Next Article in Journal
Terroir Traceability in Grapes, Musts and Gewürztraminer Wines from the South Tyrol Wine Region
Next Article in Special Issue
Seed Germination and Seedling Growth of Yellow and Purple Passion Fruit Genotypes Cultivated in Ecuador
Previous Article in Journal
Grape and Grape-Based Product Polyphenols: A Systematic Review of Health Properties, Bioavailability, and Gut Microbiota Interactions
Previous Article in Special Issue
Seed Maturity and Its In Vitro Initiation of Chilean Endemic Geophyte Alstroemeriapelegrina L.
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 8
Issue 7
10.3390/horticulturae8070585
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Seed Traits Associated with Dormancy and Germination of Herbaceous Peonies, Focusing on Species Native in Serbia and China

by
Tatjana Marković
1,*,
Željana Prijić
1,
Jingqi Xue
2,
Xiuxin Zhang
2,
Dragoja Radanović
1,
Xiuxia Ren
2,
Vladimir Filipović
1,
Milan Lukić
1 and
Stefan Gordanić
1
1
Institute for Medicinal Plants Research “dr Josif Pančić” Belgrade, Tadeuša Košćuška 1, 11000 Belgrade, Serbia
2
Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry Agriculture and Rural Affairs, Beijing 100081, China
*
Author to whom correspondence should be addressed.
Horticulturae 2022, 8(7), 585; https://doi.org/10.3390/horticulturae8070585
Submission received: 9 May 2022 / Revised: 24 June 2022 / Accepted: 27 June 2022 / Published: 28 June 2022
(This article belongs to the Collection Seed Dormancy and Germination of Horticultural Plants)
Browse Figures
Versions Notes

Abstract

:
Even though peonies are highly valued as ornamental, medicinal, and edible species and are also considered to be long-lived and relatively disease and pest resistant, they are becoming rare or endangered in their natural habitats. This could be primarily associated with climate change and unsustainable wild collecting practices. So far, in situ conservation efforts have received little attention. In addition, very little is known about the cultivation of herbaceous peonies, particularly their propagation from seeds. What is known is that their seeds possess double dormancy, often accompanied by a low germination rate, which, together, make the cultivation of herbaceous peonies more difficult. Based on a comprehensive analysis of relevant literature, this paper summarizes, analyzes, and discusses all available studies on the seed traits of herbaceous peonies associated with the effect of seed harvest time on dormancy and seed germination, with a strong focus on dormancy breaking procedures. Improving our understanding of dormancy release modalities (impacts of temperature, moisture, light, hormones, various pre-treatments, etc.) will aid the establishment and management of in situ and ex situ collections of valuable species of herbaceous peonies and enable further studies for their successful propagation, breeding, and cultivation.

1. Introduction

Herbaceous peonies are species with high ornamental [1,2], edible [3,4,5], medicinal [6,7], economic, and ecological values [8]. Apart from their valuable roots and flowers, which contain various biologically active substances [9], their seeds also attract the attention of scientists. The seeds are around 25% oil, which is rich in various unsaturated fatty acids, amino acids, and mineral elements [10,11,12]. The oil also has biologically active constituents that have several proven beneficial effects (antioxidant, anti-ageing, anti-UV and sunscreen, anti-tumour, etc.) [13]. About 30% of the dry seed weight is account for by the seed shell, which is the main co-product in peony seed oil production [14,15,16]. It contains cellulose, lignin, monoterpene glycosides, and crude protein and also has been proved to have several biological properties (strong antioxidant, antibacterial, anti-tumor, etc.) [17].
Herbaceous peonies represent the plant genus with the longest history of all flowering plants, Paeonia L. [8,18]. It is the only genus of the Paeoniaceae family and comprises about 34 species native to the northern hemisphere [19,20]. The genus is commonly divided into three sections [21,22], as presented in Figure 1, although recent study suggests reclassifying the subgenus Moutan, which includes only woody species, and the subgenus Paeonia, which includes only herbaceous species [23].
All five herbaceous species native to Serbia [24,25] are rare and endangered, with the exception of the Pannonian peony (P. banatica), which is endemic, relict, and strictly protected and is, thus, listed in the Red Book of the Flora of Serbia [26,27]. Among the eight herbaceous species native to China, only the White peony (P. sterniana) is recorded in the List of National Protected Wild Plants of China as a Class II rare species [28].
Although peonies are generally characterized as long-lived and relatively disease- and pest-resistant plants [29], in many cases they are becoming rare or endangered in their natural habitats. This can mainly be attributed to climate change and/or reckless human activity [30,31], although there could be several other reasons which contribute, such as loss of habitat, inadequate nature protection policies, susceptibility to diseases, etc. [12,31,32].
The loss of species is a risk associated with vegetation succession [32]. Apart from unsustainable wild collecting practice [33], the trade of wild herbaceous peonies and their seeds is becoming increasingly popular [34]. In the last two decades, climate change has resulted in an increase in temperature, especially during the winter period, which has impacted the timing and success of germination [35] and/or increased the incidence of abnormal seedlings [36]. Plants which are not able to adapt to climate changes or shift to northern areas and/or to higher altitudes are lost from the population, making the species rare or endangered [34,35].
Herbaceous peonies spontaneously grow and thrive in temperate and cold climates [8] and produce seeds that are double dormant as a key protection mechanism [31]. To survive, plants depend on the ability to cope with changing environmental conditions. Of the different strategies that have evolved in this respect, dormancy is a widely distributed one. Double dormancy is a combination of the seed coat (external) and internal dormancy. Peony seeds require temperature variations to progress through the many stages of the germination cycle [37], and if they are not adequate, the survival of the entire peony population in its natural habitat is jeopardized.
Even more concerning is the low rate of peony seed dispersal in nature [12,38]. The seeds mature slowly, ripen in late summer, and disperse in autumn [39]. The spatial grouping of seedlings near maternal plants indicates that their dispersal is spatially limited, as confirmed in an investigation conducted in France [40]. The spatial aggregation of wild-growing seedlings of P. officinalis ssp. macrocarpa, their significantly greater abundance down the slope of flowering plants, and a small number of seedlings observed at distances > 1.5 m from flowering individuals all pointed to the conclusion that the species is primarily barochorous [40]. The data also suggest that long-distance dispersal in P. officinalis is extremely rare and that poor seed dispersal may limit colonization of the species at favorable sites [40].
Herbaceous peonies are generally considered self-fertile, meaning that, when isolated, their flowers self-pollinate, and their seeds produce offspring that are a genetic match to the parent plant (for the appearance of herbaceous peony flowers, see the Figure S1 in the supplementary material). In the case of P. lactiflora, isolated self-pollination result in the lowest seed-setting rate of all other pollination models (natural pollination, hand cross-pollination, hand self-pollination, and natural cross-pollination) [41]. In addition, it was also reported that the pollination process in herbaceous peony species P. lactiflora [41] and P. officinalis [40] also requires insects or wind-mediated assistance.
Cultivating herbaceous peonies species is one of the most important strategies for preserving them. However, only a few studies have been conducted so far on the proper agronomic practices and conditions for their cultivation, particularly for propagation by seeds [42,43,44,45]. Such low interest could be attributed to the very slow germination procedure, which, in various natural conditions, can take up to 24 months [46].
The major goal of this review was to present up-to-date knowledge on the dormancy and seed germination of 13 herbaceous peony species native to Serbia and China, as this knowledge can contribute to the protection of their natural genetic resources and provide basic guidelines for their successful cultivation. Given the scarcity of literature on the seeds of the examined species, information that is currently available on seeds of other herbaceous peony species from the subsection Paeoniae is included in this review. This might aid researchers to narrow the field of the unknown and guide them to move towards successful propagation of these precious plant species by seeds.

2. Seed Properties

2.1. Physical and Morphological Properties

Despite the fact that morphological distinctions between the seeds of herbaceous peonies do exist (as evidenced by the literature data presented in Table 1 and supported by the seed images presented in Figure 2), it appears that they have been almost neglected in the systematics of the section Paeoniae [47].
Figure 2 shows images of the seeds of all herbaceous peony species native to Serbia and China with the exception of P. officinalis.
Species of herbaceous peonies differ in the number, size, and shape of their seed follicles which, in turn, affect the number and size of seeds [38,46]. They also differ in seed shape and in colour of testa, which is caused by the oxidation of various polyphenolic compounds in its palisade layers during maturation. The color of the seed testa in ripe seeds can range from brown to dark (Figure 2) and, in most cases, is smooth [46,52]. In addition, the seed size also depends on the locality, plant position at the locality, and year [43]. Given that the seeds of herbaceous peonies are large and dark and are not preferential rodent food (chipmunks, mice, etc.), their natural dissemination is thought to be rather low and close to the maternal plants [40,53]. On the other hand, due to their size and mass, they are less dependent on light to germinate [53] and, in harsh environmental conditions, are capable of providing enough energy to ensure survival of the species [31].

2.2. Seed Collection Period

Peony seed maturation is a complex process that includes numerous physiological and biochemical alterations [1]. In herbaceous peonies, it is considered very slow [39]. For instance, the entire development of P. lactiflora ‘Hangshao’ seeds lasts about 85–90 days [39,54], during which physiological maturation occurs between the 70th and 75th day following flowering [54]. The seeds of herbaceous peonies ripen in summer and disperse in autumn [39]. Depending on species, locality (altitude, shading, etc.), and year, the seed harvest time ranges from July to the end of October (Table 1); P. tenuifolia, P. cambessdesii, and P. veitchii mature earlier, whereas P. peregrina, P. banatica, P. mascula, P. officinalis, P. sinjiangensis, P. anomala, P. emodi, P. obovata, and P. sterniana mature a bit later. However, the optimum time to collect the seeds is when the follicle begins to open and the seed testa starts to darken [37,39]. The optimum time for collecting seeds is important as it significantly affects germination. If the seeds are collected too early, they do not reach maturity and are not fertile [37], while if they are collected too late, their coat hardens and this reduces germination [37,39]. To date, there is currently no data within the literature regarding the germination rate of seeds collected after maturation has peaked; however, it can only be assumed that it would decline, as was the case with the seeds of some tree peonies [55]. When the seeds are collected at the optimum time, the rate of germination can be as high as 90%, as already confirmed in the case of P. lactiflora [52].

2.3. Seed Dormancy

Seed dormancy is an important adaptational trait of higher plant species. It prevents seeds from germination during unfavorable ecological conditions (temperature, humidity, light, rainfall, drought, heat waves, etc.) or incidents (fire, etc.) [56]. Optimal dormancy release conditions are defined as those in which high-quality plants are produced in a short period of time [57].
Indicating its great diversity and complexity, seed dormancy is classified by the developmental status of its embryo, its water absorption capacity, and the interrelationships of its phytohormones, into many distinct categories [58]. There are two major categories of seed dormancy: exogenous and endogenous. At present, exogenous dormancy includes only physical dormancy, while endogenous dormancy includes several types: (1) morphological, (2) physiological, (3) morpho-physiological, and (4) combinational (physical + physiological). In herbaceous peonies, only two types have been confirmed so far: physical dormancy and morpho-physiological dormancy [36,59,60].
Physical seed dormancy is influenced by environmental stimulus [49] and is enabled by seed coat layer(s) which provide(s) a mechanical barrier for water and gas uptake. Thus, the seed coat is considered a major modulator of interactions between the internal seed structures and the surrounding environment, maintaining the viable status of embryos for a long period of time [36]. The mature seed of P. lactiflora is composed of the seed coat, endosperm, and embryo [52]. Its coat is made of tightly packed palisade cells with gaps between them [61]. If the seeds are exposed to appropriate dormancy breaking conditions, they became water permeable (i.e., a gap in the seed coat opens, and water reaches the embryo). Otherwise, the coat remains hard and impervious to water and gases, making germination difficult unless physically altered [37]. The alteration can be induced by dry, warm stratification or warm-water stratification, either with or without scarification. During warm stratification, the temperature should resemble that of the corresponding natural habitat, which ranges from 20 °C to 25 °C, for 1–3 months, until the radicle reaches sufficient length, which is species specific; for P. lactiflora it is about 3–4 cm [62,63], while, for P. corsica, it is 4 cm [42,54]. In nature, dry, warm stratification for physical dormancy release occurs during summer. For instance, seeds of P. tenuifolia experienced spontaneous, dry, warm stratification after a fire in Russia’s forest-steppe zone (the Khvalynsky National Park), and the post-fire community had a higher recovery and replacement rate with juvenile individuals than the intact environment [64].
The positive effects of laboratory-induced mechanical scarification of the seed coat of P. lactiflora have also been recorded; the germination rate of the seeds scraped and left at 25 °C for 70 days increased by about 50% compared to control [65]. This could be due to the enhanced speed of water uptake caused by the increased permeability of the seed coats [39,66,67] which resulted in increased seed germination [68,69].
In an attempt to understand the mechanism of breaking physical dormancy, scientists found that larger, physically dormant seeds become water permeable earlier than the smaller ones, which explains why they show faster dormancy release [62]. When compared to small seeds, large seeds show high water content and a low ratio between the palisade layer thickness and seed mass. As a result, the barrier in large seeds can be broken earlier, and, thus, they germinate faster [62]. This shows that the physical mechanism for breaking dormancy is far more complex than just the retraction and expansion of the seed coat and should be researched further for the seeds of herbaceous peonies.
Morpho-physiological seed dormancy is a combination of physiological and morphological dormancy. Morphological dormancy is present in seeds, the embryos of which are not fully developed (undifferentiated embryos) at seed dispersal. Prior to germination, the embryo within the seed has to be fully developed [58]. When it fills more than half of the seed, the embryo can continue to expand, but the radicle emerges only if the environmental conditions are favorable [36]. Such conditions are species specific and may vary even among varieties of the same peony species [37]. On the other hand, physiological dormancy is caused by the physiological state of the embryo [70]. It prevents embryo growth and further germination until chemical changes occur. Seeds may have one of the following seed dormancy levels: deep, intermediate, or non-deep [36,59,60]. According to the literature [71,72], ≥90% of physiologically dormant seeds in the world are characterized by a non-deep dormancy level, accounting for about 41% of all species. However, herbaceous peonies are not among them.
For seeds with morpho-physiological dormancy, it is believed that they cannot germinate unless their embryo elongates enough and morphologically develops inside the seed (which is expressed through the embryo-to-seed ratio), as well as overcomes any physiological limitations [36]. For herbaceous peonies, there are no data on the critical embryo:seed ratio, except for in the case of P. corsica (Sieber) ex. Tausch (syn. P. mascula ssp. russoi), which is 0.58 ± 0.09 [42]. Research on seed dormancy in herbaceous peonies revealed that the seeds of P. officinalis have an intermediate, simple dormancy [65], which means that, following the embryos’ full development, further dormancy release treatment is required. On the other hand, it confirmed that the seeds of P. corsica [42], P. tenuifolia, P. caucasica [62], P. veitchii [31], P. lactiflora [73,74], P. intermedia, and P. anomala [75] have deep, simple, epicotyl morpho-physiological dormancy. This indicates that, although the growth of an underdeveloped embryo in the seed begins in the I (warm) phase of dormancy release, it also continues into the II phase, in which seed exposure to cold is essential for full embryo development [58]. In natural habitats, after a warm dormancy breaking period, the seeds of peony species with deep, simple, epicotyl morpho-physiological dormancy do not emerge until the next season. In other words, the peony shoots do not emerge until the second spring unless the roots do not pass cold stratification, which happens during winter [58]. The peony seeds are sensitive to cold stratification only after the radicle length exceeds 3 cm; for P. lactiflora, the critical length is between 3 and 4 cm [63,64], while, for P. corsica, it is 4 cm [42]. If the low temperatures are missing, the radicle can grow further, but the epicotyl cannot extend the seed coat [76]. It is still unclear how the radicle length affects epicotyl dormancy release, but it is suggested that it probably depends on the content of hormones in the epicotyl of the seed from which the radicle emerged [39].

3. Seed Germination

Seed germination is the result of the equilibrium between the degree of dormancy and the ability of the embryo to overcome it [77]. Almost all herbaceous peonies experience hypogeal seed germination, where the epicotyl elongates and the cotyledons remain below the soil [46]. However, P. tenuifolia experiences epigeal germination, in which the hypocotyl rapidly elongates, pulling the cotyledon above the ground [78].
At seed maturity, the embryo in herbaceous peonies is differentiated but underdeveloped (rudimentary), so it must grow inside the seed until the radicle develops [36]. Fresh peony seeds are recommended for the best germination results as they germinate faster and do not require any pre-soaking treatment before planting [45]. Although germination of perennial species P. corsica started one week after seed collection [42], the rate of germination observed after 100 days was still less than 10%. One of the possible reasons for such a low germination capacity is the low activity of the peroxidase enzyme [8]. A seed can also maintain its high viability if stored for 1–2 years in a ventilated, non-soil, sterile, wet place with up to 10% moisture, either at a temperature that corresponds to its natural habitat [37] or in a refrigerator (4–6 °C) covered with wet moss [45] or sand [31]. Moisture content is one of the most important factors affecting seed viability, especially after long-term seed conservation such as cryopreservation. In the case of P. emodi, 8.77% of the seed moisture was suggested [79].
To the best of our knowledge, there are no published data on the effect of seed moisture on the germination of herbaceous peonies. A pre-soaking seed treatment is required if the seeds are air-stored or dry or if the content of germination inhibiting substances needs to be reduced. Imbibition initiates the germination process as it activates the seed respiratory metabolism, as well as transcriptional and translational activities [79]. The European Peony Society suggests soaking the seeds of herbaceous peonies at room temperature in sterile water for 3–4 days [78], whereas other authors suggest up to 7 days [39]. In particular, pre-soaking seed treatment for P. tenuifolia should last no more than one day [78] and two days for P. emodi [45] and P. lactiflora [76]. In any case, the seed absorption rate should be in the “slow–fast–slow” order [76].
Peonies have a long germination period in general. Germination of P. lactiflora seeds takes 6–7 months in controlled, optimal conditions [76], whereas, in the natural environment, it takes 8–9 months, with low seedling survival [66]. Wild peonies in Russia require 10–16 months [8], which can be extended to 2 years if the environmental conditions are harsh [77].

4. Pre-Treatments for Dormancy Release Process

4.1. Temperature

Peonies have adapted to the temperate zones of the northern hemisphere [31]. Their adaptation to the climatic cycle resulted in the development of unique growth patterns that allow them to avoid unfavorable periods and resume plant growth during favorable ones. As a result, their temperature requirements vary not only between different species but also among their varieties. In addition, peonies from warmer regions require a lower sum of temperatures to break dormancy than those from colder ones; hence, their adaptation is linked to their natural habitats.
The dormancy of peony species is temperature dependent [42]. So far, it has been tested in several herbaceous species. During warm stratification, the temperature should resemble that of the corresponding natural habitat (20 °C–25 °C) for 1–3 months until the radicle reaches sufficient length, which is species specific; for P. lactiflora it is about 3–4 cm [49,50], while, for P. corsica, it is 4 cm [42,54].
P. veitchii seeds require two months of warm stratification (15–20 °C) for embryo development, followed by three months of cold stratification (0–10 °C) for epicotyl growth [31]; P. corsica seeds require three months of warm stratification (25 °C) for embryo development, followed by two months of cold stratification (5 °C) for epicotyl growth [42]; and P. lactifora needs four months at 15 °C [80] or one month at 25 °C [39] of warm stratification for embryo development and another three months of cold stratification (4 °C) for epicotyl growth [80]. For P. tenuifolia, the EU Peony Society has no precise data but states that its seeds require cool but not very low temperatures to germinate [81].

4.2. Light

The majority of herbaceous peony species experience hypogeal seed germination [46,51], which means that the germinating seeds’ cotyledons remains below ground (i.e., is non-photosynthetic). Although the seeds germinate spontaneously in the dark [31,47], it is unknown whether and how light and its quality affect their dormancy release.
The application of red light had a positive effect on hypocotyl dormancy release as a dark condition on tree peony, whereas blue LEDs had a positive effect on epicotyl dormancy release [78].
In fact, dormancy in peonies is a self-contained process that is unaffected by photoperiod, regardless of whether the species is herbaceous or woody [82].

4.3. Hormones, Enzymes, and Genes

Seed endogenous factors, such as plant hormones, genetics, enzymes, and various physiological, biochemical, and molecular processes within the seed, are crucial in regulating its dormancy and germination [77]. The exogenous environmental factors (temperature, moisture, light, etc.) are also involved [44,78,83].
The application of the plant growth regulator GA3, alone, with/without warm stratification, has been shown to accelerate embryo growth and germination in seeds of P. corsica [42]. However, application of GA3 alone only gave a small increase in germination rate in the case of P. officinalis [84].
In a recent study of the seeds of P. lactiflora conducted under natural conditions, it was found that both natural growth regulators, abscisic acid (ABA) and gibberellic acid (GA3), are involved in regulating the seed changeover from dormancy to germination, and their activities are antagonistic [76]. Additionally, it was reported that 30 mg/L ABA had a significant inhibitory effect on the seed germination of herbaceous peony hybrid ‘Fen Yu Nu’ × ‘Fen Yu Lou’ [85]. The activities of ABA and GA3 in the seeds of various peonies were shown to be dependent on given environmental factors [60,64]; winter or low temperatures led to the accumulation of ABA in seeds, which induced dormancy, whereas spring or warm temperatures led to ABA degradation and the accumulation of GA3, which triggered dormancy release and germination [44,72,86]. In herbaceous peonies, the following optimal concentrations of GA3 for radicle emergence were reported: 250 mg L−1 for P. corsica [42] and 300 mg L−1 for P. lactiflora [76].
The impact of exogenous hormones on herbaceous peonies seeds has also been studied, and it was found that the application of 6-benzylaminopurine (BA) on seeds of P. lactiflora positively influenced the release of double dormancy [37], while the application of indole-3-acetic acid (IAA) and indole-3-butyric acid (IBA), in the case of P. veitchii, promoted root initiation and lateral root development [31,44].
Although seed dormancy and germination studies have made significant progress in the last two decades, it is still largely unknown how such complex signal transduction and gene expression regulation pathways are controlled in a coordinated and sequential manner during seed dormancy release [76,81]. Studies on the ‘Fen Yu Nu’ cultivar of the most studied herbaceous peony species P. lactiflora revealed that the expression of ABA 8′-hydroxylase genes PlCYP70A1 and PlCYP70A2 increased its seed germination, influencing ABA degradation and dormancy release [46]. The expression of genes associated with the development of the hypocotyl (the auxin response gene PlSAUR1) and epicotyl (genes PlSAUR2 and PlSAUR3) of the same species was also observed [44,78].
The germination protocol for peony species is complex and demanding as most of them have double dormancy (in hypocotyls and in epicotyls), which has to be released separately by using different methods [78]. Several methods have been described so far as effective in stimulating germination and dormancy breaking for herbaceous peonies [36,42], but they can only guide researchers in the direction of possible dormancy breaking procedures that lead to germination and seedling development in other, less studied herbaceous peony species.

5. Conclusions

We are witnessing climatic changes in temperature and rainfalls patterns, which, in combination with reckless human activities towards nature, lead to the extinction of many valuable ornamental, edible, and medicinal plant species, including herbaceous peonies. Among them, most are already rare or endangered. As the seeds of most herbaceous peonies have double dormancy, the changes in environmental factors certainly impact their spontaneous resources, jeopardizing their survival. In order to preserve those valuable plant species, it is crucial to understand the specificity of their seeds, including requirements for their dormancy release, as this will further enable the establishment of in situ and ex situ collections and studies leading towards their successful propagation, breeding, and cultivation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae8070585/s1, Figure S1: The flowers of the herbaceous peony species of the Paeonia L., subsection Paeoniae.

Author Contributions

Conceptualization, T.M., Ž.P., J.X., D.R. and X.Z.; writing—original draft preparation, T.M., Ž.P., V.F., M.L. and S.G.; visualization, T.M. and J.X.; writing—review and editing, T.M., Ž.P., J.X., X.R. and X.Z.; critical review, T.M. and J.X.; supervision T.M. and X.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by joint funding of the Ministry of Science and Technology of the Republic of Serbia (451-03-1202/2021-09) and the National Key R&D Program of China (2021YFE0110700).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Sun, J.; Guo, H.; Tao, J. Effects of harvest stage, storage, and preservation technology on postharvest ornamental value of cut peony (Paeonia lactiflora) flowers. Agronomy 2022, 12, 230. [Google Scholar] [CrossRef]
  2. Zhang, J.; Zhang, D.; Wei, J.; Shi, X.; Ding, H.; Qiu, S.; Guo, J.; Li, D.; Zhu, K.; Horvath, D.P.; et al. Annual growth cycle observation, hybridization and forcing culture for improving the ornamental application of Paeonia lactiflora Pall. in the low-latitude regions. PLoS ONE 2019, 14, e0218164. [Google Scholar] [CrossRef] [PubMed]
  3. Weixing, L.; Shunbo, Y.; Hui, C.; Yanmin, H.; Jun, T.; Chunhua, Z. Nutritional evaluation of herbaceous peony (Paeonia lactiflora Pall.) petals. Emir. J. Food Agric. 2017, 29, 518–531. [Google Scholar] [CrossRef]
  4. Batinić, P.; Milošević, M.; Lukić, M.; Prijić, Ž.; Gordanić, S.; Filipović, V.; Marinković, A.; Bugarski, B.; Marković, T. In vitro evaluation of antioxidative activities of extracts of Paeonia lactiflora and Calendula officinalis L. petals incorporated in the new forms of biobased carriers. Food Feed Res. 2022, 49, 23–35. [Google Scholar] [CrossRef]
  5. Jin, Y.S.; Xuan, Y.H.; Jin, Y.Z.; Chen, M.L.; Tao, J. Biological activities of herbaceous peony flower extracts. Asian J. Chem. 2013, 25, 3835–3838. [Google Scholar] [CrossRef]
  6. Qi, Q.; Li, Y.; Xing, G.; Guo, J.; Guo, X. Fertility variation among Paeonia lactiflora genotypes and fatty acid composition of seed oil. Ind. Crops Prod. 2020, 152, 112540. [Google Scholar] [CrossRef]
  7. He, D.Y.; Dai, S.M. Anti-inflammatory and immunomodulatory effects of Paeonia lactiflora Pall., a traditional Chinese herbal medicine. Front. Pharmacol. 2011, 2, 10. [Google Scholar] [CrossRef] [Green Version]
  8. Rudaya, O.A.; Chesnokov, N.N.; Kirina, I.B.; Tarova, Z.N.; Bobrovich, L.V.; Kiriakova, O.I. The research of seed reproduction peculiarities of wild-growing Paeonia L. genus and perspectives of using peony seeds in food-processing industry. IOP Conf. Ser. Earth Environ. Sci. 2021, 845, 012002. [Google Scholar]
  9. Demirboğa, Y.; Demirboğa, G.; Özbay, N. Types of Paeonia and Their Use in Phytotherapy. Karadeniz Bilim. Derg. 2021, 11, 318–327. [Google Scholar] [CrossRef]
  10. Ning, C.; Jiang, Y.; Meng, J.; Zhou, C.; Tao, J. Herbaceous peony seed oil: A rich source of unsaturated fatty acids and γ-tocopherol. Eur. J. Lipid Sci. Technol. 2015, 117, 532–542. [Google Scholar] [CrossRef]
  11. Ma, G.Y.; Shi, X.H.; Zou, Q.C.; Zhu, K.Y.; Liu, H.C.; Zhou, J.H.; Zhang, J.Q. Characters determination of herbaceous oil physicochemical property and comparative analysis of peony seed oil. Chin. Cereal Oil Assoc. 2017, 32, 130–1134. [Google Scholar]
  12. Andrieu, E.; Thompson, J.D.; Debussche, M. The impact of forest spread on a marginal population of a protected peony (Paeonia officinalis L.): The importance of conserving the habitat mosaic. Biodivers. Conserv. 2007, 16, 643–658. [Google Scholar] [CrossRef]
  13. Han, X.M.; Wu, S.X.; Wu, M.F.; Yang, X.M. Antioxidant effect of peony seed oil on aging mice. Food Sci. Biotechnol. 2017, 26, 1703–1708. [Google Scholar] [CrossRef] [PubMed]
  14. Deng, R.; Gao, J.; Yi, J.; Liu, P. Could peony seeds oil become a high-quality edible vegetable oil? The nutritional and phytochemistry profiles, extraction, health benefits, safety and value-added-products. Food Res. Int. 2022, 156, 111200. [Google Scholar] [CrossRef] [PubMed]
  15. Song, T.; Deng, R.; Gao, J.; Yi, Y.; Liu, P.; Yang, X.; Zhang, Z.; Han, B.; Zhang, I. Comprehensive resource utilization of peony seeds shell: Extraction of active ingredients, preparation and application of activated carbon. Ind. Crops Prod. 2022, 180, 114764. [Google Scholar] [CrossRef]
  16. Yang, Y.; He, C.; Wu, Y.; Yu, X.; Li, S.; Wang, L. Characterization of stilbenes, in vitro antioxidant and cellular anti-photoaging activities of seed coat extracts from 18 Paeonia species. Ind. Crops Prod. 2022, 177, 114530. [Google Scholar] [CrossRef]
  17. Zhang, Y.; Liu, P.; Gao, J.; Wang, X.; Yan, M.; Xue, N.; Qu, C.; Deng, R. Paeonia veitchii seeds as a promising high potential by-product: Proximate composition, phytochemical components, bioactivity evaluation and potential applications. Ind. Crops Prod. 2018, 125, 248–260. [Google Scholar] [CrossRef]
  18. Abbey, M. Paeonia spp. Production and Future Developments; Report; University of Minnesota Digital Conservancy: Minnesota, MN, USA, 2015; pp. 1–23. Available online: https://hdl.handle.net/11299/175839 (accessed on 23 March 2022).
  19. Hong, D.Y.; Pan, K.Y. Paeoniaceae. In Flora of China; Wu, Z.Y., Raven, P.H., Eds.; Science Press and Missouri Botanic Garden Press: Beijing, China, 2001; Volume 6, pp. 127–132. [Google Scholar]
  20. Wu, S.H.; Wu, D.G.; Chen, Y.W. Chemical constituents and bioactivities of plants from the genus Paeonia. Chem. Biodivers. 2010, 7, 90–104. [Google Scholar] [CrossRef]
  21. Xue, Y.; Liu, R.; Xue, J.; Wang, S.; Zhang, X. Genetic diversity and relatedness analysis of nine wild species of tree peony based on simple sequence repeats markers. Hortic. Plant. J. 2021, 7, 579–588. [Google Scholar] [CrossRef]
  22. Tank, D.C.; Sang, T. Phylogenetic utility of the glycerol-3-phosphate acyltransferase gene: Evolution and implications in Paeonia (Paeoniaceae). Mol. Phylogenet. Evol. 2001, 19, 421–429. [Google Scholar] [CrossRef] [Green Version]
  23. Zhou, S.L.; Xu, C.; Liu, J.; Yu, Y.; Wu, P.; Cheng, T.; Hong, D.Y. Out of the Pan—Himalaya: Evolutionary history of the Paeoniaceae revealed by phylogenomics. J. Syst. Evol. 2020, 59, 1170–1182. [Google Scholar] [CrossRef]
  24. Blecic, V. Paeonia L. In Flora of Serbia; Josifovic, M., Ed.; Serbian Academy of Sciences and Arts: Belgrade, Serbia, 1972; Volume 3, pp. 98–102. [Google Scholar]
  25. Lazarevic, P.; Stojanovic, V. Wild peonies (Paeonia L.) in Serbia—The distribution, state of populations, threats and protection. Nat. Conserv. 2012, 62, 19–44. [Google Scholar]
  26. Boza, P.; Stojsic, V. Paeonia officinalis L. subsp. banatica /Rochel/ Soó). In Red Book of Flora; Stevanović, V., Ed.; Serbia 1—Extinct and Extremely Endangered Taxa; Ministry of Environmental Protection of Republic of Serbia: Belgrade, Serbia, 1999; pp. 167–169. [Google Scholar]
  27. Djurdjevic, L.; Dinic, A.; Stojsic, V.; Mitrovic, M.; Pavlovic, P.; Oldja, M. Allelopathy of Paeonia officinalis L.1753 ssp. banatica (ROCHEL) s061945, a Pannonian endemic and relict species. Arch. Biol. Sci. 2000, 52, 195–201. [Google Scholar]
  28. The National Forestry and Grassland Administration of China. List of National Protected Wild Plants. 2021. Available online: http://www.forestry.gov.cn/ (accessed on 23 March 2022).
  29. American Peony Society. Available online: https://americanpeonysociety.org (accessed on 23 March 2022).
  30. Rockström, J.; Steffen, W.; Noone, K.; Persson, A.; Chapin, F.S.; Lambin, E.; Lenton, T.M.; Scheffer, M.; Folke, C.; Schellnhuber, H.; et al. Planetary boundaries: Exploring the safe operating space for humanity. Ecol. Soc. 2009, 14, 32. Available online: http://www.ecologyandsociety.org/vol14/iss2/art32/ (accessed on 23 March 2022). [CrossRef]
  31. Zhang, K.; Zhang, Y.; Tao, J. Predicting the potential distribution of Paeonia veitchii (Paeoniaceae) in China by incorpo-rating climate change into a maxent model. Forests 2019, 10, 190. [Google Scholar] [CrossRef] [Green Version]
  32. Ne’eman, G. To be or not to be—the effect of nature conservation management on flowering of Paeonia mascula (L.) Miller in Israel. Biol. Conserv. 2003, 109, 103–109. [Google Scholar] [CrossRef]
  33. Nikos, K.; Menteli, V.; Vokou, D. The Electronic Trade in Greek Endemic Plants: Biodiversity, Commercial and Legal Aspects. Econ. Bot. 2014, 68, 85–95. [Google Scholar] [CrossRef]
  34. Glick, P.; Stein, B.A.; Edelson, N.A. Scanning the Conservation Horizon: A Guide to Climate Change Vulnerability Assessment; National Wildlife Federation: Washington, DC, USA, 2011; 168p. [Google Scholar]
  35. Root, T.L.; Price, J.T.; Hall, K.R.; Schneider, S.H.; Rosenzweig, C.; Pounds, J.A. Fingerprints of global warming on wild animals and plants. Nature 2003, 421, 57–60. [Google Scholar] [CrossRef]
  36. Baskin, C.C.; Baskin, J.M. Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination; Academic Press: San Diego, CA, USA, 2014; ISBN 978012416683. [Google Scholar]
  37. Yu, X.; Zhao, R.; Cheng, F. Seed Germination of Tree and Herbaceous Peonies: A Mini-Review Seed. Sci. Biotech. 2007, 1, 11–14. [Google Scholar]
  38. Barga, S.C. Seed Dispersal of Wild Peony (Paeonia brownii): A Seed in the Pouch Is Worth Two in the Pod. Master’s Thesis, University of Nevada, Reno, Reno, NV, USA, 2011; p. 53. Available online: http://hdl.handle.net/11714/3838 (accessed on 23 March 2022).
  39. Zhang, K.; Yao, L.; Zhang, Y.; Baskin, J.M.; Baskin, C.C.; Xiong, Z.; Tao, J. A review of the seed biology of Paeonia species (Paeoniaceae), with particular reference to dormancy and germination. Planta 2018, 249, 291–303. [Google Scholar] [CrossRef]
  40. Andrieu, E.; Debussche, M.; Galloni, M.; Thomson, J.D. The interplay of pollination, costs of reproduction and plant size in maternal fertility limitation in perennial Paeonia officinalis. Oecologia 2007, 152, 515–524. [Google Scholar] [CrossRef]
  41. Gao, J.; Fu, Z.; Dong, X.; Wang, L.; Yuan, X.; Zhang, J.; Wang, H.; Li, Y.; Feng, N.; Wang, Y.; et al. Studies on Pollination Characteristics and Breeding System of Paeonia lactiflora Pall. Bot. Res. 2018, 7, 536–542. [Google Scholar] [CrossRef]
  42. Porceddu, M.; Mattana, E.; Pritchard, H.W.; Bacchetta, G. Sequential temperature control of multi-phasic dormancy release and germination of Paeonia corsica seeds. J. Plant. Ecol. 2016, 9, 464–473. [Google Scholar] [CrossRef] [Green Version]
  43. Nanjidsuren, O.; Narantsetseg, A. Seed productivity of two species of Paeonia (Paeoniaceae) in Mongolia. Agric. Sci. Res. J. 2016, 6, 1–5. [Google Scholar]
  44. Finch-Savage, W.E.; Leubner-Metzger, G. Seed dormancy and the control of germination. New Phytol. 2006, 171, 501–523. [Google Scholar] [CrossRef]
  45. Joshi, P.; Prakash, P.; Purohit, V.K. Seed germination and growth performance of Paeonia emodi Wall. ex Royle: Conservation and cultivation strategies. J. Appl. Res. Med. Aromat. Plants 2021, 25, 100338. [Google Scholar] [CrossRef]
  46. Kamenetsky, R.; Dole, J. Herbaceous peony (Paeonia): Genetics, physiology and cut flower production. Floric. Ornam. Biotechnol. 2012, 6, 62–77. [Google Scholar]
  47. Yang, Y.; Sun, M.; Li, S.; Chen, Q.; da Silva, T.J.A.; Wang, A.; Yu, X.; Wang, L. Germplasm resources and genetic breeding of Paeonia: A systematic review. Hortic. Res. 2020, 7, 107. [Google Scholar] [CrossRef]
  48. Hong, D.Y. Peonies of the World: Taxonomy and Phytogeography; Missouri Botanical Garden: St. Louis, MI, USA, 2010; p. 302. [Google Scholar]
  49. Hudson, A.R.; Ayre, D.J.; Ooi, M.K.J. Physical dormancy in a changing climate. Seed. Sci. Res. 2015, 25, 66–81. [Google Scholar] [CrossRef] [Green Version]
  50. Bojnanský, V.; Fargašová, A. Taxonomy and Morphology of Seeds. In Atlas of Seeds and Fruits of Central and East-European Flora; Springer: Dordrecht, The Netherlands, 2007; pp. 1–954. [Google Scholar] [CrossRef]
  51. Nazir, S.; Yaqoob, U.; Nawchoo, I.A.; Lone, F.A.; Rather, A.A.; Hassan, A.; Ashraf, A. Paeonia emodi: An Ethnopharmacological and Phytochemical Review. Res. Rev. J. Herbal Sci. 2017, 6, 11–20. [Google Scholar]
  52. Meng, J.; Li, M.; Zhang, K.; Zhao, D.; Tao, J. Kinetics of seed reserve compounds during the maturation of herbaceous peony (Paeonia lactiflora Pall.) seeds. J. Seed Sci. 2021, 43, e202143041. [Google Scholar] [CrossRef]
  53. Pons, T.L. Seed responses to light. In Seeds: The Ecology of Regeneration in Plant Communities; Fenner, M., Ed.; CABI Publishing: Wallingford, UK, 2000; pp. 237–260. [Google Scholar]
  54. Qi, Q.; Li, Y.; Meng, F.; Xing, G.; Zhou, J.; Guo, X. Dynamic changes of nutrient content in herbaceous peony seed. Oil Crop Sci. 2020, 5, 36–41. [Google Scholar] [CrossRef]
  55. Yang, H.C.; Per, D.L. Study on embryo culture of peony (Paeonia suffruticosa Andr. L.) seed. Guangxi Agric. Sci. 2006, 37, 108–119. [Google Scholar]
  56. Pausas, J.G.; Lamont, B.B. Fire-released seed dormancy—A global synthesis. Biol. Rev. 2022. [Google Scholar] [CrossRef]
  57. Dole, J.M. Research approaches for determining cold requirements for forcing and flowering of geophytes. Hort. Sci. 2003, 38, 341–346. [Google Scholar] [CrossRef]
  58. Baskin, J.M.; Baskin, C.C. The great diversity in kinds of seed dormancy: A revision of the Nikolaeva–Baskin classification system for primary seed dormancy. Seed. Sci. Res. 2021, 31, 249–277. [Google Scholar] [CrossRef]
  59. Nikolaeva, M.G. Factors controlling the seed dormancy pattern. In The Physiology and Biochemistry of Seed Dormancy and Germination; Khan, A.A., Ed.; Elsevier/North-Holland Biomedical Press: Amsterdam, The Netherlands, 1977; pp. 51–74. [Google Scholar]
  60. Baskin, J.M.; Baskin, C.C. A classification system for seed dormancy. Seed. Sci. Res. 2004, 14, 1–16. [Google Scholar] [CrossRef] [Green Version]
  61. Sun, X.M.; Zhang, M.M.; Gao, H.D.; Yang, H.G. Study on characteristic for seed coat of Paeonia lactifora. North. Hort. 2012, 6, 55–57. [Google Scholar]
  62. Rodrigues-Junior, A.G.; Mello, A.C.M.P.; Baskin, C.C.; Baskin, J.M.; Oliveira, D.M.T.; Garcia, Q.S. Why large seeds with physical dormancy become nondormant earlier than small ones. PLoS ONE 2018, 13, e022038. [Google Scholar] [CrossRef]
  63. Corner, E.J.H. The Seeds of Dicotyledons; Cambridge University Press: Cambridge, UK, 1976; ISBN 13 9780521116053. [Google Scholar]
  64. Suleymanova, G.; Boldyrev, V.; Savinov, V. Post-fire restoration of plant communities with Paeonia tenuifolia in the Khvalynsky National Park (Russia). Nat. Conserv. Res. 2019, 4, 57–77. [Google Scholar] [CrossRef]
  65. Tao, X.Y.; Yang, H.L.; Li, L. The research of the germination characteristic of herbaceous peony. J. Chifeng Coll. 2005, 21, 13–19. [Google Scholar]
  66. Guo, L.P. Study on Dormancy and Dormancy Breaking of Tree Peony Seeds. Master’s Thesis, Northwest A&F University, Shaanxi, China, 2016. [Google Scholar]
  67. Maeda, A.B.; Wells, L.W.; Sheehan, M.A.; Dever, J.K. Stories from the greenhouse—A brief on cotton seed germination. Plants 2021, 10, 2807. [Google Scholar] [CrossRef] [PubMed]
  68. Ren, X.; Xue, J.; Wang, S.; Xue, Y.; Zhang, P.; Jiang, H.; Zhang, X. Proteomic analysis of tree peony (Paeonia ostii ‘Feng Dan’) seed germination affected by low temperature. J. Plant. Physiol. 2017, 224–225, 56–67. [Google Scholar] [CrossRef] [PubMed]
  69. Bewley, J.D. Seed Germination and Dormancy. Plant. Cell 1997, 9, 1055–1066. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Baskin, C.C.; Baskin, J.M. Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination; Academic Press: San Diego, CA, USA, 2001; p. 666. [Google Scholar]
  71. Baskin, C.C.; Baskin, J.M. Seed dormancy in wild flowers. In Flower Seeds: Biology and Technology; McDonald, M.B., Kwong, F.Y., Eds.; CABI Publishing: Wallingford, UK, 2005; pp. 163–185. [Google Scholar]
  72. Soltani, E.; Baskin, C.C.; Baskin, J.M. A graphical method for identifying the six types of nondeep physiological dormancy in seeds. Plant. Biol. 2017, 19, 673–682. [Google Scholar] [CrossRef]
  73. Yang, Y. Research on Biological Characteristics of Paeonia lactiflora Seed’s Germination and Dormancy Breaking Technique. Ph.D. Thesis, Northeast Forest University, Harbin, China, 2009. [Google Scholar]
  74. Yuan, Y.B.; Xiao, N.Y. Effects of exogenous GA3 and chilling treatments on seed germination and seedling growth of Paeonia lactiflora. J. Anhui Agric. Univ. 2014, 41, 273–277. [Google Scholar]
  75. Nikolaeva, M.G.; Rasumova, M.V.; Gladkova, V.N. Reference Book on Dormant Seed Germination; Nauka Publishers: Leningrad, Russia, 1985. [Google Scholar]
  76. Li, X.R.; Chen, Z.; Fan, C.; Sun, X.; Min, X.J. Plant hormonal changes and differential expression profiling reveal seed dormancy removal process in double dormant plant-herbaceous peony. PLoS ONE 2020, 15, e0231117. [Google Scholar] [CrossRef] [Green Version]
  77. Bentsink, L.; Koornneef, M. Seed Dormancy and Germination. In The Arabidopsis Book; BioOne: Washington, DC, USA, 2008; Volume 6, p. e0119. [Google Scholar] [CrossRef] [Green Version]
  78. Ren, X.; Liu, Y.; Jeong, B.R. A Two-Stage Culture Method for Zygotic Embryos Effectively Overcomes Constraints Imposed by Hypocotyl and Epicotyl Seed Dormancy in Paeonia ostii ‘Fengdan’. Plants 2019, 8, 356. [Google Scholar] [CrossRef] [Green Version]
  79. Ren, R.; Zhou, H.; Zhang, L.; Jiang, X.; Zhang, M.; Liu, Y. ROS-induced PCD affects the viability of seeds with different moisture content after cryopreservation. Plant. Cell Tiss. Organ. Cult. 2022, 148, 623–633. [Google Scholar] [CrossRef]
  80. Fei, R.; Sun, X.; Yang, P.; Chen, Z.; Ma, Y. Anatomical observation of Paeonia lactiflora seeds during stratification process. J. Shenyang Agric. Univ. 2017, 48, 354–359. [Google Scholar]
  81. European Peony Society. Available online: https://www.peonysociety.eu (accessed on 23 March 2022).
  82. Halevy, A.H. Evaluation of Methods for Flowering Advancement of Herbaceous Peonies. Hort. Sci. 2002, 37, 885–889. [Google Scholar] [CrossRef] [Green Version]
  83. Vandelook, F.; Assche, J.A. Temperature requirements for seed germination and seedling development determine timing of seedling emergence of three monocotyledonous temperate forest spring geophytes. Ann. Bot. 2008, 102, 865–875. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Deno, N.C. Seed Germination Theory and Practice, 2nd ed.; Norman C. Deno: State College, PA, USA, 1993; p. 242. [Google Scholar]
  85. Fei, R.; Duan, S.; Ge, J.; Sun, T.; Sun, X. Functional Identification of 9-cis-epoxycarotenoid Dioxygenase Genes in Double Dormant Plant-herbaceous Peony. Res. Sq. 2021, 1–26. [Google Scholar] [CrossRef]
  86. Sirotyuk, A.E.; Shadge, A.E.; Gunina, G.N. Paeonia caucasica (Schipcz.) Schipcz. in phytocenoses of the Republic of Adygea. Ecol. Montenegrina 2020, 37, 43–50. [Google Scholar] [CrossRef]
Horticulturae 08 00585 g001 550
Figure 1. Division of genus Paeonia, with focus on herbaceous species native to Serbia and China.
Figure 1. Division of genus Paeonia, with focus on herbaceous species native to Serbia and China.
Horticulturae 08 00585 g001
Horticulturae 08 00585 g002 550
Figure 2. Ripe seeds of several herbaceous peony species (seed collection, 2021); (A) P. peregrina, (B) P. banatica, (C) P. tenuifolia, (D) P. daurica, (E) P. veitchii, (F) P. mairei, (G) P. emodi, (H) P. anomala, (I) P. sterniana, (J) P. obovata, (K) P. lactiflora, and (L) P. sinjiangensis.
Figure 2. Ripe seeds of several herbaceous peony species (seed collection, 2021); (A) P. peregrina, (B) P. banatica, (C) P. tenuifolia, (D) P. daurica, (E) P. veitchii, (F) P. mairei, (G) P. emodi, (H) P. anomala, (I) P. sterniana, (J) P. obovata, (K) P. lactiflora, and (L) P. sinjiangensis.
Horticulturae 08 00585 g002
Table
Table 1. Summarized literature data on seeds of most herbaceous peony species.
Table 1. Summarized literature data on seeds of most herbaceous peony species.
SpeciesSeeds Reference
Testa ColourSize (mm)ShapeMaturation
P. algeriensisblack9.0 × 7.5ovoid to oblongAugust[48]
P. anomalablack 6.6–8.8 × 5.1–6.0ellipsoidalAugust[8,38,47]
P. banaticablack6.0–8.0 × 5.0ellipsoidallate July to August[49]
P. broteriblack7.0–8.0oblongAugust to September[49]
P. cambessdesiiblack5.0globularJune to July[49]
P. clusiiblack8.0 × 5.0ovoid to ellipsoidalAugust[48]
P. coriaceablack7.0–8.0 × 5.0–6.0oblongSeptember[48]
P. corsicablack7.0 × 5.0–6.0ovoid to globularlate July to September[48]
P. dauricablack6.1–7.5 × 4.2–7.0globularAugust to September[38,50]
P. emodibrownish black2.0–3.5 globularAugust to September[51]
P. intermediablack glossy5.0–5.5 × 3.0–3.5 cylindrical to ovoidAugust to September[48]
P. lactiflorabrownish black5.5–10.0 × 4.1–6.8ellipsoidal or globular to rhomboid, flattishlate July to September[8,38,48,50]
P. maireiblack with blue shine7.0–8.0 × 4.0–5.0irregular, roundJuly to August[48]
P. masculafirst red than black7.0–8.5 × 5.0–7.0ellipsoidal to globularlate July to August[50]
P. obovatablack6.0–7.0 × 5.0–6.0ovoid to globularAugust to September[48]
P. officinalisblack6.0–9.0 × 4.5–6.5obovate to ellipsoidallate July to August[50]
P. peregrinablack7.5–10.0 × 5.0–6.0ellipsoidallate July to August[48,50]
P. sternianaindigo blue7.0–8.0 × 5.0ellipsoidalAugust to September[48]
P. tenuifoliabrownish black5.9–8.0 × 3.5–4.9cylindrical to ellipsoidalJuly to August[8,38,50]
P. veitchiidark blue 6.0 × 4.0ellipsoidal to ovalJuly[8]
P. kesrouanensisblack6.0–10.0 × 6.0–8.0ovoid to globularJuly to September[48]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Marković, T.; Prijić, Ž.; Xue, J.; Zhang, X.; Radanović, D.; Ren, X.; Filipović, V.; Lukić, M.; Gordanić, S. The Seed Traits Associated with Dormancy and Germination of Herbaceous Peonies, Focusing on Species Native in Serbia and China. Horticulturae 2022, 8, 585. https://doi.org/10.3390/horticulturae8070585

AMA Style

Marković T, Prijić Ž, Xue J, Zhang X, Radanović D, Ren X, Filipović V, Lukić M, Gordanić S. The Seed Traits Associated with Dormancy and Germination of Herbaceous Peonies, Focusing on Species Native in Serbia and China. Horticulturae. 2022; 8(7):585. https://doi.org/10.3390/horticulturae8070585

Chicago/Turabian Style

Marković, Tatjana, Željana Prijić, Jingqi Xue, Xiuxin Zhang, Dragoja Radanović, Xiuxia Ren, Vladimir Filipović, Milan Lukić, and Stefan Gordanić. 2022. "The Seed Traits Associated with Dormancy and Germination of Herbaceous Peonies, Focusing on Species Native in Serbia and China" Horticulturae 8, no. 7: 585. https://doi.org/10.3390/horticulturae8070585

APA Style

Marković, T., Prijić, Ž., Xue, J., Zhang, X., Radanović, D., Ren, X., Filipović, V., Lukić, M., & Gordanić, S. (2022). The Seed Traits Associated with Dormancy and Germination of Herbaceous Peonies, Focusing on Species Native in Serbia and China. Horticulturae, 8(7), 585. https://doi.org/10.3390/horticulturae8070585

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop