 Firmiana simplexM2
Sterculia nobilisM2
Taccaceae
 Tacca chantrieriM2
Thymelaeaceae
 Daphne sp.M3
Tiliaceae
 Grewia bilobia var. parvifoliaB3
Tilia tuanB3
Trapaceae
 Trapa bispinosaM3
Turneraceae
 Turnera ulmifoliaB3
Umbelliferae
 Heracleum moellendorffiiM3
Saposhnikovia divaricataM3
 Sphallerocarpus gracilisM3
Urticaceae
 Pilea paperomioidesM3
Urtica angustifoliaM2
Valerianaceae
 Patrinia heterophyllaB3
Patrinia scabiosaefoliaB3
 Valeriana officinalisB3
Verbenaceae
 Callicarpa arboreaM2
Clerodendron thomsonaeM2
 Clerodendron trichotomumM2
Stachytarpheta jamaicensisM3
 Tectona grandisM3
Verbena trifoliaM2
 Vitex negunda var. heterophyllaM2
Zingiberaceae
 Costus lacerusM2
Curcuma domesticaM2/3
 Etlingera erythrophyllaM2
Globba barthriB2
 Globba racemosaB2
Hedychium spicatumM2
 Zingiber purpureumB2
Zingiber zerumbetB2
Zygophyllaceae
 Tribulus terrestrisM3

a M, maternal inheritance (cytoplasmic DNA was undetected in the male reproductive cells), B, biparental inheritance (cytoplasmic DNA was detected in the male reproductive cells), B/M, biparental or maternal inheritance (cytoplasmic DNA was detectable in sperm cells from about 50% pollen but undetectable in sperm cells from the other 50% pollen); b bi-cellular (2) or tri-cellular (3) pollen.

Table 1

The mode of cytoplasmic inheritance of 295 plant species determined using epifluorescence microscopy to reveal the presence or absence of cytoplasmic DNA in the generative or sperm cells

TaxonMode aPollen b
Acanthaceae
 Adhatoda vasicaM2
Thunbergia grandifloraM2
Actinidiaceae
 Actinidia deliciosaB2
Aizoaceae
 Mesembryanthemum cordifoliumM3
Mesembryanthemum spectabileB3
Alismataceae
 Sagittaria subulataM3
Amaranthaceae
 Amaranthus lividusM3
Amaranthus tricolarM3
Amaryllidaceae
 Crinum aciaticumM2
Crinum amabileM2
 Lycoris aureaM2
Apocynaceae
 Allemanda catharticaM2/3
Allemanda neriifoliaM2
 Apocynum venetumM2
Catharanthus roseusM2
 Rauvolfia verticillataM2
Thevetia peruvianaM2
Araceae
 Pinellia ternataM2
Zantedeschia aethiopica B3
Asclepiadaceae
 Cynanchum thesioidesM2
Berberidaceae
 Nandina domesticaM2
Bigoniaceae
 Begonia argyrostigmaM2
Bigononiaceae
 Catalpa bungeiM2
Catalpa speciosaM2
 Campsis radicansB2
Incarvillea sp.B2
Bixaceae
 Bixa orellanaM2
Boraginaceae
 Cynoglossum amabileM2/3
Bromeliaceae
 Anans sp.M2
Buxaceae
 Buxus sinicaM2
Cactaceae
 Pereskia aculeataB3
Calycanthaceae
 Chimonanthus praecoxM2
Campanulaceae
 Adenophora divaricataB2
Adenophora paniculataB2
 Codonopsis lanceolataB2
Codonopsis pliosulaB2
Cannabinaceae
 Cannabis sativaM2
Cannaceae
 Canna indicaM2
Caprifoliaceae
 Abelia bifloraB3
Abelia chinensisB/M3
 Kolkwitzia amabiliaB3
Lonicera maackiiB3
 Lonicera pekinensisB3
Lonicera X TellmannianaM3
 Viburnum sargentiiM2
Weigela floridaB3
Caryophyllaceae
 Arenaria fridericaM3
Dianthus fragransM3
 Lychnis fulgensM3
Silene fortuneiM3
Ceratophyllaceae
 Ceratophyllum demersumM3
Commelinaceae
 Commelina communisM2
Compsitae
 Adenocaulon himalaicumM3
Anaphalis sinicaM3
 Aster sp.M3
Atractylodes lanceaM2
 Bidens bipinnataM2
Bupleurum chinenseM3
 Doellingeria scabraM2
Eupatorium japonicumM3
 Senecio rowleyanusM3
Galinsogo parvifloraM3
 Hemistepta lyrataM3
Ligularia lapathifoliaM3
 Ligularia intermediaM3
Myripnois dioicaM3
 Syneilesis aconitifoliaM2
Cornaceae
 Swida walteri (=Cornus walteri)B2
Cornus officinalis (= Macrocarpium officinalis)M2
Crassulaceae
 Rhodiola roseaM2
Sedum aizoonM2
Cruciferae
 Arabis pendulaM3
Hesperis trichosepalaB3
Matthiola incanaM3
 Nasturtium officinaleM2
Orychophragmus violaceusM3
 Rorippa indicaM3
Cyperaceae
 Carex baccansB3
Dioscoreaceae
 Dioscorea nipponicaM2
Dipsacaceae
 Dipsacus asperoidesB3
Morina nepalensisB3
 Scabiosa tschiliensisB3
Ebenaceae
 Diospyros lotusM3
Eucommiaceae
Eucommia ulmoidesM2
Euphorbiaceae
 Euphobia miliiM2
Leptopus chinensisM2
 Securinega suffruticosaM2
Gentianaceae
 Halenia corniculataM3
Nymphoides peltatumM3
Gesneriaceae
 Lysionotus paucilorusM2
Saintpaulia ionanthaM2
 Sinnigia speciosaM2
Graminaceae
 Melica scabrosaM3
Hamamelidaceae
 Loropetalum chinensis var. rubrumM2
Hippocastansceae
 Aesculus chinensisM2
Hydrocharitaceae
 Ottelia acuminata var. crispaB2
Hypoxidaceae
 Cucurligo capitullataM2
Iridaceae
 Belamcanda chinensisM2
Freesia refractaM2
Juglandaceae
 Juglans cathayansisM2
Labiatae
 Agastache rugosaM3
Ajuga lupulinaM2
 Clerodendranthus spicatusM2
Dracocephalum rupstreM3
Mentha haplocalyx var. piperascensM2
Phlomis jeholensisM2
 Salvia japonicaM3
Salvia miltiorrthizaM3
 Scutellaris baicalensisM2/3
Veronica linariaefoliaM2/3
Leguminosae
 Astragalus dahuricusB2
Astragalus strictusB2
 Bauhnie feberiM3
Caesalpinia pulcherrimaM2
 Caesalpinia sappanM2
Calliandra suriniaceaeM3
 Campylotropis macrocarpaM2/3
Cassia surattensisM2
 Colutea arborescensB2
Erythrina variegataM2
 Glycyrrhiza pallidifloraB2
Lespedeza davuricaM3
 Mimosa pudicaM2
Phyllodium pulchellumM2
 Sophora flavescensM2
Sophora japonica f. pendulaM2
 Trifolium repensB2
Vicia bungeiB2
 Vicia fabaB2
Vicia giganteaB2
 Vicia pseudorobusB2
Vicia unijugaB2
Liliaceae
 Allium odorumM2
Allium victorialisM2
 Aloe sp.M2
Asparagus cochinchinensisM2
 Diuranthera majorB2
Gagea sp.M2
 Lloydia ixiolirioidesB3
Ornithogalum caudatumM2
 Ophiopogon japonicusM2
Polygonatum odoratumM2
 Zephyranthes grandifloraM2
Linaceae
 Linum stelleroidesB3
Linum usitatissmumB3
Loganiaceae
 Buddleja yunnanensisM2
Lythraceae
 Lagerstroemia indicaM2
Lythrum salicariaM2
Malpighiaceae
 Malpighia glavcaM2
Malvaceae
 Malva sp.M2
Melastomataceae
 Osbeckia opiparaM2
Menispermaceae
 Stephania epigaeaM2
Moraceae
 Broussonetia papyriferaM2
Ficus elasticaM3
 Humulus scandensM2
Musaceae
 Heliconia aurantiacaM2
Heliconia pendulaM2
 Musa coccineaB2
Musa sapientumB2
 Musella lasiocarpaB2
Myrtaceae
 Callistemon rigidusM2
Syzygium cuminiM2
Nymphaeaceae
 Nelumbo nuciferaM2
Nymphaea tuberosaM2
Oleaceae
 Chionanthus retususM2
Fontanesia fortuneiM3
 Fraxinus excelsior var. aureaM2
Jasminum polyanthumB/M3
 Syringa oblataM2
Syringa pekinensisB2
Onagraceae
 Circaea quadrisulcataM2
Fuchsia hybridaM2
Orchidaceae
 Arundina graminifoliaM2
Calanthe discolorM2
 Liparis yunnanensisM2
Spiranthes lanceM2
Oxalidaceae
 Oxalis oreganaM2
Palmae
 Archontophoeni alexanandraeM2
Papaveraceae
 Chelidonium majusM2
Corydalis bungeanaB2
 Dicentra spectabilisB2
Hepecoum leptocarpumM2
 Macleaya cordataM2
Papver rhoeasM2
Phrymaceae
 Phryma leptostachyaM3
Phytolacaceae
 Rivina humilisM3
Plumbaginaceae
 Limonium sinuatumB3
Polemoniaceae
 Phlox subulataM2
Polygalaceae
 Polygala arillataM3
Polygala sibiricaM3
 Polygala tenuifoliaM3
Polygonaceae
 Fagopyrum esculentumM3
 Polygonum amplexicaule var. sinensisM2
 Polygonum senticosumM3
Polygonum suffultumM3
 Rheum offcinaleM3
Portulacaceae
 Portulaca grandifloraB3
Portulaca oleraceaM3
 Talinum patensM3
Pontederiaceae
 Eichhornia crassipesM2
Primulaceae
 Cyclamen persicumM2
Lysimachia barystachysM2
 Lysimachia clethroidesM2
Primula secundifloraM2
 Primula sikkimensisM2
Punicaceae
 Punica granatumM2
Ranuncalaceae
Aconitum alboviolaceumM2
 Anemone cathayensisM2
Anemone rivularis var. flore-minoreM2
 Clematis hexapetalaM2
Paeonia lactifloraM2
 Ranunculus japonicaM2
Thalictrum aquilegifoliumM2
 Trollius chinensisM2
Rhamnaceae
 Rhamnus floridaM2
Rosaceae
 Agrimonia pilosaM2
Chaenomeles speciosaM2
 Chamaerhodos erectaM2
Dontostemon dentatusM3
 Erysimum bungeiM3
Geum aleppicumM2
 Kerria japonicaM2
Malus hallianaM2
 Potentilla discolarM2
Rosa xanthinaM2
 Sanguisorba officinalisM2
Spiraea fritchianaM2
 Spiraea sahcifoliaM2
Sorbaria sorbifoliaM2
 Taihangia rupestrisM2
Rubiaceae
 Galium aparineM2
Gardenia jasminoidesM2
 Hamelia patensM2
Hymenodictyon flaccidumM2
 Ixora yunnanensisM2
Mussaenda erythrophyllaM2
 Mycetia gracilisM2
Serissa japonicaM2
Rutaceae
 Fortunella margaritaM2
Micromelum paniculataM2/3
Salicaceae
 Populus tomentosaM2
Salix babylonicaM2
 Salix gracilistyla M2
Sapindaceae
 Koelreuteria paniculataM2
Saururaceae
 Saururus chinensisM2
Saxifragaceae
 Astilbe chinensisM2
Deutzia grandifloraM2
Ribes fasciculatumM2
Scrophulariaceae
 Calceolaria crenatiflora M2
Digitalis purpureaM2
 Paulownia tomentosaM2
Pedicularis likiangensisM2
 Pedicularis siphonanthaM2
Pedicularis striataM2
 Rehmannia glutinosaM2
Verbascum thapsusM2
 Veronica didymaM
Veronica linariaefoliaM2/3
Simaroubaceae
 Ailanthus altissimaM2
Solanaceae
 Brunfelsia latifoliaB2
Datura sp.M2
 Lycium chinenseM2
Solanum nigrumM2
Sterculiaceae
 Firmiana simplexM2
Sterculia nobilisM2
Taccaceae
 Tacca chantrieriM2
Thymelaeaceae
 Daphne sp.M3
Tiliaceae
 Grewia bilobia var. parvifoliaB3
Tilia tuanB3
Trapaceae
 Trapa bispinosaM3
Turneraceae
 Turnera ulmifoliaB3
Umbelliferae
 Heracleum moellendorffiiM3
Saposhnikovia divaricataM3
 Sphallerocarpus gracilisM3
Urticaceae
 Pilea paperomioidesM3
Urtica angustifoliaM2
Valerianaceae
 Patrinia heterophyllaB3
Patrinia scabiosaefoliaB3
 Valeriana officinalisB3
Verbenaceae
 Callicarpa arboreaM2
Clerodendron thomsonaeM2
 Clerodendron trichotomumM2
Stachytarpheta jamaicensisM3
 Tectona grandisM3
Verbena trifoliaM2
 Vitex negunda var. heterophyllaM2
Zingiberaceae
 Costus lacerusM2
Curcuma domesticaM2/3
 Etlingera erythrophyllaM2
Globba barthriB2
 Globba racemosaB2
Hedychium spicatumM2
 Zingiber purpureumB2
Zingiber zerumbetB2
Zygophyllaceae
 Tribulus terrestrisM3
TaxonMode aPollen b
Acanthaceae
 Adhatoda vasicaM2
Thunbergia grandifloraM2
Actinidiaceae
 Actinidia deliciosaB2
Aizoaceae
 Mesembryanthemum cordifoliumM3
Mesembryanthemum spectabileB3
Alismataceae
 Sagittaria subulataM3
Amaranthaceae
 Amaranthus lividusM3
Amaranthus tricolarM3
Amaryllidaceae
 Crinum aciaticumM2
Crinum amabileM2
 Lycoris aureaM2
Apocynaceae
 Allemanda catharticaM2/3
Allemanda neriifoliaM2
 Apocynum venetumM2
Catharanthus roseusM2
 Rauvolfia verticillataM2
Thevetia peruvianaM2
Araceae
 Pinellia ternataM2
Zantedeschia aethiopica B3
Asclepiadaceae
 Cynanchum thesioidesM2
Berberidaceae
 Nandina domesticaM2
Bigoniaceae
 Begonia argyrostigmaM2
Bigononiaceae
 Catalpa bungeiM2
Catalpa speciosaM2
 Campsis radicansB2
Incarvillea sp.B2
Bixaceae
 Bixa orellanaM2
Boraginaceae
 Cynoglossum amabileM2/3
Bromeliaceae
 Anans sp.M2
Buxaceae
 Buxus sinicaM2
Cactaceae
 Pereskia aculeataB3
Calycanthaceae
 Chimonanthus praecoxM2
Campanulaceae
 Adenophora divaricataB2
Adenophora paniculataB2
 Codonopsis lanceolataB2
Codonopsis pliosulaB2
Cannabinaceae
 Cannabis sativaM2
Cannaceae
 Canna indicaM2
Caprifoliaceae
 Abelia bifloraB3
Abelia chinensisB/M3
 Kolkwitzia amabiliaB3
Lonicera maackiiB3
 Lonicera pekinensisB3
Lonicera X TellmannianaM3
 Viburnum sargentiiM2
Weigela floridaB3
Caryophyllaceae
 Arenaria fridericaM3
Dianthus fragransM3
 Lychnis fulgensM3
Silene fortuneiM3
Ceratophyllaceae
 Ceratophyllum demersumM3
Commelinaceae
 Commelina communisM2
Compsitae
 Adenocaulon himalaicumM3
Anaphalis sinicaM3
 Aster sp.M3
Atractylodes lanceaM2
 Bidens bipinnataM2
Bupleurum chinenseM3
 Doellingeria scabraM2
Eupatorium japonicumM3
 Senecio rowleyanusM3
Galinsogo parvifloraM3
 Hemistepta lyrataM3
Ligularia lapathifoliaM3
 Ligularia intermediaM3
Myripnois dioicaM3
 Syneilesis aconitifoliaM2
Cornaceae
 Swida walteri (=Cornus walteri)B2
Cornus officinalis (= Macrocarpium officinalis)M2
Crassulaceae
 Rhodiola roseaM2
Sedum aizoonM2
Cruciferae
 Arabis pendulaM3
Hesperis trichosepalaB3
Matthiola incanaM3
 Nasturtium officinaleM2
Orychophragmus violaceusM3
 Rorippa indicaM3
Cyperaceae
 Carex baccansB3
Dioscoreaceae
 Dioscorea nipponicaM2
Dipsacaceae
 Dipsacus asperoidesB3
Morina nepalensisB3
 Scabiosa tschiliensisB3
Ebenaceae
 Diospyros lotusM3
Eucommiaceae
Eucommia ulmoidesM2
Euphorbiaceae
 Euphobia miliiM2
Leptopus chinensisM2
 Securinega suffruticosaM2
Gentianaceae
 Halenia corniculataM3
Nymphoides peltatumM3
Gesneriaceae
 Lysionotus paucilorusM2
Saintpaulia ionanthaM2
 Sinnigia speciosaM2
Graminaceae
 Melica scabrosaM3
Hamamelidaceae
 Loropetalum chinensis var. rubrumM2
Hippocastansceae
 Aesculus chinensisM2
Hydrocharitaceae
 Ottelia acuminata var. crispaB2
Hypoxidaceae
 Cucurligo capitullataM2
Iridaceae
 Belamcanda chinensisM2
Freesia refractaM2
Juglandaceae
 Juglans cathayansisM2
Labiatae
 Agastache rugosaM3
Ajuga lupulinaM2
 Clerodendranthus spicatusM2
Dracocephalum rupstreM3
Mentha haplocalyx var. piperascensM2
Phlomis jeholensisM2
 Salvia japonicaM3
Salvia miltiorrthizaM3
 Scutellaris baicalensisM2/3
Veronica linariaefoliaM2/3
Leguminosae
 Astragalus dahuricusB2
Astragalus strictusB2
 Bauhnie feberiM3
Caesalpinia pulcherrimaM2
 Caesalpinia sappanM2
Calliandra suriniaceaeM3
 Campylotropis macrocarpaM2/3
Cassia surattensisM2
 Colutea arborescensB2
Erythrina variegataM2
 Glycyrrhiza pallidifloraB2
Lespedeza davuricaM3
 Mimosa pudicaM2
Phyllodium pulchellumM2
 Sophora flavescensM2
Sophora japonica f. pendulaM2
 Trifolium repensB2
Vicia bungeiB2
 Vicia fabaB2
Vicia giganteaB2
 Vicia pseudorobusB2
Vicia unijugaB2
Liliaceae
 Allium odorumM2
Allium victorialisM2
 Aloe sp.M2
Asparagus cochinchinensisM2
 Diuranthera majorB2
Gagea sp.M2
 Lloydia ixiolirioidesB3
Ornithogalum caudatumM2
 Ophiopogon japonicusM2
Polygonatum odoratumM2
 Zephyranthes grandifloraM2
Linaceae
 Linum stelleroidesB3
Linum usitatissmumB3
Loganiaceae
 Buddleja yunnanensisM2
Lythraceae
 Lagerstroemia indicaM2
Lythrum salicariaM2
Malpighiaceae
 Malpighia glavcaM2
Malvaceae
 Malva sp.M2
Melastomataceae
 Osbeckia opiparaM2
Menispermaceae
 Stephania epigaeaM2
Moraceae
 Broussonetia papyriferaM2
Ficus elasticaM3
 Humulus scandensM2
Musaceae
 Heliconia aurantiacaM2
Heliconia pendulaM2
 Musa coccineaB2
Musa sapientumB2
 Musella lasiocarpaB2
Myrtaceae
 Callistemon rigidusM2
Syzygium cuminiM2
Nymphaeaceae
 Nelumbo nuciferaM2
Nymphaea tuberosaM2
Oleaceae
 Chionanthus retususM2
Fontanesia fortuneiM3
 Fraxinus excelsior var. aureaM2
Jasminum polyanthumB/M3
 Syringa oblataM2
Syringa pekinensisB2
Onagraceae
 Circaea quadrisulcataM2
Fuchsia hybridaM2
Orchidaceae
 Arundina graminifoliaM2
Calanthe discolorM2
 Liparis yunnanensisM2
Spiranthes lanceM2
Oxalidaceae
 Oxalis oreganaM2
Palmae
 Archontophoeni alexanandraeM2
Papaveraceae
 Chelidonium majusM2
Corydalis bungeanaB2
 Dicentra spectabilisB2
Hepecoum leptocarpumM2
 Macleaya cordataM2
Papver rhoeasM2
Phrymaceae
 Phryma leptostachyaM3
Phytolacaceae
 Rivina humilisM3
Plumbaginaceae
 Limonium sinuatumB3
Polemoniaceae
 Phlox subulataM2
Polygalaceae
 Polygala arillataM3
Polygala sibiricaM3
 Polygala tenuifoliaM3
Polygonaceae
 Fagopyrum esculentumM3
 Polygonum amplexicaule var. sinensisM2
 Polygonum senticosumM3
Polygonum suffultumM3
 Rheum offcinaleM3
Portulacaceae
 Portulaca grandifloraB3
Portulaca oleraceaM3
 Talinum patensM3
Pontederiaceae
 Eichhornia crassipesM2
Primulaceae
 Cyclamen persicumM2
Lysimachia barystachysM2
 Lysimachia clethroidesM2
Primula secundifloraM2
 Primula sikkimensisM2
Punicaceae
 Punica granatumM2
Ranuncalaceae
Aconitum alboviolaceumM2
 Anemone cathayensisM2
Anemone rivularis var. flore-minoreM2
 Clematis hexapetalaM2
Paeonia lactifloraM2
 Ranunculus japonicaM2
Thalictrum aquilegifoliumM2
 Trollius chinensisM2
Rhamnaceae
 Rhamnus floridaM2
Rosaceae
 Agrimonia pilosaM2
Chaenomeles speciosaM2
 Chamaerhodos erectaM2
Dontostemon dentatusM3
 Erysimum bungeiM3
Geum aleppicumM2
 Kerria japonicaM2
Malus hallianaM2
 Potentilla discolarM2
Rosa xanthinaM2
 Sanguisorba officinalisM2
Spiraea fritchianaM2
 Spiraea sahcifoliaM2
Sorbaria sorbifoliaM2
 Taihangia rupestrisM2
Rubiaceae
 Galium aparineM2
Gardenia jasminoidesM2
 Hamelia patensM2
Hymenodictyon flaccidumM2
 Ixora yunnanensisM2
Mussaenda erythrophyllaM2
 Mycetia gracilisM2
Serissa japonicaM2
Rutaceae
 Fortunella margaritaM2
Micromelum paniculataM2/3
Salicaceae
 Populus tomentosaM2
Salix babylonicaM2
 Salix gracilistyla M2
Sapindaceae
 Koelreuteria paniculataM2
Saururaceae
 Saururus chinensisM2
Saxifragaceae
 Astilbe chinensisM2
Deutzia grandifloraM2
Ribes fasciculatumM2
Scrophulariaceae
 Calceolaria crenatiflora M2
Digitalis purpureaM2
 Paulownia tomentosaM2
Pedicularis likiangensisM2
 Pedicularis siphonanthaM2
Pedicularis striataM2
 Rehmannia glutinosaM2
Verbascum thapsusM2
 Veronica didymaM
Veronica linariaefoliaM2/3
Simaroubaceae
 Ailanthus altissimaM2
Solanaceae
 Brunfelsia latifoliaB2
Datura sp.M2
 Lycium chinenseM2
Solanum nigrumM2
Sterculiaceae
 Firmiana simplexM2
Sterculia nobilisM2
Taccaceae
 Tacca chantrieriM2
Thymelaeaceae
 Daphne sp.M3
Tiliaceae
 Grewia bilobia var. parvifoliaB3
Tilia tuanB3
Trapaceae
 Trapa bispinosaM3
Turneraceae
 Turnera ulmifoliaB3
Umbelliferae
 Heracleum moellendorffiiM3
Saposhnikovia divaricataM3
 Sphallerocarpus gracilisM3
Urticaceae
 Pilea paperomioidesM3
Urtica angustifoliaM2
Valerianaceae
 Patrinia heterophyllaB3
Patrinia scabiosaefoliaB3
 Valeriana officinalisB3
Verbenaceae
 Callicarpa arboreaM2
Clerodendron thomsonaeM2
 Clerodendron trichotomumM2
Stachytarpheta jamaicensisM3
 Tectona grandisM3
Verbena trifoliaM2
 Vitex negunda var. heterophyllaM2
Zingiberaceae
 Costus lacerusM2
Curcuma domesticaM2/3
 Etlingera erythrophyllaM2
Globba barthriB2
 Globba racemosaB2
Hedychium spicatumM2
 Zingiber purpureumB2
Zingiber zerumbetB2
Zygophyllaceae
 Tribulus terrestrisM3

a M, maternal inheritance (cytoplasmic DNA was undetected in the male reproductive cells), B, biparental inheritance (cytoplasmic DNA was detected in the male reproductive cells), B/M, biparental or maternal inheritance (cytoplasmic DNA was detectable in sperm cells from about 50% pollen but undetectable in sperm cells from the other 50% pollen); b bi-cellular (2) or tri-cellular (3) pollen.

Table 2

Summary of results

FamiliesGeneraSpecies
Total98254295
Biparental25 (11±14 a) (26%)43 (40±3 b) (17%)57 (19%)
Maternal87 (73±14 a) (87%)214 (211±3 b) (83%)240 (81%)
FamiliesGeneraSpecies
Total98254295
Biparental25 (11±14 a) (26%)43 (40±3 b) (17%)57 (19%)
Maternal87 (73±14 a) (87%)214 (211±3 b) (83%)240 (81%)

a Families in which both maternal and biparental cytoplasmic inheritance patterns were detected.

b Genera in which the mode of cytoplasmic inheritance showed interspecies variation.

Table 2

Summary of results

FamiliesGeneraSpecies
Total98254295
Biparental25 (11±14 a) (26%)43 (40±3 b) (17%)57 (19%)
Maternal87 (73±14 a) (87%)214 (211±3 b) (83%)240 (81%)
FamiliesGeneraSpecies
Total98254295
Biparental25 (11±14 a) (26%)43 (40±3 b) (17%)57 (19%)
Maternal87 (73±14 a) (87%)214 (211±3 b) (83%)240 (81%)

a Families in which both maternal and biparental cytoplasmic inheritance patterns were detected.

b Genera in which the mode of cytoplasmic inheritance showed interspecies variation.

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