Short Day Lengths Can Mitigate Excessive Stem Elongation and Promote Flowering of Echeveria Cultivars Under Low and Moderate Daily Light Integrals

Abstract

Echeveria spp. (Mexican hens and chicks) are among the most popular genera of succulents sold because they are compact and form attractive, symmetrical rosettes with brightly colored, fleshy, broad, iridescent leaves, as well as large, showy inflorescences. However, they are slow-growing, and flower induction protocols are not widely available. Therefore, the objectives of this study were (1) to determine if photoperiod and the photosynthetic daily light integral (DLI) can be manipulated to promote rapid growth and leaf expansion without excessive extension growth of several cultivars of Echeveria and (2) to establish the critical photoperiod for flower induction. Cuttings of E. spp. and hybrids ‘Apus’, ‘Canadian’, ‘Elegans Blue’, ‘Jade Point’, and ‘Topsy Turvy’ were received from a commercial breeder and grown in a greenhouse at 20 °C for 5 weeks. Photoperiods were created using a truncated 9 h short day (SD) or a SD extended to 10, 11, 13, 15, 16 h or a 4 h night-interruption (NI), using light-emitting diode (LED) lamps providing a total photon flux density of ≈2 μmol·m⁻²·s⁻¹ of red (R) + white (W) + far-red (FR) radiation. DLIs of 4.8 and 12.8 mol·m⁻²·d⁻¹ were maintained with and without shade cloth and supplemental lighting. Photoperiod and DLI interacted to influence the final height of E. ‘Canadian’, ‘Elegans Blue’, and ‘Jade Point’; plants were tallest under photoperiods > 13 h and low DLI. Similar trends were observed for growth index and average plant diameter. No clear trend was observed for leaf unfolding or leaf length across DLI or photoperiod treatments. Flower initiation of E. ‘Apus’ and ‘Jade Point’ was highest under a DLI of 12.8 mol·m⁻²·d⁻¹. Additionally, E. ‘Jade Point’ only developed inflorescences under day lengths ≤ 11 h, indicating an obligate SD response. Our results suggest that growers should maintain DLIs > 10 mol·m⁻²·d⁻¹ and SD conditions to promote flower initiation of the Echeveria cultivars tested. Such conditions would prevent excessive stem elongation and encourage flowering, increasing crop quality and marketability.

1. Introduction

Potted succulents are popular among consumers for their unique appearance, diversity, adaptability, and drought tolerance, as well as the constant stream of new varieties, colors, and forms introduced to the market [1,2,3]. Additionally, consumer interest in succulents increased during the COVID-19 pandemic as individuals sought easy-to-maintain indoor plants [4]. Their wholesale value has increased by more than 333% over the past 20 years [5,6]. However, unlike many other ornamental plants, succulents require highly specific growing conditions because they are xerophytes adapted to arid environments with sustained periods of limited water [7]. For this reason, it is difficult to propagate and grow them outdoors in areas with relatively high precipitation, making greenhouse production more suitable for succulents. Additionally, for optimal production, succulents require distinct growing conditions from those of typical ornamentals, making it difficult for growers to propagate both in the same area. That said, little research has been conducted to develop standardized greenhouse production protocols for this diverse group of plants.

While some succulent genera are native to equatorial regions, others are found in northern and southern latitudes [8]. The vast majority come from the stonecrop family Crassulaceae and include the following genera: Tree house leek (Aeonium), round-leafed navel-wort (Cotyledon), jade plant (Crassula), Mexican hens and chicks (Echeveria), kalanchoe (Kalanchoe), jewel plant (Pachyveria), stonecrop (Sedum), and houseleek (Sempervivum). Of these, Echeveria is one of the most popular genera of hybridized succulents sold in the United States, with more than 125 Echeveria species and hybrids produced as potted plants [9]. Species of Echeveria are generally slow-growing and can take as long as 4 to 6 months to become marketable from an unrooted shoot-tip cutting [10]. Their native range includes the southwestern United States and extends southward into Mexico and the highlands of Central and South America.

Succulents native to arid climates are generally regarded as using crassulacean acid metabolism (CAM) exclusively as their primary means of photosynthesis. However, the claim that all succulents photosynthesize exclusively via CAM is an oversimplification [11,12]. In general, CAM photosynthesis is considered an adaptation to regions with dry, hot days and relatively cool nights, which impose selective pressures on plants to photosynthesize at night to avoid water loss. Recent research suggests that, in some species, CAM photosynthesis is a facultative trait used during drought and not utilized during the rainy season or in wet conditions [13,14,15]. Additionally, some studies have investigated the impact of photoperiod, (day length) on facultative CAM photosynthesis. For example, Kalanchoe blossfeldiana ‘Tom Thumb’ and K. velutina both exhibited an increase in the rate of CAM metabolites under short-day (SD) conditions [16].

Some plant genera and species can initiate developmental processes, such as flowering, once a critical photoperiod is met. These plants detect light through photoreceptors, which allow them to perceive the length of the night period, leading to either promotion or suppression of flowering [17]. Phytochrome (P), a photoreceptor that detects red (R) and far-red (FR) light, has two interconvertible isomeric forms, P_R and P_FR, which can be converted depending on the relative abundance of R or FR radiation [18]. P_R, or the inactive form of P, detects R radiation. Once R light is detected, it is converted to P_FR, or the active form of P. P_FR can then be converted back to P_R upon the detection of FR radiation. The accumulation of P_R or P_FR at different levels can induce distinct physiological changes in a plant [19].

For example, in long-day plants, or plants in which flowering either only occurs or is sped up by exposure to long day lengths (typically over 12 h), lengthened exposure to R light throughout the extended day period leads to the accumulation of P_FR, which induces the expression of genes that lead to a flowering response. Day-extension (DE) or night-interruption (NI) lighting containing R and FR radiation is often used to induce long-day plants into flower, as the accumulation of P_FR initiates a flowering response [20]. In certain plants, a low R:FR light ratio can trigger a shade-avoidance response, thereby promoting stem and petiole elongation [21].

Since many succulents are slow-growing, there is interest in investigating how environmental conditions, such as photoperiod and the daily light integral (DLI), can be manipulated to promote rapid vegetative growth and flowering [22]. For example, Calle et al. conducted an observational study in which cacti and succulents native to South Africa were observed over time in conservatories at latitudes ranging from 0 to 48 °N [23]. They documented that most cacti and succulents flowered during the year’s shortest day lengths. Similarly, Currey and Erwin reported that Kalanchoe species, native to South Africa and Madagascar, differed in their responses to photoperiod [24]. For example, K. glaucescens, K. laciniata, K. manginii, K. nyikae, K. rotundifolia, K. uniflora, and K. velutina were classified as obligate SD plants, while the flowering response of K. beauvardii, K. behariensis, K. fedtschenkoi, K. longifloria, K. marmorata, K. marnieriana, K. streptantha, K. tomentosa, and K. vigueridoi appeared as day-neutral plants or had no photoperiodic response to day length. In a separate study, as day length increased from 6 to 18 h, the number of new prickly pear cactus (Opuntia ficus-indica) cladodes (water-storing stems) increased from 1 to over 4, suggesting that photoperiod may influence vegetative growth and development [25].

Currey and Erwin also investigated the effects of DLI on several species of Kalanchoe, and they indicated that the dry mass of K. glaucescens, K. laciniata, K. manginii, K. nyikae, K. rotundifolia, and K. velutina increased as the DLI increased from 4.3 to 17.2 mol·m⁻²·d⁻¹ [26]. Similarly, the dry mass of Christmas cactus (Schlumbergera × buckleyi) increased by 8.5 g as shade was reduced from 75% to 0% during the production cycle [27]. Cabahug et al. reported that extension growth of Echeveria marcus and E. agavoides was reduced from 47.0 to 41.6 mm and 44.8 to 42.0 mm, respectively, as the DLI increased from 1.7 to 6.8 mol·m⁻²·d⁻¹ [28]. Furthermore, Nam et al. found that the height of Sedeveria ‘Letizia’ increased under light-emitting diode (LED) fixtures that provided 3 h of DE lighting [29]. For example, at radiation intensities of 60 and 120 µmol·m⁻²·s⁻¹, the heights were 60.7 and 68.4 mm, respectively. However, it was not possible to isolate the main effects of photoperiod and light intensity on plant growth because a low-intensity DE treatment was not used.

To our knowledge, only a few studies have investigated the effects of DLI and various day lengths on Echeveria growth and development. For these reasons, the objectives of our study were to (1) establish the critical photoperiod for flower induction of cultivars of Echeveria; (2) determine if photoperiod and the DLI can be used to hasten production without excessive extension growth, and (3) to quantify how photoperiod and DLI influence stem elongation in Echeveria.

2. Materials and Methods

2.1. Plant Material and Propagation

Cuttings of five shoot-tip Echeveria cultivars, ‘Apus’, ‘Canadian’, ‘Elegans Blue’, ‘Jade Point’, and ‘Topsy Turvy’, containing ≈22, 23, 20, 21, and 19 leaves, respectively, were received from a commercial breeder (Dümmen Orange, Columbus, OH, USA) on 29 April, 19 May, and 27 May 2020. One day after receipt, individual cuttings were inserted into 11 cm-diameter round containers (600 mL) (East Jordan Plastics Inc., East Jordan, MI, USA) filled with 75% (by vol.) commercial soilless media, composed of 86% peat moss and 14% perlite (Suremix; Michigan Grower Products Inc., Galesburg, MI, USA), and 25% perlite (Coarse Perlite; Perlite Vermiculite Packaging Industries Inc., North Bloomfield, OH, USA). A foliar spray containing indole-3-butyric acid (Advocate; Fine Americas, Inc., Walnut Creek, CA, USA) and a surfactant (Capsil; Aquatrols, Paulsboro, NJ, USA) was applied at a concentration of 75 mg∙L⁻¹ and volume of 0.2 L·m⁻² one day after transplant to encourage rooting.

The cuttings were rooted in a glass-glazed greenhouse at Michigan State University (East Lansing, MI, USA; lat. 43° N). An environmental control computer (Priva Office version 725-3030; Priva North America, Vineland Station, ON, Canada) controlled evaporative cooling, radiant hot-water heating, exhaust fans, and supplemental lighting. A 16 h photoperiod was maintained with high-pressure sodium lamps (LR48877; P.L. Lighting, Beamsville, ON, Canada) that provided a total photon flux density of 62.5 ± 2.4 µmol·m⁻²·s⁻¹. The DLI and mean daily temperature (MDT) during propagation were 19.4 ± 4.6 and 18.7 ± 2.8 mol·m⁻²·d⁻¹, and 22.7 ± 2.4 and 22.7 ± 2.2 °C, respectively, for replications (Reps.) 1 and 2. Plants were irrigated as needed with reverse osmosis (RO) water blended with a water-soluble fertilizer (MSU Orchid RO Water Special 13N–1.3P–12.5K; Greencare Fertilizers, Inc., Kankakee, IL, USA) containing (mg·L⁻¹): 125 N, 13 P, 121 K, 78 Ca, 19 Mg, 0.17 B, 0.43 Cu, 1.7 Fe, 0.85 Mn, 0.17 Mo, and 0.43 Zn.

2.2. Greenhouse Environment and Lighting Treatments

After 44 days, rooted plants were transferred to one of 16 benches in a separate glass-glazed greenhouse. Opaque black cloth was pulled over each individual bench at 1700 h and was retracted at 0800 h to create a truncated 9 h SD. The photoperiod consisted of natural day lengths and supplemental lighting from 200 W LED fixtures (Philips GP-TOPlight DRW-MB; Koninklijke Philips N.V., Eindhoven, The Netherlands) that provided 78 ± 20 µmol·m⁻²·s⁻¹ when the outdoor light intensity was below ≈440 µmol·m⁻²·s⁻¹. The 100 nm waveband ratios (%) of the LED fixtures, defined by their blue [B (400–500 nm)], green [G (500–600 nm)], and R (600–700 nm) photon flux densities was 10:5:85. On each bench four R + white (W) + FR LED lamps (Arize Greenhouse Pro; General Electric, Boston, MA, USA) were used to create 10-, 11-, 13-, 15-, and 16 h photoperiods or a 4 h NI from 2200 to 0200 h. The lamps were covered with an aluminum mesh to reduce the total photon flux density to ≈2 µmol∙m⁻²∙s⁻¹. The 100 nm waveband ratios (%) of the lamps were 6:19:45:30, corresponding to the B, G, R, and FR photon flux densities, respectively. Two different DLIs were created: one with shade cloth placed over individual benches, reducing radiation levels by ≈60% (Harmony 5120 O E; Ludvig Svensson, Kinna, Sweden), and one without shade. The MDT and mean DLI ± standard deviation are provided in

Table 1. Daily light integral (DLI), photoperiod (h), bench mean daily temperature (MDT) (±standard deviation), and daily light integral (DLI) (±standard deviation) during two experimental replications (Rep.). Echeveria were grown under a truncated 9 h short day (SD) or under a 9 h SD extended with red+white+far-red (R+W+FR) light-emitting diode (LED) lamps to achieve 10-, 11-, 13-, 15-, and 16 h photoperiods, or a 4 h night interruption (NI).

DLI	Photoperiod (h)	Rep. 1 MDT [Mean ± SD (°C)]	Rep. 2 MDT [Mean ± SD (°C)]	Rep. 1 DLI (mol·m−2·d−1)	Rep. 2 DLI (mol·m−2·d−1)
Moderate	9	24.5 ± 1.8	24.6 ± 1.7	12.9 ± 4.5	12.5 ± 4.9
	10	23.8 ± 1.7	23.9 ± 1.5	- z	- z
	11	24.2 ± 2.3	24.2 ± 2.0	- z	- z
	13	24.9 ± 1.8	23.0 ± 1.7	12.8 ± 4.1	12.6 ± 4.5
	15	23.9 ± 1.9 y	24.2 ± 1.9 y	- z	- z
	16	23.8 ± 2.2	24.9 ± 2.2	12.7 ± 4.0	12.4 ± 4.3
	NI	23.8 ± 1.8	23.1 ± 1.7	12.9 ± 4.6	13.2 ± 4.7
Low	9	24.5 ± 2.1 y	24.7 ± 2.2 y	- z	- z
	10	23.6 ± 1.6	23.8 ± 1.6	4.2 ± 2.9	4.2 ± 3.1
	11	23.8 ± 1.8	24.0 ± 1.7	4.9 ± 1.5	5.0 ± 1.7
	13	23.6 ± 1.5	23.7 ± 1.5	4.2 ± 1.7	4.3 ± 1.9
	15	23.3 ± 1.5	23.4 ± 1.4	4.6 ± 2.6	4.8 ± 2.9
	16	24.3 ± 2.1	24.5 ± 2.0	4.4 ± 1.8	4.5 ± 2.0
	NI	23.4 ± 1.7	23.5 ± 1.6	4.7 ± 2.0	4.9 ± 2.2

^y Partial data reported; ^z Data not reported.

.

2.3. Data Collection and Analysis

After 10 weeks under individual treatments, the final length of the oldest leaf, the number of newly unfolded leaves, the node and branch number, the plant height from the base of the plant to the tallest point on the plant, the plant diameter at the widest point (plant diameter 1), and perpendicular from the widest point (plant diameter 2) were measured and recorded. The stem caliper was measured using a digital caliper (41101 DigiMax; Wiha, Buchs, Switzerland) just above the medium. Growth index was calculated through the following equation: $Growth index = {\displaystyle \frac{plant height+\frac{plant diameter 1+plant diameter 2}{2}}{2}}$ [30]. Plants were designated as reproductive or non-reproductive depending on the presence or absence of an inflorescence, and the number of inflorescences per plant was recorded. Total shoot (leaves and stems) fresh mass was quantified using a digital balance. Afterward, shoots were excised from roots and placed in a drying oven at ≥70 °C for ≥7 d, after which dry mass was recorded. For all measured parameters, data were collected from 10 plants per cultivar per replication.

The experiment was organized in a randomized complete-block design with a two-way factorial arrangement. Plants were blocked by photoperiod (seven levels) and DLI (two levels), with 10 randomly selected plants per treatment combination. The experiment was performed twice over time for the five cultivars evaluated. Data were analyzed separately by cultivar, and cultivar interaction was not evaluated. Data were analyzed using SAS version 9.4 (SAS Institute, Inc., Cary, NC, USA) with the mixed-model procedure (PROC MIXED) for analysis of variance (ANOVA). Means were separated using the Tukey–Kramer honestly significant difference test (p ≤ 0.05).

3. Results

3.1. Final Height, Growth Index, and Average Diameter

The DLI and photoperiod interacted to influence the final height of E. ‘Canadian’, ‘Elegans Blue’, ‘Jade Point’, and ‘Topsy Turvy’, but not E. ‘Apus’. However, no clear trend was present for ‘Topsy Turvy’. The tallest plants were those under 15 or 16 h photoperiods and a low DLI of 4.6 mol·m⁻²·d⁻¹ (

Table 2. Analysis of variance for final height, average width, growth index, leaf unfolding, leaf length, stem caliper, dry mass, branch number and flower number of Echeveria grown under 9-, 10-, 11-, 13-, 15-, 16 h photoperiods or a 4 h night interruption (NI) and low or moderate daily light integrals (DLI).

	Photoperiod	DLI	DLI × Photoperiod
	‘Apus’
Final height	** z	*	NS
Average width	**	***	NS
Growth index	**	***	NS
Leaf unfolding	NS	NS	NS
Leaf length	*	NS	NS
Stem caliper	NS	NS	NS
Dry mass	*	NS	NS
Branch number	NS	NS	NS
Flower number	NS	*	NS
	‘Canadian’
Final height	***	***	***
Average width	NS	NS	NS
Growth index	***	NS	**
Leaf unfolding	***	NS	*
Leaf length	NS	NS	NS
Stem caliper	NS	***	NS
Dry mass	NS	NS	NS
Branch number	NS	*	NS
Flower number	**	NS	NS
	‘Elegans Blue’
Final height	***	**	***
Average width	*	***	NS
Growth index	***	***	***
Leaf unfolding	***	NS	NS
Leaf length	*	***	NS
Stem caliper	NS	***	NS
Dry mass	NS	*	NS
Branch number	NS	NS	NS
Flower number	NS	NS	NS
	‘Jade Point’
Final height	***	NS	**
Average width	***	*	**
Growth index	***	*	**
Leaf unfolding	***	***	**
Leaf length	*	*	NS
Stem caliper	NS	*	NS
Dry mass	*	NS	*
Branch number	NS	NS	NS
Flower number	**	**	*
	‘Topsy Turvy’
Final height	NS	NS	*
Average width	NS	NS	NS
Growth index	NS	NS	NS
Leaf unfolding	***	***	*
Leaf length	NS	NS	NS
Stem caliper	*	**	NS
Dry mass	*	NS	*
Branch number	NS	NS	NS
Flower number	NS	NS	NS

^z NS, *, **, *** Nonsignificant or significant at p ≤ 0.05, 0.01, and 0.001, respectively.

; Figure 1 and Figure 2). Under a low DLI, E. ‘Elegans Blue’ was 11%, 8%, 11%, 26%, 28%, 20%, and 29% taller under a 9-, 10-, 11-, 13-, 15-, 16 h photoperiod or a 4 h NI, respectively, than under a moderate DLI (Figure 1 and Figure 2). Individually, photoperiod and DLI influenced the height of E. ‘Apus’; however, no trends existed (

Table 3. Effect of 9-, 10-, 11-, 13-, 15-, 16 h photoperiod or a 4 h night interruption (NI) lighting on final height, average width, growth index, leaf unfolding, leaf length, stem caliper, dry mass, branch, and flower number of various Echeveria cultivars. Letters indicate mean separations across photoperiodic treatments using Tukey–Kramer honestly significant difference (HSD) test at p ≤ 0.05. Bars represent the mean, and error bars indicate standard error.

Parameter	Photoperiod (h)
	9	10	11	13	15	16	NI
	‘Apus’
Final height (cm)	11.6 b	11.7 b	11.6 b	12.2 a	12.1 ab	11.9 ab	11.7 ab
Average width (cm)	10.4 b	10.8 ab	10.5 b	11.5 a	11.3 ab	10.6 b	10.5 b
Growth index	11.0 c	11.2 bc	11.1 bc	11.9 a	11.7 ab	11.2 bc	11.1 bc
Leaf length (cm)	5.7 b	6.0 ab	5.9 ab	6.5 a	6.3 ab	5.8 b	6.0 ab
Dry mass (g)	2.6 ab	2.7 ab	2.6 ab	2.8 a	2.7 a	2.4 b	2.6 ab
	‘Canadian’
Final height (cm)	11.9 b	12.0 b	12.2 b	13.1 a	13.6 a	13.4 a	12.3 b
Growth index	11.4 c	11.4 c	11.7 bc	12.3 ab	12.5 a	12.2 abc	11.6 bc
Leaf unfolding (no.)	35.6 a	34.9 a	35.0 a	34.6 ab	34.7 a	31.7 b	32.8 ab
Flower number (no.)	0.03 b	0.0 b	0.08 b	0.0 b	0.38 a	0.23 ab	0.03 b
	‘Elegans Blue’
Final height (cm)	14.3 c	14.8 c	15.2 c	20.1 b	22.2 a	21.6 a	19.4 b
Average width (cm)	7.7 ab	7.9 ab	7.6 b	8.1 a	8.1 ab	7.9 ab	8.1 ab
Growth index	11.0 c	11.4 c	11.4 c	14.0 b	15.1 a	14.7 a	13.7 b
Leaf unfolding (no.)	18.1 d	18.6 cd	18.0 d	20.8 a	20.3 ab	19.3 bcd	19.5 abc
	‘Jade Point’
Final height (cm)	11.4 c	11.9 abc	11.6 bc	12.1 a	12.1 a	12.2 ab	11.9 abc
Average width (cm)	8.7 b	9.3 ab	8.8 b	9.6 a	9.9 a	9.4 ab	9.2 ab
Growth index	10.1 c	10.6 ab	10.2 bc	10.9 a	11.0 a	10.8 ab	10.6 ab
Leaf unfolding (no.)	14.6 c	16.5 bc	14.6 c	17.5 b	22.3 a	19.0 b	19.0 b
	‘Topsy Turvy’
Stem caliper (mm)	13.2 c	12.9 ab	13.0 bc	13.8 abc	12.8 a	12.9 c	13.3 abc
Leaf unfolding (no.)	32.7 ab	36.3 ab	33.5 ab	35.3 a	36.8 b	32.7 ab	34.9 ab

and

Table 4. Effect of low or moderate daily light integral (DLI) on final height, average width, growth index, leaf unfolding, leaf length, stem caliper, dry mass, branch number, and flower number for various Echeveria cultivars. Letters indicate mean separations across DLI treatments using Tukey–Kramer honestly significant difference (HSD) test at p ≤ 0.05.

	DLI
	Low	Moderate
	‘Apus’
Final height (cm)	11.7 b	11.9 a
Average width (cm)	11.5 a	10.1 b
Growth index	11.6 a	11.0 b
Flower number (no.)	0.0 b	0.11 a
	‘Canadian’
Final height (cm)	13.2 a	12.1 b
Stem caliper (mm)	10.2 b	11.3 a
Branch number (no.)	0.12 b	0.26 a
	‘Elegans Blue’
Final height (cm)	20.3 a	16.2 b
Average width (cm)	8.1 a	7.7 b
Growth index	14.2 a	11.9 b
Leaf length (cm)	3.9 b	4.2 a
Stem caliper (mm)	6.6 b	7.2 a
Dry mass (g)	1.7 b	2.3 a
	‘Jade Point’
Average width (cm)	9.9 a	8.6 b
Growth index	10.9 a	10.2 b
Leaf unfolding (no.)	19.2 a	15.7 b
Leaf length (cm)	4.5 b	4.7 a
Stem caliper (mm)	7.8 b	8.3 a
	‘Topsy Turvy’
Stem caliper (mm)	12.9 b	13.4 a
Leaf unfolding (no.)	34.6 a	32.9 b

).

Similar to final height, the growth index of E. ‘Canadian’, ‘Elegans Blue’, and ‘Jade Point’ was influenced by the interaction of DLI and photoperiod, resulting in larger plants under longer photoperiods and lower DLIs (Table 2; Figure 3). The largest E. ‘Canadian’, ‘Elegans Blue’, and ‘Jade Point’ were generally those grown under long photoperiods and low DLIs (Figure 3). Growth index of E. ‘Topsy Turvy’ was not influenced by photoperiod or DLI (Table 2).

E. ‘Jade Point’ was the only cultivar whose diameter was influenced by the interaction of DLI and photoperiod, but no clear trend was discernible (Table 2, Figure 4). However, individually DLI and photoperiod influenced the diameter of E. ‘Apus’, ‘Jade Point’, and ‘Elegans Blue’ (Table 2). As the DLI increased from 4.6 to 12.8 mol·m⁻²·d^−1, the average diameter of E. ‘Apus’, ‘Jade Point’, and ‘Elegans Blue’ increased by 1.4, 0.4, and 1.3 cm, respectively (Table 4).

3.2. Leaf Unfolding, Leaf Length, and Stem Caliper

Although leaf unfolding was influenced by the interaction between DLI and photoperiod for E. ‘Topsy Turvy’, no trend was observed (Figure 5). Generally, leaf unfolding responses to the two environmental parameters were cultivar-specific. For example, E. ‘Apus’ was not influenced by either DLI or photoperiod, whereas E. ‘Elegans Blue’ was only influenced by photoperiod, with the highest leaf unfolding occurring under photoperiods ≥ 13 h (Table 2). Under a 13 h photoperiod, plants unfolded 2.7 and 1.5 more leaves than those plants grown under a 9 h or 16 h photoperiod, respectively (Table 3). Few differences were observed in leaf unfolding of E. ‘Canadian’ and ‘Topsy Turvy’ (Figure 5). However, E. ‘Jade Point’ had the greatest number of leaves when photoperiods were ≥15 h or included a NI with a low DLI compared to all other treatments.

No interaction between DLI and photoperiod was observed for leaf length or stem caliper for any cultivar (Table 2). Generally, DLI and photoperiod had minimal influence on leaf length (Table 3 and Table 4). However, under a moderate DLI, the stem caliper of E. ‘Canadian’, ‘Elegans Blue’, ‘Jade Point’, and ‘Topsy Turvy’ increased (Table 2). For instance, the stem caliper of E. ‘Canadian’, ‘Elegans Blue’, ‘Jade Point’, and ‘Topsy Turvy’ was 1.1, 0.6, 0.5, and 0.5 mm greater under the moderate DLI compared to the low DLI (Table 4).

3.3. Dry Mass and Inflorescence Percentage and Number

DLI and photoperiod interacted to affect the dry mass of E. ‘Jade Point’; photoperiod influenced ‘Topsy Turvy’; however, no clear trends existed (Table 3; Figure 4). Under a moderate DLI, the dry mass of E. ‘Elegans Blue’ was 35% greater compared to plants grown under a low DLI (Table 4).

E. ‘Canadian’ developed the greatest number of inflorescences per plant under 15 and 16 h photoperiods; however, flowering occurred under all photoperiods (Table 3). E. ‘Apus’ developed 0.11 inflorescences per plant under a moderate DLI, compared to 0 inflorescences under a low DLI (Table 4). DLI and photoperiod interacted to influence the number of inflorescences in E. ‘Jade Point’. The most inflorescences were observed under a day length of 9 h and moderate DLI (Figure 4). The percentage of plants developing an inflorescence was cultivar-specific. For example, the highest percentage of E. ‘Apus’, ‘Elegans Blue’, and ‘Jade Point’ developed inflorescences under photoperiods ≤ 11 h and a moderate DLI, and no plants developed inflorescences at photoperiods ≥ 13 h (Figure 6). In contrast, the highest percentage of E. ‘Canadian’ that developed an inflorescence occurred under a 15 h photoperiod and a low DLI. However, there was no clear trend for the percentage of ‘Topsy Turvy’ that developed an inflorescence.

4. Discussion

This study was developed based on preliminary data indicating that the plant diameter of Echeveria was promoted under long-day lengths created with low-intensity LEDs providing R+W+FR radiation. In the preliminary study, Echeveria ‘Domingo’ was grown for 12 weeks under 9-, 12-, 14-, and 16 h photoperiods and a much higher DLI and MDT of 22.9 mol·m⁻²·d⁻¹ and 26.7 °C, respectively. Interestingly, we found that plant diameter of E. ‘Domingo’ increased by 28% as day length increased from 9 to 16 h. This led us to hypothesize that providing long day lengths with DE or NI lighting that utilizes FR radiation would result in larger plants, as FR would promote leaf expansion, as discussed by Park and Runkle [31]. The preliminary results of our study differed substantially from those considered in this manuscript, as growing succulents under high DLIs can lead to leaf extension without stem elongation, resulting in a larger plant and no loss in quality. Additionally, E. ‘Domingo’ may respond differently to photoperiod than the cultivars selected for the current study.

A high ratio of FR radiation can lead to leaf expansion and stem elongation due to the shade avoidance response [32]. Leaf expansion resulting from FR radiation can, in some cases, be beneficial, leading to higher-quality plants or shorter production times. For example, Park and Runkle found that increasing FR radiation during geranium (Pelargonium × hortorum) ‘Pinto Premium Orange Bicolor’ and snapdragon (Antirrhinum majus) ‘Trailing Candy Showers Yellow’ seedling production resulted in increased leaf expansion and net carbon assimilation [31]. This led to larger seedlings and hastened snapdragon flowering.

The majority of DLI studies have been conducted on traditional greenhouse crops and have reported that it influences several plant growth processes, including biomass accumulation, flowering time, stem elongation, and leaf expansion [33,34,35,36]. However, few studies have investigated the effects of DLI on succulents. Currey and Erwin observed that dry mass accumulation of K. glaucescens, K. laciniata, K. manginii, K. nykae, K. rotundifolia, and K. velutina increased by 3.9, 10.5, 4.6, 7.4, 8.5, and 11.1 mg·d⁻¹, respectively, as DLI increased from 4.3 to 17.2 mol·m⁻²·d⁻¹ [26]. Our results found that the dry mass of only E. ‘Elegans Blue’ increased as DLI increased from 4.6 to 12.8 mol·m⁻²·d⁻¹ (Table 4). Additionally, we observed an increase in dry mass with increasing photoperiod for E. ‘Apus’, ‘Jade Point’, and ‘Topsy Turvy’ (Table 3). Currey and Erwin also reported that flower number increased as DLI increased for K. glaucescens, K. laciniata, K. manginii, K. nykae, K. rotundifolia, and K. velutina by 41, 32, 25, 26, 62, and 73 flowers, respectively. Our results agree, as we observed an increase in the number of inflorescences E. ‘Apus’ and ‘Jade Point’ produced under the moderate DLI (Table 4).

Plant height is generally influenced by DLI, day and night temperatures, photoperiod, and the shade-avoidance response. Cabahug et al. found that Echeveria agavoides were 7% taller when grown under a very low DLI of 1.7 mol·m⁻²·d⁻¹ compared to those grown under a low DLI of 6.8 mol·m⁻²·d⁻¹ [28]. Similarly, in the same study, Echeveria marcus plants grown under the same environmental conditions were 13% taller under the very low DLI. The diameter of E. agavoides and E. marcus was 15 and 5% larger, respectively, when grown under a DLI of 1.7 mol·m⁻²·d⁻¹ compared to plants grown under 6.8 mol·m⁻²·d⁻¹. Our results agree, as E. ‘Canadian’ and ‘Elegans Blue’ grown under low DLIs were 9% and 25% taller, respectively, compared to plants under the high DLI (Table 4). Similarly, we found that the average width of ‘Jade Point’ grown under 4.6 mol·m⁻²·d⁻¹ was 15% greater (Figure 4). However, a deterioration in plant quality was generally observed under low DLIs and photoperiods ≥ 13 h as internode elongation was excessive (Figure 2). Our results provide evidence that low DLIs, in combination with DE lighting containing FR, contributed to excessive stem elongation for some Echeveria cultivars. Further research investigating the effects of DE lighting without FR radiation may provide greenhouse growers with information on promoting the growth of succulents without excessive stem elongation.

For traditional floriculture crops, plant quality is assessed based on branching, compactness, plant health, foliage filling the container, and some open flowers [37]. However, plants sold solely for their unique foliage differ in quality attributes. They must have attractive, brightly colored leaves that are favored over their flowers and fruits and perform well in any indoor environment [38]. Similar to containerized flowering plants, they must also fill in the container, be compact, well-branched in certain genera, and be free of pests, diseases, and blemishes. Excessive stem elongation, or elongation to the point of low quality, is often not tolerated. Additionally, flowers of some succulent genera are unsightly and, as a result, may be unappealing to consumers. Research has investigated how the promotion of foliage plant benefits can influence consumer purchasing behavior [39]. Investigators have also determined that visual cues and the communication of essential information can influence the likelihood of purchase [40]. However, research on consumer preferences for the vegetative, flowering, and foliage colors of succulents is needed to provide growers with information to further increase sales.

Horticulturally, rapid, uniform, and complete flowering is essential to meet market dates. However, little research has been performed outside of Kalanchoe spp. to determine the critical photoperiod for flower initiation of succulents. Although Calle et al. observed that many South African succulents grown in public conservatories flowered under SD, they did not have large sample sizes [23]. For Kalanchoe spp., Currey and Erwin determined that many common species responded to day length as SD plants [24]. However, they were unable to classify all species due to low flowering rates. In the current study, only E. ‘Jade Point’ produced inflorescences under day lengths ≤ 11 h; thus, we have classified it as an obligate SD plant (Table 3). While we did not quantify time to flower, we observed that E. ‘Topsy Turvy’ inflorescence development was hastened under shorter day lengths, indicating that it may have a facultative SD flowering response (Figure 2). Although other cultivars in this study developed inflorescences, there was no consistent trend in response to day length, and flowering percentages were generally low.

This study has also provided important information for growers located in northern latitudes: if increasing the DLI with supplemental lighting is not possible, a grower may still be able to reduce excessive stem elongation and improve quality. Photoperiodic lighting containing FR radiation should not be used when DLIs ≤ 10 mol·m⁻²·d⁻¹, as excessive internode elongation will lead to low-quality plants. Given that some Echeveria cultivars appear to have an SD flowering response, DE or NI lighting containing R+W radiation would prevent premature flowering. To initiate flowering and produce the most compact plant, the day length could be shortened to <13 h. The low percentage of plants that flowered in this study indicates there may be additional mechanisms that influence flower initiation of Echeveria. More research is needed to investigate the effects of high DLIs, R light, temperature, photoperiod, and juvenility on the growth and development of potted succulents. Future experiments focusing on juvenility, dual photoperiods, or vernalization requirements prior to placement under various photoperiods may provide useful data on how to induce rapid, complete, and uniform flowering of succulents. Lastly, studies examining consumer preferences for flowering or non-flowering succulents and color preferences would provide insight into the potential marketability of flowering succulents.