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Article

Evaluation of Five Asian Lily Cultivars in Chongqing Province China and Effects of Exogenous Substances on the Heat Resistance

by
Ningyu Bai
1,†,
Yangjing Song
1,†,
Yu Li
1,
Lijun Tan
1,
Jing Li
1,
Lan Luo
2,
Shunzhao Sui
1,* and
Daofeng Liu
1,*
1
Chongqing Engineering Research Center for Floriculture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400715, China
2
Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing 400722, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work and share first authorship.
Horticulturae 2024, 10(11), 1216; https://doi.org/10.3390/horticulturae10111216
Submission received: 15 October 2024 / Revised: 13 November 2024 / Accepted: 14 November 2024 / Published: 17 November 2024
(This article belongs to the Special Issue Emerging Insights into Horticultural Crop Ecophysiology)
Browse Figures
Figure 1
<p>Asian lily cultivars. (<b>A</b>). ‘Tiny Double You’; (<b>B</b>). ‘Curitiba’; (<b>C</b>). ‘Tiny Diamond’; (<b>D</b>). ‘Sugar Love’; (<b>E</b>). ‘Tiny Ghost’.</p> "> Figure 2
<p>Oxidative stress indexes of ‘Tiny Diamond’ after exogenous application of different substances under high temperature stress. (<b>A</b>). The relative water content of lily. (<b>B</b>). The MDA content of lily. (<b>C</b>). The REL rate of lily. Note: CK: H<sub>2</sub>O; M1: 100 μmol/L MT; M2: 200 μmol/L MT; P1: 0.5 g/L PFA; P2: 1.0 g/L PFA; C1: 20 mmol/L CaCl<sub>2</sub>; C2: 40 mmol/L CaCl<sub>2</sub>. Different lowercase letters indicate significant differences between treatments (<span class="html-italic">p</span> &lt; 0.05).</p> "> Figure 3
<p>Chlorophyll content of ‘Tiny Diamond’ after application of exogenous substances. Different lowercase letters indicate significant differences between treatments (<span class="html-italic">p</span> &lt; 0.05).</p> "> Figure 4
<p>SOD content of ‘Tiny Diamond’ after application of exogenous substances. Different lowercase letters indicate significant differences between treatments (<span class="html-italic">p</span> &lt; 0.05).</p> "> Figure 5
<p>Content of osmoregulatory substances in ‘Tiny Diamond’ after application of exogenous substances. (<b>A</b>). Proline content. (<b>B</b>). Soluble protein content. (<b>C</b>). Total soluble sugar content. Different lowercase letters indicate significant differences between treatments (<span class="html-italic">p</span> &lt; 0.05).</p> "> Figure 6
<p>Correlation analysis of ten indicators under treatment with three exogenous substances. Note: * means correlation is extremely significant at the 0.05 level, ** means correlation is extremely significant at the 0.01 level.</p> ">
Review Reports Versions Notes

Abstract

:
Lily is one of the world’s important ornamental flowers. Potted Asiatic lily is a further selected dwarf cultivar suitable for indoor or garden planting. However, there is a lack of relevant research on the cultivation adaptability of potted Asiatic lilies cultivars in the Chongqing region which in the southwest of China. This study selected five potted Asiatic lily cultivars, and the phenological period, stem and leaf characteristics, and flowering traits were assessed through statistical observation. The Asiatic lily ‘Tiny Ghost’ and ‘Tiny Double You’ are well-suited for both spring and autumn planting in Chongqing, while ‘Sugar Love’ and ‘Curitiba’ are best planted in the spring. The ‘Tiny Diamond’ is more appropriate for autumn planting due to its low tolerance to high temperature. The application of exogenous substances, including calcium chloride (CaCl2), potassium fulvic acid (PFA) and melatonin (MT), can mitigate the detrimental effects of high-temperature stress on ‘Tiny Diamond’ by regulating photosynthesis, antioxidant systems, and osmotic substance content. A comprehensive evaluation using the membership function showed that the effect of exogenous CaCl2 treatment is the best, followed by exogenous PFA treatment. CaCl2 acts as a positive regulator of heat stress tolerance in Asian lilies, with potential applications in Asian lily cultivation. This study provides reference for cultivation and application of Asian lily varieties in Chongqing region, and also laid the foundation for further research on the mechanism of exogenous substances alleviating heat stress in lilies.

1. Introduction

Lily is a general term for perennial herbaceous bulb plants of the Liliaceae genus [1]. Due to their beautiful color, fragrance, and intricate patterns, lilies are cherished by people worldwide. They possess high ornamental value, and modern commercial breeding for lilies commenced in the Netherlands, the United States, and France at the beginning of the last century [2]. To date, breeders have developed over 10,000 cultivars of lilies [3,4]. Asiatic lilies represent a population derived from interspecific hybridized breeding within the curly petals group [5,6], characterized by diverse colors and markings [7], moderate height, light or no fragrance of flowers [8]. Potted Asiatic lily is a further selected dwarf cultivar suitable for indoor or garden planting [9].
There are many cultivars of lilies on the market, but the characteristics of lily cultivars are different. In order to promote the application of lilies in various places, it is also necessary to screen for suitable cultivars based on the climate. Therefore, the introduction of lilies in various places to observe their adaptability is often the first thing to do [10]. Lilies prefer cool and humid climates, and the optimal temperature for growth and development is 18–22 °C. High temperatures can result in developmental delays and bud abortion of lilies, leading to a deterioration of their germplasm and causing significant harm to their ornamental and economic value [11,12]. The growth performance of Asiatic lilies is adversely affected by high temperature conditions, with certain cultivars exhibiting symptoms such as bud extinction, abortion, and lodging [13,14]. The Asian hybrid lily ‘Akita Petit Whit’ is a selected antherless cultivar, but high temperature will make the cultivar develop a complete anther, which seriously affects the economic benefit [15]. The cultivation of the Asian lily ‘Elite’ at temperatures exceeding 30 °C led to aberrant growth and a decline in the quality of cut flowers [16]. In addition, high temperature also hindered the synthesis of key compounds for the lily’s fragrance and color, greatly reducing the ornamental value of lily [17,18]. Exploring specific solutions to problems faced by lily in the process of high temperature stress is not only conducive to reducing the damage caused by high temperature stress on the growth and development of lily, but also can improve the heat resistance of lily to a certain extent and improve the germplasm resources of lily in this region.
Studies have demonstrated that the utilization of appropriate concentrations of exogenous substances can effectively mitigate the damage caused to plants by high temperature stress [19,20,21,22]. Ca2+ is a well-known and widely used exogenous substance in agricultural production. Numerous studies have demonstrated that the application of exogenous Ca2+ in suitable amounts can significantly enhance plant heat tolerance [23,24]. Research indicates that exogenous CaCl2 can activate heat stress transcription factors, thereby improving the heat tolerance of Lilium longiflorum [23,25]. MT is a growth regulator, an indirect antioxidant, and a signaling molecule in plants [26]. Exogenous MT can safeguard buckwheat seeds under high temperature stress by increasing osmotic substance content and antioxidant enzyme activity, and enhance their germination rate [27]. High temperature stress can directly result in membrane system damage and antioxidant system disorder in lilies. MT can mitigate the damage caused by high temperature stress by enhancing the activity of antioxidant enzymes. Currently, the research on MT is mostly focused on cash crops, but its role and regulation mechanism in ornamental plants are seldom reported. PFA is a type of highly efficient potassium fertilizer formed through the chelation of fulvic acid extracted from natural humic acid and K+ [28]. PFA alleviates abiotic stress in plants by regulating photosynthesis and maintaining the balance of osmotic substances and the antioxidant system [28,29].
Chongqing province in the southwest of China, features a humid subtropical monsoon climate and is renowned for its high summer temperatures [30]. Currently, there is a lack of relevant research on the cultivation adaptability of potted Asiatic lilies cultivars in the Chongqing region. To identify suitable Asiatic lily cultivars for planting in Chongqing, five potted Asiatic lily cultivars were selected, and the phenological period, stem and leaf characteristics, and flowering traits were assessed through statistical observation. The Asiatic lily ‘Tiny Diamond’ was found to be sensitive to high temperatures, and different concentrations of exogenous substances were applied to enhance its high temperatures tolerance. The exogenous substances used in this study included CaCl2, PFA, and MT solution. Indicators such as chlorophyll content, leaf relative water content (RWC), relative electrolytic leakage (REL) rate, malondialdehyde (MDA) content, Superoxide dismutase (SOD) activity, and osmotic substance content in Asiatic lilies under different treatments were measured. The effects of these treatments on the high temperatures tolerance of Asiatic lilies were evaluated. This study aims to provide scientific evidence for the introduction and cultivation of potted Asiatic lilies in Chongqing. It is hoped that the application of exogenous substances can optimize the cultivation of Asiatic lilies during the high-temperature season in Chongqing and lay the groundwork for breeding new heat-tolerant Asiatic lily cultivars.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

The Asian lily bulbs of Lilium Asiatica Hybrida ‘Tiny Double You’, ‘Sugar love’, ‘Tiny Diamond’, ‘Curitiba’, and ‘Tiny Ghost’ are imported from the Netherlands. The diameter of bulbs are 12–18 cm. The introduction and planting trials were conducted in Beibei District, Chongqing, at Southwest University (29°48′ N, 106°24′ E), in a subtropical monsoon humid climate. The spring trial ran from 7 March to 20 May 2023, and the autumn trial from 17 October 2023, to 5 February 2024.
The ‘Tiny Diamond’ was selected for the high-temperature stress experiment in an artificial climate chamber(TENLIN, SPX-1500F, Jiangsu, China). Under normal conditions, the chamber was set to 23 °C/17 °C (day/night) with a 14/10-h photoperiod, 60% relative humidity, and 14,000 lx light intensity. For the high-temperature treatment, the temperature was adjusted to 36 °C/31 °C (day/night), while other conditions remained the same.

2.2. Morphological Observations

Growth conditions of each lily cultivar were regularly monitored throughout the growth period, and growth and morphological indices were recorded at scheduled intervals. Observations began at planting and continued through seedling emergence, squaring date, first-flowering date, full-blossom date, and final-flowering date. The flowering period and life cycle of Asiatic lilies in both spring and autumn were calculated. After bud formation, the number of flower buds was recorded. At full-blossom date, plant height, stem diameter, and leaf number were measured. At final-flowering date, the flowering rate was calculated. For each morphological index, 10 plants were sampled, with measurements repeated three times.

2.3. Exogenous Substances Treatment

When the surface part of the lily grew to approximately 20–25 cm, root irrigation treatment and leaf spraying treatment were conducted with MT (Macklin M813985, 98%, C13H16N2O2), PFA (Mumantian NY1106-2010, N + P2O5 + K2O ≥ 20%), and CaCl2 (Macklin C805225, 96%) solutions of various concentrations (Table 1). To avoid MT photolysis, spraying treatment was typically carried out at night, and deionized water treatment was employed as a control. The treatment was administered once every 5 days for a total of 3 times. Each treatment consisted of 7 pots and was repeated 3 times. After 72 h of high-temperature stress, leaves from the middle section of similarly positioned plants were collected for physiological index measurements.

2.4. Dermination of Physiological Index

2.4.1. Determination of RWC

Three leaves were taken from each lilies, the surface was wiped clean and precisely their fresh weight (Wf) was measured. Subsequently, the leaves were immersed in deionized water for one day. Then, filter paper was used to absorb the surface moisture, and the saturated fresh weight (Wt) was weighed. Finally, the material was placed in the oven at 105 °C for 15 min, and then dried at 80 °C until a constant weight was achieved, and the dry weight (Wd) was weighed [31]. The calculation formula is as follows:
R e l a t i v e   W a t e r   C o n t e n t ( % ) = W f − W d × 100 % W t − W d

2.4.2. Determination of Chlorophyll Content

The fresh leaves of 0.2 g was weighted. Cut the leaves and placed them into a centrifuge tube. Subsequently, 10 mL of 95% anhydrous ethanol was added, and the samples were soaked in a dark place at room temperature for 3 days. Then, the absorbance values were read respectively at the wavelengths of 649 nm and 665 nm using spectrophotometer (Shanghailingguang, 722 s, Shanghai, China), and the calculation formula is as follows [32]:
C a ( m g ⋅ g − 1 ) = ( 13.95 A 665 − 6.88 A 649 ) × V 1000 W
C b ( m g ⋅ g − 1 ) = ( 24.96 A 649 − 7.32 A 665 ) × V 1000 W
C h l   C o n t e n t ( m g ⋅ g − 1 ) = C a + C b
V: Total volume of extract (mL);
W: Sample weight (g).

2.4.3. Determination of REL Rate and MDA Content

The sample of 0.5 g leaf was cut into small pieces and placed in a test tube with 30 mL of deionized water. The tube was shaken at 100 rpm at room temperature for 3 h, after which the solution’s REL rate (S1) was measured (Leici DDS-307, Shanghai, China). The sample was then boiled, and the REL rate (S2) was measured again. The calculation formula is as follows [33]:
R E L r a t e ( % ) = S 1 × 100 % S 2
The 0.5 g of leaf sample were homogenated 5 mL of 5% trichloroacetic (TCA), and then centrifuged (ThermoFisher ST8R, Shanghai, China) with 4000 rpm at 4 °C for 10 min. The 2 mL supernatant was mixed with 2 mL of 0.67% thiobarbituric acid (TBA) then react in boiling water bath for 15 min. After cooling to room temperature, the absorbance was measured at 532 nm, 600 nm and 450 nm, respectively [34]. The calculation formula is as follows:
M D A   c o n t e n t n m o l / g = 6.45 A 532 − A 600 − 0.56 × A 450 × V W
V: Total volume of extract (mL);
W: Sample weight (g).

2.4.4. Determination of SOD Content

The 0.2 g of leave sample were homogenized with 10 mL phosphate buffer saline (PBS, 0.05 mol/L, pH 7.8), and centrifuged at 4 °C, 10,000 rpm for 15 min. The supernatant was the crude enzyme extract, which was collected and used to determine the activity of SOD. The reaction solution for SOD activity consisted of 0.1 mL of crude enzyme extract, 1.5 mL of PBS (0.05 mol/L, pH 7.8), 0.3 mL of methionine (Met, 130 mmol/L), 0.3 mL of nitrogen blue tetrazole (NBT, 750 µmol/L), 0.3 mL of ethylenediaminetetraacetic acid disodium salt (EDTA-Na2, 100 μmol/L), 0.5 mL deionized water, and 0.3 mL riboflavin solution (20 µmol/L) The reaction was incubated at 4000 lux for 25 min before measuring at 560 nm. The PBS (0.05 mol/L, pH 7.8) used as the blank. The calculation formula is as follows [35]:
S O D   c o n t e n t U / g = A c k − A E × V A c k × W × V t × 0.5
A c k : Absorbance of light contrast tube;
A E : Absorbance of the sample tube;
V: Total volume of extract (mL);
V t : Sample dosage at the time of determination (mL);
W: Sample weight (g).

2.4.5. Determination of Osmoregulatory Substances Content

Proline content was determined according to acidic ninhydrin method [36]. A 0.2 g leaf sample was ground and mixed with 5 mL of 3% sulfosalicylic acid. After heating in a boiling water bath for 5 min, 2 mL of the upper clear liquid was collected and mixed with 2 mL of glacial acetic acid and 2 mL of ninhydrin solution. The mixture was heated again in a boiling water bath, then 4 mL of toluene was added for extraction. Using toluene as the blank control, absorbance was measured at 520 nm. Proline content was calculated using the formula:
P r o l i n e   c o n t e n t m g ⋅ g − 1 = C × V A × W
C: Standard curve value (μg);
V: Total volume of extract (mL);
A: The volume of extracted liquid taken during the determination (mL);
W: Sample weight (g).
Soluble protein content was determined according to coomassie brilliant blue G-250 method [37]. Leaf samples were homogenized with 5 mL PBS (0.05 mol/L, pH 7.8) and then centrifuged at 4 °C, 10,000 rpm for 15 min. The 0.1 mL supernatant was mixed with 0.9 mL of water and 5 mL of coomassie brilliant blue G-250 The absorbance was measured at 595 nm. Soluble protein content was calculated using the formula:
S o l u b l e   p r o t e i n   c o n t e n t m g ⋅ g − 1 = C × V t × N W × V s × 1000
C: The soluble protein content of the standard curve (ug);
V t : Total volume of extract (mL);
V s : Sample supernatant liquid volume (mL);
N: Dilution multiple;
W: Sample weight (g).
Soluble sugar content was determined according to anthrone reagent method [38]. The residual enzyme solution from the soluble protein assay was used for soluble sugar determination. The solution was heated in a boiling water bath for 30 min, and then centrifuged at 4 °C, 8000 rpm for 10 min, and take the supernatant and dilute to 25 mL. Then, 0.5 mL of the supernatant was mixed with 0.5 mL of anthrone reagent and 5 mL of concentrated sulfuric acid, shaken, and immediately heated in a boiling water bath. The absorbance was measured at 630 nm, and soluble sugar content was calculated using the formula:
S o l u b l e   s u g a r   c o n t e n t m g · g − 1 = C × V t × N W × V s × 1000
C: The sugar content of the standard curve (μg);
V t : Total volume of extract (mL);
V s : Sample dosage in determination (mL);
N: Dilution multiple;
W: Sample weight (g).

2.5. Data Analysis and Processing

Excel 2022 was utilized for data analysis, SPSS 27.0 was employed to analyze various indicators, and the membership function method was applied to assess the heat resistance of the Asian lily ‘Tiny diamond’ under high temperature stress through exogenous application of CaCl2, MT and PFA. The calculation formula is as follows:
f x i = X i − X m i n ∕ X m a x − X m i n
f x i = X i − X m i n ∕ X m a x − X m i n − 1
The value of f x i represents the membership function, where X i denotes the average measured value of an indicator in each treatment group, and X m a x and X m i n represent the maximum and minimum values of an indicator in each treatment group, respectively. Formula (1) is utilized for positive correlation with heat resistance, while Formula (2) is employed for negative correlation.
After obtaining the membership function values for each group, the comprehensive heat resistance indexes of three exogenous substances to ‘Tiny diamond’ were calculated using the following methods:
V i = ∑ i = 1 n X i − X ¯ i 2 X ¯ i
w i = V i ∑ i = 1 n V i
D = ∑ i = 1 n f x i × W i
In each treatment group, V i represents the standard deviation coefficient of an indicator, while X ¯ i   represents the average value of the indicator. W i denotes the weight of a specific index in each treatment group, the variable D signifies a comprehensive assessment, with higher values indicating greater index comprehensiveness.

3. Results

3.1. Observation on the Introduction of Five Asiatic Lily Cultivars in Chongqing Region

To evaluate the adaptability of five Asiatic lily cultivars in Chongqing region, planting observations were conducted in spring and autumn respectively. Morphological observations revealed distinct differences in the flowers of the five lily cultivars (Figure 1). The data showed significant seasonal variation in both the florescence and growth cycle. On average, the flowering period lasted 21.6 days in spring but extended to 52.6 days in autumn. Similarly, the growth cycle increased from 65.8 days in spring to 96 days in autumn (Table 2). Temperature trends in Beibei District, Chongqing, during the study indicated that the average daily temperature in autumn was lower than in spring (Figure S1). An analysis of the growth characteristics revealed minimal differences between the main vegetative organ traits of ‘Sugar Love’ and ‘Curitiba’ across both seasons. However, both the number of buds and the flowering rate significantly declined in autumn (Table 3). In contrast, ‘Tiny Ghost’ and ‘Tiny Double You’ demonstrated relatively stable performance in both seasons. ‘Tiny Diamond’ exhibited poor growth in spring, with leaf burn, yellowing buds, bud abortion, and other adverse conditions during the late growth stage, with more than half of the plants affected by leaf burn (Figure S2). However, autumn cultivation showed significantly improvement, particularly in the flowering rate, which increased by 56.67%. These results indicate that ‘Tiny Diamond’ is highly sensitive to high temperatures, resulting in poor growth and flowering outcomes in spring, making it more suitable for autumn cultivation. The other four cultivars performed well in both seasons, with ‘Sugar Love’ and ‘Curitiba’ particularly suited for spring cultivation, while ‘Tiny Ghost’ and ‘Tiny Double You’ are ideal for planting in both spring and autumn.

3.2. Exogenous Application of Different Substances Remission Oxidative Stress of Lily Under High Temperature Stress

In order to improve the heat resistance of Asiatic lily, we choose ‘Tiny diamond’ with high temperature sensitive for treatment. Three types of exogenous substances were applied to explore their effects on the heat resistance of Asiatic lilies, and to determine whether these substances can enhance the adaptability of Asiatic lilies to high-temperature climates.
The physiological responses of lilies to high-temperature stress were assessed by measuring key indicators. Leaf RWC, which reflects the plant’s water status and indicates the degree of heat-induced damage, increased in all treatment groups compared to the control. Notably, treatments with 40 mmol/L CaCl2 (C2) and 100 μmol/L MT (M1) significantly improved leaf RWC, showing increases of 6.37% and 5.45%, respectively, compared to the control (Figure 2A). The remaining four treatment groups had no significant change compared with the control group. These results indicated that the application of CaCl2 and MT could increase the water content of lily leaves to a certain extent.
High temperature stress will first leads to plant dehydration and lipid peroxidation of cells. During this process, reactive oxygen accumulate in large quantities on the cell membrane, resulting in lipid peroxidation and electrolyte leakage [39]. MDA is one of the products of membrane peroxidation, which has cytotoxicity. Excessive accumulation will damage the structure and function of cell membrane. Under high temperature stress, the content of MDA in all treatment groups was lower than that in control group. The MDA content of 1.0 g/L PFA (P2) and 40 mmol/L CaCl2 (C2) treatments were significantly reduced by 37.65% and 37.21% respectively, compared with the control (Figure 2B). Other treatments had no significant effect. These results indicate that exogenous application of PFA and CaCl2 can effectively reduce MDA content in lily leaves, and has a significant effect on alleviating MDA accumulation in plant cells under high temperature stress.
The relative electrolyte leakage rate of leaves is an important indicator of cell membrane damage [40]. Compared with the control, the relative electrolyte leakage rate of all the treatment groups were significantly reduced. The most effective treatment was 1.0 g/L PFA (P2), which reduced electrolyte leakage by 12.84%, followed by 40 mmol/L CaCl2 (C2), which decreased leakage by 10.35%. Other treatments, including 100 μmol/L MT (M1), 0.5 g/L PFA (P1), 200 μmol/L MT (M2) and 20 mmol/L CaCl2 (C1), the relative electrolyte leakage rate was reduced by 9.21%, 9.04%, 6.70% and 4.56%, respectively, compared with the control (Figure 2C). These results indicate that exogenous application of CaCl2, MT and PFA can effectively reduce the electrolyte leakage rate and remission the damage of cell membrane of lily under high temperature stress.

3.3. Effects of Exogenous Application of Different Substances on Chlorophyll Content of Lily Under High Temperature Stress

Chlorophyll content influences the primary metabolic activities of plants and directly reflects the plant’s response to high-temperature stress [41]. Under high-temperature stress, the application of different concentrations of MT, PFA, and CaCl2 significantly increased the chlorophyll a, chlorophyll b, and total chlorophyll contents in lilies. Among these treatments, 40 mmol/L CaCl2 (C2) and 20 mmol/L CaCl2 (C1) were the most effective, with chlorophyll a content increasing by 43.59% and 38.46%, respectively, compared to the control. The highest chlorophyll b content was recorded after treatment with 40 mmol/L CaCl2 (C2) and 20 mmol/L CaCl2 (C1), which was 1.35 times higher than that of the control (Figure 3). No significant differences in chlorophyll b content were observed following the other treatments. The increase in total chlorophyll content over the control for the various exogenous substance treatments was 28.81% (M1, 100 μmol/L MT), 22.03% (H2, 200 μmol/L MT), 28.81% (P1, 0.5 g/L PFA), 23.73% (P2, 1.0 g/L PFA), 37.29% (C1, 20 mmol/L CaCl2), and 40.68% (C2, 40 mmol/L CaCl2).

3.4. Effects of Exogenous Application of Different Substances on SODcontent in Lily Under High Temperature Stress

SOD is the first line of defense of plant antioxidant enzyme system, which plays an important role in scavenging free radicals, preventing oxygen free radicals from destroying cell components, structure and function, and protecting cells from oxidative damage [42]. The SOD activity of 40 mmol/L CaCl2 (C2) treatment was reached the highest level compare to the control under high temperature stress.And the SOD activity of 100 μmol/L MT (M1), 200 μmol/L MT (M2), 1.0g/L PFA (P2) and 20 mmol/L CaCl2 (C1) treatment were increased by 16.93%, 9.62%, 9.73% and 1.89% respectively, however, there was no significant difference compare to the control (Figure 4). In addition, SOD activity of 0.5 g/L PFA (P1) treatment was significantly lower than that of control. These results suggest that exogenous CaCl2 significantly enhances SOD activity in lilies, providing better protection against oxidative stress under high-temperature conditions, while the effects of MT and PFA on SOD activity were less pronounced.

3.5. Effects of Different Substances Applied Externally on Osmoregulatory Substances of Lily Under High Temperature Stress

Osmotic regulation is an important mechanism for plants to respond to stress. Plants can enhance their stress resistance by accumulating osmotic substances [43]. In this study, the proline content, soluble protein and soluble sugar in lily treated with different exogenous substances under high temperature stress were determined. The content of proline can reflect the stress resistance of the plant to a certain extent. Under high temperature stress, the proline content of all the treatment groups were all higher than the control to varying degrees. After treatment with 40 mmol/L CaCl2 (C2), the proline content increased the most, reaching 77.47 μg/g. Followed by 1.0 g/L PFA (P2), 200 μmol/L MT (M2), 20 mmol/L CaCl2 (C1) and 0.5 g/L PFA (P1) treatments, the proline content was 1.63 times, 1.58 times, 1.57 times and 1.35 times of the control, respectively (Figure 5A). The results showed that exogenous application of CaCl2 and PFA increased the content of proline in lily leaves under high temperature stress.
Soluble protein is an important osmoregulatory substance, which can reflect the overall metabolic level of cells to a certain extent [44]. After treatment with 40 mmol/L CaCl2 (C2), 1.0 g/L PFA (P2) and 0.5 g/L PFA (P1), the soluble protein content in lily leaves was significantly increased by 38.02%, 33.80% and 29.13% compared with the control group, respectively. Compared with the control, the contents of soluble protein after treatment with 20 mmol/L CaCl2 (C1), 100 μmol/L MT (M1) and 200 μmol/L MT (M2) were also significantly increased by 23.62%, 20.96% and 14.06%, respectively (Figure 5B). The results showed that exogenous application of CaCl2, MT and PFA could effectively increase the content of soluble protein in lily leaves under high temperature stress.
Soluble sugars include sucrose and reducing sugars. Sugar provides energy for the life activities of plant, and also regulates osmotic pressure and maintains the stability of cell membrane [45]. Under high-temperature stress, the soluble sugar content in lily leaves increased significantly after treatment with 1.0 g/L PFA (P2), 40 mmol/L CaCl2 (C2), and 20 mmol/L CaCl2 (C1). The most pronounced effect was observed with 1.0 g/L PFA (P2), which resulted in a 48.24% increase compared to the control group, followed by 40 mmol/L CaCl2 (C2) and 20 mmol/L CaCl2 (C1), with increases of 17.74% and 6.53%, respectively (Figure 5C). There was no significant difference between residual treatment and control. Among them, the soluble sugar content in lily decreased following the application of 200 μmol/L MT (M2) and 0.5 g/L PFA (P1). These results indicate that exogenous application of PFA and CaCl2 can effectively increase the soluble sugar content in lily leaves.

3.6. Comprehensive Evaluation of Heat Resistance of Lily ‘Tiny Diamond’ by Exogenous Application of Different Substances

Based on the results of correlation analysis, chlorophyll a (chl a), chlorophyll b (chl b), total chlorophyll content, REL rate, RWC, MDA, proline (Pro), soluble protein, total soluble sugar, and SOD activity exhibited significant correlations (Figure 6). These nine indicators were chosen for membership function analysis, and their membership function values were calculated using weighted arithmetic average. This approach allowed for the determination of synthetic membership function values for each treatment group, reflecting the overall effect of different exogenous substances on the heat resistance of the Asiatic lily ‘Tiny Diamond’. The ranking of the comprehensive membership function values, from highest to lowest, was C2 > P2 > C1 > P1 > M1 > M2 > CK (Table 4). This indicates that the application of MT, PFA, and CaCl2 effectively reduced high temperature stress damage in lilies. Among the treatments, the most effective was 40 mmol/L CaCl2, followed by 1.0 g/L PFA and 20 mmol/L CaCl2. These results suggest that CaCl2, particularly at a concentration of 40 mmol/L, offers the most substantial improvement in heat resistance, with PFA also significantly mitigating high-temperature stress.

4. Discussion

Introduced cultivars are an important way to enrich plant cultivars in a certain region, and it is also one of the main methods of innovative utilization of germplasm resources, which is of positive significance for production and cultivation, and innovative breeding. Compared with the origin, if introduced cultivars can grow over one year without special measures, complete the life cycle, and retain their ornamental traits and other good qualities of the plant have not been reduced, this can be considered a successful introduction. Previous studies conducted across Northeast, Central-South, and Eastern China have evaluated the growth adaptability and ornamental traits of various lily cultivars, demonstrating that all tested cultivars can grow and develop normally in these regions [46,47,48]. This study expands on these findings by analyzing the seasonal cultivation characteristics of five lily cultivars specifically in Chongqing. Our results indicate that four of the cultivars are well-suited for cultivation in Chongqing, with cultivation temperature emerging as the critical factor influencing successful introduction. High temperature stress shortened the florescence of lily and made lily complete the growth cycle more quickly. Notably, ‘Tiny Diamond’ was identified as a heat-sensitive cultivar, suggesting its limited adaptability to high-temperature conditions in this region.
High temperature stress induced dehydration in plants can trigger oxidative stress, leading to lipid peroxidation and electrolyte leakage. MDA, a primary product of lipid peroxidation, disrupts cell membrane integrity [49]. SOD as the first line of defense in the antioxidant system, works alongside other antioxidant enzymes to enhance plant stress resistance [50]. This study indicated that the application of CaCl2, MT, and PFA effectively reduces water loss in Asian lilies, decreases relative conductivity and MDA content in the leaves, and increases SOD activity. It has reported that Ca2+ stabilizes cell osmotic pressure in plants, protecting membrane structure and function, and elucidated the physiological mechanism by which exogenous Ca2+ repair high-temperature stress-induced membrane damage [51]. It also suggests that exogenous CaCl2 alleviates high temperature stress in peony primarily by enhancing SOD activity [52]. Furthermore, the fulvic acid (FA) and PFA were reported that they could enhance the activity of various antioxidant enzymes, thereby protecting plants from oxidative damage [53]. Similarly, researches demonstrated that exogenous MT helps maintain cellular homeostasis in plant cells by increasing SOD activity and reducing oxidative damage [54].
Chlorophyll content is directly related to photosynthetic rate and is crucial for plant growth and development [55]. This study shows that exogenous application of CaCl2, MT, and PFA delays chlorophyll degradation in lily leaves, promotes photosynthesis, and mitigates heat damage. Similar results have been reported, indicating that CaCl2 enhances heat tolerance in roses by increasing chlorophyll content and regulating photosynthesis [56].
Osmotic regulation is a crucial mechanism for plants to cope with stress conditions, as they accumulate osmolytes to adjust cellular osmotic potential and maintain osmotic pressure [57,58]. The upregulation of proline synthesis has been confirmed as a key stress adaptation mechanism, helping to maintain intracellular homeostasis and redox balance by modulating the antioxidant system [59]. Soluble proteins, as major components of the cell and organelle matrix, play an important role in regulating cellular osmotic potential [60]. Soluble sugars are essential for plant growth, development, and the response to abiotic stress [61]. This study showed that the exogenous application of CaCl2 or PFA can significantly increase the levels of proline, soluble proteins, and soluble sugars in Asian lilies under high temperature stress, thereby enhancing heat tolerance. Similarly, CaCl2 treatment enhanced leaf dry matter and proline content, improving the potential for recovery from oxidative damage in tea plants [62].
In this study, the effects of three exogenous substances on Asian lilies were assessed by measuring their physiological and biochemical responses to high-temperature stress, followed by membership function analysis. The combination of multiple indicators and the membership function method effectively evaluated the relationship between exogenous substances and heat tolerance in lilies. Indicator weights were determined using principal component analysis. These results indicated that 40 mmol/L CaCl2 was the most effective treatment, outperforming both the control and other groups across various physiological indicators. This is consistent with previous studies showing that CaCl2 alleviates oxidative stress in tomatoes under abiotic stress and mitigates stress in cucumbers by maintaining redox and osmotic balance, improving photosynthesis, and enhancing stress resistance [44,63]. In conclusion, exogenous CaCl2 acts as a positive regulator of heat stress tolerance in Asian lilies, with potential applications in Asian lily cultivation.

5. Conclusions

Asiatic lily ‘Tiny Ghost’ and ‘Tiny Double You’ are well-suited for both spring and autumn planting in Chongqing, while ‘Sugar Love’ and ‘Curitiba’ are best planted in the spring. The ‘Tiny Diamond’, however, is more appropriate for autumn planting due to its low tolerance to high temperature. The application of exogenous substances such as CaCl2, MT, and PFA can mitigate the detrimental effects of high-temperature stress on ‘Tiny Diamond’. Analysis of heat tolerance indicators revealed that high temperature stress primarily affects the antioxidant system and osmotic regulation mechanisms. A comprehensive evaluation using the membership function showed that the effect of exogenous CaCl2 treatment is the best, followed by exogenous PFA treatment.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/horticulturae10111216/s1. Figure S1: Temperature changes during lily cultivation in Chongqing region. A. Temperature changes in spring; B. Temperature changes in autumn. Figure S2: Phenotype of Asiatic lily ‘Tiny diamond’ after infection with leaf burn disease.

Author Contributions

The authors confirm their contribution to the paper as follows: study conception and design, J.L., L.L., S.S. and D.L.; data collection, N.B., Y.S., Y.L. and L.T.; analysis and interpretation of results, N.B., Y.S. and Y.L.; Funding acquisition, S.S., L.L. and D.L.; draft manuscript preparation, N.B., Y.S. and D.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Key Project of Chongqing Technology Innovation and Application Development Special Project (Grant Nos. CSTB2023TIAD-LUX0005) and the Chinese Academy of Sciences STS supporting project of Fujian Province (Grant Nos. 2022T3031).

Data Availability Statement

Data is contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Asian lily cultivars. (A). ‘Tiny Double You’; (B). ‘Curitiba’; (C). ‘Tiny Diamond’; (D). ‘Sugar Love’; (E). ‘Tiny Ghost’.
Figure 1. Asian lily cultivars. (A). ‘Tiny Double You’; (B). ‘Curitiba’; (C). ‘Tiny Diamond’; (D). ‘Sugar Love’; (E). ‘Tiny Ghost’.
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Figure 2. Oxidative stress indexes of ‘Tiny Diamond’ after exogenous application of different substances under high temperature stress. (A). The relative water content of lily. (B). The MDA content of lily. (C). The REL rate of lily. Note: CK: H2O; M1: 100 μmol/L MT; M2: 200 μmol/L MT; P1: 0.5 g/L PFA; P2: 1.0 g/L PFA; C1: 20 mmol/L CaCl2; C2: 40 mmol/L CaCl2. Different lowercase letters indicate significant differences between treatments (p < 0.05).
Figure 2. Oxidative stress indexes of ‘Tiny Diamond’ after exogenous application of different substances under high temperature stress. (A). The relative water content of lily. (B). The MDA content of lily. (C). The REL rate of lily. Note: CK: H2O; M1: 100 μmol/L MT; M2: 200 μmol/L MT; P1: 0.5 g/L PFA; P2: 1.0 g/L PFA; C1: 20 mmol/L CaCl2; C2: 40 mmol/L CaCl2. Different lowercase letters indicate significant differences between treatments (p < 0.05).
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Figure 3. Chlorophyll content of ‘Tiny Diamond’ after application of exogenous substances. Different lowercase letters indicate significant differences between treatments (p < 0.05).
Figure 3. Chlorophyll content of ‘Tiny Diamond’ after application of exogenous substances. Different lowercase letters indicate significant differences between treatments (p < 0.05).
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Figure 4. SOD content of ‘Tiny Diamond’ after application of exogenous substances. Different lowercase letters indicate significant differences between treatments (p < 0.05).
Figure 4. SOD content of ‘Tiny Diamond’ after application of exogenous substances. Different lowercase letters indicate significant differences between treatments (p < 0.05).
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Figure 5. Content of osmoregulatory substances in ‘Tiny Diamond’ after application of exogenous substances. (A). Proline content. (B). Soluble protein content. (C). Total soluble sugar content. Different lowercase letters indicate significant differences between treatments (p < 0.05).
Figure 5. Content of osmoregulatory substances in ‘Tiny Diamond’ after application of exogenous substances. (A). Proline content. (B). Soluble protein content. (C). Total soluble sugar content. Different lowercase letters indicate significant differences between treatments (p < 0.05).
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Figure 6. Correlation analysis of ten indicators under treatment with three exogenous substances. Note: * means correlation is extremely significant at the 0.05 level, ** means correlation is extremely significant at the 0.01 level.
Figure 6. Correlation analysis of ten indicators under treatment with three exogenous substances. Note: * means correlation is extremely significant at the 0.05 level, ** means correlation is extremely significant at the 0.01 level.
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Table 1. Experimental design of treatment of different exogenous substances.
Table 1. Experimental design of treatment of different exogenous substances.
TreatmentExogenous Substances
CKH2O
M1100 μmol/L MT
M2200 μmol/L MT
P10.5 g/L PFA
P21.0 g/LPFA
C120 mmol/L CaCl2
C240 mmol/L CaCl2
Table 2. Spring and autumn phenological periods of five Asiatic lily cultivars.
Table 2. Spring and autumn phenological periods of five Asiatic lily cultivars.
CultivarSeasonSeedling Emergence (Day)Planting to Bud (Day)Planting to Flower Initiation (Day)Planting to Full Bloom (Day)Planting to Final Flowering (Day)Florescence (Day)Growth Cycle (Day)
Tiny Double Youspring8253844582058
autumn821496011162111
Curitibaspring5153942592059
autumn7174155904990
Tiny Diamondspring17304757672067
autumn8164957904190
Sugar Lovespring18324755712471
autumn12275373954295
Tiny Ghostspring15335055742474
autumn8142551946994
Table 3. Characteristics of five cultivars of Asian lily.
Table 3. Characteristics of five cultivars of Asian lily.
CultivarSeasonPlant Height
(cm)		Stem Diameter
(mm)		Leaf Wide
(cm)		Number of
Flower Buds		Flower Diameter
(cm)		Flowering Rate (%)
Tiny Double Youspring31.58 ± 1.005.36 ± 0.1775.30 ± 1.234.30 ± 0.379.44 ± 0.12100.00%
autumn41.19 ± 1.355.22 ± 0.1478.30 ± 1.718.40 ± 0.699.49 ± 0.15100.00%
Curitibaspring37.41 ± 0.936.19 ± 0.1264.40 ± 3.235.30 ± 0.2114.22 ± 0.10100.00%
autumn47.11 ± 0.406.67 ± 0.1090.90 ± 4.254.30 ± 0.2614.68 ± 0.1260.00%
Tiny Diamondspring37.73 ± 1.508.00 ± 0.13126.40 ± 2.803.50 ± 0.5817.43 ± 0.4040.00%
autumn54.00 ± 1.228.66 ± 0.10118.00 ± 3.017.20 ± 0.3316.04 ± 0.1496.67%
Sugar Lovespring47.03 ± 1.097.02 ± 0.20138.30 ± 4.159.50 ± 0.2713.55 ± 0.17100.00%
autumn48.61 ± 1.267.47 ± 0.09146.80 ± 2.456.90 ± 0.1814.68 ± 0.1966.67%
Tiny Ghostspring42.72 ± 1.187.85 ± 0.17144.20 ± 3.417.20 ± 0.3315.20 ± 0.28100.00%
autumn40.35 ± 1.027.74 ± 0.20131.20 ± 2.564.30 ± 0.4213.98 ± 0.2186.67%
Note: The data in the table are mean ± standard error.
Table 4. Comprehensive indexes of heat resistance of ‘Tiny Diamond’ by three exogenous substances.
Table 4. Comprehensive indexes of heat resistance of ‘Tiny Diamond’ by three exogenous substances.
TreatmentSpraying HormoneComposite IndexSort
CKH2O0.0567
M1100 μmol/L MT0.5215
M2200 μmol/L MT0.4066
P10.5 g/L PFA0.5344
P21.0 g/L PFA0.8282
C120 mmol/L CaCl20.5983
C240 mmol/L CaCl20.8431
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Bai, N.; Song, Y.; Li, Y.; Tan, L.; Li, J.; Luo, L.; Sui, S.; Liu, D. Evaluation of Five Asian Lily Cultivars in Chongqing Province China and Effects of Exogenous Substances on the Heat Resistance. Horticulturae 2024, 10, 1216. https://doi.org/10.3390/horticulturae10111216

AMA Style

Bai N, Song Y, Li Y, Tan L, Li J, Luo L, Sui S, Liu D. Evaluation of Five Asian Lily Cultivars in Chongqing Province China and Effects of Exogenous Substances on the Heat Resistance. Horticulturae. 2024; 10(11):1216. https://doi.org/10.3390/horticulturae10111216

Chicago/Turabian Style

Bai, Ningyu, Yangjing Song, Yu Li, Lijun Tan, Jing Li, Lan Luo, Shunzhao Sui, and Daofeng Liu. 2024. "Evaluation of Five Asian Lily Cultivars in Chongqing Province China and Effects of Exogenous Substances on the Heat Resistance" Horticulturae 10, no. 11: 1216. https://doi.org/10.3390/horticulturae10111216

APA Style

Bai, N., Song, Y., Li, Y., Tan, L., Li, J., Luo, L., Sui, S., & Liu, D. (2024). Evaluation of Five Asian Lily Cultivars in Chongqing Province China and Effects of Exogenous Substances on the Heat Resistance. Horticulturae, 10(11), 1216. https://doi.org/10.3390/horticulturae10111216

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