Seed Dormancy and Germination in <I>Cardiocrinum Giganteum</I>

Home , Cardiocrinum, Cardiocrinum cordatum, Cardiocrinum giganteum

Li, Song, Guan and Li (2020). Seed Science and Technology, 48, 2, 303-314. https://doi.org/10.15258/sst.2020.48.2.17

Seed dormancy and germination in Cardiocrinum giganteum var. yunnanense, a perennial herb in China with post-dispersal embryo growth

Ye-Fang Li1, Jie Song2, Wen-Ling Guan1* and Feng-Rong Li1

1 Faculty of Horticulture and Landscape, Yunnan Agricultural University, Kunming 650201, PR China 2 Flowers Research Institute, Yunnan Academy of Agricultural Sciences, Kunming 650204, PR China *Author for correspondent (E-mail: [email protected])

(Submitted February 2020; Accepted May 2020; Published online June 2020)

Abstract

Seeds of Cardiocrinum giganteum var. yunnanense, which is native to China, has underdeveloped embryos when dispersed from parent plants that did not grow until the second autumn and winter after exposure to summer temperatures. Radicles and cotyledons emerged in late winter and spring. Thus, a 15–16 month period was required from dispersal to seed germination. Under laboratory conditions, this period could be shortened to 5–6 months in a 25°C / 15°C (60 days) → 15°C / 5°C (60 days) → 5°C (60 days) temperature sequence. Based on dormancy-breaking requirements, the seeds have deep simple morphophysiological dormancy (MPD). This is practical knowledge for propagation of the species from seeds.

Keywords: Cardiocrinum giganteum var. yunnanense, embryo development, morphophysiological dormancy, seed germination, temperature requirement

Introduction

Dormancy is a mechanism whereby seeds do not germinate during periods that may be favourable for germination but unfavourable for subsequent seedling establishment (Vleeshouwers et al., 1995). Differing climatic conditions are often reflected in the dormancy breaking requirements of seeds (Skordilis and Thanos, 1995). Some species have an underdeveloped embryo at the moment of dispersal, meaning that it has to grow within the seed before germination. These seeds are described as morphologically dormant (MD) or morphophysiologically dormant (MPD), with an additional physiological block preventing germination (Nikolaeva, 1977). Species with underdeveloped embryos are especially common in Liliales and certain Asparagales families (Kondo et al., 2006). Although dormancy has been studied in some monocotyledon taxa, data on embryo growth requirements are particularly scarce.

© 2020 Li et al. This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/licenses/by-nc/4.0 303 YE-FANG LI, JIE SONG, WEN-LING GUAN AND FENG-RONG LI

The genus Cardiocrinum (Liliaceae s. str.) grows in the Sino-Himalaya, and consists of three species: C. giganteum, C. cathayanumm and C. cordatum. Cardiocrinum giganteum is distributed in Nepal, Sikkim, Bhutan into north-west Burma and south-west China. The variety found in Yunnan, C. giganteum var. yunnanense has bronze-coloured stems and greener flowers. Cardiocrinum cathayanum occurs from central to east China; and C. cordatum from Sakhalin Island to Japan (Wu and Peter, 2000). This group of species are bulbous plants in the Liliaceae, distinguished from the genus Lilium by their heart-shaped leaves and hapaxanthic life history (bulbs die after flowering, but produce new bulbous offsets, which root and grow independently). In China, C. giganteum var. yunnanense grows in forests (altitudes 1200-3600 m a.s.l.) in Gansu, Guangdong, Guangxi, Guizhou, Henan, Hubei, Hunan, Shaanxi, Sichuan and Yunnan (Wu, 1993; Wu and Peter, 2000). The sweetly scented flowers are enormous and appear in May-July. In addition to being an introduced ornamental in Yunnan, the species has edible and medicinal value (Liu, 1984; Pei and Long, 1998; Shou et al., 2018). Unfortunately, this lily resource has been declining rapidly due to changing environmental conditions over past decades and excessive harvesting of the wild plants from native fields in Yunnan (own unpublished survey data). To mitigate this undesirable situation, it is necessary not only to prevent further loss of the native plants, but also to reproduce them horticulturally. Cardiocrinum giganteum var. yunnanense can propagate by seeds or through division, although the asexual propagation rate by plant division is much lower than from seedlings. The main disadvantage to seed propagation is that the breeding of commercial plants from seedlings takes 5–7 years. Many growers have long awaited the development of a method to shorten the seedling production time. Seeds with an underdeveloped embryo at the time of dispersal and requiring specific temperature conditions over a prolonged period of time for embryo growth and for radicle or cotyledon emergence are described as having morphophysiological dormancy (MPD) (Nikolaeva, 1977; Baskin and Baskin, 1998, 2004). Seeds of Cardiocrinum var. glehnii have an underdeveloped embryo at dispersal and require a sequence of warm and cold temperatures to break dormancy and to germinate (Kondo et al., 2006), so seeds of this taxon have deep simple morphophysiological dormancy (MPD). Phartyal et al. (2012) reported that the seeds of the Himalayan Cardiocrinum giganteum var. giganteum from India has similar dormancy and germination requirements as C. cordatum var. glehnii from Japan. However, so far, there are no reports on the germination of C. giganteum var. yunnanense seeds. The primary objective of the study was to clarify whether the Cardiocrinum from China has the same characteristics for dormancy break and germination as the other Cardiocrinum species. In order to achieve these goals, two experimental studies have been carried out on seeds of C. giganteum var. yunnanense: (1) phenology of embryo growth and of seedling emergence outdoors in Kunming; (2) testing temperature requirements for dormancy break and for seedling emergence in laboratory conditions. The results were compared with those of previous reports on seed germination of C. cordatum var. glehnii from Japan by Kondo et al. (2006) and C. giganteum var. giganteum from India by Phartyal et al. (2012).

304 SEED DORMANCY IN CARDIOCRINUM GIGANTEUM VAR. YUNNANENSE

Materials and methods

Seed collection Eighty mature capsules were collected from ten plants in a population of Cardiocrinum giganteum var. yunnanense growing naturally in a moist subtropical evergreen broadleaved forest woodland at an altitude of 2400 m a.s.l. in the Ailaoshan Mountain of Yunnan Province, China (101°01'E, 24°32'N), on 10 November 2015. Mean air temperatures in January and July at the nearest weather station (Ailaoshan National Ecosystem Observation Research Station Network, CERN, Yunnan; 2450 m a.s.l., 101°01'E, 24°32'N), were 5 and 15.3°C, respectively (China FLUX). The area is located in the southwest monsoon climate zone and is a subtropical mountain climate. Thus, November-April is the dry season, and May–October is the peak wet season in the natural habitat of the study species. The capsules harvested from different plants were combined and were put into non- woven fabric envelopes. The capsules arrived at Yunnan Agricultural University, Kunming, Yunnan, China on 11 November 2015 and were allowed to dry naturally in a laboratory (approximately 20°C) for three days, during which time the capsules dehisced. Then, seeds were collected by hand from the opened capsules and were spread onto porcelain dishes and allowed to dry naturally again at ambient room temperature (approximately 20°C) for three days. Undeveloped seeds were discarded. Only visibly well-developed dry seeds were put into plastic envelopes and stored in a drying basin with silica gel at 4°C until used in germination studies.

Phenology of embryo growth and of seed germination When a seed of C. giganteum var. yunnanense germinates, the radicle emerges first and then the cotyledon emerges. In this study, the criteria for radicle and cotyledon emergence were when the radicle tip had emerged 1 mm or more from the seed coat (figure 1A) and when the cotyledon tip had completely emerged above ground (figure 1B).

(A) (B)

radicle Figure 1. Seedling emergence in Cardiocrinum giganteum var. yunnanense. (A) growing radicle inside seed; (B) cotyledon emergence complete.

305 YE-FANG LI, JIE SONG, WEN-LING GUAN AND FENG-RONG LI

The phenology of embryo growth and of radicle and cotyledon emergence was scored in a non-temperature-controlled shade shed located outdoors on the campus of Yunnan Agricultural University. In order to simulate conditions in a native forest habitat, the shade shed was covered with shade cloth throughout the year, so that illuminance inside this structure was about 30% of that in the open (measured with an illuminance meter). Pots and trays containing the seeds (see later in this section) were placed in the shade shed. Soil (1:1 v/v mixture of pearl rock and peat) in the tray was kept moist throughout the experiment. Monthly mean, maximum and minimum temperatures were collected from the nearest weather station (Jindian Reservoir, Kunming). The study continued from 20 November 2015 through 10 April 2017.

Embryo development On 20 November 2015, about 30 seeds were placed in each of 20 fine-mesh polyester bags and buried at a soil depth of 30 mm in a tray in the shade shed. On the same day, ten seeds were used to observe embryo development and the initial embryo length of each seed was measured with a micrometer after scraping the seed coat with a scalpel under an anatomical microscope. Subsequently, one bag was removed at random from the tray at about 30-day intervals until 18 March 2017 and embryo length for each of ten seeds was measured using a dissecting microscope equipped with a micrometer. After 20 November 2016, when embryos began to curve (figure 2D), embryos were cut into 3–4 straight sections and their lengths measured and summed to get total embryo length. On 18 February 2017 (figure 2E), the lengths of 10 fully elongated embryos (9.94 ±

0.73 mm) (mean ± SE, N = 10), i.e., embryo length just prior to radicle emergence, was recorded. Embryo length during the study period was calculated as a percentage of that of fully elongated embryos.

Observation of radicle emergence after sowing On 20 November 2015, 100 seeds were placed in each of three fine-mesh polyester bags and buried 30 mm deep in the soil in a tray in the shade shed. Before 16 February 2017, when radicles began to emerge, seeds in the bags were checked for radicle emergence at about 30-day intervals and then at 10-day intervals. Seeds with an emerged radicle were counted and removed from the bags, and non-germinated seeds were reburied.

Observation of cotyledon emergence after sowing On 20 November 2015, 100 seeds were sown on the soil surface in each of three pots in the shade shed and covered with about 10 mm of moist soil. Pots were checked for cotyledon emergence at about 30-day intervals until 25 February 2017, when no cotyledons had emerged, and then at 10-day intervals until cotyledons had emerged from all seedlings.

Experiments in the laboratory For all experiments in the laboratory, seeds were placed in 90-mm-diameter × 10-mm- deep plastic Petri dishes on two sheets of qualitative filter paper moistened with distilled water. Petri dishes were sealed with parafilm to retard water loss during incubation. The daily photoperiod was 12 hours in both constant and daily alternating temperature regimes.

306 SEED DORMANCY IN CARDIOCRINUM GIGANTEUM VAR. YUNNANENSE

In the alternating temperature regimes, high temperature was given for 12 hours in light each day and low temperature for 12 hours in darkness. Seeds incubated at 5°C were kept in constant darkness. The light source was cool white fluorescent tubes, and photon -2 -1 irradiance (400–700 nm) at seed level was 10–15 µmol m second . Seeds were examined at intervals of 15–20 days. In several laboratory experiments, arrows (→) indicate when seeds were moved to the next temperature regime in the sequence. At each observation, seeds with an emerged radicle were recorded and then removed from the dishes. Water was added to dishes as needed to keep the filter paper moist.

Temperature dependence of embryo growth On 23 November 2015, three Petri dishes containing 50 seeds each were placed respectively at three single temperature regimes of (a) 5°C, (b) 15 / 5°C and (c) 25 / 15°C and at three sequences of temperature regimes of (d) 15 / 5°C (60 days) → 5°C (60 days) → 15 / 5°C (60 days), (e) 25/15°C (60 days) → 5°C (60 days) → 15 / 5°C (60 days) and (f) 25 / 15°C (60 days) → 15 / 5°C (60 days) → 5°C (60 days). Ten seeds were chosen at random and removed from each of the three dishes in each temperature treatment at 30- day intervals and lengths of the 10 embryos measured as previously described.

Radicle and cotyledon emergence during the annual temperature sequence Starting from 23 November 2015, three replicate Petri dishes with 100 seeds each were placed in the temperature sequence 25 / 15°C (60 days) → 15 /5°C (60 days) → 5°C (60 days) → 15 / 5°C, which simulates the annual temperature cycle. Seeds with an emerged radicle were recorded and removed from the dishes at 3- to 5-d intervals, and then they were used for observing cotyledon emergence. In order to observe cotyledon emergence, plastic pots (10 × 10 × 8.5 mm, length × width × depth), each with eight drainage holes in the bottom, were filled with soil (1:1 v/v mixture of pearl rock and peat). Three pots were prepared, corresponding to three Petri dishes in which radicle emergence was recorded. Seeds with an emerged radicle in Petri dishes were buried about 10 mm-deep in soil in the container. Dates of radicle emergence and burial in soil were recorded for each seed. The pots were kept at the last temperature regimes (15 / 5°C) for cotyledon emergence. Pots were watered from the bottom and covered with plastic film with small holes to reduce evaporation of water but to allow exchange of oxygen and carbon dioxide. Cotyledon emergence was recorded daily. The experiment was terminated 210 days after the seeds were sown.

Statistical analyses Statistical analyses were carried out using Microsoft Excel 2010 and SPSS 22.0. Means and standard errors were calculated for embryo length and for radicle and cotyledon emergence. Percent value of embryo length and final cumulative percentage of radicle and of cotyledon emergence for different treatments were analysed using either t-test or one-way ANOVA followed by the Tukey test (P < 0.05), if ANOVA showed significant differences. Final percentage values for radicle and cotyledon emergence were arcsine square-root transformed for normal distribution before statistical analysis; non-transformed data are shown in the figures.

307 YE-FANG LI, JIE SONG, WEN-LING GUAN AND FENG-RONG LI

Results

Phenology of embryo growth and of radicle and cotyledon

The initial embryo length was 1.06 ± 0.07 mm, which was only 10.7 ± 0.39% of that of the fully elongated embryo (9.94 ± 0.73 mm) (figure 2A). Embryos grew only a little during summer 2016. Mean embryo length in mid-August 2016 was 14.2 ± 2.0% of that of fully elongated embryos (figures 2B and 3). However, embryos grew rapidly to 51.37 ± 5.81% of the length of fully elongated embryos by 17 November in autumn 2016 (figures 2C-D and 3). In winter, embryos continued to grow and reached 99.0 ± 4.8% of the length of the fully elongated embryos in mid-February 2017 (figures 2E and 3).

(A) (B) 1 mm

15 August 2016 10 November 2015

10 October 2016 20 November 2016

(E) (F) (Radicle emergence)

(fully elongated embryos)

18 February 2017 22 February 2017

Figure 2. Embryo (arrow) growth in seeds of Cardiocrinum giganteum var. yunnanense outdoors in a shade shed in Kunming, China.

308 SEED DORMANCY IN CARDIOCRINUM GIGANTEUM VAR. YUNNANENSE

100 Radicle emergence

Cotyledon emergence

80 Embryo length

20 cotyledon emergence (%)

Embryo length, radicle emergence and 0 30 60 90 120 150 180 210 240 270 300 330 360 390 420 450 480 510 DN J F M A M J J A S O N D JFMA 2015 2016 2017 Length of time from sowing (days) and corresponding month and year Figure 3. Phenology of embryo growth and of radicle and cotyledon emergence in Cardiocrinum giganteum var. yunnanense outdoors in a shade shed, Kunming, China. Embryo length is expressed as a percentage of that of the fully developed embryo. Vertical bars show ± SD.

Radicle emergence began at the end of February 2017 (figures 2F and 3), and by 20 March 2017 radicles had emerged from 82.2% of the seeds. By 25 February 2017, cotyledons began to emerge, and by 6 April 2017 cotyledons had emerged from 82.4% of the seeds (figure 3).

Laboratory experiments Effect of temperature on embryo growth No embryo growth at all was observed at 5°C. At 25 / 15°C, embryo growth began between days 90 and 120 and embryos had grown up to only 28.72% of their full length after 300 days (figure 4A). At 15 / 5°C, embryo growth began between days 90 and 120, and had grown up to 97.28% of their full length by 300 days (figure 4B). However, no radicles had emerged by 300 days after sowing under the above temperature regime. In the temperature-sequence 25 / 15°C (60 days) →15 / 5°C (60 days) → 5°C (60 days), embryo growth was significantly (P ≤ 0.001, figure 4B) higher than it was in the other temperature regimes by 120 days after sowing. Under this sequence, embryos hardly grew during the first temperature regime (i.e., 25 / 15°C) but began to grow rapidly in the second regime (i.e., 15 / 5°C), reaching 42.9% of their full length by the end of the second regime (120 days). Embryos continued growing rapidly at 5°C, and they became fully elongated 50 days after transfer to the third stage (5°C) in the temperature sequence, by which time radicles had emerged from 27.2% of the seeds. In contrast, at other temperature-sequence treatments, elongation of embryos was later and lower; they grew to only 11.14–68.29% of their final length by 210 days and no radicles had emerged.

309 YE-FANG LI, JIE SONG, WEN-LING GUAN AND FENG-RONG LI

(A) 110 100 5ºC 90 25/15ºC 80 15/5ºC 70 60 50 40 30 Embryo length (%) 20 10 0 0 30 60 90 120 150 180 210 240 270 300 330

Time after sowing (days)

(B) 110 27.2% of seeds with 15/5ºC 4ºC 15/15ºC emerged radicles 100 25/15ºC 4ºC 15/15ºC 90 25/15ºC 15/5ºC 5ºC 80 70 60 50 40 30 Embryo length (%) 20 10 0 0 30 60 90 120 150 180 210 240 270 300 330 Time after sowing (days) Figure 4. Effect of single temperature regimes (A) and of sequences of temperature regimes (B) on embryo growth of Cardiocrinum giganteum var. yunnanense. Seeds in a sequence of temperatures were held at each temperature for 60 days. For a given temperature regime, embryo length is expressed as a percentage of that of fully developed embryos on day-300. Vertical bars show ± SD.

Embryo growth and radicle and cotyledon emergence during the annual temperature sequence

The embryo growth began at the simulated autumn temperature regime (15 / 5°C) following 60 days at the simulated summer temperature (25/15°C). Embryos continued to grow at the simulated winter temperature (5°C) and reached their full length after 170 days of incubation, when radicle emergence began. Radicles had emerged from 89.5% of the seeds after the winter (5°C) temperature (figure 5). Cotyledon emergence occurred by 180 days and emerged from 91.67% of the seeds at the spring temperature regime (15 / 5°C). It took about 10 days from radicle emergence to cotyledon emergence for seeds.

310 SEED DORMANCY IN CARDIOCRINUM GIGANTEUM VAR. YUNNANENSE

and cotyledon emergence (%)

Embryo length, radicle emergence Time after sowing (days) Figure 5. Effect of annual temperature sequence on embryo growth and on radicle and cotyledon emergence in Cardiocrinum giganteum var. yunnanense. Embryo length is expressed as a percentage of that of fully elongated embryos. Vertical bars show ± SD.

Discussion

Seeds of Cardiocrinum giganteum var. yunnanense are dispersed in November, when the embryos do not entirely fill the seed. In near-natural conditions in Kunming, embryos had grown only a little before August in the following year, but they began to grow in the autumn of the following year. Embryos continued to grow in winter until the middle of February, when the embryos had completely filled with seeds. In contrast, C. cordatum var. glehnii embryos elongated fully before the first winter (Kondo et al., 2006). In the population of C. cordatum var. glehnii seeds, radicles emerged in February until mid- March, about 18 months after seed dispersal. Cotyledon emergence also occurred in mid-March, soon after radicle emergence. In other words, under near-natural conditions, embryos in seeds of C. cordatum var. glehnii complete elongatation in the second autumn after seed dispersal, and radicles appear in the second winter, while cotyledons appear in early spring after the second winter. Hence, the onset of embryo growth in seeds of C. giganteum var. yunnanense in Kunming was delayed compared with that of C. cordatum var. glehnii. However, radicles from the seeds appeared immediately after completing embryo growth in winter. In C. cordatum var. glehnii, the release of seed dormancy is divided into two stages: (1) embryo growth in fall at around 10°C, and (2) release of physiological dormancy of mature embryos at 0–5°C in winter. As there was no delay between embryonic development and radicle emergence in C. giganteum var. yunnanense (figure 3), dormancy break in seeds of this taxon seems to be a continuous process, rather than two independent stages, as in C. cordatum var. glehnii. Thus, the two taxa differ in seed germination phenology.

311 YE-FANG LI, JIE SONG, WEN-LING GUAN AND FENG-RONG LI

Under natural conditions, seeds of C. giganteum var. yunnanense take about 16 months from dispersal to germination, but in a temperature sequence of 25 / 15°C (60 days) → 15 / 5°C (60 days) → 5°C (60 days), seeds germinated after about 5-6 months. The practical significance of this study for gardeners, horticulturists and restoration ecologists to propagate C. giganteum var. yunnanense from the seeds is that, under controlled temperature conditions, seedlings can be obtained in about 5-6 months vs. 16 months if fresh seeds are sown under natural conditions following dispersal in autumn. Comparatively, it took about 18-19 months from seed dispersal to germination for C. cordatum var. glehnii (Kondo et al., 2006) and C. giganteum var. giganteum (Phartyal et al., 2012). Further, several laboratory tests have shown that seeds of C. cordatum var. glehnii and C. giganteum var. giganteum require 9 and 10-11 months, respectively, for embryo development to cotyledon emergence. This is in contrast with seeds of C. giganteum var. yunnanense which need less time to germinate. The study indicates that seeds of C. giganteum var. yunnanense have an under developed embryo at the time of seed dispersal and require specific temperature conditions for embryo growth and physiological dormancy break, and thus they have morphophysiological dormancy (MPD) (Nikolaeva, 1977; Baskin and Baskin, 1998, 2004). MPD has been divided into nine levels, six of which belong to the simple type and three to the complex type (Baskin and Baskin, 2004; Baskin et al., 2008). In seeds with the simple type of MPD, embryos grow at warm temperatures, while in those with the complex type of MPD, embryos grow at low temperatures. Cardiocrinum cordatum var. glehnii is a classic example of a species whose seeds have deep simple MPD (Kondo et al., 2006). Seeds of C. cordatum var. glehnii usually disperse in autumn and germinate in the second spring after dispersal, i.e., 18–20 months after dispersal (Kondo et al., 2006). Seeds of C. cordatum var. glehnii require high temperatures (e.g., 25 / 15°C) followed by moderate temperatures (15 / 5°C) for embryo growth (Kondo et al., 2006). Seeds with fully elongated embryos require pretreatment at low temperature (e.g., 0°C) for radicle emergence (Kondo et al., 2006). Seeds of C. giganteum var. giganteum had similar requirements (Phartyal et al., 2012). As embryos in seeds of C. giganteum var. yunnanense require high (25 / 15°C) followed by moderate temperature (15 / 5°C) and then a low temperature (5°C) for growth and germination, seeds would have one of the levels of simple MPD, which is the same as that for seeds of C. cordatum var. glehnii and C. giganteum var. Giganteum (Kondo et al., 2006; Shyam et al., 2012). Therefore, it appears that seeds of the three taxa of Cardiocrinum have physiological dormancy but differ in degree of dormancy. The dormancy releasing requirements of different species also varied, correlating with their genetic backgrounds. As a whole, seeds of var. yunnanense exhibited a lower degree of dormancy, compared with a relatively high degree of dormancy for the other two taxa in the genus. Seed dormancy degrees of Cardiocrinum might be related to their genetic backgrounds and habitat adaptation. Seeds of some temperate species, e.g., Aconitum lycoctonum (Vandelook et al., 2009) and Aegopodium podagraria (Phartyal et al., 2009), have complex MPD, in which dormancy is broken only by cold temperature and seeds germinate in spring. Seeds of some temperate species or high-altitude subtropical species have simple MPD and require first warm stratification in summer/autumn and then cold stratification (in winter) for seed

312 SEED DORMANCY IN CARDIOCRINUM GIGANTEUM VAR. YUNNANENSE germination in the second spring after seed dispersal (Baskin and Baskin, 1989; Zhao, 1997; Hu and Fu, 1988; Kondo et al., 2004, 2006; Li, 2005; Meng et al., 2006; Wei, 2007; Duan et al., 2011; Qin et al., 2009; Vandelook and Van Assche, 2009). The present study shows that the overall seed dormancy and germination pattern in C. giganteum var. yunnanense is very similar to that of many other species of temperate forests regions or high-altitude subtropical forests regions, which are colder in winter. This suggests that C. giganteum var. yunnanense could regenerate by seeds and easily naturalise in other regions with similar climatic conditions. In conclusion, seeds of C. giganteum var. yunnanense were morphophysiological dormancy (MPD) and could effectively be broken by the sequence of high → moderate → low temperature for more than five months. Seeds of the species exhibited a lower degree of dormancy, compared with a relatively high degree of dormancy for the other two species (C. cordatum var. glehnii and C. giganteum var. giganteum) in the genus (Kondo et al., 2006; Shyam et al., 2012). Seed dormancy degrees of Cardiocrinum might be related to their genetic backgrounds and adaptations to environment. This work is helpful for seeding and conservation of this precious horticultural plant.

Acknowledgements

The research was supported by National Natural Science Foundation of China (Grant no. 31560227).

References

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