Sexual and Apomictic Seed Reproduction in Aronia Species with Different Ploidy Levels

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  • 1 Department of Plant Science and Landscape Architecture, University of Connecticut, Storrs, CT 06269
  • | 2 Department of Biology, Framingham State University, Framingham, MA 01701
  • | 3 Department of Plant Science and Landscape Architecture, University of Connecticut, Storrs, CT 06269

The genus Aronia Medik., also known as chokeberry, is a group of deciduous shrubs in the Rosaceae family, subtribe Pyrinae. The four commonly accepted species include A. arbutifolia (L.) Pers., red chokeberry; A. melanocarpa (Michx.) Elliott, black chokeberry; A. prunifolia (Marshall) Reheder, purple chokeberry; and A. mitschurinii (A.K. Skvortsov & Maitul). Wild and domesticated Aronia species are found as diploids, triploids, and tetraploids. Genetic improvement of polyploid Aronia genotypes has been limited by suspected apomixis, which may be widespread or distinct to tetraploids. The objectives of this study were to elucidate the reproductive mechanisms of Aronia species and reveal the occurrence of apomixis within the genus and along ploidy lines. Twenty-nine Aronia accessions [five A. melanocarpa (2×), five A. melanocarpa (4×), eight A. prunifolia (3×), four A. prunifolia (4×), six A. arbutifolia (4×), and one A. mitschurinii (4×)] were used in this study. Intra-accession variability was evaluated by growing out progeny from each open-pollinated maternal accession and comparing plant phenotypes, ploidy levels, and amplified fragment length polymorphism (AFLP) marker profiles between the progeny and maternal accession. Progeny of diploid and tetraploid maternal plants had ploidy levels identical to maternal plants, except for UC009 (A. melanocarpa, 2×) which produced a mix of diploids and tetraploids. UC143 and UC149 (A. prunifolia, 3×) produced all triploid offspring, whereas all other triploid accessions produced offspring with variable ploidy levels including 2×, 3×, 4×, and 5×. Pentaploid Aronia has not been previously reported. Diploid accessions produced significant AFLP genetic variation (0.68–0.78 Jaccard’s similarity coefficient) in progeny, which is indicative of sexual reproduction. Seedlings from tetraploid accessions had very little AFLP genetic variation (0.93–0.98 Jaccard’s similarity coefficient) in comparison with their maternal accession. The very limited genetic variation suggests the occurrence of limited diplosporous apomixis with one round of meiotic division in tetraploid progeny. Triploid accessions appear to reproduce sexually or apomictically, or both, depending on the individual. These results support our understanding of Aronia reproductive mechanisms and will help guide future breeding efforts of polyploid Aronia species.

Abstract

The genus Aronia Medik., also known as chokeberry, is a group of deciduous shrubs in the Rosaceae family, subtribe Pyrinae. The four commonly accepted species include A. arbutifolia (L.) Pers., red chokeberry; A. melanocarpa (Michx.) Elliott, black chokeberry; A. prunifolia (Marshall) Reheder, purple chokeberry; and A. mitschurinii (A.K. Skvortsov & Maitul). Wild and domesticated Aronia species are found as diploids, triploids, and tetraploids. Genetic improvement of polyploid Aronia genotypes has been limited by suspected apomixis, which may be widespread or distinct to tetraploids. The objectives of this study were to elucidate the reproductive mechanisms of Aronia species and reveal the occurrence of apomixis within the genus and along ploidy lines. Twenty-nine Aronia accessions [five A. melanocarpa (2×), five A. melanocarpa (4×), eight A. prunifolia (3×), four A. prunifolia (4×), six A. arbutifolia (4×), and one A. mitschurinii (4×)] were used in this study. Intra-accession variability was evaluated by growing out progeny from each open-pollinated maternal accession and comparing plant phenotypes, ploidy levels, and amplified fragment length polymorphism (AFLP) marker profiles between the progeny and maternal accession. Progeny of diploid and tetraploid maternal plants had ploidy levels identical to maternal plants, except for UC009 (A. melanocarpa, 2×) which produced a mix of diploids and tetraploids. UC143 and UC149 (A. prunifolia, 3×) produced all triploid offspring, whereas all other triploid accessions produced offspring with variable ploidy levels including 2×, 3×, 4×, and 5×. Pentaploid Aronia has not been previously reported. Diploid accessions produced significant AFLP genetic variation (0.68–0.78 Jaccard’s similarity coefficient) in progeny, which is indicative of sexual reproduction. Seedlings from tetraploid accessions had very little AFLP genetic variation (0.93–0.98 Jaccard’s similarity coefficient) in comparison with their maternal accession. The very limited genetic variation suggests the occurrence of limited diplosporous apomixis with one round of meiotic division in tetraploid progeny. Triploid accessions appear to reproduce sexually or apomictically, or both, depending on the individual. These results support our understanding of Aronia reproductive mechanisms and will help guide future breeding efforts of polyploid Aronia species.

Native to eastern regions in North America, the genus Aronia is a group of deciduous shrubs in the Rosaceae family, subtribe Pyrinae. The Pyrinae subtribe has a base chromosome count of n = 17 (Postman, 2011), and Aronia species are commonly found as diploids (2n = 2x = 34) and tetraploids (2n = 4x = 68) with some occurrence of triploids (Brand, 2010; Hovmalm et al., 2004; Leonard et al., 2013). Polyploidization events in Aronia likely resulted from the fusion of unreduced gametes from the same or different species to produce autopolyploids and allopolyploids, respectively. The three commonly accepted Aronia species include A. arbutifolia (L.) Pers., red chokeberry (tetraploid); A. melanocarpa (Michx.) Elliott, black chokeberry (diploid and tetraploid); and A. prunifolia (Marshall) Reheder, purple chokeberry (triploid and tetraploid). A fourth species of Aronia has been recognized as A. mitschurinii [(A.K. Skvortsov & Maitul) tetraploid], and it is used in commercial fruit production, usually as the cultivars Viking or Nero (Leonard et al., 2013). However, genetic marker and phenotypic data suggest that nearly all A. mitschurinii cultivars, an intergeneric hybrid involving A. melanocarpa × Sorbus aucuparia L. (Leonard et al., 2013; Skvortsov and Mautulina, 1982), are genetically identical and likely renames of a single genotype (J.D. Mahoney and M.H. Brand, unpublished data). Interest in Aronia is high because their fruits contain high levels of antioxidants and polyphenols (Brand et al., 2017; Wu et al., 2004; Zheng and Wang, 2003), they are valuable as replacements for invasive exotic ornamental plants (Brand, 2010), and they are widely adapted to various geographic regions (Dirr, 2009; McKay, 2001).

Aronia flowers are thought to be protogynous and self-compatible (Connolly, 2014). Polyploid Aronia species have been reported to reproduce apomictically, via gametophytic apomixis, resulting in embryos that are identical or nearly identical to maternal plants (Brand, 2010). Hovmalm et al. (2004) reported that diploid A. melanocarpa produced highly heterogeneous offspring and tetraploid plants produced homogeneous offspring, suggesting that polyploid Aronia reproduce apomictically. Gametophytic apomixis occurs when a progenitor cell in the megasporangium forms a megagametophyte (Grossniklaus et al., 2001; Richards, 2003). Gametophytic apomixis is further classified into two categories: diplospory and apospory. In diplosporous apomictic plants, the megagametophyte forms from an unreduced or partially reduced megaspore. When a partially reduced megaspore is involved, meiosis is initiated but fails before completion and cell division continues mitotically (Bicknell and Koltunow, 2004). The result is an unreduced megagametophyte derived from a megaspore in which homologous recombination and one round of segregation may have occurred. Apospory refers to an unreduced megagametophyte arising from nucellar or integument tissue (Koltunow and Grossniklaus, 2003). Talent (2009) mentions that pseudogamous gametophytic apospory is common in the Maloid Rosaceae (Pyrinae), where seed development requires pollination, but the embryo has no paternal inheritance and only the endosperm is fertilized. Both diplospory and apospory have been reported to occur in the same species, including the Pyrinae genera Crataegus (Muniyamma and Phipps, 1979, 1984a, 1984b) and Sorbus (Jankun and Kovanda, 1988).

In normal sexual reproduction, genetic uniformity and hybrid vigor are lost after the F1 generation, but with apomixis these traits can be maintained through many generations due to a fixed heterozygosity (Koltunow et al., 1995; Ortiz et al., 2013; Richards 2003). For this reason, seed propagation of apomictic selections is possible and allows growers to achieve high yields while avoiding more expensive vegetative propagation methods (Barcaccia and Albertini 2013). In apomictic temperate fruit crops, it is advantageous to use vegetative propagation from mature phase plants rather than regenerate from juvenile seed. Aronia requires 3 to 5 years before reaching the mature phase for flowering to occur, so use of apomictic seeds delays fruit production. However, Mahoney et al. (2018) report that cotyledons have a greater shoot regeneration rate than mature phase leaf explants; therefore, it may be advantageous to use apomictic seed tissue (i.e., cotyledons) for genetic transformation of Aronia. Although apomixis can be an advantage, it also can present challenges to controlled breeding and genetic exchange. For example, genetic improvement of polyploid Aronia genotypes has been hindered by the occurrence of apomixis during attempted crosses.

A number of molecular marker techniques such as random amplified polymorphic DNA (RAPD), intersimple sequence repeat, and cpDNA marker analysis have been popular in identifying apomixis in plants (Arnholdt-Schmitt, 2000; Hovmalm et al., 2004; Ludwig et al., 2013; Robertson et al., 2010; Smolik et al., 2011). AFLP analysis often has been preferred over other molecular methods for its efficiency (Leonard et al., 2013; Lubell et al., 2008; Obae and Brand, 2013). The AFLP technique has proven to be a more cost-effective way of producing a large number of markers (Mueller and Wolfenbarger, 1999). In this study, we use AFLP, in conjunction with ploidy analysis and plant phenotype, to elucidate the reproductive mechanisms of Aronia species and reveal the occurrence of apomixis within the genus and among ploidy levels.

Materials and Methods

Plant material.

Twenty-nine Aronia accessions [five A. melanocarpa (2×), five A. melanocarpa (4×), eight A. prunifolia (3×), six A. prunifolia (4×), four A. arbutifolia (4×), and one A. mitschurinii (4×)] were used in this study as maternal genotypes (Table 1). Plants were maintained at the University of Connecticut Research Farm in Storrs, CT. The maternal accessions were grown in a randomized field planting consisting of 120 Aronia accessions (with three replicates) and representing all four species and various ploidy levels. Intra-accession progeny variability was evaluated by growing out seedlings from their open-pollinated maternal accessions. Each maternal plant had the opportunity to be pollinated by any other accession in the field collection. Seeds were collected from a single maternal accession plant of each by cleaning them from the fruits and air drying them before placement in cool, dark storage (13 ± 2 °C, relative humidity 55 ± 5%) until further use. Seeds were cold stratified in moist sand for 90 d in 50-mL conical centrifuge tubes at 5 °C. Stratified seeds were sowed in 32-oz. clear plastic salad trays containing potting medium with a ratio of 5:3:1 screened composted pine bark, sphagnum peatmoss, and sand and placed under cool white fluorescent light (80 μmol·m−2·s−1) at 24 °C. Seedlings were transferred to standard 50-cell plug trays with the same 5:3:1 mix and eventually transferred to 1-gallon pots. Four clonal softwood stem cuttings from A. mitschurinii (4×) were rooted in mid-June and served as a control.

Table 1.

Aronia accessions, species, ploidy, geographic origin, and number of progeny regenerated from each open-pollinated maternal plant.

Table 1.

Phenotypic observations.

Within accessions, maternal plants and 2-year-old progeny were compared for overall plant form or habit, branching structure, leaf shape and size, phyllotaxy, degree of pubescence, and leaf and stem color. Floral and fruit traits were not used due to the juvenile and nonreproductive nature of the plants. Progeny were scored as either homogeneous or heterogeneous in comparison with each other and their maternal parent based on the composite characteristics of each plant. Homogeneity/heterogeneity scores were the combined opinions of five researchers knowledgeable about Aronia.

Flow cytometry.

A modified version of the protocol in Arumuganathan and Earle (1991), summarized in Lehrer et al. (2008), was followed. Two to three newly emerged leaves were macerated using a fresh razor blade in nuclei suspending solution in a 55-mm petri dish on a freeze pack. The suspending solution was filtered, centrifuged to form a nuclei pellet, and resuspended in nuclei staining solution containing propidium iodide. Relative fluorescence of total DNA was measured using a Becton-Dickson FACS Calibur Dual Laser Flow Cytometer (Becton, Dickson and Co., Franklin Lakes, NJ) at the Flow Cytometry and Confocal Imaging Facility at the University of Connecticut in Storrs, CT. The cytometer was equipped with an argon ion laser emitting radiation at 488 nm. For each sample, 10,000 to 20,000 particles were measured. Data were logged and displayed in histograms by BD Cellquest TM software (Becton, Dickson and Co.). Histogram peaks from known ploidy levels of Aronia were compared with samples of unknown ploidy.

DNA extraction and AFLP procedure.

A subset of 20 Aronia accessions [five A. melanocarpa (2×), four A. melanocarpa (4×), three A. prunifolia (3×), four A. prunifolia (4×), three A. arbutifolia (4×), and one A. mitschurinii (4×)] were used for AFLP analysis. Genomic DNA was extracted following the protocol outlined in Leonard et al. (2013). The quality and concentration of extracted DNA were determined using a NanoDrop-1000 spectrophotometer (Thermo Scientific, Willington, DE). The AFLP steps including restriction digestion, adaptor ligation, and preselective and selective amplication reactions were carried out as outlined in the AFLP plant mapping protocol (Anonymous, 2007). Preselective primers had one selective nucleotide (EcoRI-A + MseI-C). Seven primer combinations were used for selective amplification (EcoRI-AGG + MseI-CAC, EcoRI-ACT + MseI-CAC, EcoRI-AGG + MseI-CAT, EcoRI-ACT + MseI-CAT, EcoRI-AGG + MseI-CTC, EcoRI-ACT + MseI-CTA, and EcoRI-ACT + MseI-CTG) and were fluorescently labeled EcoRI and unlabeled MseI probes. The DNA fragments from selective polymerase chain reaction were visualized by capillary electrophoresis on an ABI3730xl DNA analyzer (Applied Biosystems, Foster City, CA) using the 500 LIZ® Size Standard (Thermo Fisher Scientific, Waltham, MA).

AFLP data analysis.

AFLP fragment files were processed into binary matrices using GeneMarker Version 1.95 software (SoftGenetics, State College, PA). Peaks were first scored with a 1 for present and 0 for absent, using automatic settings followed by visual inspection and manual adjustment of each peak to ensure accurate scoring. Jaccard’s similarity coefficients were calculated using the vegan (Oksanen et al., 2017) package in R.

Results

Phenotypic observations.

All diploid maternal A. melanocarpa accessions produced progeny that were heterogeneous in appearance (Table 2; Fig. 1). Progeny from diploids exhibited plant habits that would range from very upright and narrow plants to nearly prostrate plants. Progeny from diploids also differed in plant height, plant width, and branch density. Other common phenotypic differences among progeny from diploids included changes in leaf size and shape.

Table 2.

Ploidy level and phenotypic observations of open-pollinated progeny, from maternal accessions of Aronia arbutifolia, A. melanocarpa, A. prunifolia, and A. mitschurinii with varying ploidy levels.

Table 2.
Fig. 1.
Fig. 1.

Phenotypic characteristics of seedlings grown from various maternal plants of Aronia arbutifolia (4×), A. melanocarpa (2×), A. melanocarpa (4×), A. mitschurinii (4×), A. prunifolia (3×), and A. prunifolia (4×). Progeny exhibited either phenotypic homogeneity, which is consistent with apomixis, or heterogeneity, which is consistent with sexual reproduction.

Citation: HortScience horts 54, 4; 10.21273/HORTSCI13772-18

Progeny from tetraploid plants, whether they were from A. melanocarpa, A. prunifolia, A. arbutifolia, or A. mitschurinii maternal plants, exhibited morphological uniformity (Table 2; Fig. 1). Within accessions, progeny were phenotypically similar to each other and to their maternal parent. The morphological uniformity exhibited by progeny from tetraploids was on par with that observed in clonal populations propagated by cuttings. One exception was PI545682, where nine of the 10 progeny were homogeneous, but one pentaploid seedling exhibited distinct morphology.

The majority of triploid A. prunifolia accessions produced progeny that exhibited heterogeneous phenotypes (Table 2). UC143 and UC149 were exceptions and produced progeny with homogeneous phenotypes. In addition, eight of the 10 progeny from UC011 were phenotypically indistinguishable, but two seedlings exhibiting distinct phenotypes were shown by flow cytometry to be pentaploids (Table 2).

Ploidy level.

Diploid accessions of A. melanocarpa produced diploid progeny with the single exception of accession UC009 (Table 2). Accession UC009 produced mostly diploid seedlings but also produced two tetraploid seedlings.

Triploid A. prunifolia accessions UC143 and UC149 produced only triploid progeny and UC011 produced mostly triploid progeny (Table 2). UC011 also produced two pentaploid plants sharing a distinct phenotype. Triploid A. prunifolia accessions UC141, UC145, and UC146 produced a mix of ploidy levels within their progeny, including 2×, 3×, 4×, and 5× plants. The triploids UC150 and UC156 produced seedlings at the 2×, 4×, and 5× ploidy levels but did not produce 3× seedlings. The relatively small progeny sample size may be responsible for the absence of 3× plants, or these accessions may not produce 3× progeny.

Tetraploid accessions, whether they were A. melanocarpa, A. prunifolia, A. arbutifolia, or A. mitschurinii, only produced tetraploid progeny (Table 2). The single exception was one pentaploid seedling that was produced by the tetraploid A. melanocarpa accession PI545682.

AFLP.

Seedlings from diploid accessions produced a significant amount of intra-accession genetic variation in progeny (Jaccard’s similarity coefficient of 0.64 to 0.82), which was indicative of sexual reproduction (Fig. 2). These sets of progeny from diploid maternal plants also exhibited variable phenotypes that corroborate sexual seed production within this taxonomic group.

Fig. 2.
Fig. 2.

Jaccard’s similarity coefficients for Aronia progeny compared with their maternal accessions. Bars represent se.

Citation: HortScience horts 54, 4; 10.21273/HORTSCI13772-18

Maternal triploid plants that produced heterozygous phenotypes in their progeny, such as UC141 and UC150, also showed significant intra-accession genetic variation (Jaccard’s similarity coefficient of 0.65 to 0.80), providing support for sexual seed development in these accessions (Fig. 2). In contrast, maternal triploid plants that produced phenotypically homogeneous progeny, such as UC143, showed very little intra-accession genetic variation (Jaccard’s similarity coefficient of 0.90 to 0.99).

Seedlings from tetraploid accessions of A. melanocarpa, A. prunifolia, A. arbutifolia, and A. mitschurinii all exhibited small amounts of intra-accession genetic variation (Jaccard’s similarity coefficient of 0.89 to 0.98) (Fig. 2). These tetraploid accessions also displayed homogeneous phenotypes. In contrast, clonally propagated plants of UC003 (A. mitschurinii, 4×) propagated by cuttings produced AFLP profiles that were identical to the stock plant (Jaccard’s similarity coefficient of 1.00).

Discussion

In this study, we found very limited genetic and phenotypic variation in most polyploid offspring, providing strong evidence of diplosporus apomixis. Diploid and several triploid accessions produced significant variation in offspring, demonstrating that seed reproduction occurred sexually. In diplosporous apomicts, the small amount of genetic recombination that occurs during seed formation may produce phenotypic variability in progeny only after many generations (Campbell and Dickinson, 1990). For example, morphological variation has been detected in offspring of heavily cultivated apomictic lineages of Taraxacum (Sorensen and Gudjonsson, 1946 cited by Baarlen et al., 2000). However, it would require a significant amount of time to observe this variation in temperate shrubs because of their generation times.

There are several explanations for the variation in ploidy levels we observed in diploid and triploid Aronia progeny. As mentioned previously, the Aronia maternal accessions were planted in a randomized field design, which allowed open-pollination to occur and potential outcrossing between different species and ploidy levels. UC009 (A. melanocarpa, 2×) produced eight diploid offspring but also produced two tetraploid offspring that could have been either self-fertilized with an unreduced 2n gamete or out-crossed with a reduced 2n gamete from a tetraploid Aronia spp. Similarly, UC141, UC145, UC146, UC150, and UC156 (A. prunifolia, 3×) produced variable ploidy levels in their offspring (diploids, triploids, tetraploids, and pentaploids). This suggests that the megagametophyte was reduced, partially reduced, or unreduced and then self-fertilized or out-crossed with reduced or unreduced paternal gametes from diploids, triploids or tetraploids.

In this study, we focused our analysis on within intra-accession variability, whereas other studies have looked at within- and among-population variability. Hovmalm et al. (2004) evaluated eight native populations of Aronia for genetic variation and ploidy. They that found populations that had high within-population diversity and high among-population similarity were all diploid, whereas tetraploid populations tended to have lower within-population diversity and significantly greater among-population diversity. This suggests that tetraploid populations were restricted in outcrossing with other populations because of their apomictic reproductive mechanisms. We found tetraploid and several triploid Aronia accessions to have a high genetic similarity to their maternal accession, which provides additional evidence to support apomictic seed reproduction in tetraploid and at least some triploid Aronia. Since Aronia apomicts reproduce through pseudogamy, fusion of the polar nuclei with one of the sperm nuclei may produce endosperm that contains some paternal inheritance. The sexually reproducing accessions in this study produced a wide range of Jaccard’s similarity coefficients from 0.64 to 0.82, which suggests that progeny from these accessions were the outcome of outcrossing or selfing.

Sources of genetic variation during meiosis include homologous recombination of chromosomes (crossing over) and random separation of homologous chromosomes. Homologous recombination, which takes place during prophase I, involves the exchange of genes between nonsister chromatids. The process of diplospory involves the apomeiotic formation of an unreduced female gametophyte from an apomictic initial cell, which will either omit or abort meiosis (Schmidt et al., 2015). During meiotic restitution, homologous recombination still takes place, creating a limited amount of genetic variation, which may explain the AFLP variation we observed in the polyploid apomictic offspring. In this study, we found that tetraploid and several triploid Aronia produced progeny with high Jaccard’s similarity coefficients of 0.89 to 0.98, which was indicative of apomictic diplospory. These similarity coefficients are significantly greater than the 0.64 to 0.82 we observed for diploid, sexually reproducing Aronia. In a study similar to ours with apomictic Cotoneaster, Bartish et al. (2001) reported some differences between RAPD marker profiles within progeny populations grown out from three maternal accessions and found Jaccard’s similarity coefficient of 0.97, 0.98, and 1.00. When comparing RAPD similarity coefficients for plants from different accessions, but still belonging to the same taxon, they obtained values of 0.77, suggesting sexual reproduction. Bartish et al. (2001) describe the very small marker differences as “in most likelihood, artefactual…” or derived from somatic mutations. An alternative explanation is that the similarity values are the result of diplospory and apospory apomixis occurring in the same species. Both forms of apomixis have been reported to occur within the same species of a closely related genus, Crataegus (Muniyamma and Phipps, 1979, 1984a, 1984b). In our study, we included vegetatively propagated material as a control to check for error. We did not find any genetic differences between clonal vegetative cuttings, providing evidence that AFLP markers were reliable and that the genetic differences we detected were a product of diplosporous apomixis.

The combination of homogeneous phenotypes and small amounts of genetic variation suggests that tetraploid and some triploid Aronia species produced seed through gametophytic diplosporous apomixis with one round of meiosis occurring. In contrast, heterogenous phenotypes and large amounts of genetic variation suggest that diploid and some triploid accessions reproduce sexually. Aronia has the potential to be a valuable study system because of its relatively short juvenile phase, compared with other temperate fruit crops, along with the ability to develop autotetraploids via somatic doubling from diploid material. This would allow for further investigation into the genetic mechanisms involved with sexual and apomictic reproduction in Aronia using nearly isogenic diploid and tetraploid genotypes, respectively. Furthermore, our results will enhance and guide future breeding efforts for genetic improvement of polyploid Aronia.

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  • Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.M., Szoecs, E. & Wagner, H. 2017 vegan: Community Ecology Package. R package version 2.5-2. 2 July 2018. <https://CRAN.R-project.org/package=vegan>

  • Ortiz, J.P.A., Quarin, C.L., Pessino, S.C., Acuña, C., Martínez, E.J., Espinoza, F., Hojsgaard, D., Sartor, M.E., Cáceres, M.E. & Pupilli, F. 2013 Harnessing apomictic reproduction in grasses: What we have learned from Paspalum Ann. Bot. 112 767 787

    • Search Google Scholar
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  • Postman, J. 2011 Intergeneric hybrids in Pyrinae Acta Hort. 918 937 943

  • Richards, A.J. 2003 Apomixis in flowering plants: An overview Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 1085 1093

  • Robertson, A., Rich, T., Allen, A., Houston, L., Roberts, C., Bridle, J., Harris, S. & Hiscock, S. 2010 Hybridization and polyploidy as drivers of continuing evolution and speciation in Sorbus Mol. Ecol. 19 1675– 1690

    • Search Google Scholar
    • Export Citation
  • Schmidt, A., Schmid, M.W. & Grossniklaus, U. 2015 Plant germline formation: Common concepts and developmental flexibility in sexual and asexual reproduction Development 142 229 241

    • Search Google Scholar
    • Export Citation
  • Skvortsov, A.K. & Mautulina, Y.K. 1982 On the differences between the cultivated chokeberry and its wild progenitors Bull. Central Botanical Garden 126 35 40

    • Search Google Scholar
    • Export Citation
  • Smolik, M., Ochimian, I. & Smolik, B. 2011 RAPD and ISSR methods used for fingerprinting selected, closely related cultivars of Aronia melanocarpa Not. Bot. Horti Agrobo. 39 276 284

    • Search Google Scholar
    • Export Citation
  • Talent, N. 2009 Evolution of gametophytic apomixis in flowering plants: An alternative model from Maloid Rosaceae Theory Biosci. 128 121 138

  • Wu, X., Gu, L., Prior, R.L. & McKay, S. 2004 Characterization of anthocyanins and proanthocyanidins in some cultivars of Ribes, Aronia, and Sambucus and their antioxidant capacity J. Agr. Food Chem. 52 7846 7856

    • Search Google Scholar
    • Export Citation
  • Zheng, W. & Wang, S.Y. 2003 Oxygen radical absorbing capacity of phenolics in blueberries, cranberries, chokeberries, and lingonberries J. Agr. Food Chem. 51 502 509

    • Search Google Scholar
    • Export Citation

Contributor Notes

This research was partially supported by the U.S. Department of Agriculture Multistate Hatch NC007 Plant Germplasm and Information Management and Utilization.

Corresponding author. E-mail: mark.brand@uconn.edu.

  • View in gallery

    Phenotypic characteristics of seedlings grown from various maternal plants of Aronia arbutifolia (4×), A. melanocarpa (2×), A. melanocarpa (4×), A. mitschurinii (4×), A. prunifolia (3×), and A. prunifolia (4×). Progeny exhibited either phenotypic homogeneity, which is consistent with apomixis, or heterogeneity, which is consistent with sexual reproduction.

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    Jaccard’s similarity coefficients for Aronia progeny compared with their maternal accessions. Bars represent se.

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  • Ortiz, J.P.A., Quarin, C.L., Pessino, S.C., Acuña, C., Martínez, E.J., Espinoza, F., Hojsgaard, D., Sartor, M.E., Cáceres, M.E. & Pupilli, F. 2013 Harnessing apomictic reproduction in grasses: What we have learned from Paspalum Ann. Bot. 112 767 787

    • Search Google Scholar
    • Export Citation
  • Postman, J. 2011 Intergeneric hybrids in Pyrinae Acta Hort. 918 937 943

  • Richards, A.J. 2003 Apomixis in flowering plants: An overview Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 1085 1093

  • Robertson, A., Rich, T., Allen, A., Houston, L., Roberts, C., Bridle, J., Harris, S. & Hiscock, S. 2010 Hybridization and polyploidy as drivers of continuing evolution and speciation in Sorbus Mol. Ecol. 19 1675– 1690

    • Search Google Scholar
    • Export Citation
  • Schmidt, A., Schmid, M.W. & Grossniklaus, U. 2015 Plant germline formation: Common concepts and developmental flexibility in sexual and asexual reproduction Development 142 229 241

    • Search Google Scholar
    • Export Citation
  • Skvortsov, A.K. & Mautulina, Y.K. 1982 On the differences between the cultivated chokeberry and its wild progenitors Bull. Central Botanical Garden 126 35 40

    • Search Google Scholar
    • Export Citation
  • Smolik, M., Ochimian, I. & Smolik, B. 2011 RAPD and ISSR methods used for fingerprinting selected, closely related cultivars of Aronia melanocarpa Not. Bot. Horti Agrobo. 39 276 284

    • Search Google Scholar
    • Export Citation
  • Talent, N. 2009 Evolution of gametophytic apomixis in flowering plants: An alternative model from Maloid Rosaceae Theory Biosci. 128 121 138

  • Wu, X., Gu, L., Prior, R.L. & McKay, S. 2004 Characterization of anthocyanins and proanthocyanidins in some cultivars of Ribes, Aronia, and Sambucus and their antioxidant capacity J. Agr. Food Chem. 52 7846 7856

    • Search Google Scholar
    • Export Citation
  • Zheng, W. & Wang, S.Y. 2003 Oxygen radical absorbing capacity of phenolics in blueberries, cranberries, chokeberries, and lingonberries J. Agr. Food Chem. 51 502 509

    • Search Google Scholar
    • Export Citation
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