A Low Ratio of Red to Far-red Radiation (R:FR) Throughout the Photoperiod but Not at End-of-day Promotes Shade Avoidance for Petunia ×hybrida Seedlings

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Anthony C. Percival Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Ave, Fort Collins, CO 80521-1173, USA

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Joshua K. Craver Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Ave, Fort Collins, CO 80521-1173, USA

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Abstract

Electric lighting is often necessary to achieve a target daily light integral (DLI) for the production of high-quality young annual bedding plants (plugs). Early in production, plugs have a low leaf area index that limits light interception and likely results in wasted radiation supplied by electric sources. Previous research has shown that the addition of far-red radiation (700–780 nm) to the radiation spectrum in sole-source lighting experiments or the use of end-of-day far-red (EOD-FR) radiation treatments can promote an increase in leaf expansion and leaf area for many species. However, leaf expansion in response to far-red radiation may depend on other factors such as the ratio of red (600–699 nm) to far-red radiation (R:FR) and air temperature. Thus, the objectives of this work were to examine the effects of far-red radiation applied throughout the photoperiod and as an end-of-day radiation treatment on the morphology of petunia ‘Dreams Midnight’ seedlings grown under different temperature conditions. Specifically, petunia seed was sown in 128-cell trays and moved to one of two growth chambers set at 16 or 21 °C when cotyledons unfolded. Seedlings received an equal total photon flux density (400–780 nm) of 164 µmol·m−2·s−1 for a 17.25-hour photoperiod, and either a high (∼10.7) or low R:FR (0.5). Low R:FR-treated seedlings were grown at a constant temperature of either 16 or 21 °C and placed under blackout conditions at the end of the photoperiod. High R:FR-grown seedlings received either a 1-hour end-of-day white (EOD-W) or EOD-FR treatment at the end of the photoperiod, and were grown at a constant 16 or 21 °C; one EOD-FR treatment was also shifted from the 21 °C chamber to the 16 °C at the end of the photoperiod for both the EOD-FR treatment and subsequent dark period. Seedlings were harvested at 21 and 28 days after treatment initiation. For petunia seedlings grown at 21 °C, EOD-FR treatments had minimal effect on morphology or dry mass as all measured parameters, including total and average leaf area and stem length, were similar to EOD-W treatments. In contrast, low R:FR-treated seedlings showed responses characteristic of plants grown under shade, including significant stem elongation, an increase in total and average leaf area, and a reduction in leaf mass per unit area. As expected, production at 16 °C slowed the growth of petunia seedlings resulting in much smaller plants compared with the 21 °C grown plants, but shade responses such as elongated leaves and stems under a low R:FR were apparent. The EOD-FR–treated seedlings that received the diurnal temperature shift also showed reduced leaf area and dry mass compared with their constant 21 °C counterparts. Shade responses were observable at both 16 and 21 °C for low R:FR-grown plants, but the quantifiable impact of temperature on far-red responses could not be fully determined in the present study. Further research is warranted investigating crop responses to far-red radiation as well as potential interacting environmental factors as the promotion of morphological responses, such as leaf expansion, early in production may prove a useful strategy.

A low natural DLI in winter at northern latitudes in North America often necessitates the use of supplemental electric lighting to produce high-quality young annual bedding plants (plugs) in commercial greenhouses (Poel and Runkle 2017; Pramuk and Runkle 2005). The reduced emission of radiant heat from light-emitting diodes (LEDs) as well as the small size, short crop cycle, and high value of plugs makes high-density multilayer indoor production using sole-source lighting a feasible option to produce highly uniform seedlings (Craver et al. 2018; Park and Runkle 2017; Wu et al. 2020). In either case, a low leaf area index (LAI) early in the production cycle likely results in wasted radiation striking substrate or bench space, and promoting an early increase in leaf area may be advantageous for increasing seedling light interception and reducing wasted radiation.

Supplementing sole-source white (400–700 nm) or red-blue (600–700 nm; 400–500 nm) with far-red radiation (700–780 nm) can increase leaf area and light interception of some species such as lettuce (Lactuca sativa; Li and Kubota 2009; Zhen and Bugbee 2020b; Zou et al. 2019), petunia (Petunia ×hybrida; Park and Runkle 2018), and tomato (Solanum lycopersicum; Kalaitzoglou et al. 2019). For example, Zhen and Bugbee (2020b) found that for lettuce ‘Waldmann’s Dark Green’ grown under a photon flux density (400–750 nm) of 350 µmol·m−2·s−1 provided by red-blue or white LEDs, substituting 50 µmol·m−2·s−1 of far-red radiation (700–750 nm in this study) within either spectrum resulted in greater leaf area and light interception, and overall higher fresh and dry mass. In nature, environments such as crowded plant canopies or underneath overhanging vegetation are enriched in far-red radiation relative to shorter wavelengths, as the latter is efficiently absorbed by green vegetation while the former is readily transmitted or reflected; the resulting environment provides two important signals of vegetational shade to plants: 1) a low photosynthetic photon flux density (PPFD; 400–700 nm) and 2) a low ratio of red to far-red radiation (R:FR). In response to these shade signals, shade-intolerant species undergo a series of morphological shade avoidance responses such as stem elongation and leaf hyponasty to increase light capture while leaf growth may be inhibited (Carabelli et al. 2007; Casal 2013; Franklin 2008). An increase in leaf area in response to far-red radiation or a low R:FR appears to be species specific as well as dependent on an adequate PPFD to support leaf development (Casal et al. 1987; Heraut-Bron et al. 2000; Park and Runkle 2018; Patel et al. 2013; Zhen and Bugbee 2020b).

While leaf expansion may be advantageous for increasing light capture, it is important to note that shade avoidance responses such as stem elongation and a reduction in leaf mass per unit area (LMA) have been observed in tandem with an increase in leaf area for species such as petunia (Park and Runkle 2018) and tomato (Kalaitzoglou et al. 2019). Excessive stem elongation can be a negative quality for plug production where compact growth is advantageous for transplant and shipping practices (Pramuk and Runkle 2005), and a reduction in LMA may make leaves more vulnerable to mechanical stress (Gommers et al. 2013). In addition, elongated stems and reduced LMA in response to far-red radiation also increase plant vulnerability to herbivory through greater visibility and a reduced resistance to chewing insects (Ballaré and Austin 2019; Gommers et al. 2013). Furthermore, growth under a low R:FR increases plant susceptibility to pathogens through the inhibition of salicylic acid and jasmonate-regulated chemical defense responses (Ballaré 2014; Fernández-Milmanda and Ballaré 2021).

Applying end-of-day (EOD) radiation with a low R:FR (EOD-FR) has also been shown to promote leaf area expansion in lettuce (Zou et al. 2019) and Petunia axillaris (Casal et al. 1987), but it also may be species specific as this response is not apparent for tomato (Kalaitzoglou et al. 2019) and poinsettia (Euphorbia pulcherrima; Islam et al. 2014). Other shade avoidance responses such as hypocotyl and stem elongation are also promoted by EOD-FR, but responses to EOD-FR are often less intense compared with growth under a constant low R:FR (Kalaitzoglou et al. 2019; Sellaro et al. 2012; Zou et al. 2019). For example, Sellaro et al. (2012) found that Arabidopsis (Arabidopsis thaliana) hypocotyl elongation was intensely promoted by growth under a constant R:FR of 0.1 (characteristic of deep shade; Ballaré and Pierik 2017), whereas plants treated with a 2-hour shade event (R:FR = 0.1) during the last 2 h of the photoperiod or a 10-minute EOD-FR treatment showed less than 40% of the low R:FR-induced elongation responses and similar hypocotyl length compared with control plants, respectively. For lettuce, Zou et al. (2019) found that a 1-hour EOD-FR treatment resulted in a 27% increase in leaf area relative to plants that did not receive EOD-FR, but lettuce that received supplemental far-red radiation throughout the regular photoperiod showed a 49% increase in leaf area compared with control plants. It is also important to note that responses to EOD-FR may depend on the duration of the treatment, as with the preceding Arabidopsis example, as well as the far-red dose that has been documented for hypocotyl elongation in both tomato (Chia and Kubota 2010) and squash (Cucurbita maxima × Cucurbita moschata; Yang et al. 2012). These responses indicate that EOD-FR may be an effective method to promote leaf expansion while minimizing undesired elongation responses for seedlings. Further, EOD-FR may be more relevant for greenhouse production applications compared to supplemental far-red when the overall contribution of supplemental radiation to DLI is low, as the effects of supplemental radiation quality may be limited in these scenarios (Craver et al. 2019).

The R:FR is sensed primarily by the photoreceptor phytochrome B (phyB), which photoconverts between a biologically active far-red absorbing form (Pfr) and inactive red absorbing (Pr) form on absorption of red and far-red radiation, respectively. The Pfr form of phyB regulates shade avoidance responses through the inhibition of phytochrome interacting factors that promote auxin biosynthesis, leading to an increase in indole acetic acid levels and associated growth responses (Ballaré and Pierik 2017; Fernández-Milmanda and Ballaré 2021; Küpers et al. 2020). Importantly, Pfr also reverts to Pr independent of radiation at a temperature-dependent rate; the reversion rate is increased under higher ambient temperatures leading to associated growth responses that resemble those under a low R:FR such as enhanced hypocotyl growth and leaf hyponasty (Casal and Balasubramanian 2019; Küpers et al. 2020). In addition, responses to the difference in day (DT) and night (NT) temperature (DIF), wherein for several species stem elongation is promoted when DT>NT (+DIF) and inhibited when NT>DT (−DIF) (Blom and Kerec 2003; Myster and Moe 1995; Patel et al. 2013; Thingnaes et al. 2008; Xiong et al. 2002), were found to be attenuated for phyB-deficient mutants of Arabidopsis (Thingnaes et al. 2008) and cucumber (Cucumis sativus; Xiong et al. 2002). EOD-FR treatments have also been found to enhance responses to +DIF and partially counteract responses to −DIF (Blom and Kerec 2003; Thingnaes et al. 2008; Xiong et al. 2002).

The effects of shade and temperature have been examined in species such as Arabidopsis (Patel et al. 2013; Romero-Montepaone et al. 2020, 2021), Oenothera biennis (Qaderi et al. 2015), and Brassica napus (Slauenwhite and Qaderi 2013). Romero-Montepaone et al. (2020, 2021) examined the effects of warm temperatures and shade on the growth of Arabidopsis and found that warmer temperatures enhance shade avoidance responses and promote phototropism to further increase access to light in warmer environments. Patel et al. (2013) examined the effects of reduced ambient temperature on shade avoidance responses in Arabidopsis growing under a low (0.1) or high (cool white fluorescence lamps) R:FR ratio with an equal intensity of photosynthetically active radiation (PAR) at either 16 or 22 °C. Ler, a temperate accession of Arabidopsis, was found to display the more typical elongated petioles common in this species under a low R:FR when grown at 22 °C, but at 16 °C showed highly reduced petiole elongation, as well as increased leaf area and thickness. One conclusion of this study was that these temperature-dependent growth forms may be advantageous in light capture in climates where heat or freezing stress are common issues. In contrast to Ler, the subtropical Cape Verde islands accession of Arabidopsis showed intense petiole elongation under a low R:FR regardless of air temperature showing variability in temperature-dependent shade avoidance responses within species (Patel et al. 2013).

As described previously, responses to far-red radiation differ depending on the method of application and can also be influenced by ambient temperature as well as DIF; thus, the objective of this study was to investigate the effect of all-day simulated shade light and EOD-FR treatments on leaf expansion and shade avoidance responses for petunia ‘Dreams Midnight’ at two ambient temperatures, 16 and 21 °C, as well +DIF for EOD-FR–treated plants. The following questions were proposed: 1) Do EOD-FR treatments differently promote leaf expansion and shade avoidance responses compared with shade light treatments? 2) Does temperature influence shade avoidance responses promoted by shade light and EOD-FR treatments? To answer these questions, petunia ‘Dreams Midnight’ was grown in two growth chambers using multiple tunable LEDs to allow for air temperature and radiation quality manipulation.

Materials and Methods

Plant material and germination environment.

Seeds of petunia ‘Dreams Midnight’ were sown in 128-cell trays (15-mL individual cell volume) using a commercial soilless germination medium (BM2 Germinating Mix; Berger Horticultural Products Ltd., Saint-Modeste, QC, Canada), and placed in a reach-in growth chamber (PG2500; Conviron, Winnipeg, MB, Canada) after sowing. Air temperature and day/night relative humidity in the chamber were set at 21 °C and 55%/65%, respectively. An average total photon flux density (TPFD; 400–780 nm) at canopy height of 164 µmol·m−2·s−1 with 10% blue (400–500 nm), 15% green (500–600 nm), 69% red (600–700 nm), and 6% far-red (700–780 nm) was provided by tunable LED fixtures (tunable fixtures; Elixia; Heliospectra, Gothenburg, Sweden) for a 16-hour photoperiod (0600–2200 HR). On cotyledon unfolding, trays were moved to treatment conditions and grown for 28 d. Trays were thinned to one seedling per cell 1 d after treatment initiation, and watered as needed using tap water with added water-soluble fertilizer (Jack’s 13N–0.9P–10.8K Plug LX; J.R. Peters, Inc., Allentown, PA, USA) providing (in mg·L−1) 150 nitrogen (N), 23 phosphorus (P), 150 potassium (K), 69 calcium (Ca), 34 magnesium (Mg), 0.15 boron (B), 0.07 copper (Cu), 0.75 iron (Fe), 0.37 manganese (Mn), 0.07 molybdenum (Mo), and 0.37 zinc (Zn). The pH and electrical conductivity of the fertilizer solution was confirmed using a handheld meter (Growline H19814; Hanna Instruments, Woonsocket, RI, USA); the average ± SD EC and pH were 1.32 ± 0.04 and 6.81 ± 0.09, respectively.

Growth chamber conditions.

Two reach-in growth chambers described previously were used to create two temperature conditions. For each experiment replication, one chamber had a temperature setpoint of 21 °C, and the second had a temperature setpoint of 16 °C; the day/night relative humidity was set at 55%/65% in both chambers. Chambers were divided using white vinyl fabric to allow for two concurrent radiation treatments. Air temperature was measured using two precision thermistors (ST-100; Apogee Instruments, Inc., Logan, UT, USA) per chamber with one thermistor on each side of the vinyl cloth. Leaf temperature of at least one treatment per chamber was measured with fixed mounted infrared thermocouples with acrylonitrile butadiene styrene plastic housing (OS36–01–T–80F; Omega Engineering Inc., Norwalk, CT, USA). Environmental data were measured every 15 s, and the average was logged every 15 min by a data logger (CR1000X; Campbell Scientific, Inc., Logan, UT, USA). The recorded mean air temperature ± SD averaged across three replications in the 21 and 16 °C chambers were 20.92 ± 0.12 °C and 15.97 ± 0.11 °C, respectively, and the recorded mean leaf temperature ± SD averaged across three replications in the 21 and 16 °C chambers were 20.35 ± 0.18 °C and 15.74 ± 0.1 °C, respectively.

Two concurrent radiation treatments were provided by tunable fixtures (Elixia; Heliospectra) hung ∼0.9 m above canopy level during the normal photoperiod (17.25 h; 1645–1000 HR) and EOD photoperiod (1 h; 1000–1100 HR). Seedlings received either a high R:FR (HI) or a low R:FR “shade light” radiation treatment (SHD), and both daily radiation treatments had the same average TPFD, blue photon flux density (PFD), and green PFD (Table 1). High R:FR and SHD treatments differed in red PFD, far-red PFD, R:FR (600–700 nm/700–780 nm), and extended DLI (eDLI; Westmoreland et al. 2023) (Table 1). For this experiment, extended PAR (ePAR, 400–750 nm) as defined by Zhen et al. (2021) was used to calculate the eDLI for HI and SHD light treatments. The eDLI for HI and SHD treatments were 10.1 and 7.2 mol·m−2·d−1, respectively. Recent research has indicated that the addition of far-red photons to shorter wavelengths (white or red-blue LEDs) increases photosynthesis similarly to the same quantity of added white photons, with the specific caveat that far-red photons do not exceed 30% of the extended PPFD (ePPFD, 400–750 nm; Zhen and Bugbee 2020a, 2020b; Zhen et al. 2021). Because the tunable fixtures emitted photons with wavelengths >750 nm, those photons were not included in eDLI calculations for either treatment. In addition, 48% of the ePPFD of SHD treatments were within 700–750 nm, so ∼53% of the photons from 700–750 nm were not included in eDLI calculations, resulting in a lower eDLI for SHD compared with HI treatments. All photons ranging from 600–780 nm were used to calculate the R:FR (600–700 nm/700–780 nm) for each treatment.

Table 1.

The average ± SD of blue (400–499 nm), green (500–599 nm), red (600–699 nm), and far-red (700–780 nm) photon flux densities (PFD; µmol·m−2·s−1), the ratio of red to far-red radiation (R:FR), and extended daily light integral (eDLI; mol·m−2·d−1) of the high R:FR (HI), shade light (SHD), end-of-day white (EOD-W), and end-of-day far-red (EOD-FR) radiation treatments provided by tunable light-emitting diode (LED) fixtures in growth chambers with air temperature set points of 16 or 21 °C. The eDLI was calculated using the ePAR definition (400–750 nm); because of this, photons with wavelengths >750 nm were not included in eDLI calculations for any treatments, and 53% of far-red photons falling within 700–750 nm in the shade light treatments were not included in eDLI calculations. The total photon flux density (TPFD; 400–780 nm) is equal between the SHD and HI, and the EOD-W and EOD-FR treatments, respectively.

Table 1.

All HI-treated seedlings received either an end-of-day white (EOD-W) or EOD-FR treatment that provided the same average TPFD with different red, blue, green, and far-red PFD, and a different R:FR (Table 1). Shade light–treated seedlings did not receive an EOD treatment and were instead placed under small blackout structures within the chambers at 1000 HR. EOD-FR treatments were included in both 16 and 21 °C chambers, while the EOD-W treatment was only present in the 21 °C chamber. Radiation intensity and spectrum of all treatments at canopy level were measured before the start of each replication using a spectrometer (LI-180; LI-COR Biosciences, Lincoln, NE, USA) with no fewer than nine scans per treatment. The eDLI, as well as blue, green, red, and far-red PFDs, and R:FR ratio of HI, SHD, EOD-W, and EOD-FR for each temperature treatment are summarized in Table 1.

Radiation and temperature treatments.

Seedlings received either HI or SHD during the normal 17.25-hour photoperiod, a 1-hour EOD treatment if grown under HI, and no EOD treatment if grown under SHD. Every day for the duration of the experiment, trays were moved under normal photoperiod conditions at 1645 HR, and then under respective EOD or blackout conditions at 1000 HR the following morning. All treatments are summarized in Table 2. Seedlings received one of the following treatments: HI + EOD-W at 21 °C (control; CN), HI + EOD-FR at 21 °C (EOD21), HI + EOD-FR at 16 °C (EOD16), HI at 21 °C + EOD-FR and dark period at 16 °C (EODDIF), SHD at 21 °C (SHD21), or SHD at 16 °C (SHD16).

Table 2.

Radiation and temperature conditions for each of the six lighting treatments. Radiation treatments consisted of either a high ratio of red to far-red radiation (R:FR) for 17.25 hours (HI) followed by a 1-hour end-of-day (EOD) treatment with either a high (EOD-W) or low R:FR (EOD-FR); or a low R:FR shade light environment for 17.25 hours (SHD) with no EOD treatment. Temperature treatments were established with air temperature set points of 16 or 21 °C. CN = control; EOD16 = EOD-FR at 16 °C; EOD21 = EOD-FR at 21 °C; EODDIF = end-of-day far-red and subsequent dark period at 16 °C; SHD16 = shade light radiation treatment at 16 °C; SHD21 = shade light radiation treatment at 21 °C.

Table 2.

Constant exposure to 16 °C was found to slow the growth of petunia ‘Dreams Midnight’ seedlings resulting in much smaller plants compared with all other treatments; thus, SHD16 and EOD16 were not included in the statistical analysis for this study. These treatments are still commented on briefly in the results and discussion section, and the results for these two treatments, as well as the 21 °C counterparts for comparison, are available in Supplemental Tables 1 and 2.

Data collection and statistical analysis.

Seedling data were collected 21 and 28 d after treatment initiation, and five seedlings from each treatment were randomly selected for measurement and analysis. Roots of selected seedlings were thoroughly washed, and measurements were taken including stem length (centimeters; measured from the base of the hypocotyl to the shoot apical meristem), stem diameter [millimeters; measured directly under and perpendicular to cotyledons using a digital caliper (Fisherbrand™ Traceable™; Thermo Fisher Scientific, Waltham, WA, USA)], and relative chlorophyll content [RCC; measured on the youngest fully expanded leaf using a SPAD chlorophyll meter (Chlorophyll Meter SPAD-502Plus; Konica Minolta, Inc., Chiyoda City, Tokyo, Japan)].

Leaves were removed from seedlings at the node, and total leaf area (square centimeters) was determined using a leaf area meter (LI-3100; LI-COR Biosciences). Average leaf area (square centimeters) was calculated by dividing the total leaf area by the number of counted leaves and the length of the youngest fully expanded leaf was measured (leaf length; centimeters). Leaves, stems, and roots of each measured seedling were separated and dried at 70 °C for at least 5 d to determine the dry mass of each using an analytical microbalance (Analytical Balance ME54E; Mettler-Toledo, LLC, Columbus, OH, USA). LMA (milligrams per square millimeter) was calculated by dividing total leaf area by leaf dry mass, and stem dry mass per unit stem length (milligrams per centimeter) was calculated by dividing stem length by stem dry mass.

This experiment was a randomized complete block design with radiation-temperature treatments (four levels) as treatment factors and replication as the block. Three replications were conducted from January through June 2021, and chamber temperature conditions were switched between each replication to control for any effect of the chamber. The treatment effects on total leaf area, leaf dry mass, LMA, leaf length, RCC, and stem diameter were compared by one-way analysis of variance (ANOVA) and pairwise comparison of estimated marginal means averaged over replication using Tukey’s honestly significant difference at P < 0.05. The treatment effects on root dry mass, stem dry mass, stem length, stem dry mass per unit length, and average leaf area were compared by Welch’s one-way ANOVA and pairwise comparison of means averaged over replication using the Holm-Bonferroni method at P < 0.05; this was done because the assumption of homogeneity of variance was violated for these variables and a standard ANOVA was considered inappropriate. All statistical analyses were completed using R statistical software (R Core Team 2022).

Results and Discussion

Far-red radiation is an important signal of vegetational shade for plants, but has also been shown to promote potentially beneficial plant responses such as an increase in leaf area when added to a background of red-blue or white radiation, as well as when applied as EOD light (Casal et al. 1987; Park and Runkle 2018; Zhen and Bugbee 2020b; Zou et al. 2019); this may be an effective strategy for the production of young annual bedding plants early in the production cycle when the LAI is low to improve light interception and reduce wasted radiation. As noted in the introductory paragraphs, far-red light can also promote significant stem elongation, which is undesirable for plug production (Kalaitzoglou et al. 2019; Park and Runkle 2018; Pramuk and Runkle 2005). In the present study, petunia ‘Dreams Midnight’ seedlings responded differently to shade light and EOD-FR treatments. For seedlings grown at a constant average temperature of 21 °C, EOD-FR (EOD21) had minimal effects and seedlings were similar to CN for all measured variables. In contrast, seedlings grown under shade light (SHD21) showed a large increase in leaf area along with other shade avoidance responses including stem elongation and a reduction in LMA and stem dry mass per unit length.

Effects of EOD-FR.

In a previous experiment, seedlings of petunia ‘Dreams Midnight’ grown in a greenhouse under a DLI of 5.26 mol·m−2·d−1 received 0.5-hour and 4-hour EOD-FR treatments with a R:FR of 0.15 and far-red PFD of 20 mol·m−2·d−1; both EOD-FR treatments resulted in seedlings with longer stems and similar leaf area to control plants that received no EOD-FR treatment (Percival and Craver 2023). It was thought that lack of leaf expansion and significant stem elongation in that study were at least in-part due to the low DLI limiting seedling growth. In the present study, petunia ‘Dreams Midnight’ seedlings were grown at the recommended minimum DLI (10 mol·m−2·d−1, eDLI in this experiment) for quality plug production with a 1-hour EOD-FR treatment to investigate if EOD-FR promotes leaf expansion as well as other common shade avoidance responses, such as stem elongation, when the DLI is not excessively limiting for growth. Under a constant temperature, all measured variables including total leaf area, average leaf area, leaf length, stem length and diameter, RCC, and all dry mass parameters were similar under CN and EOD21 at days 21 and 28 (Figs. 1 and 2, Table 3). The lack of a significant effect on leaf area in response to EOD-FR contrasts with the responses of some species, such as lettuce (Zou et al. 2019) and Petunia axilaris (Casal et al. 1987), but is similar to others such as tomato (Kalaitzoglou et al. 2019) and poinsettia (Islam et al. 2014). For example, for poinsettia cultivars ‘Christmas Eve’ and ‘Christmas Spirit’, 30-minute EOD-FR treatments resulted in plants with similar leaf area compared with EOD red (EOD-R) treatments, whereas Petunia axillaris EOD-FR–treated plants had greater leaf area compared with EOD-R–treated plants (Casal et al. 1987, Islam et al. 2014). In both studies, EOD-R– and EOD-FR–treated plants had a similar leaf number, indicating leaf area differences and similarities were due to the size of individual leaves (Casal et al. 1987; Islam et al. 2014.); this is similar to the present study, as CN and EOD21 plants had a similar average leaf area at days 21 and 28 (Fig. 1). For both poinsettia and tomato, EOD-FR did promote an increase in shoot length and plant height, respectively (Islam et al. 2014, Kalaitzoglou et al. 2019). In the present study, although stem length was slightly longer for EOD21 compared with CN at days 21 and 28, these differences were not statistically significant (Fig. 2). In place of an EOD-R treatment, the EOD-W treatment in the present study was designed to mimic the spectral quality during the day at a much lower intensity, meaning it had similar percentages of blue, green, red, and far-red radiation (Table 1). An overall reduction in radiation intensity as well as the specific reduction of blue radiation due to absorption by vegetation are known to induce shade avoidance responses such as internode elongation (Ballaré et al. 1991, Ballaré and Pierik 2017). The overall low intensity as well as the blue and green radiation present in the EOD-W treatment may have affected plant responses differently if the EOD-W treatment only contained red and far-red radiation, but the specific effects of the radiation intensity of the EOD-W treatment as well as blue and green radiation were not tested in this study.

Fig. 1.
Fig. 1.

Total leaf area, average leaf area, and leaf mass per unit area for Petunia ×hybrida ‘Dreams Midnight’ seedlings 21 (A, C, F) and 28 (B, D, E) days post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 hours at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade light treatment for 17.25 hours at 21 °C (SH21). For total leaf area and leaf mass per unit area, means sharing a letter are not statistically different by Tukey’s honestly significant difference test at P ≤ 0.05. For average leaf area, means sharing a letter are not statistically different by the Holm-Bonferroni multiple comparisons method at P ≤ 0.05. Error bars represent 1 standard error of the mean.

Citation: HortScience 59, 1; 10.21273/HORTSCI17420-23

Fig. 2.
Fig. 2.

Stem length and stem dry mass per unit length for Petunia ×hybrida ‘Dreams Midnight’ seedlings 21 (A, C) and 28 (B, D) days post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 h at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade light treatment for 17.25 hours at 21 °C (SH21). Means sharing a letter are not statistically different by the Holm-Bonferroni multiple comparisons method at P ≤ 0.05. Error bars represent 1 standard error of the mean.

Citation: HortScience 59, 1; 10.21273/HORTSCI17420-23

Table 3.

Relative chlorophyll content (RCC), leaf length, stem diameter, leaf dry mass, stem dry mass, and root dry mass for Petunia ×hybrida ‘Dreams Midnight’ 21 and 28 d post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 hours at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade radiation treatment for 17.25 hours at 21 °C (SHD21).

Table 3.

The length of the normal photoperiod (17.25 h) may have also attenuated some EOD-FR responses. Lund et al. (2007) found that chrysanthemum (Chrysanthemum morifolium) ‘Coral Charm’ grown under a 9-hour photoperiod and 30-minute EOD-FR treatments with R:FRs of 0.4 or 0.7 displayed increased plant height compared with an EOD-R (R:FR = 2.4) treatment; these authors cited earlier work by Mortensen and Moe (1992) showing that natural EOD radiation quality did not affect chrysanthemum grown under longer photoperiods (12–18.5 hours), as well as work by Downs et al. (1957) showing that the effect of EOD-FR on elongation was reduced for bean (Phaseolus vulgaris) when grown under longer relative to shorter photoperiods. Lund et al. (2008) conducted further work using the same EOD-FR treatments and study taxa as Lund et al. (2007), but with photoperiod durations of 9, 14, and 19 hours; they found EOD-FR was more effective in promoting an increase in plant height when grown under the 9-hour treatment compared with the 14- and 19-hour treatments. Thus, another possible explanation for the lack of significant EOD-FR–induced shade avoidance responses in our study may have been due to the photoperiod duration. However, Lund et al. (2008) also found that EOD-FR applied after longer photoperiods resulted in increased leaf area relative to the shorter photoperiods followed by EOD-FR treatments. Different photoperiod durations were not implemented in the present study so the effect of photoperiod duration on EOD-FR treatments could not be examined.

Notably, LMA was also statistically similar between CN and EOD21 at days 21 and 28; at day 21 LMA was slightly greater under CN while the opposite was true at day 28 (Fig. 1). A reduction in LMA is a common response for both shade-tolerant and -intolerant species under vegetational shade; this has been reported for plants grown under a lower R:FR or given EOD-FR treatments, but a strong correlation with radiation quantity has also been observed, with decreasing DLI resulting in reduced LMA (Ballaré and Pierik 2017; Gommers et al. 2013; Poorter et al. 2009; Zou et al. 2019). The similar LMA for CN and EOD21 plants may be attributable to both treatments being grown under the same eDLI.

Effects of shade light.

Smith and Whitelam (1997) noted that when PPFD remained adequate for growth, reducing the R:FR would elicit exaggerated responses in shade-intolerant species such as sunflower (Helianthus annus). In their discussion of ePAR, Zhen et al. (2021) also wrote that the effects of far-red radiation on elongation responses may practically limit far-red photons to 20% of the TPFD for most crops. In the present study, far-red photons made up ∼50% of the TPFD for SHD, and growth under this treatment promoted significant shade avoidance responses for petunia seedlings in contrast to EOD21. Compared with CN seedlings, SHD21 seedlings had longer leaves and stems, as well as reduced leaf dry mass, root dry mass, LMA, stem dry mass per unit length, and RCC at days 21 and 28 (Table 3, Figs. 1 and 2); these responses are characteristic of shade avoidance (Franklin 2008; Gommers et al. 2013; Smith and Whitelam 1997).

The use of supplemental far-red radiation has been shown to increase total and average leaf area in lettuce (Zou et al. 2019), petunia (Park and Runkle 2018), and tomato (Kalaitzoglou et al. 2019), and these increases are attributed to cell expansion that occurs when plant growth is not limited by a low PPFD, which is an important characteristic of natural vegetational shade (Ballaré and Pierik 2017; Carabelli et al. 2007; Patel et al. 2013; Zou et al. 2019). Total leaf area and average leaf area were found to be similar between CN and SHD21 treatments at day 21, but at day 28 SHD21 treatments had significantly greater total leaf area and average leaf area compared with CN (Table 3, Fig. 1). These results show that the difference in total leaf area between these treatments was due to individual leaf size rather than the number of leaves. However, the increase in total leaf area was not accompanied by a proportional increase in biomass (Table 3), as the LMA for SHD21 was much lower compared with CN21 (Fig. 1). As mentioned previously, LMA has been shown to decrease under a low R:FR, EOD-FR treatments, and a lower DLI. In the present experiment, the reduced LMA under SHD21 may be attributable to both a low R:FR and lower eDLI.

The stems of petunia seedlings grown under SHD21 were longer than CN, but the stem dry mass per unit length (inverse of specific stem length) of CN was nearly double that of SHD21 (Fig. 2); these results are in line with previous research wherein growth under a low R:FR results in an increase in specific stem length (Poorter et al. 2009). Working with foxglove (Digitalis purpurea) grown under different supplemental far-red treatments, Elkins and van Iersel (2020) used a similar metric, compactness (shoot dry mass per unit plant height), to differentiate between shade-induced elongation without a proportional increase in biomass and faster growth wherein if plant height were increased there would be a proportional increase in biomass. These authors found that compactness was unaffected by supplemental far-red radiation, but the highest percentage of far-red used in their lighting treatments was 26.9% compared with ∼50% in the present study, which likely reflects comments from Zhen et al. (2021) on the practical limitation of the fraction of far-red photons.

The increase in leaf area as well as stem length for petunia seedlings under SHD21 compared with CN could potentially facilitate an increase in light interception, but the decrease in LMA and stem dry mass per unit length likely reduce the ability of leaves and stems to resist mechanical stress (Gommers et al. 2013). Although not recorded as data, stems of SHD21 seedlings were notably unstable; this may have been a result of the reduced stem dry mass per unit length of SHD21 seedlings, but the reduced root dry mass of SHD21 plants compared with CN may also have contributed to the reduction in mechanical stability (Table 3). Although the SHD21 treatment was not designed to evaluate a specific plug production strategy, the reduced structural stability and exaggerated elongation demonstrate that the deleterious shade avoidance responses outweigh potential benefits of leaf expansion and potential increased light interception under these conditions, and highlight the practical limits of the fraction of far-red photons noted by Zhen et al. (2021).

Effects of growth at 16 °C.

Previous research has shown that temperature can affect morphological responses to far-red radiation, whereas growth outside of a plant’s optimal temperature range can inhibit plant growth and development (Bahuguna and Jagadish 2015; Hatfield and Prueger 2015; Patel et al. 2013; Xiong et al. 2002). As discussed previously, tropical and temperate ecotypes of Arabidopsis have been shown to respond differently to growth under a constant R:FR of 0.1 at 16 and 22 °C (Patel et al. 2013). In the present study, a constant air temperature of 16 °C generally stunted growth of petunia ‘Dreams Midnight’ regardless of lighting treatment. Specifically, relative to their 21 °C counterparts (EOD21 and SHD21), EOD16 and SHD16 had lower leaf area and length, leaf number, stem diameter, and all dry mass parameters sans LMA; LMA was greater under EOD16 and SHD16 compared with 21 °C counterparts (Supplemental Tables 1 and 2). Increased LMA is a common response of plants growing under low temperature, thus increased LMA at 16°C is likely a more general temperature response (Poorter et al. 2009). Last, although growth was slowed under 16°C for both EOD16 and SHD16, several shade responses were observable for SHD16, including stem and leaf elongation as well as reductions in LMA and stem dry mass per unit length, at least compared with EOD16 (Supplemental Tables 1 and 2).

As exposure to a constant 16 °C was expected to result in slower growth, we implemented one +DIF treatment (EODDIF) wherein seedlings were grown under a high R:FR during the day at 21 °C, and were moved to the 16 °C chamber for the EOD-FR and dark period. The effects of +DIF and −DIF have been shown to be enhanced and attenuated, respectively, by EOD-FR treatments in multiple species including cucumber (Xiong et al. 2002) and lily (Lillium longiflorum; Blom and Kerec 2003). In the present study, petunia ‘Dreams Midnight’ was shifted to a growth chamber set at 16 °C for both the EOD-FR treatment and the subsequent dark period to examine the effects of a reduced temperature on EOD-FR responses.

Several measured variables were found to be smaller under EODDIF compared with EOD21 including total leaf area, leaf dry mass, average leaf area, stem dry mass, stem diameter, and root dry mass, but not all differences were significant on both measurement days (Table 3, Figs. 1 and 2). Notably, the dry mass of roots, leaves, and stems was reduced at days 21 and 28 under EODDIF compared with EOD21. The total leaf area of EODDIF seedlings was also less than that under EOD21 at days 21 and 28, but the difference at day 21 was due to a higher average leaf area under EOD21 whereas at day 28 the difference was due to the number of leaves, as both treatments had a similar average leaf area. These results are somewhat expected, as at a constant temperature of 21 °C the EOD-FR treatment had no significant effects on seedlings relative to the control treatment, and the reductions in all dry mass parameters as well as total leaf area under EODDIF show that 16 °C likely slowed growth of petunia ‘Dreams Midnight’ at this colder temperature. In addition to examining the potential factors affecting general responses to EOD-FR discussed previously, further research using moderate decreases in night temperature is warranted to better understand the interactive effects of EOD-FR radiation and the difference in day and night temperatures.

Conclusion

In this study, a shade light treatment providing a low R:FR (0.5) throughout the day promoted significant shade avoidance responses for petunia ‘Dreams Midnight’ including stem elongation, a reduction in plant dry mass, and larger but very thin leaves. Although leaf expansion and stem elongation may be advantageous in improving light interception, the reduction in LMA and stem dry mass per unit length also indicate that shade light–treated seedlings would be very easily damaged by mechanical stressors during plug transplant or shipping. In contrast, seedlings that received a 1-hour EOD-FR treatment with a very low R:FR (0.14) were similar to those that received an EOD-W treatment with a very high R:FR (10.9) for all measured parameters. This may indicate that EOD-FR treatments are not effective in promoting leaf expansion for petunia ‘Dreams Midnight’, as responses may be species specific. However, leaf expansion in response to EOD-FR treatments may also depend on several other factors including radiation intensity or DLI, photoperiod duration, and temperature. Thus, further research is warranted to examine these potential interacting factors, as the early expansion of leaves may be advantageous in improving light capture for young plants and in reducing wasted electric light.

References Cited

  • Bahuguna RN, Jagadish KSV. 2015. Temperature regulation of plant phenological development. Environ Exp Bot. 111:8390. https://doi.org/10.1016/j.envexpbot.2014.10.007 0098-8472/ã.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL. 2014. Light regulation of plant defense. Annu Rev Plant Biol. 65:355363. https://doi.org/10.1146/annurev-arplant-050213-040145.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL, Austin AT. 2019. Recalculating growth and defense strategies under competition: Key roles of photoreceptors and jasmonates. J Expt Bot. 30(13):34253436. https://doi.org/10.1093/jxb/erz237.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL, Pierik R. 2017. The shade-avoidance syndrome: Multiple signals and ecological consequences. Plant Cell Environ. 40:25302543. https://doi.org/10.1111/pce.12914.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL, Scopel AL, Sánchez RA. 1991. Photocontrol of stem elongation in plant neighborhoods: Effects of photon fluence rate under natural conditions of radiation. Plant Cell Environ. 40:25302543. https://doi.org/10.1111/j.1365-3040.1991.tb01371.x.

    • Search Google Scholar
    • Export Citation
  • Blom T, Kerec D. 2003. Effects of far-red light/temperature DIF and far-red light/temperature pulse combinations on height of lily hybrids. J Hortic Sci Biotechnol. 78:278282. https://doi.org/10.1080/14620316.2003.11511618.

    • Search Google Scholar
    • Export Citation
  • Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I. 2007. Canopy shade causes a rapid and transient arrest in leaf development through auxin induced cytokinin oxidase activity. Genes Dev. 21:18631868. https://doi.org/10.1101/gad.432607.

    • Search Google Scholar
    • Export Citation
  • Casal JJ. 2013. Photoreceptor signaling networks in response to shade. Annu Rev Plant Biol. 64:403427. https://doi.org/10.1146/annurevarplant-050312-120221.

    • Search Google Scholar
    • Export Citation
  • Casal JJ, Aphalo PJ, Sánchez R. 1987. Phytochrome effects on leaf growth and chlorophyll content in Petunia axilaris. Plant Cell Environ. 10:509514. https://doi.org/10.1111/j.1365-3040.1987.tb01829.x.

    • Search Google Scholar
    • Export Citation
  • Casal JJ, Balasubramanian S. 2019. Thermomorphogenesis. Annu Rev Plant Biol. 70:321346. https://doi.org/10.1146/annurev-arplant-050718-095919.

    • Search Google Scholar
    • Export Citation
  • Chia P, Kubota C. 2010. End-of-day far-red light quality and dose requirements for tomato rootstock hypocotyl elongation. HortScience. 45:15011506. https://doi.org/10.21273/HORTSCI.45.10.1501.

    • Search Google Scholar
    • Export Citation
  • Craver JK, Boldt JK, Lopez RG. 2018. Radiation intensity and quality from sole-source light-emitting diodes affect seedling quality and subsequent flowering of long-day bedding plant species. HortScience. 53:14071415. https://doi.org/10.21273/HORTSCI13228-18.

    • Search Google Scholar
    • Export Citation
  • Craver JK, Boldt JK, Lopez RG. 2019. Comparison of supplemental lighting provided by high-pressure sodium lamps or light-emitting diodes for the propagation and finishing of bedding plants in a commercial greenhouse. HortScience. 54:5259. https://doi.org/10.21273/HORTSCI13471-18.

    • Search Google Scholar
    • Export Citation
  • Downs RJ, Hendricks SB, Borthwick HA. 1957. Photoreversible control of elongation of pinto beans and other plant under normal conditions of growth. Bot Gaz. 18:199208. https://doi.org/10.1086/335946.

    • Search Google Scholar
    • Export Citation
  • Elkins C, van Iersel MW. 2020. Supplemental far-red light emitting diode light increases growth of foxglove seedlings under sole-source lighting. HortTechnology. 30:564569. https://doi.org/10.21273/HORTTECH04661-20.

    • Search Google Scholar
    • Export Citation
  • Fernández-Milmanda GL, Ballaré CL. 2021. Shade avoidance: Expanding the color and hormone palette. Trends Plant Sci. 26:509523. https://doi.org/10.1016/j.tplants.2020.12.006.

    • Search Google Scholar
    • Export Citation
  • Franklin KA. 2008. Shade avoidance. New Phytol. 179:930944. https://doi.org/10.1111/j.1469-8137.2008.02507.x.

  • Gommers CMM, Visser EJW, St Onge KR, Voesenek LACJ, Pierik R. 2013. Shade tolerance: When growing tall is not an option. Trends Plant Sci. 18(2):6571. https://doi.org/10.1016/j.tplants.2012.09.008.

    • Search Google Scholar
    • Export Citation
  • Hatfield JL, Prueger JH. 2015. Temperature extremes: Effect on plant growth and development. Weather Clim. 10:410. https://doi.org/10.1016/j.wace.2015.08.001 22120947/Published.

    • Search Google Scholar
    • Export Citation
  • Heraut-Bron V, Robin C, Varlet-Grancher C, Afif D, Guckert A. 2000. Light quality (red:far-red ratio): Does it affect photosynthetic activity, net CO2 assimilation, and morphology of young white clover leaves? Can J Bot. 77:14251431. https://doi.org/10.1139/b99-099.

    • Search Google Scholar
    • Export Citation
  • Islam MA, Tarkowská D, Clarke JL, Blystad D, Gislerød HR, Torre S, Olsen JE. 2014. Impact of end-of-day red and far-red light on plant morphology and hormone physiology of poinsettia. Scientia Hortic. 174:7786. https://doi.org/10.1016/j.scienta.2014.05.013.

    • Search Google Scholar
    • Export Citation
  • Kalaitzoglou P, van Leperen W, Harbinson J, van der Meer M, Martinakos S, Weerheim K, Nicole CCS, Marcelis LFM. 2019. Effects of continuous or end-of-day far-red light on tomato plant growth, morphology, light absorption, and fruit production. Front Plant Sci. 10:111. https://doi.org/10.3389/fpls.2019.00322.

    • Search Google Scholar
    • Export Citation
  • Küpers JJ, Oskam L, Pierik R. 2020. Photoreceptors regulate plant developmental plasticity through auxin. Plants. 9(8):116. https://doi.org/10.3390/plants9080940.

    • Search Google Scholar
    • Export Citation
  • Li Q, Kubota C. 2009. Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce. Environ Exp Bot. 67:5964. https://doi.org/10.1016/j.envexpbot.2009.06.011.

    • Search Google Scholar
    • Export Citation
  • Lund JB, Blom TJ, Aaslyng JM. 2007. End-of-day lighting with different red/far-red ratios using light-emitting diodes affects plant growth of chrysanthemum × morifolium Ramat. ‘Coral Charm’. HortScience. 42:16091611. https://doi.org/10.21273/HORTSCI.42.7.1609.

    • Search Google Scholar
    • Export Citation
  • Lund JB, Körner O, Aaslyng JM. 2008. Stem elongation of chrysanthemum in response to end-of-day light treatments and photoperiod. Acta Hortic. 766:127135. https://doi.org/10.17660/ActaHortic.2008.766.12.

    • Search Google Scholar
    • Export Citation
  • Mortensen LM, Moe R. 1992. Effects of selective screening of the daylight spectrum and of twilight on plant growth in greenhouse. Acta Hortic. 305:103108. https://doi.org/10.17660/ActaHortic.1992.305.14.

    • Search Google Scholar
    • Export Citation
  • Myster J, Moe R. 1995. Effect of diurnal temperature alternations on plant morphology in some greenhouse crops—a mini review. Scientia Hortic. 62:205215. https://doi.org/10.1016/0304-4238(95)00783-P.

    • Search Google Scholar
    • Export Citation
  • Park Y, Runkle ES. 2017. Far-red radiation promotes growth of seedlings by increasing leaf expansion and whole-plant net assimilation. Environ Exp Bot. 136:4149. https://doi.org/10.1016/j.envexpbot.2016.12.013.

    • Search Google Scholar
    • Export Citation
  • Park Y, Runkle ES. 2018. Far-red radiation and photosynthetic photon flux density independently regulate seedling growth but interactively regulate flowering. Environ Exp Bot. 115:206216. https://doi.org/10.1016/j.envexpbot.2018.06.033.

    • Search Google Scholar
    • Export Citation
  • Patel D, Basu M, Hayes S, Majláth I, Hetherington FM, Tschaplinski TJ, Franklin KA. 2013. Temperature-dependent shade avoidance involves the receptor-like kinase ERECTA. Plant J. 73:980992. https://doi.org/10.1111/tpj.12088.

    • Search Google Scholar
    • Export Citation
  • Percival A, Craver JK. 2023. End-of-day far-red lighting with a low daily light integral increases stem length but does not promote early leaf expansion for Petunia ×hybrida seedlings. HortScience. 58:10101017. https://doi.org/10.21273/HORTSCI17132-23.

    • Search Google Scholar
    • Export Citation
  • Poel BR, Runkle ES. 2017. Seedling growth is similar under supplemental greenhouse lighting from high-pressure sodium lamps or light emitting diodes. HortScience. 52:388394. https://doi.org/10.21273/HORTSCI11356-16.

    • Search Google Scholar
    • Export Citation
  • Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R. 2009. Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis. New Phytol. 182:565588. https://doi.org/10.1111/j.1469-8137.2009.02830.x.

    • Search Google Scholar
    • Export Citation
  • Pramuk LA, Runkle ES. 2005. Photosynthetic daily light integral during the seedling stage influences subsequent growth and flowering of celosia, impatiens, salvia, tagetes, and viola. HortScience. 40:13361339. https://doi.org/10.21273/HORTSCI.40.5.1336.

    • Search Google Scholar
    • Export Citation
  • Qaderi M, Godin VJ, Reid DM. 2015. Single and combined effects of temperature and red:far-red light ratio on evening primrose (Oenthera biennis). Botany. 93(8):475483. https://doi.org/10.1139/cjb-2014-0194.

    • Search Google Scholar
    • Export Citation
  • R Core Team. 2022. R-4.2.2 for macOS. R Foundation for Statistical Computing, Vienna, Austria. https://archive.linux.duke.edu/cran/. [accessed 27 Jul 2023].

  • Romero-Montepaone S, Poodts S, Fischbach P, Sellaro R, Zurbriggen MD, Casal JJ. 2020. Shade avoidance responses become more aggressive in warm environments. Plant Cell Environ. 43(7):16251636. https://doi.org/10.1111/pce.13720.

    • Search Google Scholar
    • Export Citation
  • Romero-Montepaone S, Sellaro R, Esteban Hernando C, Costigliolo-Rojas C, Bianchimano L, Ploschuk EL, Yanovsky MJ, Casal JJ. 2021. Functional convergence of growth responses to shade and warmth in Arabidopsis. New Phytol. 231(5):18901905. https://doi.org/10.1111/nph.17430.

    • Search Google Scholar
    • Export Citation
  • Sellaro R, Pacín M, Casal JJ. 2012. Diurnal dependence of growth response to shade in arabidopsis: Role of hormone, clock, and light signaling. Mol Plant. 5:619628. https://doi.org/10.1093/mp/ssr122.

    • Search Google Scholar
    • Export Citation
  • Slauenwhite KLI, Qaderi MM. 2013. Single and interactive effects of temperature and light quality on four canola cultivars. J Agron Crop Sci. 199:286298. https://doi.org/10.1111/jac.12014.

    • Search Google Scholar
    • Export Citation
  • Smith H, Whitelam GC. 1997. The shade avoidance syndrome: Multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20:840844. https://doi.org/10.1046/j.13653040.1997.d01-104.x.

    • Search Google Scholar
    • Export Citation
  • Thingnaes E, Torre S, Moe R. 2008. The role of phytochrome B, D and E in thermoperiodic responses of Arabidopsis thaliana. Plant Growth Regulat. 56:5359. https://doi.org/10.1007/s10725-008-9283-6.

    • Search Google Scholar
    • Export Citation
  • Westmoreland FM, Kusuma P, Bugbee B. 2023. Elevated UV photon fluxes minimally affected cannabinoid concentration in a high-CBD cultivar. Front Plant Sci. 14:1220585. https://doi.org/10.3389/fpls.2023.1220585.

    • Search Google Scholar
    • Export Citation
  • Wu B, Hitti Y, Macpherson S, Orsat V, Lefsrud MG. 2020. Comparison and perspective of conventional and LED lighting for photobiology and industry applications. Environ Exp Bot. 171:103953. https://doi.org/10.1016/j.envexpbot.2019.103953.

    • Search Google Scholar
    • Export Citation
  • Xiong J, Patil GG, Moe R. 2002. Effect of DIF and end-of-day light quality on stem elongation in Cucumis sativus. Scientia Hortic. 94:219229. https://doi.org/10.1016/S0304-4238(02)00002-X.

    • Search Google Scholar
    • Export Citation
  • Yang Z, Kubota C, Chia P, Kacira M. 2012. Effect of end-of-day far-red light from a movable LED fixture on squash rootstock hypocotyl elongation. Scientia Hortic. 136:8186. https://doi.org/10.1016/j.scienta.2011.12.023.

    • Search Google Scholar
    • Export Citation
  • Zhen S, Bugbee B. 2020a. Far-red photons have equivalent efficiency to traditional photosynthetic photons: Implications for redefining photosynthetically active radiation. Plant Cell Environ. 43:12591272. https://doi.org/10.1111/pce.13730.

    • Search Google Scholar
    • Export Citation
  • Zhen S, Bugbee B. 2020b. Substituting far-red for traditionally defined photosynthetic photons results in equal canopy quantum yield for CO2 fixation and increased photon capture during long-term studies: Implications for re-defining PAR. Front Plant Sci. 11:581156. https://doi.org/10.3389/fpls.2020.581156.

    • Search Google Scholar
    • Export Citation
  • Zhen S, van Iersel M, Bugbee B. 2021. Why far-red photons should be included in the definition of photosynthetic photons and the measurement of horticultural fixture efficacy. Front Plant Sci. 12:693445. https://doi.org/10.3389/fpls.2021.693445.

    • Search Google Scholar
    • Export Citation
  • Zou J, Zhang Y, Zhang Y, Bian Z, Fanourakis D, Yang Q, Li T. 2019. Morphological and physiological properties of indoor cultivated lettuce in response to additional far-red light. Scientia Hortic. 257:108725. https://doi.org/10.1016/j.scienta.2019.108725.

    • Search Google Scholar
    • Export Citation
  • Fig. 1.

    Total leaf area, average leaf area, and leaf mass per unit area for Petunia ×hybrida ‘Dreams Midnight’ seedlings 21 (A, C, F) and 28 (B, D, E) days post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 hours at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade light treatment for 17.25 hours at 21 °C (SH21). For total leaf area and leaf mass per unit area, means sharing a letter are not statistically different by Tukey’s honestly significant difference test at P ≤ 0.05. For average leaf area, means sharing a letter are not statistically different by the Holm-Bonferroni multiple comparisons method at P ≤ 0.05. Error bars represent 1 standard error of the mean.

  • Fig. 2.

    Stem length and stem dry mass per unit length for Petunia ×hybrida ‘Dreams Midnight’ seedlings 21 (A, C) and 28 (B, D) days post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 h at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade light treatment for 17.25 hours at 21 °C (SH21). Means sharing a letter are not statistically different by the Holm-Bonferroni multiple comparisons method at P ≤ 0.05. Error bars represent 1 standard error of the mean.

  • Bahuguna RN, Jagadish KSV. 2015. Temperature regulation of plant phenological development. Environ Exp Bot. 111:8390. https://doi.org/10.1016/j.envexpbot.2014.10.007 0098-8472/ã.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL. 2014. Light regulation of plant defense. Annu Rev Plant Biol. 65:355363. https://doi.org/10.1146/annurev-arplant-050213-040145.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL, Austin AT. 2019. Recalculating growth and defense strategies under competition: Key roles of photoreceptors and jasmonates. J Expt Bot. 30(13):34253436. https://doi.org/10.1093/jxb/erz237.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL, Pierik R. 2017. The shade-avoidance syndrome: Multiple signals and ecological consequences. Plant Cell Environ. 40:25302543. https://doi.org/10.1111/pce.12914.

    • Search Google Scholar
    • Export Citation
  • Ballaré CL, Scopel AL, Sánchez RA. 1991. Photocontrol of stem elongation in plant neighborhoods: Effects of photon fluence rate under natural conditions of radiation. Plant Cell Environ. 40:25302543. https://doi.org/10.1111/j.1365-3040.1991.tb01371.x.

    • Search Google Scholar
    • Export Citation
  • Blom T, Kerec D. 2003. Effects of far-red light/temperature DIF and far-red light/temperature pulse combinations on height of lily hybrids. J Hortic Sci Biotechnol. 78:278282. https://doi.org/10.1080/14620316.2003.11511618.

    • Search Google Scholar
    • Export Citation
  • Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I. 2007. Canopy shade causes a rapid and transient arrest in leaf development through auxin induced cytokinin oxidase activity. Genes Dev. 21:18631868. https://doi.org/10.1101/gad.432607.

    • Search Google Scholar
    • Export Citation
  • Casal JJ. 2013. Photoreceptor signaling networks in response to shade. Annu Rev Plant Biol. 64:403427. https://doi.org/10.1146/annurevarplant-050312-120221.

    • Search Google Scholar
    • Export Citation
  • Casal JJ, Aphalo PJ, Sánchez R. 1987. Phytochrome effects on leaf growth and chlorophyll content in Petunia axilaris. Plant Cell Environ. 10:509514. https://doi.org/10.1111/j.1365-3040.1987.tb01829.x.

    • Search Google Scholar
    • Export Citation
  • Casal JJ, Balasubramanian S. 2019. Thermomorphogenesis. Annu Rev Plant Biol. 70:321346. https://doi.org/10.1146/annurev-arplant-050718-095919.

    • Search Google Scholar
    • Export Citation
  • Chia P, Kubota C. 2010. End-of-day far-red light quality and dose requirements for tomato rootstock hypocotyl elongation. HortScience. 45:15011506. https://doi.org/10.21273/HORTSCI.45.10.1501.

    • Search Google Scholar
    • Export Citation
  • Craver JK, Boldt JK, Lopez RG. 2018. Radiation intensity and quality from sole-source light-emitting diodes affect seedling quality and subsequent flowering of long-day bedding plant species. HortScience. 53:14071415. https://doi.org/10.21273/HORTSCI13228-18.

    • Search Google Scholar
    • Export Citation
  • Craver JK, Boldt JK, Lopez RG. 2019. Comparison of supplemental lighting provided by high-pressure sodium lamps or light-emitting diodes for the propagation and finishing of bedding plants in a commercial greenhouse. HortScience. 54:5259. https://doi.org/10.21273/HORTSCI13471-18.

    • Search Google Scholar
    • Export Citation
  • Downs RJ, Hendricks SB, Borthwick HA. 1957. Photoreversible control of elongation of pinto beans and other plant under normal conditions of growth. Bot Gaz. 18:199208. https://doi.org/10.1086/335946.

    • Search Google Scholar
    • Export Citation
  • Elkins C, van Iersel MW. 2020. Supplemental far-red light emitting diode light increases growth of foxglove seedlings under sole-source lighting. HortTechnology. 30:564569. https://doi.org/10.21273/HORTTECH04661-20.

    • Search Google Scholar
    • Export Citation
  • Fernández-Milmanda GL, Ballaré CL. 2021. Shade avoidance: Expanding the color and hormone palette. Trends Plant Sci. 26:509523. https://doi.org/10.1016/j.tplants.2020.12.006.

    • Search Google Scholar
    • Export Citation
  • Franklin KA. 2008. Shade avoidance. New Phytol. 179:930944. https://doi.org/10.1111/j.1469-8137.2008.02507.x.

  • Gommers CMM, Visser EJW, St Onge KR, Voesenek LACJ, Pierik R. 2013. Shade tolerance: When growing tall is not an option. Trends Plant Sci. 18(2):6571. https://doi.org/10.1016/j.tplants.2012.09.008.

    • Search Google Scholar
    • Export Citation
  • Hatfield JL, Prueger JH. 2015. Temperature extremes: Effect on plant growth and development. Weather Clim. 10:410. https://doi.org/10.1016/j.wace.2015.08.001 22120947/Published.

    • Search Google Scholar
    • Export Citation
  • Heraut-Bron V, Robin C, Varlet-Grancher C, Afif D, Guckert A. 2000. Light quality (red:far-red ratio): Does it affect photosynthetic activity, net CO2 assimilation, and morphology of young white clover leaves? Can J Bot. 77:14251431. https://doi.org/10.1139/b99-099.

    • Search Google Scholar
    • Export Citation
  • Islam MA, Tarkowská D, Clarke JL, Blystad D, Gislerød HR, Torre S, Olsen JE. 2014. Impact of end-of-day red and far-red light on plant morphology and hormone physiology of poinsettia. Scientia Hortic. 174:7786. https://doi.org/10.1016/j.scienta.2014.05.013.

    • Search Google Scholar
    • Export Citation
  • Kalaitzoglou P, van Leperen W, Harbinson J, van der Meer M, Martinakos S, Weerheim K, Nicole CCS, Marcelis LFM. 2019. Effects of continuous or end-of-day far-red light on tomato plant growth, morphology, light absorption, and fruit production. Front Plant Sci. 10:111. https://doi.org/10.3389/fpls.2019.00322.

    • Search Google Scholar
    • Export Citation
  • Küpers JJ, Oskam L, Pierik R. 2020. Photoreceptors regulate plant developmental plasticity through auxin. Plants. 9(8):116. https://doi.org/10.3390/plants9080940.

    • Search Google Scholar
    • Export Citation
  • Li Q, Kubota C. 2009. Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce. Environ Exp Bot. 67:5964. https://doi.org/10.1016/j.envexpbot.2009.06.011.

    • Search Google Scholar
    • Export Citation
  • Lund JB, Blom TJ, Aaslyng JM. 2007. End-of-day lighting with different red/far-red ratios using light-emitting diodes affects plant growth of chrysanthemum × morifolium Ramat. ‘Coral Charm’. HortScience. 42:16091611. https://doi.org/10.21273/HORTSCI.42.7.1609.

    • Search Google Scholar
    • Export Citation
  • Lund JB, Körner O, Aaslyng JM. 2008. Stem elongation of chrysanthemum in response to end-of-day light treatments and photoperiod. Acta Hortic. 766:127135. https://doi.org/10.17660/ActaHortic.2008.766.12.

    • Search Google Scholar
    • Export Citation
  • Mortensen LM, Moe R. 1992. Effects of selective screening of the daylight spectrum and of twilight on plant growth in greenhouse. Acta Hortic. 305:103108. https://doi.org/10.17660/ActaHortic.1992.305.14.

    • Search Google Scholar
    • Export Citation
  • Myster J, Moe R. 1995. Effect of diurnal temperature alternations on plant morphology in some greenhouse crops—a mini review. Scientia Hortic. 62:205215. https://doi.org/10.1016/0304-4238(95)00783-P.

    • Search Google Scholar
    • Export Citation
  • Park Y, Runkle ES. 2017. Far-red radiation promotes growth of seedlings by increasing leaf expansion and whole-plant net assimilation. Environ Exp Bot. 136:4149. https://doi.org/10.1016/j.envexpbot.2016.12.013.

    • Search Google Scholar
    • Export Citation
  • Park Y, Runkle ES. 2018. Far-red radiation and photosynthetic photon flux density independently regulate seedling growth but interactively regulate flowering. Environ Exp Bot. 115:206216. https://doi.org/10.1016/j.envexpbot.2018.06.033.

    • Search Google Scholar
    • Export Citation
  • Patel D, Basu M, Hayes S, Majláth I, Hetherington FM, Tschaplinski TJ, Franklin KA. 2013. Temperature-dependent shade avoidance involves the receptor-like kinase ERECTA. Plant J. 73:980992. https://doi.org/10.1111/tpj.12088.

    • Search Google Scholar
    • Export Citation
  • Percival A, Craver JK. 2023. End-of-day far-red lighting with a low daily light integral increases stem length but does not promote early leaf expansion for Petunia ×hybrida seedlings. HortScience. 58:10101017. https://doi.org/10.21273/HORTSCI17132-23.

    • Search Google Scholar
    • Export Citation
  • Poel BR, Runkle ES. 2017. Seedling growth is similar under supplemental greenhouse lighting from high-pressure sodium lamps or light emitting diodes. HortScience. 52:388394. https://doi.org/10.21273/HORTSCI11356-16.

    • Search Google Scholar
    • Export Citation
  • Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R. 2009. Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis. New Phytol. 182:565588. https://doi.org/10.1111/j.1469-8137.2009.02830.x.

    • Search Google Scholar
    • Export Citation
  • Pramuk LA, Runkle ES. 2005. Photosynthetic daily light integral during the seedling stage influences subsequent growth and flowering of celosia, impatiens, salvia, tagetes, and viola. HortScience. 40:13361339. https://doi.org/10.21273/HORTSCI.40.5.1336.

    • Search Google Scholar
    • Export Citation
  • Qaderi M, Godin VJ, Reid DM. 2015. Single and combined effects of temperature and red:far-red light ratio on evening primrose (Oenthera biennis). Botany. 93(8):475483. https://doi.org/10.1139/cjb-2014-0194.

    • Search Google Scholar
    • Export Citation
  • R Core Team. 2022. R-4.2.2 for macOS. R Foundation for Statistical Computing, Vienna, Austria. https://archive.linux.duke.edu/cran/. [accessed 27 Jul 2023].

  • Romero-Montepaone S, Poodts S, Fischbach P, Sellaro R, Zurbriggen MD, Casal JJ. 2020. Shade avoidance responses become more aggressive in warm environments. Plant Cell Environ. 43(7):16251636. https://doi.org/10.1111/pce.13720.

    • Search Google Scholar
    • Export Citation
  • Romero-Montepaone S, Sellaro R, Esteban Hernando C, Costigliolo-Rojas C, Bianchimano L, Ploschuk EL, Yanovsky MJ, Casal JJ. 2021. Functional convergence of growth responses to shade and warmth in Arabidopsis. New Phytol. 231(5):18901905. https://doi.org/10.1111/nph.17430.

    • Search Google Scholar
    • Export Citation
  • Sellaro R, Pacín M, Casal JJ. 2012. Diurnal dependence of growth response to shade in arabidopsis: Role of hormone, clock, and light signaling. Mol Plant. 5:619628. https://doi.org/10.1093/mp/ssr122.

    • Search Google Scholar
    • Export Citation
  • Slauenwhite KLI, Qaderi MM. 2013. Single and interactive effects of temperature and light quality on four canola cultivars. J Agron Crop Sci. 199:286298. https://doi.org/10.1111/jac.12014.

    • Search Google Scholar
    • Export Citation
  • Smith H, Whitelam GC. 1997. The shade avoidance syndrome: Multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20:840844. https://doi.org/10.1046/j.13653040.1997.d01-104.x.

    • Search Google Scholar
    • Export Citation
  • Thingnaes E, Torre S, Moe R. 2008. The role of phytochrome B, D and E in thermoperiodic responses of Arabidopsis thaliana. Plant Growth Regulat. 56:5359. https://doi.org/10.1007/s10725-008-9283-6.

    • Search Google Scholar
    • Export Citation
  • Westmoreland FM, Kusuma P, Bugbee B. 2023. Elevated UV photon fluxes minimally affected cannabinoid concentration in a high-CBD cultivar. Front Plant Sci. 14:1220585. https://doi.org/10.3389/fpls.2023.1220585.

    • Search Google Scholar
    • Export Citation
  • Wu B, Hitti Y, Macpherson S, Orsat V, Lefsrud MG. 2020. Comparison and perspective of conventional and LED lighting for photobiology and industry applications. Environ Exp Bot. 171:103953. https://doi.org/10.1016/j.envexpbot.2019.103953.

    • Search Google Scholar
    • Export Citation
  • Xiong J, Patil GG, Moe R. 2002. Effect of DIF and end-of-day light quality on stem elongation in Cucumis sativus. Scientia Hortic. 94:219229. https://doi.org/10.1016/S0304-4238(02)00002-X.

    • Search Google Scholar
    • Export Citation
  • Yang Z, Kubota C, Chia P, Kacira M. 2012. Effect of end-of-day far-red light from a movable LED fixture on squash rootstock hypocotyl elongation. Scientia Hortic. 136:8186. https://doi.org/10.1016/j.scienta.2011.12.023.

    • Search Google Scholar
    • Export Citation
  • Zhen S, Bugbee B. 2020a. Far-red photons have equivalent efficiency to traditional photosynthetic photons: Implications for redefining photosynthetically active radiation. Plant Cell Environ. 43:12591272. https://doi.org/10.1111/pce.13730.

    • Search Google Scholar
    • Export Citation
  • Zhen S, Bugbee B. 2020b. Substituting far-red for traditionally defined photosynthetic photons results in equal canopy quantum yield for CO2 fixation and increased photon capture during long-term studies: Implications for re-defining PAR. Front Plant Sci. 11:581156. https://doi.org/10.3389/fpls.2020.581156.

    • Search Google Scholar
    • Export Citation
  • Zhen S, van Iersel M, Bugbee B. 2021. Why far-red photons should be included in the definition of photosynthetic photons and the measurement of horticultural fixture efficacy. Front Plant Sci. 12:693445. https://doi.org/10.3389/fpls.2021.693445.

    • Search Google Scholar
    • Export Citation
  • Zou J, Zhang Y, Zhang Y, Bian Z, Fanourakis D, Yang Q, Li T. 2019. Morphological and physiological properties of indoor cultivated lettuce in response to additional far-red light. Scientia Hortic. 257:108725. https://doi.org/10.1016/j.scienta.2019.108725.

    • Search Google Scholar
    • Export Citation

Supplementary Materials

Anthony C. Percival Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Ave, Fort Collins, CO 80521-1173, USA

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Joshua K. Craver Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Ave, Fort Collins, CO 80521-1173, USA

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Contributor Notes

This work was funded by US Department of Agriculture–National Institute of Food and Agriculture–Specialty Crop Research Initiative Project “Lighting Approaches to Maximize Profits” (Award Number 2018-51181-28365).

We gratefully acknowledge Ben Sharp and Ann Hess for assistance with statistical analysis; Graham Peers and Steve Newman for advisement; Mike Hazlett, David McKinney, Lauren Waters, and Lauryn Schriner for greenhouse and laboratory assistance; and Ball Seed for donation of seeds. The use of trade names in this publication does not imply endorsement by Colorado State University of products named nor criticism of similar ones not mentioned.

J.K.C. is an Assistant Professor.

J.K.C. is the corresponding author. E-mail: Joshua.Craver@colostate.edu.

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  • Fig. 1.

    Total leaf area, average leaf area, and leaf mass per unit area for Petunia ×hybrida ‘Dreams Midnight’ seedlings 21 (A, C, F) and 28 (B, D, E) days post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 hours at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade light treatment for 17.25 hours at 21 °C (SH21). For total leaf area and leaf mass per unit area, means sharing a letter are not statistically different by Tukey’s honestly significant difference test at P ≤ 0.05. For average leaf area, means sharing a letter are not statistically different by the Holm-Bonferroni multiple comparisons method at P ≤ 0.05. Error bars represent 1 standard error of the mean.

  • Fig. 2.

    Stem length and stem dry mass per unit length for Petunia ×hybrida ‘Dreams Midnight’ seedlings 21 (A, C) and 28 (B, D) days post-treatment initiation under a high ratio of red to far-red radiation (R:FR) for 17.25 hours followed by a 1-hour end-of-day white treatment at 21 °C (control; CN) or end-of-day far-red treatment at 21 °C (EOD21); a high R:FR for 17.25 h at 21 °C followed by a 1-hour end-of-day far-red and subsequent dark period at 16 °C (EODDIF), or a low R:FR shade light treatment for 17.25 hours at 21 °C (SH21). Means sharing a letter are not statistically different by the Holm-Bonferroni multiple comparisons method at P ≤ 0.05. Error bars represent 1 standard error of the mean.

 

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