A current review of the modulatory effects of LED lights on

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Review

A current review of the modulatory effects of LED lights on photosynthesis of secondary metabolites and future perspectives of microgreen vegetables Oday Alrifai, Xiuming Hao, Massimo F. Marcone, and Rong Tsao J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.9b00819 • Publication Date (Web): 25 Apr 2019 Downloaded from http://pubs.acs.org on April 25, 2019

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Journal of Agricultural and Food Chemistry

For Graphics TOC only

↑carotenoids ↓phenolics ↑sinigrin

species-dependent modulation of phytochemical synthesis

↑glucosinolates ↑carotenoids ↓chlorophylls ↑flavonoids

1 ACS Paragon Plus Environment


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A current review of the modulatory effects of LED lights on photosynthesis of secondary metabolites and future perspectives of microgreen vegetables

Oday Alrifai†, #, Xiuming Hao‡, Massimo F. Marcone#, Rong Tsao†,*

† Guelph

Research & Development Center, Agriculture and Agri-Food Canada, 93 Stone Road West, Guelph, Ontario, Canada, N1G 5C9

‡ Harrow

Research & Development Center, Agriculture and Agri-Food Canada, 2585 County Road 20, Harrow, Ontario. Canada, N0R 1G0

# Department

of Food Science, Ontario Agricultural College, University of Guelph, Guelph, Ontario, Canada, N1G 2W1

* Corresponding

author: [email protected] (R. Tsao)


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ABSTRACT: Light-emitting diode (LED) lights have recently been applied in controlled

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environment agriculture towards growing vegetables of various assortments including

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microgreens. Spectral qualities of LED light on photosynthesis in microgreens are currently being

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studied for their ease of spectral optimization and high photosynthetic efficiency. This review aims

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to summarize most recent discoveries and advances in specific phytochemical biosyntheses

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modulated by LED and other conventional lighting, to identify research gaps and to provide future

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perspectives in this emerging multi-disciplinary field of research and development. Specific

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emphasis was made on the effect of light spectral qualities on the biosynthesis of phenolics,

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carotenoids and glucosinolates as these phytochemicals are know for their antioxidant, anti-

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inflammatory effects and many health benefits. Future perspectives on enhancing biosynthesis of

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these bioactives using the rapidly progressing LED light technology is further discussed.

12 13

KEYWORDS: light-emitting diodes, ultraviolet light, microgreens, photosynthesis, antioxidants,

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anti-inflammatory, phytochemicals, secondary metabolites

15 16 17 18 19 20 21



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INTRODUCTION

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Plant secondary metabolites are known to play a significant role in delaying or inhibiting oxidative

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damage caused by free radicals. It is the antiradical or antioxidant capability of these compounds

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that are believed to potentially benefit human health through direct reduction of oxidative stresses

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or indirectly modulating activities of antioxidant enzymes.1-2 Recent research has shown the

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importance of dietary antioxidants in modulating inflammation and immune system responses at

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the cellular level, and in animal models and human trials.3 Photosynthetic processes can be

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modified in plants growing under artificial lighting where wavebands, intensities, and

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photoperiods can be controlled.4 Plants have specialized photoreceptors, some of which can be

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pigment-protein complexes for harvesting light energy to drive photosynthesis and others to

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respond to light quality and quantity changes.5 Individual photoreceptors are uniquely encoded by

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individual genes, and photoreceptors of the same family often share a high degree of similarity.6

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Major plant photoreceptors responsible for plant morphology and development are phytochromes

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(PHYA to PHYE), cryptochromes (CRY1 to CRY3), phototropins (PHOT1 and PHOT2), and one

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UV-B resistance locus 8 (UVR8). Phytochromes are responsible for the absorption of red (R)/far-

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red (FR) light controlling plant physiological responses2 and synthesis of phytochemicals (i.e.

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phenolics)7 while cryptochromes for blue (B)/ultraviolet A (UV-A) light are responsible for

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regulating stomatal opening, biomass production and biosynthesis of anthocyanins8, carotenoids9

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and chlorophyll.10 Phototropins are known to mediate phototropic responses and the first to

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modulate stem elongation in response to B light prior to cryptochrome activation.11 Outside the

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visible range of the light spectrum, the UVR8 receptor is a UV-B sensing protein photoreceptor

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regulating growth and development in response to sunlight. Sunlight is integral in reaching the

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surface of the earth and induces a range of physiological responses in plants.12 1 ACS Paragon Plus Environment

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Recent and current studies show the potential of regulating light quality with LED lights to enhance

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cellular metabolism and synthesis of defense-related secondary metabolites (phytochemicals).13

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Recent research has shown the importance of dietary antioxidants in modulating inflammation and

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immune system responses at the cellular level, and in animal models and human trials.3 While

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plants can sense multiple parameters of ambient light signals, quantity, quality, direction and

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duration,14 of importance is the effects of light spectral quality which are not fully understood with

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mixed results reported in microgreens.8, 15 Therefore it is necessary to compile a timely review of

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the available literature on the modulatory effects of LED lights on photosynthesis in microgreens,

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and a few other species of vegetables, to allow for a better understanding of the underlying

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mechanisms of such effects, to develop LED species-specific systems with tailored profiles and to

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identify future direction in this emerging area of research. Abbreviations and acronyms used in

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this review are listed in Table 1.

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FACTORS OF LED LIGHT ON SYNTHESIS OF BIOACTIVE COMPOUNDS

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LED lights have been employed as energy-efficient tools for indoor controlled environment

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agriculture (CEA) and have been the subject of interest for tailored production of important

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bioactive compounds. Over the last few years microgreen vegetables have emerged in the market

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and have been popularized for their higher nutrient densities in their pair of first true leaves

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compared to their mature leaf counterparts.16 However despite the popularity and diversity of

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microgreen vegetables, information on exact phytochemical profiles and how these compounds

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respond to LED lighting is limited. A recent review by Choe et al. discussed the potential health

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benefits of microgreens, however due to the lack of such studies most discussions and conclusions

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were drawn based on data from regular vegetables.17



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With light being a crucial factor in plant growth and development, understanding the modulatory

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effects on biosynthesis of specific defense-related secondary metabolites also become critical.

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Table 2 summarizes current research on the effect of LED light spectral qualities on modulation

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of secondary metabolites and their synthesis in microgreens and other vegetables. LED light

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sources with defined wavelengths and optimized parameters can affect the accumulation of

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bioactive compounds, flavor and pigmentation of vegetables. Spectral light qualities imparted by

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R, B, or RB light as well as their corresponding intensities can variably affect the synthesis of

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bioactive compounds, and the effect also seems to depend on plant species (Figure 1). For these

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reasons studies on microgreens using LED lights are carried out in CEA systems.

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Light Quality. Light quality (spectral quality) has a pronounced effect on accumulating

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plant secondary metabolites in CEA,4,

18-19

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understood and specific effects of LED light regulating gene expression in microgreens are limited.

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It is proposed that photosynthesis can be modulated in plants grown under artificial light and that

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synthesis and accumulation of secondary metabolites are more pronounced under monochromatic

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B or R LED light when compared to conventional white (W) light.8, 20-22 Monochromatic R LED

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light caused elongated hypocotyls and cotyledons in lettuce,23 a phytochrome-dependent process

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that can be adjusted with additional B light.24 Supplementary or increased monochromatic R LED

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light downregulated lutein and β-carotene synthesis in basil25 while B LED light produced larger

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cotyledon area with higher fresh mass in basil microgreens,20 greater anthocyanin content and

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accumulation of carotenoids in lettuce21, 26 and kale sprouts.13 R (650-665 nm) wavebands match

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the absorption peaks of chlorophylls and phytochrome receptors27, therefore R light would be most

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efficient to supplement existing light conditions to aid photosynthesis.4 The combination of R and

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B (RB) LED lights23, 27 were shown to enhance total phenolic content (TPC) in kale28 and total

however mechanisms of such effects are not fully


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carotenoids content (TCC) in lettuce.23 Spectral effects of RB LED light on phenolics and

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carotenoids accumulation are dependent on various factors, with plant species and conditions of

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cultivation being the most important.19-20 RB LED lights are predominately employed for plant

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growth as their wavelengths correspond to absorption by chlorophyll a and b (Figure 1).23 RB

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LED lights enhanced growth and antioxidant activity in red- and green- leaf lettuce over

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monochromatic R LED light by upregulating the gene controlling phenylalanine ammonia-lyase

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(PAL) which lead to enhancing the TPC.18 In this study, lettuce biomass was enhanced under R

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light however abnormal leaf shape, decreased phenolics synthesis and antioxidant activity was

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observed. These findings correspond to other research data that supplementary or increased B LED

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light can enhance TPC and antioxidant activity in lettuce.21 A study showed that 17 days after

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sowing (DAS), B LED light treated lettuce had reddish colored leaves compared to R LED light

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treatment indicating a modulatory effect on anthocyanin biosynthesis by upregulating

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phenylpropanoid enzyme activity. These studies show that monochromatic R, B, and RB LED

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light can modulate the biosynthesis of phytochemicals by regulating key enzymes in vegetable

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plants because of varied absorption of light wavebands by light-harvesting molecules such as

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chlorophylls and phytochromes. Not all plant phytochemical groups or sub-groups have been

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studied on their response towards light during growth. Below are a select group of phytochemical

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compounds whose biosynthesis in different microgreens have been shown to be modulated by

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quality, duration and intensity of LED lights.

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Phenolics (polyphenols). These compounds have at least one aromatic ring and contain

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one or more hydroxyl unit as a functional derivative. As the most common phytochemicals found

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in food plants (Figure 2), phenolics are grouped and classified according to their structural

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features: simple phenols and phenolic acids (including benzoic and cinnamic acids), flavonoids, 4 ACS Paragon Plus Environment


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and others like ellagic acids, lignans and stilbenes. Flavonoids can be further divided into sub-

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groups which include anthocyanins, flavonols, flavanols, flavones and isoflavones. Some

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flavonoids such as flavanols can also exist in polymeric forms.29-30 The benefits of consuming

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phenolics-rich food come from their inherent antioxidant potentials, which has been intensely

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studied in the past two decades, and from more recent findings showing phenolics at

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physiologically relevant concentrations exhibiting immune-regulatory and anti-inflammatory

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activities.3 TPC has been positively correlated to antioxidant activity, which could be considered

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a reason behind the many health benefits of such compounds especially with risk reduction of

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oxidative-stress induced chronic diseases such as cancer, cardiovascular disease and type 2

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diabetes.3, 31-34

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Flavonoids. Flavonoids are the most abundant, widespread and diverse sub-group of

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polyphenols.30, 35 The flavonoid structure containing two aromatic rings connected by a three-

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carbon bridge (C6-C3-C6) is an extended conjugated system that absorbs UV and visiblelight,

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allowing these secondary metabolites to act as protectants against UV radiation in addition to other

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roles as pollinating, pigmentation and chemical defence against diseases.36 Flavonoids exist mainly

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as glycosides in plants and are usually conjugated with glucose or galactose.37 Among the

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flavonoids, flavonols quercetin and kaempferol (including derivatives) are nearly ubiquitous in

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vegetables (Figure 2) and quercetin is the most common and biologically active flavonol in human

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diet.29 Quercetin, kaempferol and isorhamnetin are the main flavonols in Brassica crops and exist

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as O-glycosides.38 UV radiation in open field conditions on green and red loose-leaf lettuce

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(Lactuca sativa) showed overall greater accumulation of flavonol and anthocyanin compounds

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compared to greenhouse cultivation.39 UV-B light irradiation was shown to enhance key secondary

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compounds in the leaves during acclimation, however little research has been conducted on the 5 ACS Paragon Plus Environment

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effects of UV-A and -C light on flavonoid biosynthesis in microgreens. Only a few studies exist

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on the modulatory effects on flavonol synthesis in response to narrow band LED lighting, with

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most reporting an increase in synthesis upon UV exposure40 and under FL lighting.41 Broccoli

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florets grown under 12 h of FL light with supplementary R LED light accumulated higher levels

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of quercetin and kaempferol content compared to supplementary B (460 nm), FR (730 nm), R +

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FR (660+730 nm), or no LED (12 h and 24 h) lights.42 Cyclocarya paliurus, a popularized medical

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tea in China, was grown under 4 LED light treatments: W (445 and 560 nm), B (456 nm), R (653

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nm), and green (G) (514 nm) under constant photosynthetic photon flux density (PPFD) of 800

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µmol m-2s-1.43 Higher total flavonoids content (TFC), specifically kaempferol, isoquercitrin and

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quercetin, were accumulated under B LED light compared to W LED light. A significant

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correlation between leaf flavonoid content and gene expression of key enzymes (PAL, 4-

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coumaroyl CoA-ligase (4CL), and chalcone synthase (CHS)) was found, suggesting LED lights

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may have modulated genes coding these enzymes (Figure 3).43 It is also shown that higher

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expressions of PAL is often reported with higher TFC.44 Understanding the modulatory effect of

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LED lights on genes responsible for coding key enzymes in the biosynthetic pathways, such as the

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isoprenoid or phenylpropanoid pathways, will unquestionably help reveal the mechanisms behind

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the increased or altered levels of phytochemicals and lead to the development of antioxidant-rich

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vegetables solely by the use of LED light. The effect of single-spectral LED wavelengths on

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flavonol accumulation in microgreens in CEA such as vertical farming is also an untapped, but

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important, area of research.

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Research to date indicates that light quality significantly affects the production of secondary

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metabolites especially those with strong antioxidant activities such as phenolics and carotenoids.

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A study looked at the correlation between accumulation of compounds involved in 6 ACS Paragon Plus Environment


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phenylpropanoid synthesis and the corresponding gene expression for the key enzymes under LED

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lighting in buckwheat (F. tataricum) sprouts.45 The sprouts were exposed to R (660 nm), B (450

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nm), and W (380 nm) wavebands. Transcript levels of key phenylpropanoid genes were monitored

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over 10 days with measurements taken every other day following LED treatment. All genes were

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upregulated following 2 days of light exposure, however genetic expression involved in the

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flavonoid pathway varied among the treatments. Under B and W LED light treated sprouts, higher

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expression levels of PAL and flavonoid 3’ hydroxlyase (F3’H) were seen compared to R LED light

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treatment. PAL is a key enzyme in catalyzing the first step of the phenylpropanoid pathway and is

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likely to be responsible for controlling the flux into phenylpropanoid biosynthesis (Figure 3).46

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C4H, CHI, flavone synthase II (FLSII), anthocyanin synthase (ANS) gene expression levels were

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higher under B LED light compared to R and W LED lights. Additionally, W LED light enhanced

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dihydroflavonol 4-reductase (DFR) expression compared to B and R LED light treatments (Figure

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3). Generally, it was shown that higher transcript levels occurred under B and W LED compared

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to R LED.45 A similar phenomenon was observed in Chinese cabbage where B (470 nm) LED

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light was more effective in enhancing phenylpropanoid biosynthesis and transcript levels of F3’H

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and FLS compared to W and R LED light.47 Maximum rutin and cyanidin-3-O-glucoside content

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were observed in sprouts at 4 and 10 DAE to B light, respectively. Therefore, a similar approach

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can be taken for microgreens to induce or enhance phenolics, particularly anthocyanins, by

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supplementing existing conditions with B LED light. In general the combination of RB LED lights

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are found more efficient in enhancing synthesis of phenolic compounds than by monochromatic R

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or B LED light, although can be dependent on other factors particularly plant species.48 In the

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absorption spectrum (Figure 1) this can be attributed to chlorophyll a and b absorbing both R and


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B wavelengths more significantly than others, and their combined effect can modulate different

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pathways for different syntheses.

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Anthocyanins are sub-groups of flavonoids and are pigments of plants that are responsible for red,

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purple and blue colors and are mostly associated with sugars as glycosides, although aglycones

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(anthocyanidins) do exist. Highly acylated anthocyanins with ferulic, coumaric and sinapic acids

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are known to account for superior stability and colors of these pigments.49 These anthocyanins

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have the potential to exhibit strong anti-inflammatory effects that may contribute to enhanced gut

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health and immunity.50 Their primary role in photosynthesis are attributed to their protection of

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plants against excessive light.38 Anthocyanin accumulation is closely related to light which is a

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prerequisite for anthocyanin synthesis, while distinct light spectral qualities modulate its

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synthesis.13 The most common anthocyanidin in Brassica crops is cyanidin, and to a lesser extent

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pelargonidin, delphinidin, peonidin, petunidin and malvidin (Figure 2). Studies have highlighted

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the importance of B light in modulating anthocyanin biosynthesis.8 Delphinidin-3-glucoside was

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highest in lettuce when grown under RB (53:47) and RB (58:42), but not at RB (89:11) LED lights,

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while cyanidin-3- and peonidin-3-glucoside contents remained unchanged.26 On the contrary, high

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pressure sodium (HPS) light with supplementary short-term pulsed R (665 nm) LED light (LED

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photosynthetically active radiation (PAR): 210 μmol m-2 s-1; total PAR 300 μmol m-2 s-1) 3 days

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pre-harvest increased total anthocyanin content in microgreens of broccoli, kale, amaranth, tatsoi,

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parsley, and pea but decreased in mustard, beet, and borage, compared to control (only HPS at 300

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μmol m-2 s-1) suggesting a species dependent response.51 The microgreens showed mild

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photooxidative stress to supplementary high PPFD R LED light. The accumulation of

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anthocyanins seems to be related to chlorophyll synthesis, where chlorophyll contributes some sort

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of reflectance in this spectral region.52 G LED light was shown to decrease B LED light-induced 8 ACS Paragon Plus Environment


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accumulation of anthocyanins, while FR and B LED lights enhanced anthocyanin accumulation

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with increasing intensity in kale, broccoli and beet microgreens.53 A study done on Arabidopsis

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thaliana showed the ability of G light to reverse cryptochrome activation by B light. Generally,

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the results indicate that B light activated CRY1 initiates flavosemiquinone signaling states that can

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be converted to an inactive form by G light.53 Anthocyanin accumulation was also determined by

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germinating under monochromatic B (445 ± 10 nm, 10 μmol m-2 s-1) light for 48 h or with

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supplemented G (582 ± 10 nm, 20 μmol m-2 s-1) light. The addition of G light decreased

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anthocyanin accumulation and formed a long-lived neutral flavin semiquinone intermediate that is

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G light absorbing in addition to B light in vitro.54

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The studies mentioned above and in Table 2 clearly show a modulatory effect on phytochemical

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synthesis by LED light in vegetables and that LED light quality on their synthesis is species-

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specific. Through LED-light induced genetic expression of different photoreceptors, this would

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have a modulatory effect on the molecular pathways related to photosynthesis as well as secondary

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metabolism. Exact mechanisms relating to microgreens are currently unexplored.

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Higher phytochemical concentrations in vegetables e.g. pea,22,

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cabbage28 generally show higher antioxidant activity under monochromatic R or B LED light, as

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well as RB LED versus W LED, fluorescent (FL) and HPS lamps. Light quality affects plant photo-

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oxidative (defense-related) properties by modulating antioxidant defense systems and increasing

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key metabolic enzyme activities.4 Manipulating the light spectrum during plant growth has a

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modulatory effect on antioxidant activity in herbs like parsley and basil microgreens through

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significant improvements in synthesis of key antioxidant compounds by LED lights.25 R LED light

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dose and wavelength photoresponse of antioxidants were studied in basil and parsley herb

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microgreens under 3 different conditions 3 days pre-harvest: 1. monochromatic R (638 and 665

55

tomato,56-57 and Chinese


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nm) lights were studied in combination with basal LED lighting with increasing PPFD; 2. only

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HPS; 3. HPS + R (638).25 Monochromatic R (665 or 638 nm) was greater at enhancing antioxidant

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activity in parsley compared to supplementary or increased R (638 and 665 nm) LED light for

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basil. Supplemental or increased R light significantly increased TPC, α-tocopherol, and ascorbic

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acid, however carotenoid synthesis (mainly lutein and β-carotene) was downregulated in

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comparison to those grown solely by HPS lamps and HPS + R LED light in basil, whereas β-

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carotene and antioxidant activity were increased in parsley. The data shows that photoprotective

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mechanisms are stimulated by both light-dose and wavelength dependent reactions and differences

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in phenolic compositions in basil and parsley are significantly influenced by light quality.25 44

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Monochromatic R LED light was better than monochromatic B LED and RB LED at enhancing

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sinigrin content in kale, whereas RB LED light increased TPC, particularly the flavonoids.28 Kale

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sprouts grown under B (470 nm) LED light showed the highest antioxidant activity and

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anthocyanin content compared to those grown under W (440-660 nm) LED light, followed by

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kale grown under R (660 nm) LED light and dark control.13 Similarly an increase in TPC was

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found in lettuce seedlings grown under similar wavelengths of B (468 nm) LED light compared to

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those grown under white FL or R (660 nm) LED light.21 TPC was highly correlated with

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antioxidant activity. The same study also showed that B light can enhance key antioxidant

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compounds (carotenoids and phenolics) when combined with R light (467 + 655 nm,

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respectively).21 A similar study showed that under 5:1 (R – 638 nm; B – 447 nm; FR – 731 nm)

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LED lights, coriander had significantly higher antioxidant activity compared to those grown under

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100% R LED light.58 Under these conditions, basal R and FR LED light, red pac choi and tatsoi

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microgreens had higher antioxidant activity with higher B light dosage (~75 µmol m-2s-1) in a

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DPPH (2,2-diphenyl-1-picrylhydrazyl) assay.58 This indicates that supplementary B light may be 10 ACS Paragon Plus Environment


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a necessary component to add to existing conditions to stimulate the synthesis of antioxidant

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phenolic compounds via modulation of PAL during flavonoid biosynthesis. 59, 60-62

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Phenolic Acids. Within the group of simple phenolic compounds, phenols like carvacrol and

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thymol (Figure 2) exist in many herbs like oregano and thyme.63 These compounds along with

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phenolic acids (Figure 2) are good antimicrobial agents64-65 as well as strong antioxidant agents.66-

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67

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microgreens showed that synthesis of cinnamic acid (CA) derivatives, particularly caffeic (4-fold

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increase) and rosmarinic acid (15-fold increase), were significantly enhanced under R:B (40:80

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μmol m-2s-1) compared to W LED light.20 Chlorogenic acid (CGA) concentration in lettuce was

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increased 5-fold (60 mg 100 g FW-1) under supplemental RB LED with FL (W) lamps as the main

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light source compared to those grown under no supplemental lighting. R LED light was more

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effective than B LED light at promoting CGA synthesis, which is done via a cryptochrome-

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mediated pathway. It could be that hydroxycinnamoyl CoA quinate hydroxycinnamoyl transferase

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(HQT), hydroxycinnamoyl

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coumarate 3′-hydroxlase (C3H) enzymes were upregulated in response to R light, however

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synthesis of CGA is largely debated and is species-specific (Figure 3).68 The same study also

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showed that increasing light intensity resulted in higher accumulation of CGA, irrespective of R

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or B light.69

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The effects of R, B, and yellow (Y) LED lights were evaluated in pea sprouts and were compared

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to those by FL lamps and darkness on phenolic compound synthesis.55 Six phenolic acids including

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hydroxybenzoic acids (gallic, o-phthalic, p-hydroxbenzoic) and hydroxycinnamic acids (HCAs)

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(CGA, caffeic, p-coumaric, ferulic), three flavonoids (rutin, phloridzin, kaempferol), and

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resveratrol were detected for the first time in pea sprouts. B LED light significantly increased the

A study on LED light modulation of phytochemicals in red leaf basil (Ocimum basilicum)

D-glucose:quinate

hydroxycinnamoyl transferase (HCGQT) or p-


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concentration of all individual phenolic compounds, especially CGA but not phloridizin, which

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was only detected in those grown under Y LED light and in dark conditions.55 B LED light was

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also more effective than R LED light in increasing TPC, TFC, anthocyanin content and antioxidant

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capacity in common buckwheat (Fagoprum esculentum Möench) sprouts.70,

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consistent with data suggesting B LED light is important in stimulating the synthesis of phenolic

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compounds.59-62 Brassica vegetables in particular contain higher contents of HCAs like p-coumaric

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and ferulic acids.38 LED lights clearly impact the genes and enzymes involved in the

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phenylpropanoid pathway. Key enzymes of these pathways known to be regulated by LED lights

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are indicated in Figure 3.

45

These results are

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Carotenoids. Carotenoids are lipophilic tetraterpenoid pigments of plants with distinctive

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yellow, orange and red colors. Carotenoids function as photosensitizers and play important roles

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as scavengers of reactive oxygen species. The highly conjugated double bond system in

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carotenoids makes it possible for these compounds to absorb direct light energy to chlorophylls to

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initiate photosynthesis (Figure 1).71 As light-harvesting pigments in chloroplasts, carotenoids play

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two roles in photosynthesis: collect light to pass on the energy to chlorophylls and photoprotection

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to divert energy from chlorophylls.72 Carotenoids are classified into 2 groups based on their

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structures: carotenes that only contain hydrogen and carbon thus hydrocarbons (ex. β-carotene and

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lycopene), and xanthophylls that contain oxygen atoms additionally (ex. lutein, neoxanthin,

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zeaxanthin, and violaxanthin) (Figure 4).9, 35, 73 Xanthophylls like lutein and zeaxanthin comprise

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the macular pigment of the eye and protect the macula from light-induced degeneration.9 Although

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zeaxanthin is found in minor concentrations, it accompanies lutein in leaf tissues and plays an

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important antioxidant role.74



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Antioxidant activity in mustard, beet, and parsley microgreens were studied under B LED light

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dosage, focusing particularly on the effect on carotenoids and tocopherols accumulation.10

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Carotenoids content (lutein, neoxanthin, violaxanthin, α- and β-carotene) was highest under 33%

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B (447 nm, 300 μmol m-2s-1) LED light compared to those in dark (control) and 8, 16, and 25% B

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LED treatments. On the other hand, α-tocopherol responded better to lower (16%) B light dosage.10

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It could be that carotenoid content is influenced by biochemical transformation of one pigment to

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another, such as violaxanthin into zeaxanthin, in response to increased light intensity (Figure 5).10,

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75-76

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greens have been reported.77-78 Recently, TCC in kale shoots were enhanced under R:B (80:20)

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LED light 15 d prior to harvest compared to 37 d under W LED light treatment.79 Neoxanthin

305

concentrations were highest under R:B (80:20) at 30 d and lowest at 20 d, while β-carotene and

306

lutein contents were enhanced under R:B (95:5) at 37 d. Supplementary G LED light to R and B

307

LED lights also enhanced β-carotene content and lutein/zeaxanthin ratio in mustard microgreens.9,

308

21, 80

309

further into leaf tissue and is absorbed by the chloroplasts in lower leaves in a canopy thereby

310

further increasing photosynthesis to already existing conditions and can be more effective than any

311

supplementary R and B LED lights.81

312

While carotenoids and photosynthesis are closely related, LED light intensity and duration also

313

significantly modulate the accumulation of carotenoids in addition to spectral quality. Carotenoids

314

such as β-carotene and lutein are synthesized via the isoprenoid pathway, and mainly found in

315

leafy plant tissue while lutein is highest in dark leafy green vegetables like kale, collard greens and

316

spinach. A study looked at LED-regulated expression of carotenoid biosynthetic genes and the

317

accumulation of the corresponding carotenoids in Tartary buckwheat (Fagopyrum tataricum

A positive correlation between B LED light treatments and carotenoids accumulation in leafy

Although G light is not as photosynthetically effective as R and B lights, G light can penetrate


Page 17 of 50


318

Gaertn.) sprouts.82 Lutein and β-carotene contents were greatest grown under W LED light (380

319

nm) compared to those under monochromatic B (470 nm) and R (660 nm) LED lights, although

320

all treatments exhibited similar accumulation patterns of carotenoids. Elevated transcription levels

321

of FtPSY, FtLCYB, FtLCYe, FtCHXB, FtCHXE, and FtZEP were higher 8 DAS under W light then

322

B and R lights, but no significant differences in expression levels were found from 2 to 7 DAS.

323

Maximum carotenoid accumulation occurred 10 DAS which could indicate a benefit of W light

324

radiation at certain stages of plant growth to target compounds of interest during photosynthesis.82

325

Genes/enzyme expressions of the carotenoid biosynthesis pathway that were modulated by LED

326

lights are shown in Figure 6.

327

Total carotenoids, and specifically β-carotene content, in tomato was higher under direct sunlight

328

compared to shaded fruits, however lycopene levels fluctuated with temperature changes.83 This

329

could indicate the use of UV light in the biosynthesis of carotenoids, however further research is

330

warranted on the spectral qualities of combined RB LED lights and the response in microgreens

331

for further modifications. Evidence shows that light intensity may also be equally important to

332

light quality in carotenoid biosynthesis (refer below to section 2.2). Understanding these helps

333

identify and prioritize gaps for future research, especially on the influence of specific

334

monochromatic LED lights or combinations of lights on gene expression of phenolics and

335

carotenoid compounds.

336

Glucosinolates. Glucosinolates (GSLs) are hydrophilic, sulfur-containing secondary plant

337

metabolites (Figure 7). Over 130 GSLs are known in various vegetable species and more than 20

338

are predominantly found in Brassica spp.

339

plants, GSLs and their metabolites have long been recognized for their fungicidal,86 nematicidal,87

340

and bacteriocidal88 properties.5 Intense research activities have also stemmed from their potential

84-85

Although having no known primary function in



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341

chemoprotective attributes against cancer.89 GSLs can be categorized into aliphatic, aromatic, and

342

indole types, all of which can yield glucose, sulfate and aglycones by myrosinase (β-glucosidase)

343

during tissue disruption. The aglycones rearrange to give bioactive isothiocyanates, thiocyanates

344

and indoles.85 The most common and naturally occurring isothiocyanate, allyl isothiocyanate

345

(AITC), has been shown to exhibit many desired attributes of an anticarcinogenic and

346

chemoprotective agent.90 Various LED wavebands (730, 640, 535, 440 and 400 nm) have been

347

examined for their effect on sinigrin in kale (B. oleracea L.). Kale plants grown under R

348

wavebands (730 and 640 nm), with the latter showing a more significant effect, were greater than

349

400 to 524 nm wavebands. From the data it is clear that B wavelengths inhibit the synthesis of

350

sinigrin in kale and is likely to be due to the downregulating 2-oxoglutarate-dependent

351

dioxygenase (AOP2) activity converting methylsulfinylalkyl GLSs to the alkenyl form (sinigrin).91

352

The AOP2 gene in A. thaliana controlling the enzyme responsible for this conversion was shown

353

to be highly expressed by light in the photosynthetic parts of the plant and decreases rapidly in its

354

absence (Figure 8).92-93 The mechanism for this observation is not clear and further research is

355

needed to elucidate the effects of irradiance versus wavelength using LED lights.77 In other studies,

356

B LED light shows opposite results in GSL biosynthesis. Short-duration 100% B LED light (41

357

µmol m-2s-1) for 5 days enhanced aliphatic and aromatic (gluconasturtiin) GSL concentrations in

358

broccoli (B. oleacea) microgreens over a mixed lighting of 88% R (627 nm)/12% B (470 nm) LED

359

lights (350 µmol m-2s-1) however the treatments did not differ significantly and neither indole GLS

360

was impacted by the treatments. Interestingly out of four aliphatic GSLs only glucoraphanin and

361

epiprogoitrin responded to B LED light. 36 It is possible that B light only affects methionine and

362

phenylalanine originated GLSs (aliphatic and aromatic, respectively), and not those from


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363

tryptophan (indole GLS). Mechanistic studies of LED light effects on their synthesis should be

364

further examined.

365

Modulation of GSLs synthesis can be species-specific, and is likely also mediated through

366

phototropism which senses B light and controls stomatal activities and membrane transport

367

activities.5 From the limited literature data it appears that LED light quality and intensity may

368

significantly impact the biosynthesis of GSLs and, to a larger extent, GLS profiles are highly

369

dependent on their genotype. For example, a nulling effect of B LED treatment on GSL content

370

was observed in kale baby greens,79, 94 but an enhancing effect on sinigrin was found in broccoli

371

microgreens,95 Chinese cabbage and kale.28 A study looked at the modulatory effects of

372

biosynthetic genes in GLS synthesis under FL light mixed with R (625 nm) and B (455 nm) LED

373

lights in B. rapa (3 Chinese cabbage varieties) seedlings.96 Following seven days of growth,

374

seedlings were cultured for four days under FL and 2 days in the dark and were then treated for 24

375

hrs under three light conditions (FL, FL+ R LED, and FL+ B LED). A variety that is naturally low

376

in GLS content showed an increase in total GLS content under FL+ R as well as other compounds,

377

regardless of light quality. The other variety known for having high GLS content responded to

378

FL+ B by increasing all 6 GLS compounds, particularly gluconapin and progoitrin. It was shown

379

that FL+ R highly expressed three genes of the GLS pathway while FL+B expressed a few others.

380

This demonstrated the differences in GLS biosynthesis, which is highly influenced by sulphate

381

assimilation depending on the amount of daylight.96 Diurnal and light regulation has been shown

382

to influence GLS biosynthesis and sulphur assimilation in Arabidopsis.97

383

Secondary plant metabolism (flavonol glycosides and GLSs) of broccoli plants (B. oleacea) were

384

studied. Broccoli grown under different narrow-bandwidths of LED light (V, B, and G) was

385

compared to those grown under short-wavelength light (UV-A LED), with control being FL light.98 16 ACS Paragon Plus Environment


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With FL light (400 – 700 nm) supplementing all treatments to ensure equal photo flux densities of

387

PAR, the concentration of 3-indolylmethyl (IM) GLS and its methoxylated forms (1-methoxy- and

388

4-methoxy-IM GLS) was increased under UV-A (365 nm) compared to narrow bandwidth

389

lighting. The concentration of 4-hydroxyIM GLS was significantly enhanced with V (420 nm)

390

LED light treatment. Additionally, 5-methylthiobutyl GLS was also enhanced under V light

391

whereas B light enhanced 3-methylsulfinylpropyl and 4-methylsulfinylbutyl. 98 B light treatments

392

were not significant from control, however R background light with specific UV-A or UV-B

393

profiles and V light treatments were shown to enhance GLSs and flavonol glycosides.99 A more

394

recent study using FL broad spectra PAR as basal lighting, supplementary V (420 nm) LED light

395

increased contents of quercetin and kaempferol glycosides in broccoli (B. oleacea var. italica).98

396

This highlights the importance of less utilized wavelengths within this region for further

397

photosynthetic activity. Further studies on the effects of LED light quality and quantity on

398

individual GSLs in different Brassica species and cultivars should help to understand the overall

399

mechanism of action on GSL biosynthesis and regulation.

400

Light Intensity. High intensity light often produces excess heat that must be removed

401

from photosynthetic systems to prevent damage to plants. Antenna pigments like carotenoids

402

absorb light and transfer this energy to chlorophylls, which initiate the sequence of photochemical

403

events of photosynthesis.71 Carotenoids also channel energy away from chlorophylls as a

404

photoprotectant.72 Chlorophyll a and b significantly absorb wavelengths of visible light in the red

405

(maximum at 663 and 642 nm, respectively) and B (maximum at 430 and 453 nm, respectively)

406

region,100 while carotenoid pigments such as lutein and β-carotene absorb primarily in the blue

407

region (maximum at 448 and 450 nm, respectively) (Figure 1)90. Given this, light intensity levels72

408

and other environmental factors such as temperature89 can directly affect the rate of photosynthesis 17 ACS Paragon Plus Environment

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409

and enzymatic activity, thus greatly influence modulation of plant pigments and other compounds

410

such as GSLs in cruciferous vegetables.

411

biosynthesis of GSLs, particularly by LED light, are needed.

Further evaluation of light intensity effects on

412

Carotenoids. Recently, it was shown that biosynthesis of phenolics and carotenoids in five

413

tomato cultivars grown in a greenhouse were influenced by the type of covering materials that can

414

affect light quantity by altering direct and diffusive light transmission.101 High intensity of 440-

415

545 μmol m-2s- was shown to elongate microgreen hypocotyls of kohlrabi (B. oleracea L. var.

416

gongylodes), mustard (B. juncea L.), and tatsoi (B. rapa var. rosularis) while lower intensity (220

417

μmol m-2s-1) inhibited stem elongation. 1, 7 Light intensity has also been shown to directly influence

418

the accumulation of pigments like α- and β- carotene and chlorophyll b by stimulating enzymatic

419

activity in response to light induced stress.77 Brassica microgreens (mustard, red pac choi, and

420

tatsoi) accumulated higher content of carotenoids at 330-440 μmol m-2s-1, but less at 100 μmol m-

421

2s-1

422

and TPC in Orthosiphon stimaneus, a common edible herb,102 indicating a species-specific

423

response of photoinhibition. Kale shoots grown under R LED (640 nm) light at an irradiance of

424

226.5 μmol m-2s-1 led to maximum accumulation of lutein, chlorophyll a and b, and sinigrin.

425

Research insofar has shown that in terms of carotenoid synthesis, light intensity or irradiance has

426

a greater and more significant effect than light quality i.e. LED light of different wavelengths (400,

427

440 and 525 nm). 77 It was shown that under high light stress, Arabidopsis leaves produce bioactive

428

compounds derived from β-carotene oxidation which act as stress responses to remodify genetic

429

expression for cellular defense mechanisms.103 While the combined effects of light quality and

430

intensity on carotenoid synthesis are not yet clear, further studies are warranted to determine

431

whether modulatory effects are a result of wavelength and/or irradiance levels or both.104

and no impact at 545 μmol m-2s-1 PPFD.9 Increasing LED light intensity decreased flavonoid



Page 22 of 50

432

Phenolics. Increasing light intensity also increased TPC, anthocyanin content and

433

antioxidant activity, and oppositely a lower intensity down-regulated their synthesis. Recently ice

434

plants treated under B LED light with low intensity (120 μmol m-2s-1) had higher TPC than high

435

intensity B LED light (150 μmol m-2s-1), and R LED light (with similar intensities), but the

436

antioxidant activity under B light treatment were similar under both intensities. It was shown that

437

B LED light treated plants accumulated a higher content of antioxidant compounds than R LED

438

light treatments which could be explained by their wavelength energies. The shorter B light

439

wavelength has higher photon energy that likely induced photooxidative stress thereby

440

accumulating greater antioxidant phenolics in the ice plant for defense.105

441

Photoperiod. As with light quality and intensity, research is limited on the effects of

442

photoperiod in microgreens. A study evaluating the effects of an 18 h photoperiod on lettuce

443

growth showed higher photosynthetic capacity than shorter photoperiods of 9 and 6 h.106 Similar

444

results were obtained with watercress under a 16 h photoperiod which had at least 50% higher

445

gluconasturtiin concentrations than 8 h under metal halide (W) lighting enriched with R light

446

compared to W light.107 Application of W and incandescent lights under a 14 h photoperiod

447

(totalling 36 h of light treatment during the entire experiment) on mustard (B. juncea L.)

448

microgreens showed altered pigment concentrations. Under this photoperiod regime, lutein was

449

unchanged, chlorophyll a and b and β-carotene content decreased, and zeaxanthin and

450

antheraxanthin contents increased when light intensity increased from 275 to 463 µmol m-2s-1.108

451

The effect of LED light radiation on trolox equivalent antioxidant activity (TEAC, µM) in pea

452

seedlings (Pisum sativum L.) using R (625-630 nm), B (465-470 nm) and W LEDs were studied.22

453

R LED enhanced β-carotene content and TEAC values 96 h after cultivation compared to B and

454

W LED treatments, while B LED light radiation rapidly enhanced chlorophyll synthesis. Short19 ACS Paragon Plus Environment

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455

duration i.e. 2 h photoperiod for 5 days, low intensity (41 μmol m-2s-1) B LED light in broccoli

456

plantlets prior to harvest significantly increased shoot concentrations of β-carotene, violaxanthin,

457

total xanthophyll pigments, glucoraphanin, epiprogoitrin and aliphatic GLSs.100 Sinigrin content

458

in B. oleracea plants under an 18 h photoperiod using FL and incandescent lights were found to

459

be 45% and 25% higher than in stems grown with 12 and 24 h regimes, respectively.109 Results

460

from the studies above suggest a link between photoperiod and photosynthesis, but there is no

461

clear correlation between light duration and accumulation of phytochemicals. It is well known that

462

daily light integral (DLI) represents the accumulated quantity of photosynthetic photon flux

463

emitted by a light source within 24 hours and the product of both PPFD and photoperiod. DLI is

464

shown to be linearly correlated with crop yield and synthesis of phytochemicals. This was

465

demonstrated in a recent study on sweet basil grown under increased DLI. It was found that basil

466

had higher net leaf photosynthetic rate, transpiration rate, and stomatal conductance and was

467

positively correlated with TPC, total anthocyanin and TFC at 12.9, 16.5, or 17.8 mol mL2 dL-1

468

compared with those under lower DLIs of 9.3 and 11.5 mol mL2 dL-1.110

469

ULTRAVIOLET (UV) LIGHT

470

In addition to the visible spectrum of light, UV radiation (~200 – 400 nm) is also involved in the

471

photophysiological processes of plants.111 Exposure to UV can stimulate metabolic responses

472

involved in antioxidant system and photosynthetic pigment production, expression of genes in UV

473

repair and protection, and accumulation of UV-absorbing and defense-related phytochemicals

474

(e.g., carotenoids and GSLs).112-113 Literature data shows many successes of plants cultivated

475

under various supplementary UV lighting that includes combinations with R, B, RB, and FR LEDs,

476

which may have a promising space for cultivating microgreens.



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477

UV radiation is divided into three wavelength ranges which can stimulate various responses in

478

higher plants (Figure 1).114 UV-C (100 – 280 nm) radiation is harmful to living organisms due to

479

tissue permeability and the ability to modify DNA however, in hormic doses, it may stimulate

480

beneficial photophysiological responses. Although considerable literature is available on the use

481

of low dose UV-C LED radiation for post-harvest quality enhancement, 115 116-117 the use for UV-

482

C light to stimulate biosynthesis of phytochemicals during growth are currently not well studied.

483

UV-B (280 – 315 nm) radiation can cause significant damage to vital molecules such as DNA,

484

membranes, and proteins, however hormic doses have been shown to stimulate the accumulation

485

of UV-absorbing pigments like flavonoids in mung bean sprouts118 and phenolics in sweet basil.119

486

UV-A (315 – 395 nm) is considered the least hazardous part of UV.111 A study evaluated the degree

487

of anthocyanin biosynthesis in red turnip under low intensity UV-A light. 120 The study showed

488

increasing expression of PAL, CHS, F3H, DFR and ANS enzyme genes with time over a 24 h

489

photoperiod to UV-A (320-380 nm) (Figure 3). Results also show that co-irradiation of UV-A

490

with R (660 nm) or FR (735 nm) LED did not induce further anthocyanin accumulation.

491

Additionally, R, B (465-475 nm) and RB LEDs and UV-B (280-330nm) irradiation did not express

492

CHS (Figure 3). In comparing the response of B light and UV-B with UV-A, this indicates that

493

anthocyanin biosynthesis had unique genetic expression upon UV-A irradiation by a specialized

494

UV-A photoreceptor and that phytochromes, UV-A/B light and UV-B photoreceptors were not

495

involved, rather a separate regulatory mechanism. 120

496

It is difficult to achieve full synthesis of certain compounds in some species of microgreens in

497

greenhouses due to cover materials blocking some UV light.121-122 Photosynthetically active photo

498

flux (deep R, R, and B LEDs; peak wavelengths of 665, 638, and 447 nm, respectively) with

499

supplementary UV-A (366 nm, 12.4 µmol m-2s-1 PPFD) LED light increased overall TPC and 21 ACS Paragon Plus Environment

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500

antioxidant activity in pac choi, beet and basil microgreens compared to similar treatment but using

501

UV-A (402 nm). 114 Although UV-A increased plant height and hypocotyl length, or had no effect,

502

in all treatments, the modulatory effects by UV-A treatment varied among species and is likely

503

dependent on the wavelength and intensity.

504

Increased intensity of supplemental UV-A LED light showed an 11% increase in anthocyanin

505

concentration in baby leaf lettuce but had no effect on TPC.

506

synthesis and increased TPC in broccoli sprouts.112 Because B light and UV-A wavelengths are

507

close and both depend on cryptochromes, it is likely that UV-A light is involved in phenolics

508

synthesis in a similar manner to B light in microgreens. Research to date is promising in that UV

509

lights do have the potential to modulate photosynthesis in microgreens.

510

SUMMARY AND FUTURE PERSPECTIVES

511

Biosynthesis of antioxidant phytochemicals, as demonstrated in the present review, is influenced

512

by the quality (wavelength) and quantity (intensity, photoperiod) of light. Conventional lights and

513

more modern lighting systems like LED lights exist to supplement the natural light in greenhouse

514

conditions and have been extensively studied on numerous species using various combinations to

515

enhance photosynthesis of bioactive phytochemicals and overall productivity. Microgreens are

516

packed with these antioxidant phytochemicals, and their production is an emerging niche area of

517

high-value novel and functional foods. Microgreens have previously been investigated for their

518

response to traditional lighting sources in controlled, greenhouse, and open-environment settings

519

owing to their increased nutritional value and faster production cycle than their mature

520

counterparts. Additionally, the popularity of consuming microgreens comes from their various

521

flavors, colors and textures that are useful in the culinary industry.123 LED lights can now be

522

custom-designed and controlled to provide desirable wavelengths that can be efficient for the

Different results were found in other studies.

8

UV-A light also triggered GSL



Page 26 of 50

523

synthesis of several antioxidant related compounds in comparison to traditional FL light or HPS

524

lamps.

525

UV LED lights are emerging as supplementary lighting to enhance metabolism and production of

526

important defense-related compounds that can offer further photoprotective responses and the

527

potential for enhancing accumulation of bioactive compounds in other species or varieties. Little

528

research is carried in studying the modulatory roles of UV-A LED light on photosynthesis of

529

important defense-related compounds in microgreens when used with basal LED lighting. Because

530

of B light and UV-A wavelength being close to one another on the spectrum and both depend on

531

cryptochromes, it can be hypothesised that UV-A LED light modulates phenolics synthesis in a

532

similar manner to B light in microgreens. Additionally, considerable literature is available on the

533

use of low dose UV-C LED radiation for post-harvest quality enhancement, however their use in

534

photosynthesis is limited and not well understood. Therefore, future research should examine UV

535

LED wavelengths to further modulate and promote photosynthesis.

536

It is also important to note that W, Y, G and O wavelengths lay in the PAR range and those outside

537

the PAR range (UV and FR wavelengths) (Figure 1) are not as efficiently matched with the

538

chlorophyll absorption peaks and rarely employed for photosynthesis studies in most cases.

539

However, recent research has shown that these lights may modulated metabolic and physiological

540

processes in vegetables by regulating gene and enzyme expressions of the biosynthetic pathways

541

(Figures 3, 6 and 8). More research is therefore needed to better understand the mechanisms of

542

such regulatory effects. To date, studies on LED-induced gene expression mainly use

543

monochromatic B, R, and W light or in combination. With the genetic expression of various

544

photoreceptors simultaneously being activated by LED light, this would have a modulatory effect

545

on the molecular pathways related to photosynthesis, resulting in up- or down-regulated enzyme 23 ACS Paragon Plus Environment

Page 27 of 50


546

activities and synthesis of secondary metabolites. Such studies on microgreens are particularly

547

important as currently they are largely unexplored.

548

Future research should also investigate supplementary G LED light with basal R and B lighting.

549

This demonstrates the potential usefulness of these LEDs for photosynthesis to further modulate

550

secondary metabolism right below and close to the B light spectrum. Although not as strongly

551

absorbed by chlorophylls, G light can penetrate further into leaf tissue and is absorbed by the

552

chloroplasts in lower leaves in a canopy which can increase photosynthesis to already existing

553

conditions. Additionally, flavonoid synthesis in response to narrow band LED lighting warrants

554

closer investigation as thus far most research has been related to the use of UV and FL lighting.

555

Further research into the modulatory effect of LED lighting on the genes responsible for coding

556

key enzymes in biosynthetic pathways, such as the isoprenoid or phenylpropanoid pathways, will

557

accelerate the development of microgreens as functional foods.

558

Existing literature also points to the need in more in-depth studies on the effects of LED light

559

quality and quantity on photosynthetic pathways of GSLs and carotenoids in microgreens

560

particularly in different Brassica species and cultivars.

561

As the demand for production and wider selection of microgreens increases, more efforts are called

562

for research into the effects of light quality on the synthesis of secondary metabolites in response

563

to LED and UV lighting as well as ideal combinations of lights, not only in frequently grown

564

microgreens, but in new and emerging varieties. Current available data shows that LED lighting

565

systems have tremendous capabilities of regulating genes involved in metabolic pathways, defense

566

systems and photoreceptors. Thus far, predominant species belonging to the families of

567

Brassicaceae,

568

Amaranthceae and Cucurbitaceae are the most explored for their phytochemical profiles and ease

Asteraceae,

Chenopodiaceae,

Lamiaceae,

Apiaceae,

Amarillydaceae,



Page 28 of 50

569

of growing as microgreens.124 Extensively studied vegetables like leafy greens (e.g. lettuce and

570

kale) appear in many research papers however spinach, radish and collards, for example, have

571

rarely been investigated for their responses to LED light. New and emerging microgreens like

572

alfalfa, celosia, chichory, dill, purslane, shiso, and aromatic herbs like fennel, borage, arugula,

573

anise and ornamental herbs such as dark opal basil (purple basil varieties) and certain varieties of

574

sage have not yet been explored. Understanding the modulatory role of LEDs on molecular genetic

575

control will surely lead to the development of species-specific lighting systems to enhance all-

576

around productivity and to enhance important antioxidant compounds that could be beneficial. The

577

field of metabolomics and proteomics could offer information on plant genetic pre-disposition and

578

the influence from the external environment such as by LED lighting on how genetic functions

579

can manipulate and/or modulate plant metabolism. Genomics, proteomics and metabolomics could

580

be tremendously helpful tools to identify large global sets of data and their corresponding pathways

581

to improve the production and nutritional quality of microgreens. Success in this field will also

582

largely depend on how to take advantage of the rapidly developing LED technology, and on

583

collective efforts from the industry and researchers in food bioactives chemistry, biochemistry and

584

human nutrition to enhance the production of secondary metabolites and to ultimately reduce the

585

prevalence of chronic disease.

586

ACKNOWLEDGMENTS

587

This study was supported by the A-base funds of Agriculture & Agri-Food Canada (AAFC) (#J-

588

001322.001.04 ; #J-001328.001.04)


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105. Kim, Y. J.; Kim, H. M.; Kim, H. M.; Jeong, B. R.; Lee, H.-J.; Kim, H.-J.; Hwang, S. J., Ice plant growth and phytochemical concentrations are affected by light quality and intensity of monochromatic lightemitting diodes. Horticulture, Environment, and Biotechnology 2018, 59 (4), 529-536. 106. Kang, J. H.; KrishnaKumar, S.; Atulba, S. L. S.; Jeong, B. R.; Hwang, S. J., Light intensity and photoperiod influence the growth and development of hydroponically grown leaf lettuce in a closedtype plant factory system. Horticulture Environment and Biotechnology 2013, 54 (6), 501-509. 107. Engelen-Eigles, G.; Holden, G.; Cohen, J. D.; Gardner, G., The effect of temperature, photoperiod, and light quality on gluconasturtiin concentration in watercress (Nasturtium officinale R. Br.). Journal of Agricultural and Food Chemistry 2006, 54 (2), 328-334. 108. Kopsell, D. A.; Pantanizopoulos, N. I.; Sams, C. E.; Kopsell, D. E., Shoot tissue pigment levels increase in 'Florida Broadleaf' mustard (Brassica juncea L.) microgreens following high light treatment. Scientia Horticulturae 2012, 140, 96-99. 109. Charron, C. S.; Sams, C. E., Glucosinolate Content and Myrosinase Activity in Rapid-cycling Brassica oleracea Grown in a Controlled Environment. Journal of the American Society for Horticultural Science 2004, 129 (3), 321-330. 110. Dou, H.; Niu, G.; Gu, M.; Masabni, J. G., Responses of sweet basil to different daily light integrals in photosynthesis, morphology, yield, and nutritional quality. HortScience 2018, 53 (4), 496-503. 111. Vaštakaitė, V. V., A.; Brazaitytė, A.; Samuolienė, G.; Jankauskienė, J.; Sirtautas, R.; Duchovskis, P. In The effect of UV-A supplemental lighting on antioxidant properties of Ocimum basilicum L. microgreens in greenhouse., Proceedings of the 7th International Scientific Conference Rural Development 2015, Lithuania, 19-20 November; Lithuania. 112. Moreira-Rodriguez, M.; Nair, V.; Benavides, J.; Cisneros-Zevallos, L.; Jacobo-Velazquez, D. A., UVA, UVB Light Doses and Harvesting Time Differentially Tailor Glucosinolate and Phenolic Profiles in Broccoli Sprouts. Molecules 2017, 22 (7). 113. Moreira-Rodríguez, M.; Nair, V.; Benavides, J.; Cisneros-Zevallos, L.; Jacobo-Velazquez, D. A., UVA, UVB Light, and Methyl Jasmonate, Alone or Combined, Redirect the Biosynthesis of Glucosinolates, Phenolics, Carotenoids, and Chlorophylls in Broccoli Sprouts. International Journal of Molecular Sciences 2017, 18 (11), 2330. 114. Brazaitytė, A.; Viršilė, A.; Jankauskienė, J.; Sakalauskienė, S.; Samuolienė, G.; Sirtautas, R.; Novičkovas, A.; Dabašinskas, L.; Miliauskienė, J.; Vaštakaitė, V.; Bagdonavičienė, A.; Duchovskis, P., Effect of supplemental UV-A irradiation in solid-state lighting on the growth and phytochemical content of microgreens. In International Agrophysics, 2015; Vol. 29, p 13. 115. Wu, J.; Liu, W.; Yuan, L.; Guan, W. Q.; Brennan, C. S.; Zhang, Y. Y.; Zhang, J.; Wang, Z. D., The influence of postharvest UV-C treatment on anthocyanin biosynthesis in fresh-cut red cabbage. Sci Rep 2017, 7 (1), 5232. 116. Crupi, P.; Pichierri, A.; Basile, T.; Antonacci, D., Postharvest stilbenes and flavonoids enrichment of table grape cv Redglobe (Vitis vinifera L.) as affected by interactive UV-C exposure and storage conditions. Food Chemistry 2013, 141 (2), 802-808. 117. Maharaj, R., Effects of Abiotic Stress (UV-C) Induced Activation of Phytochemicals on the Postharvest Quality of Horticultural Crops. IntechOpen: 2015. 118. Wang, H.; Gui, M.; Tian, X.; Xin, X.; Wang, T.; li, J., Effects of UV-B on vitamin C, phenolics, flavonoids and their related enzyme activities in mung bean sprouts (Vigna radiata). International Journal of Food Science & Technology 2017, 52 (3), 827-833. 119. Mosadegh, H.; Trivellini, A.; Ferrante, A.; Lucchesini, M.; Vernieri, P.; Mensuali, A., Applications of UV-B lighting to enhance phenolic accumulation of sweet basil. Scientia Horticulturae 2018, 229, 107116.



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120. Zhou, B.; Li, Y.; Xu, Z.; Yan, H.; Homma, S.; Kawabata, S., Ultraviolet A-specific induction of anthocyanin biosynthesis in the swollen hypocotyls of turnip (Brassica rapa). Journal of Experimental Botany 2007, 58 (7), 1771-1781. 121. Dannehl, D.; Schmidt, U.; Rocksch, T., Light transmission (PAR, UVA and UVB) of different greenhouse glass materials and effects on physiological and morphological parameters of ornamental plants. 2008. 122. Baeza, E.; López, J. C. In LIGHT TRANSMISSION THROUGH GREENHOUSE COVERS, International Society for Horticultural Science (ISHS), Leuven, Belgium: 2012; pp 425-440. 123. Mir, S. A.; Shah, M. A.; Mir, M. M., Microgreens: Production, shelf life, and bioactive components. Critical Reviews in Food Science and Nutrition 2017, 57 (12), 2730. 124. Rouphael, Y.; Kyriacou, M. C.; Petropoulos, S. A.; De Pascale, S.; Colla, G., Improving vegetable quality in controlled environments. Scientia Horticulturae 2018, 234, 275-289.

Note The authors declare no competing financial interest.


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Figure captions

Figure 1. The electromagnetic spectrum of ultraviolet (UV) and visible lights, and absorption wavelengths of selected phytochemicals with antioxidant activity.

Figure 2. Common phenolic compounds (simple phenols, phenolic acids, and flavonoids) whose biosynthesis in microgreen vegetables are modulated by LED lighting.

Figure 3. The modulatory effects of white (W), blue (B), and red (R) LED (light emitting diode) lights on key enzymes of phenylpropanoid pathway. Colored figures (lightening bolts) represent the LED light treatment imparted by W, R and B lights and the corresponding synthesis of the listed antioxidant compounds. All enzymes with a colored figure were upregulated by the LED lights. PAL – phenylalanine ammonia-lyase; C4H – cinnamate-4-hydroxlase; 4C:CoA-L – 4coumaroyl:CoA-ligase; CHS – chalcone synthase; CHI – chalcone isomerase; F3H – flavanone3-hydroxlase; F3’H – flavanoid-3-hydroxlase; F3’5’H – flavanoid-3’5’-hydroxlase; FSII – flavone synthase II; DFR – dihydroflavonol 4-reductase; ANS – anthocyanidin synthase; LAR – leucocyanidin reductase. Data and information were collected from Thwe et al. (2014)

45

and

Chang et al. (2009)46

Figure 4. Common carotenoid compounds found in microgreen vegetables that can be modulated by LED light.

Figure 5. Reversible conversion of violaxanthin to zeaxanthin via antheraxanthin in response to light conditions. These reactions, under low (addition of epoxy group) or high light (removal of 8 ACS Paragon Plus Environment


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epoxy group) are catalyzed by two separate enzymes (zeaxanthin epoxidase and violaxanthin deepoxidase) located on opposite sides of the thylakoid membrane in the cell. Information were collected and redesigned from Jahns et al. (2009).76

Figure 6. Carotenoid biosynthetic pathway and the modulatory effects of white (W), blue (B), and red (R) LED lights on enzymes in Tartary buckwheat (Fagopyrum tataricum Gaertn.) sprouts. Size of colored figures represent LED lights and the magnitude of modulation with respect to each other, with highest imparted by W followed by R and B LED lights. Enzymes with arrows represent upregulated activity and synthesis of these antioxidant compounds. Carotenoid biosynthetic pathway in plants. I-PP - isopentenyl diphosphate; D-PP – dimethylallyl pyrophosphate; GGPP - geranylgeranyl diphosphate; GGPS – geranylgeranyl pyrophosphate synthase; PSY - phytoene synthase; LCYB - lycopene β-cyclase; LCYE - lycopene ε-cyclase; CHXB - β-ring carotene hydroxylase; CHXE - ε-ring carotene hydroxylase; ZEP - zeaxanthin epoxidase. Data and information were collected from Tuan et al. (2013).82

Figure 7. Common glucosinolate (GLS) compounds whose biosynthesis in microgreens are modulated by LED lighting.

Figure 8. The modulatory role of B LED light in kale plants is shown by downregulating 2oxoglutarate-dependent dioxygenase (AOP2) activity and inhibiting the formation of alkenyl (3butenyl) glucosinolate (GLS),


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Table 1. A list of abbreviations and acronyms used in the review.

Abbreviation/ acronym LED R RB B G

light-emitting diode Red Red/Blue Blue Green

Abbreviation/ac ronym CHS F3’H ANS FLS DFR

Y V

Yellow Violet

HPS PAR

O

Orange

PPFD

W UV FR

White ultraviolet far-red

FL CGA HQT

CEA

controlled environment agriculture

HCGQT

TPC

total phenolics content total carotenoids content days after sowing phenylalanine ammonia-lyase total flavonoids content 4-coumaroyl CoAligase

C3H

chalcone synthase flavonoid 3’ hydroxylase anthocyanin synthase flavone synthase dihydroflavonol 4reductase high-pressure sodium photosynthetically active radiation photosynthetic photon flux density fluorescent chlorogenic acid hydroxycinnamoyl CoA quinate hydroxycinnamoyl transferase hydroxycinnamoyl Dglucose:quinate hydroxycinnamoyl transferase p-coumarate 3′-hydroxlase

HCA

hydroxycinnamic acid

AITC AOP2 IM

allyl isothiocyanate 2-oxoglutarate-dependent dioxygenase indolylmethyl

DLI

daily light integral

TCC DAS PAL TFC 4CL

definition

definition



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Table 2. Modulatory effects of different LED lights on biosynthesis of phytochemicals in vegetables, including microgreens.

Species

LED light

λ (nm)

Amaranth

R

638

Arugula

*(HPS) + B B-violet

(max. 660) + 450 420 and 440

UV-A

390

Basil

AA, total anthocyanins ↓ total phenolics

1R:2B N/A 2R:1B R

638

R

638

*(B, R, FR) + UV-A

(447, 638, 731) + +366 +390

*(HPS) + B

B-violet *(HPS) + enhanced B

modulation

(max. 660) + 450

420 and 440

51

59

isorhamnetin-diglycoside, luteolin-glycoside derivatives, apigenin derivatives AA total anthocyanins, AA flavonols

111

phenolic acids, anthocyanins, flavonoids flavonoids total phenolics ↓ AA total phenolics, AA ↓ β-carotene, ↓ lutein

20

51

25

114

total phenolics, α-tocopherol ↓ total anthocyanins, ↓ AA ↓ total anthocyanins phenolic acids (chlorogenic derivatives, chicoric, hydroxcinnamic) phenolic acids (chicoric, hydroxycinnamic) 36 d chicoric acid

59

60

400-500 48 d

Beet

ref

R

638

*(B, R, FR) + UV-A

(447, 638, 731) +366

*(R, R, FR) + 16% B

+390 +402 (638, 660, 731) + 447

0% B

447

quercetin rhamnoside

total phenolics ↓ total anthocyanins

51

114

flavonols, total anthocyanins, αtocopherol total anthocyanins total phenolics 10

total tocopherol, lutein, neoxanthin, violaxanthin, βcarotene total tocopherol


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Kale

Broccoli

B R W

470 660 440-660

anthocyanins, total phenolics, GSLs GSLs

13

R R/B

N/A

GSLs polyphenols, flavonoids

28

R

638

AA, total anthocyanins, total phenolics

51

B

470

total carotenoids, β-carotene, total xanthophyll cycle pigments, GSLs

100

4R/1B

622-632/442-452

total carotenoids, β-carotene, total GSLs, aliphatic and indole GSLs

R

638

Cabbage Coriander Mizuna

R R/B R84:FR7:B9

Parsley

R

N/A 661/449 total flux : 400800 nm 638

R

665 or 638

*(R, R, FR) + 16% B

(638, 660, 731) + 447

0% B R

447 638

R87:B13 R84:FR7:B9 R74:G18:B8 R

total flux : 400800 nm

*(B, R, R, FR) + G Y O *(R, R, FR) + 16% B

(447, 638, 665, 731) + 520 595 622 (638, 660, 731) + 447

Royal B B C Y R R87:B13

455 470 505 590 627 total flux: 400800 nm

Pea Kohlrabi Mustard

R84:FR7:B9

638

95

AA, total anthocyanins, total phenolics GSLs total antioxidants α-carotene, ↓ total carotenoids^

51

AA, total anthocyanins, total phenolics total phenolics, AA

51

28 48

25

10

total tocopherol, lutein, neoxanthin, violaxanthin total tocopherol AA, total anthocyanins, total phenolics total anthocyanins total anthocyanins, total phenolics ↓ total anthocyanins^ AA, total phenolics, ↓ total anthocyanins

51

104

51

114

α/β-carotene lutein/zeaxanthin total carotenoids total carotenoids tocopherol, lutein, neoxanthin, violaxanthin, zeaxanthin

10

61

total phenolics ↓ total carotenoids, ↓ β-carotene^, anthocyanins, ↓ lutein^, ZA/ZAV^, α-carotene

104

↓ total carotenoids, ↓ β-carotene^, ↓ lutein^



R74:G18:B8 Pac choi

Orach Tatsoi

Borage Lettuce

↓ total carotenoids^, α-carotene

*(B, R, R, FR) +

(447, 638, 665, 731) +

G Y O

520 595 622

*(B, R, FR) + UV-A

(447, 638, 731) + 366 390 455

Royal B R R *(B, R, R, FR) +

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114

violaxanthin and neoxanthin ↓ neoxanthin ↓ β-carotene, ↓ violaxanthin ↓ lutein

Y O

638 638 (447, 638, 665, 731) + 595 622

Royal B B C R R

455 470 505 627 638

B R/B

114

total phenolics, flavonols, αtocopherol, total anthocyanins xtotal phenolics total phenolics total phenolics, total anthocyanins

61

51 51 114

total carotenoids, violaxanthin ↓ α/β-carotene ↓ total carotenoids 61 xALL:

total phenolics 51

454 659/454

total phenolics ↓ AA, ↓ total anthocyanins anthocyanins carotenoids

B UV-A B R B 70R:30B W

470 373 476 658 460-475 650-665 380-760

carotenoids, total polyphenolics anthocyanins anthocyanins, carotenoids phenolics AA total phenolics total phenolics

21

*(HPS) + enhanced B

400-500

36 d

62

8

23

protocatechuic acid, chicoric acid, quercetin rhamnoside 60

48 d

quercetin-malonyl diglucoside, quercetin 3malonylglucoside

B – blue; R – red; W – white; O – orange; G – green; FR – far-red; C – cyan; HPS – highpressure sodium (light); *basal lighting; ^increasing intensity, xpulsed-light; AA – ascorbic acid; ZA/ZAV = zeaxanthin + antheraxanthin/zeaxanthin + antheraxanthin + violaxanthin; d: days


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Figure 1



Page 44 of 50

Figure 2

O

R1

R1

R5

R2

R4

O OR5

OH

R2O

R3 benzoic acids

R3 cinnamic acids

vanillic R1=R4=H, R2=R5=OH, R3=OCH3; syringic R2=R5=OH, R1=R3=OCH3, R4=H; gallic R1=R2=R3=R5=OH, R4=H; protocatechuic R2=R5=R3=OH, R1=R4=H; p-hydroxybenzoic R2=R5=OH, R1=R3=R4=H;

carvacrol p-coumaric R1=R2=R3=R5=H; f erulic R1=R2=R5=H, R3=OCH3; rosmarinic R1=R2=R3=H, R5=caf f eic acid; caf f eic R1=R2=R5=H, R3=OH; chicoric R1=OH, R3=R2=H, R5=tartaric acid; chlorogenic R1=R2=H, R3=H, R5=(-)-quinic acid

OH thymol

OH HO

O OH O

R3

R1 OR2

flavonols

kaempf erol R1=R2=H; HO querctin R1=OH, R2=H; isoquercetin R1=OH, R2=glucose; rutin R1=OH, R2=rutinose; isorhamnetin R1=OCH3, R2=H

O+

OH R5

OH OH anthocyanidins

cyanidin R3=OH, R5=H; delphinidin R3=R5=OH; peonidin R3=OCH3. R5=H; petunidin R3=OH, R5=OCH3; pelargonidin R3=R5=H; malvidin R3=R5=OCH3


Page 45 of 50


Figure 3 O

O OH

PAL

O C4H

OH

OH

NH2

HO trans-cinnamic acid

phenylalanine

HO

OH

F3H OH HO

HO

OH

p-coumaroylCoA

naringenin chalcone

naringenin

DFR

SCoA

CHS

CHI

O

OH O

O

OH O

OH HO

4C:CoA-L p-coumaric acid

OH

OH HO

O

F3'H OH

O

OH HO

F3'5'H

OH O

OH OH O

dihydrokaempferol

OH OH

O

dihydroquercetin

DFR

apiforol OH

OH OH HO

O

LAR

HO

OH HO

OH OH leucocyanidin

catechin

OH

O OH

OH OH

FSII

OH

O OH OH O quercetin

ANS OH OH HO

O OH OH cyanidin



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Figure 4 xanthophylls OH lutein

HO OH zeaxanthin

HO

ß-cryptoxanthin

HO

neoxanthin

C O

HO OH

HO

O violaxanthin

HO

OH

O OH

antheraxanthin

HO

O

carotenes lycopene

ß-carotene


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Figure 5

violaxanthin de-epoxidase

O HO

OH

O violaxanthin

pH

A current review of the modulatory effects of LED lights on

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