Photosynthetic Responses of Anthurium × ‘Red’ under Different Light Conditions

Light is an essential energy source for plant photosynthesis, although it can also be a stress-causing element. Therefore, the current research was aimed to compare photosynthetic responses of Anthurium × ‘Red’ leaves at different positions (bottom old leaf, 1; center mature leaf, 2; top expanded leaf, 3) established under three photosynthetic photon flux densities (PPFDs): 550 μmol·m−2·s−1 as high (H), 350 μmol·m−2·s−1 as medium (M), and 255 μmol·m−2·s−1 as low (L). After six months, all the replicates were relocated to interior rooms with a PPFD of 30 μmol·m−2·s−1. There were no significant differences in chlorophyll concentration of the old leaf among treatments, before (Day 0) and after shifting the plants to interior rooms (Day 30). The total chlorophyll concentrations of the mature and top leaves increased significantly. In greenhouse conditions, H and M treatments did not show any significant change for net photosynthetic rate (Pn) at various leaf positions. However, M2 exhibited an improved Pn in the interior conditions. Plants grown under M treatment were greener and had bigger leaves compared to other treatments. Our study reveals that Anthurium × ‘Red’ photosynthesis responses to different light conditions varied distinctly. However, M treatment can keep the plants looking green by accumulating enough energy for indoor conditions, and middle and lower leaves may be triggered to restore photosynthetic activity under low light or indoor conditions.


Introduction
Shading is widely employed during the growth of plants, particularly plants with ornamental foliage to prevent damage triggered by high light intensity [1,2]. When lightharvesting antennas absorb more light energy than their potential for photochemical and non-photochemical energy dissipation, photodamage can occur [3]. In the most severe cases, this may result in the discoloration of leaves or necrosis. Light damage happens often as a result of continuous exposure to high light intensity levels [4]. As a result, growers apply shades to foliage or shade plants by covering the shutter or using a whitewash on the greenhouse cover to avoid direct exposure under high light conditions.
Light is an essential energy source for plant photosynthesis, although it can cause photodamage [5]. Light is a key environmental factor that influences the morphological and physiological performance of plants. Plants that are exposed to a specific irradiance are mostly adapted to this light environment [6]. For instance, plants exhibit notable adaptability and plasticity to varying light conditions by modifying their photosynthetic apparatus and morphological traits [5]. Various indoor, foliage plants are exposed to low-light environments for a long time after being sold [1]. The plants with a high photosynthesis ability under low light or shade conditions acclimate naturally to survive by decreasing their light compensation points and increasing leaf size and chlorophyll contents [7,8].
based information on better production and indoor use of Anthurium, and foliage plants in general.

Changes in Net Photosynthetic
Rate of Anthurium × 'Red' before and after Placement in Interior Rooms from Greenhouse During the six months of greenhouse growth, the Pn varied among the three shade levels in different months ( Figure 1). H treatment (550 µmol·m −2 ·s −1 ) did not show any significant change in Pn at various leaf positions (1, 2, and 3 represent the bottom old leaf, center mature leaf, and the top young expanded leaf, respectively) within each month. The Pn was not significantly influenced in different months at the same leaf positions for the plants established under H treatment. However, in October, the Pn of H2 was significantly (P < 0.05) higher compared to that in April ( Figure 1A). Under M treatment (350 µmol·m −2 ·s −1 ), no significant differences were noticed among the three leaf positions within the same month. In December, a significantly (P < 0.05) greater Pn was recorded compared to that in April for M1. For M2, Pn decreased significantly in April compared to that in other months, and the same trend was observed for M3 ( Figure 1B).
In October, under L treatment (255 µmol·m −2 ·s −1 ), L3 showed a significantly higher Pn compared to that of L1 and L2. Whereas in December, L2 responded with higher (P < 0.05) Pn relative to that of L1 and L3. In February and April, the Pn of L3 decreased significantly (P < 0.05) relative to that of L1 and L3 ( Figure 1C).
After moving into the interior rooms with a PPFD of 30 µmol·m −2 ·s −1 , the Pn values of all the plants dropped to negative ( Figure 2). On the first day, the Pn values were negative and continued to be negative until the 12th day. However, the Pn started to recover on the 12th day after being relocated to the interior rooms. All the marked leaves under three treatments exhibited a very low Pn value from the 12th day to the 18th day, then became negative again on the 24th day except for L1 and L2. In terms of various leaf positions within each day, in the plants established under H treatment, we found no significant differences (Figure 2A). Under M treatments, M2 showed significantly higher Pn values over those of M1 and M3 on the 12th day after moving to the interior room ( Figure 2B). However, for the plants established under the L treatments, Pn at three leaf positions did not show any differences from the 1st to the 18th day. However, from the 12th day, the plants restored their Pn and then became stable; close to 0 CO 2 (µmol·m −2 ·s −1 ), particularly the Pn of L1 and L2 increased slowly. On the 24th day, the Pn values of L3 were significantly lower than those of L1 and L2 ( Figure 2C). The numeric values 1, 2, and 3 represent the bottom old leaf, center mature leaf, and the top young expanded leaf, respectively. Vertical lines at each bar are the standard errors, and ns represent the non-significant differences at three leaf positions Different lowercase and uppercase letters represent significant differences among leaves in tested days and leaf positions on the same day, respectively, based on Tukey HSD test at P < 0.05 level.

Light-Response Curves of Photosynthesis of Anthurium × 'Red' before and after Placement in Interior Rooms
The photosynthetic parameters of the leaves under different light conditions in the greenhouse are depicted in Table 1. Where α is the initial slope of the photosynthesis curve, which indicates light use efficiency (LUE) in the low light condition. Under H treatment, α values for the three positioned leaves showed no significant differences. In plants under M treatment, α values of M1 were significantly lower than those in M2 and M3. However, for plants grown under L treatment, α values had a significant trend of L2 > L1 > L3. Plant's Pn-max under H treatments showed that H3 was significantly higher than H1 and H2; similarly, under M treatment M3 was significantly higher than M2 and M1. However, for the plants established under L treatments, Pn-max for L1 was significantly higher than that of L2 and L3. It suggested that the young leaves on the top had a stronger photosynthetic ability under H and M treatments, while bottom old leaves (L1) had a stronger photosynthetic ability than L2 and L3 when grown under the low light level. Overall, leaf position influenced the Pn-max of Anthurium (Table 1). Moreover, Isat (the saturation irradiance) of M3 was significantly higher than that of other treatments. Ic (light compensation point) decreased when the light level decreased as well as when the leaf position declined, especially under H and M treatments. The Ic levels of top new leaves were significantly higher than those of middle mature and bottom old leaves, but under L treatment, the differences in Ic between three positions were not significant. According to the differences of the α value, Pn-max, and Ic, among the leaves of different positions under various treatments, it appeared that the new leaves of plants under M treatment showed better photosynthetic ability. While the leaves around the bottom parts showed a higher photosynthesis ability than the top and middle parts under L treatment. Where H, M, and L represent PPFDs at 550, 350, and 255 µmol·m −2 ·s −1 , respectively, and numeric values 1, 2, and 3 represent the bottom old leaf, center mature leaf, and the top young expanded leaf, respectively. Data are presented as means ± standard error (n = 5). Different letters represent significant differences among treatments based on Tukey HSD test at a P < 0.05 level.
After moving the plants to the interior rooms, compared to the greenhouse conditions, the Pn-max and Isat values were lower, but Ic values were higher (Tables 1 and 2). Compared with different leaf positions under each treatment, H2 and M2 showed significantly higher Pn-max values than other positioned leaves under H and M treatment, respectively, but under L treatment, L1 and L2 showed a significantly higher Pn-max than that of L3 indicating the middle mature leaf under H and M treatment played a major role in photosynthesis. While under L treatment, the bottom old and middle mature leaves showed a higher photosynthetic ability than the top leaf, which is similar to the greenhouse condition. Where H, M, and L represent PPFDs at 550, 350, and 255 µmol·m −2 ·s −1 , respectively, and numeric values 1, 2, and 3 represent the bottom old leaf, center mature leaf, and the top young expanded leaf, respectively. Data are presented as means ± standard error (n = 5). Different letters represent significant differences among treatments based on Tukey HSD test at a P < 0.05 level.
Results of two-way ANOVA revealed that in the greenhouse, the light condition, leaf position, and their interactions significantly (P < 0.05) influenced the α. Only leaf position significantly impacted both the Pn-max (P < 0.05) and Isat (P < 0.01), whereas light condition and its interaction with leaf position did not show any influence. Furthermore, leaf position and light condition both affected the Ic, but their interaction was not significant (Table 3). However, in interior conditions, leaf position and its interaction with light condition influenced both the α (P < 0.05) and Isat (P < 0.01) significantly. Light condition, leaf position, and their interaction also significantly impacted the Pn-max (P < 0.05) as depicted in Table 3. According to the light-response curve of photosynthesis, the result showed significant differences among leaves at different positions. In the greenhouse high light conditions, the top new leaves (H3) had a higher Pn than the leaves in other positions (H1 and H2), i.e., the top expanded leaves were largely responsible for improved photosynthetic activity ( Figure 3A). After the plants moved to the interior rooms, the three photosynthetic fitting curves did not show any difference, all the Pn values stayed at low levels. However, center mature leaves (H2) had a higher Pn value than that of H1 and H3, which means the center mature leaves played an increasing role in photosynthesis ( Figure 3B).   Table 1), suggesting that the bottom old leaf had a better performance in photosynthesis under L treatment in the greenhouse. However, in the interior room, the Pn was not larger than that at 0.5 µmol·m −2 ·s −1 ( Figure 5B). According to the photosynthetic parameters and the light response curve of plants under L treatment in the interior rooms, L1 and L2 showed a better photosynthesis performance than L3, which shows that the new top leaves hardly contribute to the energy accumulation in the interior conditions (Table 2).

Chlorophyll Concentration of Anthurium × 'Red' Leaves before and after Placement in Interior Rooms
In greenhouse conditions, the leaf's color established under M and L treatments was dark-green (more fit to the requirement of horticulture products) whereas the leaf color of plants under H treatment was yellow-green with sun scorch. For the first leaf under all treatments, there was no significant difference in chlorophyll concentration before (Day 0) and after moving the plants to interior rooms (Day 30). However, the chlorophyll concentrations of both the second and third leaves of all the three treatments (H, M, and L) increased significantly (P < 0.05) since they moved to the interior room (Day 0 to 30; Tables 4 and 5).   Table 6 compares the leaf number, flower counts, and longevity and growth index between the plants before (greenhouse) and after moving to the interior room. The results revealed compared to greenhouse conditions, that plants established under M and L treatment had better flower longevity after moving to the interior room, in which the flower longevity of the M treatment was better. However, H treatment did not show any difference from greenhouse conditions to the interior room, but because of a high amount of accumulated energy, the flower had a long performance time.

Appearances of Anthurium × 'Red' under Different Light Condition
Morphologically, Anthurium × 'Red' plants under H treatments showed yellowish spots, which turned to brownish (burning) in the lateral stage ( Figure 6A). Whereas plants under M treatment were comparatively greenish and had larger leaves than other treatments ( Figure 6B). However, under L treatments, the leaves were darker in color with a smaller size ( Figure 6C).

Anthurium Showed Different Performance under Different Light Conditions
In the present study, Anthurium × 'Red' showed divergent adaptability under various light intensities. When the plants were exposed to the high light (H) initially, the chlorophyll contents decreased to prevent photoinhibition and light burn or sunburn, whereas, under low light level (L), chlorophyll contents increased to improve the light use efficiency. Variation in chlorophyll concentrations is thought to be an ubiquitous trend in plants, they are indices of plant metabolism and are primarily assessed by the availability of nutrients and ecological factors [27]. Moreover, it is a well-known phenomenon for shadetolerant species to increase chlorophyll contents with decreasing irradiance to facilitate light-harvesting [28,29]. Under high light conditions, chl-b degradation is induced by an isozyme; [30], while it increases under low light [31]. Secondly, the compensation irradiance decreased to improve the photosynthesis ability of plants under L treatments. Thirdly, plants reactivate the photosynthesis ability of older leaves to adapt to low light conditions. Leaves at different positions exhibited different photosynthetic responses to production light levels. The role of the middle and top leaves of Anthurium × 'Red' was significant to regulate photosynthesis. Compared to the H treatment, Pn-max, Isat, and Ic values of the leaves in the middle and on the top positions decreased under L treatment. However, the older leaves in the bottom showed a higher Isat under L treatment relative to that under H treatment. Photosynthetic pigments in the mesophyll cells determine the color and photosynthetic function of the leaves [31]. Under low light, plants change their physiological characteristic to get more light energy, for example, increasing leaf chlorophyll contents [32]. However, under extreme light stress, the photosynthetic process is restricted, leading to leaves etiolating [33]. It has been reported previously that plants under low light were less productive than those under high light [34]. Compared with low light, excessive light generates harmful oxygen radicals that may give rise to the process of photoinhibition and reduction in the primary productivity of plants [35], which can explain the scorches on leaves of plants under H treatment. There have been few reports that medium light conditions (about 50% of full sunlight) led to higher levels of biomass production in few species [36], which is similar to the case for Anthurium. Furthermore, previous studies have indicated that under normal environments, plants have to adapt themselves in response to fluctuations in light intensity [37,38].

Appropriate Light Could Improve Anthurium × 'Red' Performance Indoors
Apart from the natural environment, indoor ornamental plants can adapt to stressful environments by different types of receptors, including photoreceptors [39]. Under the absence of light or in limited light conditions, plants develop etiolation symptoms, such as a decrease in chlorophyll contents, reduction in leaf area, or hypocotyl elongation [33]. In this experiment, the compensation irradiance of Anthurium × 'Red' was below 5 µmol·m −2 ·s −1 while the saturation irradiance range was from 347.40 to 483.96 µmol·m −2 ·s −1 (Table 1), and the PAR of the indoor condition was about 30 µmol·m −2 ·s −1 , so the Pn reduced greatly (Figures 3-5) and influenced the plant growth. Nevertheless, the plants under different light treatments in greenhouse conditions showed a different response than those under interior conditions. Therefore, we conclude that Anthurium × 'Red' plants during the course of nursey production undergo a process of accumulating light energy. Plants under a suitable light condition accumulated light energy resulting in greater photosynthetic ability. After shifting the plant to interior conditions, the flower counts and longevity remained comparably appealing for 24 days. However, Pn values of all marked leaves quickly dropped one day after placement indoors, recovered 12 days later, but became negative again on the 24th day except for L1 and L2. These results suggest that a long time under 30 µmol·m −2 ·s −1 indoors will decrease the photosynthesis ability of Anthurium × 'Red' and low-light acclimatization in the greenhouse can delay the process [1]. However, exposure to high light and high temperature should be avoided, which may affect plant quality by chlorosis and sunburn as evidenced in previous reports on other ornamental plants [38]. To improve the quality of indoor ornamental plants and extend the flowering time, light intensity must be adjusted properly during the production, and plants must be acclimatized under a low light level before placement indoors, which could improve the indoor performance of foliage plants [1].

Leaf Position Will Influence the Photosynthesis Character
Leaf position can affect photosynthesis and transpiration. In normal conditions, the Pn of fully expanded mature leaf tends to be higher than that of the newly emerged leaf at the top and the descended leaf [11,40]. Quite the reverse, some plants show a different trend, such as kiwifruit, the expanded leaves of which had a lower Pn [21]. Our findings indicated that leaves at the central position may better exploit low irradiance than young leaves on the top and the oldest leaves at the bottom, while the young leaves perform better under greenhouse conditions. A similar phenomenon was observed in our previous study with Anthurium 'Red Hot' [8] and also in grapevine [41]. It is obvious that the Pn of leaves at different positions might show a significant difference, and leaf senescence will affect photosynthetic efficiency. Leaf photosynthesis can be influenced by stomatal conductance and intercellular carbon dioxide [10,42]. The relative importance of these two factors has been studied in several plants, which suggests that intercellular carbon dioxide is the predominant factor. As in the previous research, the stomatal conductance fluctuation was positively correlated with leaf age but no interaction was found with intercellular carbon dioxide [41]. In young and old leaves, lower soluble protein and chlorophyll concentrations per unit leaf area result in alleviation of Pn [16,41,43]. Contradictory to previous findings, under L treatment in the greenhouse and interior conditions, Anthurium × 'Red' mature leaves at the middle and bottom position may be triggered to rejuvenate or regain photosynthetic activity [8]. Therefore, this mechanism needs further exploration.

Plant Materials and Growth Conditions
The current study was conducted in Central Florida from October 2018 to April 2019. Tissue-cultured liners of Anthurium × 'Red' were transplanted to 15 cm diameter containers (height = 30 cm and diameter = 15 cm) filled with Vergo Mix A. Each container was top-dressed with 5 g of an eight-month formulation of Osmocote 17-7-12 (The Scott Co., Marysville, OH, USA) and watered once a week. Fifteen plants with a similar growth size and leaf color were selected, divided into three groups, and grown in a shaded greenhouse under three light levels. The greenhouse was covered by double layer polyethylene film, and shade cloth with three different densities was installed inside, resulting in three sections with daily maximum PPFDs of 550, 350, and 255 µmol·m −2 ·s −1 as high (H), medium (M), and low (L) levels, respectively. The experiment was arranged as a completely randomized design with five replications. After plants were established in a shaded greenhouse for six months, three leaves were selected and marked as 1, 2, and 3 for a bottom old leaf, center mature leaf, and top young expanded leaf, respectively on each plant. We marked the leaves of H group as H1, H2, and H3, M group as M1, M2, and M3, and L group as L1, L2, and L3. Thereafter, all the replicates were moved to the interior room with a light intensity of 30 µmol·m −2 ·s −1 ,12 h a day, provided by white fluorescent lamps following Li et al. [2].

Leaf Greenness Estimated by SPAD
Leaf SPAD (Soil-Plant Analysis Development) readings of the marked leaves were recorded before and one-month after plants were moved to the interior rooms by using a SPAD-502 m (Konica-Minolta, Japan) as described by Wang et. al. [44]. Five independent SPAD measurements were determined on each marked leaf of each plant, and total chlorophyll concentrations were determined following Wang et al. [45].

Net Photosynthetic Rate Comparison of Anthurium × 'Red' under 30 PPFD
The Pn was measured once every two months (10/15/2018, 12/18/2019, 2/15/2019, and 4/16/2019) during greenhouse growing as well as 1, 2, 3, 6, 8, 12, 18, and 24 days after moving to the interior room, respectively. All the measurements were carried out at a photosynthetic photon flux density (PPFD) value of 30 µmol·m −2 ·s −1 , which was the same as the interior room light condition, a CO 2 concentration of 400 µmol·mol −1 on a sunny day between local time 9:00 and 12:00 a.m. by using the Li-6800 portable photosynthesis system (LI-COR, Inc., Lincoln, NE, USA). Three leaves from different positions on each plant were measured and there were five plants in each group.
The irradiance (I)-response curves of photosynthesis were fitted following the modified model of the rectangular hyperbola [46] as follows: where P(I) is Pn; Rd is the rate of dark respiration; and α, β, and γ are the coefficients that are independent of I.
The compensation irradiance, Ic, was calculated as follows [47]: The saturation irradiance, Isat, was determined using the following formula [47]: The maximum photosynthetic rate, Pn-max, was calculated as follows [47]:

Changes in Plant Morphology before and after Moving into the Interior Rooms
The number of leaves, newly emerged leaves, flower count, flower longevity, and growth index were also determined monthly for the first six months, then, all the plants were moved to interior rooms, where these attributes were recorded weekly.

Data Analysis
SPSS software (version 19.0, IBM Corp., Armonk, NY, USA) was used for the statistical analysis of the data. All data were subjected to analysis of variance (ANOVA). If significance occurred among treatments, means were separated by Tukey HSD (honestly significant difference) test at P < 0.05 level. All the values were presented as mean ± standard errors. Additionally, the software Origin ® v. 8.5 (Origin-Lab Corp., Northampton, MS, USA), Prism v. 8.0.1 (GraphPad, San Diego, CA, USA), and Microsoft Excel-2016 were used for visualization (light-response curve fitting model) and tables, respectively.

Conclusions
The purpose of this research was to investigate variations in photosynthesis of Anthurium × 'Red' under different light conditions and compared the photosynthetic potential of leaves at different positions during plant production and interiorscaping to document plant dynamic responses for adapting to different growing conditions. We conclude that plants grown under a medium light level (350 µmol·m −2 ·s −1 ) can maintain green-colored leaves and accumulate substantial energy for sustaining indoor growth. Furthermore, Anthurium × 'Red' has shown the ability to survive in low light conditions, which could be in part attributed to the rejuvenation of leaves at middle and bottom positions for enhanced photosynthesis.

Data Availability Statement:
The data presented in this study are available in the article.

Acknowledgments:
The authors wish to express gratitude to t he anonymous reviewers who gave valuable feedback and critical remarks on this manuscript.

Conflicts of Interest:
The authors declare no conflict of interest.