Received: 6 March 2021 Revised: 22 June 2021 Accepted: 25 June 2021

DOI: 10.1111/pce.14142

REVIEW

Pest and disease management by red light

Agnes Gallé1 | Zalán Czékus1
th2,3
| Liliána To
Galgo
| Lászlo
czy2,3 |
r1
Péter Poo

1
Department of Plant Biology, University of
Szeged, Szeged, Hungary Abstract
2
Department of Biotechnology, University of Light is essential for plant life. It provides a source of energy through photosynthe-
Szeged, Szeged, Hungary
sis and regulates plant growth and development and other cellular processes, such
3
Institute of Plant Biology, Biological Research
Centre, Eötvös Loránd Research Network, as by controlling the endogenous circadian clock. Light intensity, quality, duration
Szeged, Hungary and timing are all important determinants of plant responses, especially to biotic

Correspondence stress. Red light can positively influence plant defence mechanisms against differ-
Péter Poo
r, Department of Plant Biology, ent pathogens, but the molecular mechanism behind this phenomenon is not fully
University of Szeged, H-6726 Szeged, Közép
fasor 52, Hungary. understood. Therefore, we reviewed the impact of red light on plant biotic stress
Email: [email protected] responses against viruses, bacteria, fungi and nematodes, with a focus on the physi-

Funding information ological effects of red light treatment and hormonal crosstalk under biotic stress in
Magyar Tudományos Akadémia, Grant/Award plants. We found evidence suggesting that exposing plants to red light increases
Number: János Bolyai Research Scholarship;
Ministry for Innovation and Technology, levels of salicylic acid (SA) and induces SA signalling mediating the production of
Grant/Award Number: ÚNKP-20-5 - New reactive oxygen species, with substantial differences between species and plant
National Excellence Program; Nemzeti Kutatási
Fejlesztési és Innováci
os Hivatal, Grant/Award organs. Such changes in SA levels could be vital for plants to survive infections.
Numbers: FK 124871, FK 134343, PD Therefore, the application of red light provides a multidimensional aspect to devel-
134284; Szegedi Tudományegyetem, Grant/
Award Number: Open Access Fund (5376) oping innovative and environmentally friendly approaches to plant and crop disease
management.

KEYWORDS
LED, light, pathogens, phytochrome, reactive oxygen species, resistance, salicylic acid

1 | I N T RO DU CT I O N sustainable plant and crop protection strategies to elevate food pro-

pez-Calcagno, &
duction (Roberts & Mattoo, 2018, 2019; Simkin, Lo
Rapid human population growth is increasing the pressure on agricul- Raines, 2019). The key to overcoming these problems is the develop-
ture for increased crop production (Foley et al., 2011; Godfray ment of environmentally friendly and high-yielding approaches with
et al., 2010). The use of irrigation, synthetic fertilizers, supplemental fewer adverse effects on the environment.
lighting and pesticides in greenhouses are beneficial to increasing crop Light is a dynamic component of the terrestrial environment, and
yields (Damalas & Eleftherohorinos, 2011; Roberts & Mattoo, 2018). it plays a pivotal role in regulating plant life, such as optimal plant
However, increases in agricultural production lead to increased cli- growth and development, as well as different defence responses
mate change and have negative impacts on biodiversity, soil and the against pathogens (Hua, 2013). Light has both quantitative and quali-
availability and quality of freshwater (Palm, Blanco-Canqui, DeClerck, tative features, and plants, as well as microorganisms, are able to
Gatere, & Grace, 2014; Power, 2010). These effects of the agricultural sense light using various photoreceptors (Folta & Carvalho, 2015).
sector and the high costs of crop production have resulted in signifi- Light-induced signal transduction pathways, the circadian clock and
cant scientific and social debates around the development of new and photosynthetic activity mediate the molecular, biochemical and

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2021 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.

Plant Cell Environ. 2021;44:3197–3210. wileyonlinelibrary.com/journal/pce 3197

3198
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physiological responses of both plants and microorganisms different metabolic pathways in plant–pathogen interactions
(Ballaré, 2014; Chen, Chory, & Fankhauser, 2004; Fernández- (Purschwitz, Müller, Kastner, & Fischer, 2006; Thind & Schilder, 2018;
Milmanda et al., 2020; Kazan & Manners, 2011; Roberts & Tisch & Schmoll, 2010; van der Horst, Key, & Hellingwerf, 2007). In
Paul, 2006). The presence or absence, period, quality, intensity and contrast to optimal light conditions, high and low light intensity,
timing of available light can alter and influence plant responses including darkness, induce different signalling and regulation path-
and metabolism to various stress effects, as well as the composition, ways modulated by phytohormones, especially jasmonic acid (JA) and
habits and lifestyle of microorganisms in the phyllosphere (Carvalho & salicylic acid (SA) (Ballaré, 2014; Deepika, Sagar, & Singh, 2020; Rob-
Castillo, 2018). Therefore, artificial manipulation of light characteris- erts & Paul, 2006).
tics during cultivation can influence crop production and trigger plant Light is interpreted as an informational signal by photoreceptors,
defence mechanisms against pathogens. which absorb photons via a specific prosthetic chromophore and
This review aims to summarize available knowledge on red light- induce structural changes in the protein part of the receptor (Folta &
regulated plant defence mechanisms, especially focusing on the role Carvalho, 2015). There are various photoreceptors in plants: red/far-
of phytohormones in these processes. This knowledge could contrib- red-light-sensing phytochromes (phyA–phyE), blue-light-sensing
ute to the development of new strategies for plant protection and cryptochromes (cry1-3) and phototropins (phot1 and phot2), Zeitlupe
crop science. family members (ZTL, FKF1 and LKP2) and UV-B receptor UVR8
(Demarsy, Goldschmidt-Clermont, & Ulm, 2018; Paik & Huq, 2019)
(Figure 1).
2 | L I G H T SE N S I N G A N D P L A N T The analysis of Arabidopsis thaliana photoreceptor mutants
RESPONSES showed that phyB is the primary photoreceptor for red light percep-
tion and inhibits hypocotyl growth, whereas phyA senses far-red light
Light is electromagnetic radiation from the sun. White light is a mix- and induces hypocotyl growth and shade avoidance. PhyA and phyB,
ture of the colours of the visible spectrum, which ranges from 400 to which are a unique type of photoreceptors, are synthesized in the
700 nm: violet (400 nm), indigo (445 nm), blue (475 nm), green cytosol in an inactive form and they are transported within minutes
(510 nm), yellow (570 nm), orange (590 nm) and red (650 nm). Infra- into the nucleus after the activation by red light (Sheerin et al., 2015;
red radiation has a longer wavelength than visible red light, and ultra- Yamaguchi, Nakamura, Mochizuki, Kay, & Nagatani, 1999). Red light
violet (UV) radiation has a shorter wavelength than visible violet light absorption results in a photoreversible conformational change from
(Thind & Schilder, 2018). the inactive cytosol-localized red-light-absorbing form (Pr) to the
Light is as essential as an energy source and environmental signal active far-red-light-absorbing form (Pfr), which induces phy-mediated
for plants. It regulates a wide range of developmental processes, physiological responses through the transcriptional regulation of
including germination, de-etiolation, stomatal development, circadian numerous genes (Nagatani, 2004; Su et al., 2017).
rhythm and flowering (de Wit, Galv~
ao, & Fankhauser, 2016). Further- Activated phytochromes induce a network of downstream pro-
more, it can influence growth and developmental processes, including cesses. They mediate the phosphorylation and degradation of

F I G U R E 1 Plant photoreceptors
and their role in plant life regulation.
Red/far-red-light is sensed by
phytochromes (phyA–phyE), blue-light
is absorbed by cryptochromes (cry1-3),
phototropins (phot1 and phot2) and
Zeitlupe family members (ZTL, FKF1
and LKP2). UV-B is perceived by
UVR8. Photoreceptors mediated plant
responses are shown in boxes (based
on Paik & Huq, 2019)
PEST AND DISEASE MANAGEMENT BY RED LIGHT 3199

phytochrome-interacting factors (PIFs), as they repress the activity of defence of plants against herbivores by inducing the synthesis of pro-
the constitutively photomorphogenic 1 (COP1)/suppressor of phyA- teinase inhibitors and polyphenol oxidases. Further, JA increases the
105 (SPA) complex, which inhibits the photomorphogenesis or shade- activity of other defensive enzymes, such as peroxidase (POD), chi-
avoidance responses through the transcriptional inhibition of the tinase and lipoxygenase, and it promotes the accumulation of some
auxin biosynthetic genes (Casal, 2013; Hoang, Han, & Kim, 2019; Li secondary metabolites responsible for plant defence responses, such
et al., 2012; Sheerin et al., 2015). as alkaloids, flavonoids and other phenolic compounds (Vasyukova &
There is a close interaction between light signalling and photo- Ozeretskovskaya, 2009; Wasternack & Hause, 2013). The direct
morphogenesis, which is regulated by phytohormones, such as by JA effects of JA and ET on microbes were also reported. JA reduced the
(Goossens, Fernández-Calvo, Schweizer, & Goossens, 2016). If the spore germination and mycelium growth of Fusarium oxysporum f. sp.
ratio between red and far-red is high, phyB suppresses the shade-
l, Igielski, Pollmann, & Kępczyn
lycopersici in vitro (Kro
ska, 2015). In
avoidance response and enhances sensitivity to JA, and promotes addition, ET also affected spore germination and hyphal growth of
defence mechanisms (Robson et al., 2010; Xiang, Wu, Jing, Chen, & Botrytis cinerea (Chagué et al., 2006). At the same time, the SA-
Yu, 2021). In a low ratio of red/far-red light, phyB is inactivated, shade dependent defence is antagonistic with JA /ET-dependent defence
responses are activated and sensitivity to JA is reduced (Moreno, Tao, signalling, but this hormonal crosstalk could be different and highly
Chory, & Ballaré, 2009). Besides their essential role in shade avoid- depends on other phytohormones (e.g., gibberellins), on the plant–
ance, phytochromes regulate seed germination, de-etiolation, photo- pathogen systems or environmental conditions, such as available light
morphogenesis, photoperiodic flowering and the circadian clock (De Vleesschauwer et al., 2016; Klessig et al., 2018; Koo, Heo, &
(Casal, 2013; Hernando, Murcia, Pereyra, Sellaro, & Casal, 2021; Choi, 2020; Robert-Seilaniantz, Grant, & Jones, 2011). Therefore, it
Pierik & de Wit, 2014; Su et al., 2017). can be concluded that the presence or absence of light is a crucial fac-
tor in phytohormone-mediated responses.
At the same time, endogenous contents of SA and JA in plants
3 | T H E R O L E O F LI G H T A N D TH E K E Y show daily changes (Wasternack & Hause, 2013). The basal levels of
D E F E N C E - RE L A T E D P H Y T O H O R M O N E S I N these phytohormones, which affect plant immunity, are regulated also
PLANTS by the circadian clock (Karapetyan & Dong, 2018; Lu, McClung, &
Zhang, 2017; Roden & Ingle, 2009; Spoel & van Ooijen, 2014). Time
Various phytohormones play a role in the regulation of plant defence for coffee (TIC), a night-expressed clock gene, inhibits JA signalling in
responses depending on the light (Ballaré, 2014; Deepika et al., 2020; the evening and contributes to a stronger JA responsiveness in the
Roberts & Paul, 2006). SA is required to establish both local and sys- morning. JA content shows a high peak in the middle of the day,
temic acquired resistance after pathogen infection. The elevated con- whereas SA peaks in the middle of the night, because the expression
centration of SA under stress conditions induces the rapid of the key enzyme responsible for SA biosynthesis (e.g., isochorismate
accumulation of reactive oxygen- (ROS) and nitrogen species synthase 1) is driven by the evening-phased clock transcription factor
(e.g., nitric oxide; peroxynitrite), leading to oxidized proteins and CCA1 hiking expedition (CHE) (Zheng et al., 2015). Considering these
hypersensitive response-like cell death in infected tissues, which is observations, not only the availability of light but the circadian rhythm

r, 2020;
more pronounced under high light (Loake & Grant, 2007; Poo can also influence the basal phytohormone-mediated defence
Vlot, Dempsey, & Klessig, 2009). Moreover, SA plays a crucial role in responses of plants.
systemic responses, which promotes a faster and stronger response Finally, it should be mentioned that there is a dynamic interaction
to a secondary infection (Arif, Sami, Siddiqui, Bajguz, & Hayat, 2020; between plants and other microbes, which can modulate the phyto-
Klessig, Choi, & Dempsey, 2018). SA regulates various components of hormone levels in the host by regulating the mutualistic and/or patho-
defence responses, such as synthesis of antioxidants, such as ascor- genic strategies of bacteria or fungi (Fonseca, Radhakrishnan,
bate; disease inhibitor polyphenols and flavonoids; antimicrobial phy- Prasad, & Chini, 2018). Namely, plant pathogens are able to manipu-
toalexins, such as camalexin; and pathogenesis-related (PR) proteins, late and/or diminish phytohormone signalling for their own benefit,
such as β-1,3-glucanases and chitinases (Klessig et al., 2018; Tripathi, and as a consequence promote the infection development in the host
Raikhy, & Kumar, 2019). At the same time, it was also reported that organism (Shen, Liu, & Naqvi, 2018). There are many data confirming
SA had a direct effect on microbes. Among the others, SA inhibited that abscisic acid, gibberellic acid and ET produced by fungi influence
the spore germination and colony growth rate of Harpophora maydis the pathogenicity (Chanclud & Morel, 2016). Among others, the nec-
(Degani, Drori, & Goldblat, 2015) and reduced hyphal growth of Asper- rotrophic Moniliophthora perniciosa can produce SA and JA, which
gillus flavus (Panahirad, Zaare-Nahandi, Mohammadi, Alizadeh-Sal- manipulate the defence signalling in the host, cocoa plants (Chaves &
teh, & Safaie, 2014). Gianfagna, 2006; Kilaru, Bailey, & Hasenstein, 2007). Some publica-
Although SA plays a primary role in resistance against biotrophic tions suggested that auxin and cytokinins produced by fungi could be
and hemibiotrophic pathogens, JA and gaseous ethylene (ET) regulate positive regulators of virulence (Chanclud & Morel, 2016; Shen
the plant immune response against necrotrophic and herbivorous et al., 2018). Similar phytohormone level modulating ability of auxin,
insect pathogens (Glazebrook, 2005; Vlot et al., 2009). Numerous cytokinins and gibberellic acid has been reported in various bacteria
studies have already indicated that JA activates the anti-nutritive (Olanrewaju, Glick, & Babalola, 2017). The ET generation inhibition by
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the bacterial 1-aminocyclopropane-1-carboxylate (ACC) deaminase is Peronospora belbahrii (Cohen, Vaknin, Ben-Naim, & Rubin, 2013),
one of the well-investigated interaction in rhizobacteria-plant relation Phakopsora pachyrhizi (Li, Mo, Guo, & Yang, 2010), Plasmopara viticola
(Singh, Shelke, Kumar, & Jha, 2015). (Rumbolz et al., 2002), and Puccinia hemerocallidis (Dong &
Buck, 2011; Mueller & Buck, 2003).
It is evident that life in the phyllosphere depends on whether it is
4 | L I G H T SE N S I N G A N D day or night, and on light quantity and quality. Therefore, understand-
PHYTOPATHOGEN RESPONSES ing perception regulation and the effects of different light spectra, sig-
nalling and metabolism are crucial to providing deeper insight into
In contrast to plants, little information is available about the impact of plant–microbe interactions. Such knowledge could inform the devel-
light signals on microbial virulence (Santamaría-Hernando opment of alternative methods of effective plant disease control and
et al., 2018). Similar to plants, plant pathogenic bacteria possess pest management.
diverse photoreceptors, which can be classified into six families
according to the chemical structure of chromophores: rhodopsins,
red-light-sensing phytochromes, xanthopsins, cryptochromes, blue- 5 | LE D A S TH E N E W SU N
light-sensing light, oxygen and voltage (LOV) and blue-light sensing
using flavin (BLUF) proteins (van der Horst et al., 2007). Light not only Light sources are generally used in modern agriculture in addition to
provides positional information to pathogens on top of the soil/leaf natural sunlight to maximize the photosynthetic activity of plants and
surface (Carvalho & Castillo, 2018), but several studies have reported improve crop yield (Massa, Kim, Wheeler, & Mitchell, 2008). Many
that it regulates numerous physiological features, especially motility, conventional light systems are already available on the market, such
adhesion and virulence of plant pathogens, for example, in Pseudomo- as fluorescent light, metal halide, high-pressure sodium and incandes-
nas syringae pv. syringae B728a (McGrane & Beattie, 2017; Wu, cent lamps, with a wide range of wavelengths from 350 to 750 nm.
McGrane, & Beattie, 2013), P. syringae pv. tomato (Moriconi However, emitted photosynthetically active radiation from above
et al., 2013; Río-Alvarez et al. 2014; Ricci, Dramis, Shah, Gärtner, & could be limited in the phyllosphere, and then utilized light cannot
Losi, 2015; Shah, Pathak, Drepper, & Gärtner, 2016; Santamaría- reach its goal to sustain high crop productivity (Olle & Viršile, 2013).
Hernando et al., 2018; Moyano et al., 2020), Pseudomonas cichorii New and highly developed light-emitting diode (LED) technology pro-
(Nagendran & Lee, 2015; Rajalingam & Lee, 2018), Agrobacterium vides an economically viable option to improve crop production. LED
fabrum (Bai, Rottwinkel, Feng, Liu, & Lamparter, 2016), Xanthomonas is a unique type of semiconductor diode that can emit a wide range of
campestris (Bonomi et al., 2016) and Xanthomonas citri subsp. citri light from UV-C (250 nm) to infrared (1,000 nm) (Bourget, 2008).
(Kraiselburd et al., 2012). Moreover, LED technology has many other advantages over other
Light also regulates the life cycle of fungi by controlling gene light sources. It is relatively cheap, energy-saving, functional, not frag-
expressions, and it has a significant effect on sporulation, primary ile, emits minimal heat and not hazardous. Furthermore, it can easily
metabolic pathways and secondary metabolite production. However, be integrated into a digital control system (Morrow, 2008; Olle &
only a few different photoreceptors have been described in fungi, Viršile, 2013; Singh, Basu, Meinhardt-Wollweber, & Roth, 2015). In
such as flavin-binding blue-light receptors, retinal-containing green- addition, LED is the first light source that can control the light spectra
light sensors and red-light sensor-containing proteins with a linear during a cultivation period. Therefore, it can be used for precise
tetrapyrrole as the functional part of the chromophore. Blue- and red- manipulation of biological plant responses to light, such as photosyn-
light receptors have nuclear functions, and they can directly regulate thesis, photomorphogenesis, flowering, metabolite production and
the expression of different genes and metabolic and morphogenetic
mez & Izzo, 2018). However,
plant defence (Davis & Burns, 2016; Go
pathways (Thind & Schilder, 2018; Yu & Fischer, 2019). Light has an precise control of spectral quality and light intensity requires funda-
effect on fungal growth, and it can directly inhibit metabolism, hyphal mental knowledge about the responses of plants and their associated
development, sexual reproduction and sporulation. Furthermore, it microorganisms. The use of LEDs provides many eco-friendly and sus-
can reduce virulence. These effects have been proven for Alternaria tainable solutions for the regulation of plant growth, development and
alternata (Hubballi, Nakkeeran, Raguchander, Anand, & productivity, as well as defence against microbial pathogens. LEDs can
Samiyappan, 2010), Aspergillus carbonarius (Cheong et al., 2016), be used as a supplemental light source and for inter-light systems, ver-
Botryodiplodia theobromae (Alam, Begum, Sarkar, Islam, & Alam, 2001), tical farming in conventional and urban agriculture and disease and
B. cinerea (Caires, Rodrigues, & Furtado, 2015; Canessa, Schumacher,
mez & Izzo, 2018; Olle &
pest control (Davis & Burns, 2016; Go
Hevia, Tudzynski, & Larrondo, 2013; Schumacher, Simon, Cohrs, Viršile, 2013; Wu, Hitti, MacPherson, Orsat, & Lefsrud, 2020). More-
Viaud, & Tudzynski, 2014; Zhu et al., 2013), Bremia lactucae over, LED technology provides a daily light system or photoperiodic
(Nordskog, Gadoury, Seem, & Hermansen, 2007), Colletotrichum lighting with different spectra. These applications can revolutionize
acutatum (Yu, Ramkumar, & Lee, 2013), Cryptonectria parasitica greenhouse farming and horticultural technologies.
(Hillman, Shapira, & Nuss, 1990), Fusarium graminearum (Beyer, Precise manipulation of light intensity and quality has already
Röding, Ludewig, & Verreet, 2004), Fusarium verticillioides been proposed as a novel plant disease management strategy. How-
(Velmurugan et al., 2010), Magnaporthe oryzae (Lee et al., 2006), ever, the physiological and molecular mechanism is not fully
PEST AND DISEASE MANAGEMENT BY RED LIGHT 3201

understood (Demotes-Mainard et al., 2016). Therefore, investigating 6.2 | ROS metabolism regulation
red light-induced molecular, biochemical and physiological changes in
both the host and its particular pathogens is essential to accelerate Changes in ROS metabolism upon red light under the infection can be
the application of red light as supplemental lighting, inter-lighting and an integrated part of the plant defence. This was supported by the
nocturnal lighting in plant disease management. observation that the plasma membrane-localized NADPH oxidase is a
In the next subchapter, the effects of red light on plant–viruses, crucial component of PR defence signalling under red light, contribut-
plant–bacteria, plant–fungi and plant–nematode interactions are col- ing to the first, priming oxidative burst after pathogen infection
lated and critically discussed based on the process of pathogenesis. (Jiménez-Quesada, Traverso, & Alché, 2016) and mediating
The role of ROS and SA in red light-induced resistance of plants is programmed cell death (Van Aken & Van Breusegem, 2015). NADPH
particularly scrutinized in these interactions. oxidase is able to translocate electrons from cytosolic NADPH to oxy-
gen, leading to the generation of superoxide in the apoplast (Sagi &
Fluhr, 2006). This was confirmed in broad beans (Vicia faba L.) against
6 | RED LIGHT INHIBITS THE B. cinerea infection where the activation of NADPH oxidase was
PATHOGENESIS inhibited by diphenyleneiodonium, therefore, necrotic lesions were
formed by the pathogen (Khanam, Kihara, Honda, Tsukamoto, &
While beneficial role of red light treatment for plants was described Arase, 2005; Khanam, Ueno, Kihara, Honda, & Arase, 2005). More-
under the infection of many different types of pathogens, the com- over, 12 hours-long red light exposure at night up-regulated the
mon protective effect of red light in different pathosystems is still expression of NADPH oxidase (Respiratory burst oxidase homologue;
unclear. Despite the mechanism of pathogenesis depends on the type RBOH) in tomato plant leaves under P. syringae infection (Yang
of infectious agents (Brader et al., 2017; Grimmer, John Foulkes, & et al. 2015).
Paveley, 2012; Serrano, Coluccia, Torres, L'Haridon, & Besides the NADPH oxidase-generated superoxide, hydrogen
Métraux, 2014), the rapid local and long-term systemic defence peroxide (H2O2) plays also a crucial role in cellular responses of the
responses by plants upon red light are general. In this subchapter, living organism under the infection. These reactive molecules are
these responses are collected and compared. In addition, various light- generated by plants rapidly and as strong oxidizing compounds can
ening methods are also discussed. disturb the cell integrity by targeting lipids, proteins and nucleic
acids. As a consequence, programmed cell death at the site of the

ski, 2018; Noctor,
infection is induced (Czarnocka & Karpin
6.1 | Pathogen perception Reichheld, & Foyer, 2018). H2O2 is known as the most stable and
diffusible ROS. H2O2 works as a signalling molecule at low concen-
Limited information is available in the literature about the effects of tration mediating defence responses of plants by influencing anti-
red light on pattern recognition receptors such as LRR receptor-like oxidant enzymes even in distal parts from the site of the infection.
serine/threonine-protein kinase FLS2, calcium signalling, activation At high concentration, it induces oxidative stress (Kocsy
of calmodulin and calcium-dependent protein kinases or mitogen- et al., 2013; Van Aken & Van Breusegem, 2015). H2O2 is generated
activated protein kinase during the pathogenesis (Feng & by superoxide dismutase (SOD) from the conversion of superoxide
Zhou, 2012; Serrano et al., 2012). Yang et al. (2015) found that to molecular oxygen and water (Alscher et al., 2002) and degraded
nightly red light illumination enhanced resistance against P. syringae enzymatically in several ways. Peroxisome-localized catalase (CAT)
pv. tomato, which was correlated with increased SA accumulation and the cytosolic or chloroplastic ascorbate peroxidase (APX), as
and the transcription of defence-related genes in tomato plant well as several other enzymes (e.g., other peroxidases, POD)
leaves (Solanum lycopersicum L.). Using RNA-seq analysis, they degrade H2O2 to water. Other non-enzymatic systems such the
observed that 12 h of red light exposure at night up-regulated cal- ascorbate/dehydroascorbate and the glutathione/glutathione dis-
cium homeostasis-related genes (calmodulin and calmodulin-binding ulphide are also able to diminish the H2O2 level (Foyer &
protein) (Yang et al. 2015). Calcium, as a second messenger regu- Noctor, 2009; Mhamdi et al., 2010).
lates downstream signalling resulting in the activation of defence- Significant changes in ROS metabolism mediated by red light in
and/or cell death-related genes (Ranf, Eschen-Lippold, Pecher, various plant species and organs were observed under plant–virus,
Lee, & Scheel, 2011; Wang et al., 2019). In addition, there is a strong bacterium, fungi and nematode interactions, respectively. Mosaic
interaction between intercellular elevation of calcium and ROS, viruses, such as cucumber mosaic viruses, have a wide host range and
which in waves transmit long-distance signals via cell-to-cell com- cause severe damage to various crops (Palukaitis, Roossinck,
munication pathway under stress (Fichman & Mittler, 2020; Gilroy Dietzgen, & Francki, 1992). Symptoms of cucumber mosaic virus are
et al., 2014). Moreover, there is a strong interaction between ROS significantly decreased under red light exposure at 7 days post-
and defence-related phytohormone signalling such as in the case of infection in tobacco (Nicotiana tabacum L.) leaves (Chen, Zhao, Zhang,
SA locally and systemically (Klessig et al., 2018; Vlot et al., 2009). In Lin, & Xi, 2015). In addition, red light reduces ROS formation and the
the next paragraphs, the role of ROS and SA signalling in the patho- production of superoxide and H2O2. In parallel, it induces SOD, CAT
genesis under red light exposure is discussed. and POD activities, as well as increases ascorbate and glutathione
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level in tobacco leaves under cucumber mosaic virus infection (Chen found to be significantly lower except for H2O2, which showed ele-
et al., 2015). vated levels (Meng, Höfte, & Van Labeke, 2019). Rice blast caused by
Beneficial effects of red light illumination in the defence against M. oryzae, is one of the most severe diseases of rice plants
fungal pathogens regulated by ROS metabolism were found in various (Ebbole, 2007). Interestingly, red light exposed a significant effect on
plant species (Figure 2). The grey mould, B. cinerea, is one of the most H2O2 reduction via increasing CAT activity under M. grisea infection
significant necrotrophs and causes severe economic losses in at least in detached rice (Oryza sativa L.) leaves (Ueno, Imaoka, Kihara, &
200 plant species worldwide. B. cinerea produces a range of cell-wall- Arase, 2007). Podosphaera species are one of the most important fun-
degrading enzymes and toxins triggering programmed cell death in the gal pathogens of greenhouse-grown plants (Debener & Byrne, 2014).
host (Williamson, Tudzynski, Tudzynski, & van Kan, 2007); however, Under Podosphaera xanthii infection, decreased H2O2 content and
red light exposure for 3 and 4 days significantly reduce B. cinerea- increased content of lignin-binding hydroxyproline-rich glycoprotein,
induced lesion development in tomato detached leaves in contrast to POD activity and gene expression were found upon red light applica-
those ones kept in the dark (Hui, Fu, Li, & Rui, 2017). In addition, red tion compared with white light, which mainly play a role in cell wall
light treatment significantly induced the activity of SOD, CAT and modification (Jing et al., 2018). Activation of defence mechanisms in
POD after 2 days during a B. cinerea infection event, and in parallel, Sphaerotheca fuligine-infected cucumber (Cucumis sativus L.) leaves
they significantly decreased the superoxide and H2O2 content in after red light treatment was described by Wang et al. (2010). Red
detached tomato leaves (Hui et al., 2017). A photoperiod of 16 h red light illumination decreased the powdery mildew colony number after
light increased total phenol, flavonoid, chlorophyll and anthocyanin 10 days of infection and H2O2 accumulation was observed in these
contents but significantly decreased H2O2 level after 4 weeks in leaves in the consequence of the decreased APX and CAT enzyme
strawberry (Fragaria  ananassa “Elsanta”) leaves compared to those activities (Wang et al., 2010). The red light-modified ROS metabolism
ones kept under white light where the level of these compounds was is also a significant part of defence mechanisms against nematodes.

F I G U R E 2 Effects of red light in plant–fungi interactions. APX: ascorbate peroxidase; CAT: catalase; Glu: β-1,3 glucanase; GPX: glutathione
peroxidase; GST: glutathione-S-transferase; HRGP: hydroxyproline-rich glycoprotein; LOX: lipoxygenase; OSM: osmotin; MAO: monoamine
oxidase; PAL: phenylalanine ammonia-lyase; PILP: protease inhibitor-like protein; POD: peroxidase; PR: pathogen-related; SOD: superoxide
dismutase; STS: stilbene synthase; TDC: tryptophan decarboxylase; TLP: thaumatin-like protein [Colour figure can be viewed at
wileyonlinelibrary.com]
PEST AND DISEASE MANAGEMENT BY RED LIGHT 3203

Not only viruses and fungi but also the endoparasitic nematode ammonia-lyase and PR-1a genes. This upregulation effect was not
Meloidogyne incognita causes significant yield losses in different crops, observed at plants that were kept in the dark (Nagendran & Lee, 2015).
such as tomato, cucumber, celery and watermelon (Chitwood, 2002). The protective effect of red light illumination on rotting disease caused
The supportive effects of red light exposure in the systemic resistance by Pseudomonas putida has also been described in soybean (Glycine max
of watermelon (Cucumis melo L.) against this root-knot nematode, are L. Merr.) seedlings. Red light increased resistance of plant against this
coordinated by both SA and JA, and are also regulated by changes in bacterium after 5 days of infection. Elevated SA level, but not the accu-
redox homeostasis, which were reported by Yang et al. (2018). The mulation of JA, was detected in infected hypocotyl after red light treat-
combined treatment (red light + root-knot nematode) resulted in sig- ment. Moreover, upregulation of SA biosynthetic genes, such as
nificantly higher H2O2 levels, increased activities of SOD, CAT, APX isochorismate synthase and phenylalanine ammonia-lyase, and the SA
and POD, moreover, higher glutathione and ascorbate contents in response gene PR-1 were also recorded after red light exposure (Dhakal,
both the leaves and roots (Yang et al., 2018). Park, Lee, & Baek, 2015). SA-dependent disease development was con-
firmed by investigating transgenic SA-non-accumulating nahG Arabidopsis
plants under P. syringae infection (Islam, Babadoost, Bekal, &
6.3 | Effects on the defence-related Lambert, 2008). Later, Yang et al. (2015) studied the protective effect of
phytohormone signalling nightly red light treatment in tomato plant leaves. They found that red
light illumination enhanced resistance against P. syringae pv. tomato,
Changes in ROS metabolism and redox homeostasis contribute to the which was correlated with increased SA accumulation and the transcrip-
biosynthesis and activation of defence-related phytohormones tion of defence-related genes. They observed that 12 h of red light expo-
(Glazebrook, 2005; Vlot et al., 2009). Among these, elevated endoge- sure at night upregulated biosynthesis genes of phytohormones (e.g., SA,
nous SA levels and highly activated SA signalling were observed in auxin, JA and ET) and transcription factors responsible for defence
case of all biotic stressors under red light exposure. First of all, hormone-related (e.g., SA and JA) gene expression and disease resistance
increased SA levels and SA-mediated PR-1, PR-2 and PR-5 expression (WRKY18, WRKY53, WRKY60, and WRKY70) (Yang et al., 2015). This arti-
have been observed under red light illumination in tobacco leaves cle informs the potential application of nightly red light treatment to con-
exposed to cucumber mosaic virus (Chen et al., 2015). trol P. syringae infection (Figure 4).
Besides the cucumber mosaic virus, red light significantly influ- Effects of red light treatment on SA metabolism during fungal
ences SA signalling in bacteria-infected plants (Figure 3). Red light infection were investigated only by Wang et al. (2010). Red light illu-
decreased the incidence of Gram-negative P. cichorii infection and mination decreased the powdery colony number (S. fuligine) after
reduced the bacterial burden in tomato (S. lycopersicum) seedlings 10 days of infection in cucumber leaves parallel with SA level eleva-
and leaves after 4 days in comparison with white light illumination or tion. In addition, the transcript levels of SA-regulated defence-related
keeping the plants in the dark. In addition, red light defended the genes, such as PR-1, WRKY30 and WRKY6, were also significantly
tomato plants against this infection by upregulating the expression of higher as compared with those in white light-treated samples (Wang
defence-, SA biosynthesis- and signalling-related phenylalanine et al., 2010). These results allow the conclusion that SA is an

F I G U R E 3 Effects of red light in

plant–bacterium interactions CHS:
chalcone synthase; GST: glutathione-S-
transferase; ICS: isochorismate
synthase; PAL: phenylalanine
ammonia-lyase; PR: pathogenesis
related; SA: salicylic acid; TLP:
thaumatin-like protein [Colour figure
can be viewed at
wileyonlinelibrary.com]
3204
ET AL.
GALLE

F I G U R E 4 Nocturnal red light

effects in plants. Red light activates
phytochromes and the activated Pfr
forms translocate into the nucleus
where inactivate phytochrome-
interacting factors (PIFs) by promoting
proteasomal (26S) protein degradation
and the constitutively
photomorphogenic 1 (COP1)-
suppressor of phyA-105 (SPA1)
complex by causing its dissociation
and subsequent nuclear exclusion of
COP1. This contributes to the
accumulation of key transcription
factors (e.g., HY5) of light responses.
Nocturnal red light elevates the
expression of various circadian
rhythm-, photosynthesis-, calcium
signalling-, phytohormone
biosynthesis-, redox- and defence-
related genes, as well as, transcription
factors based on the RNA-seq analysis
(Yang et al., 2015) [Colour figure can
be viewed at wileyonlinelibrary.com]

important element of the red light-mediated defence responses of antiviral and antimicrobial compounds are limited. Red light induced the
plants against fungal pathogens. accumulation of disease inhibitor polyphenols and flavonoids in straw-
The role of SA was also investigated in plant-nematode interaction berry leaves and muskmelon seedlings under B. cinerea (Meng
under red light illumination. Four weeks of red light treatment for 12 h at et al., 2019) and P. xanthii (Jing et al., 2018) infection, respectively. In
night reduced the incidence of nematode infection in tomato plants also, addition, red light elevated the activity and expression of phenylalanine
and it elevated the root and shoot biomass. Significant increases in ammonia-lyase, which involves in the biosynthesis of the phenolic com-
endogenous free SA levels, PR-1 and proteinase inhibitor protein 1 expres- pounds such as flavonoids, phenylpropanoids and lignin in plants (Sharma
sions were measured under red light exposure (Yang et al., 2015). It was et al., 2019). This was observed in P. cichorii-infected tomato seedlings
found that the daily used red light-induced systemic resistance of water- (Nagendran & Lee, 2015), P. putida-infected soybean seedlings (Dhakal
melon against root-knot nematode is coordinated by SA and JA levels, et al., 2015), grapevine (Vitis vinifera L.) cultivars exposed to B. cinerea
and changes in redox homeostasis (Yang et al., 2018). Recently, it was (Ahn, Kim, & Yun, 2015) and rice leaves treated with M. oryzae
found that red light enhances the expression of the JA biosynthesis- (Shirasawa, Ueno, Kihara, & Arase, 2012). The potential role of the
related gene, allene oxide synthase in the root-knot nematode-infected phenylpropanoid or tryptophan pathways in red light-induced resistance
leaves and roots of watermelon, which implies that allene oxide synthase was proven with the application of 0.5 mM aminooxy acetic acid or
plays role in the JA-mediated red light-induced resistance against this 0.1 mM s-α-fluoromethyltryptophan pre-treatments for 24 h before the
pathogen (Zhou et al., 2019). Moreover, the induction (ClabZIP6 and infection with B. oryzae in detached leaves of rice plants. The application
ClabZIP56) or repression (ClabZIP37 and ClabZIP57) of several basic leu- of both inhibitors reduced the resistance development in response to red
cine zipper (bZIP) genes were also described in root-knot nematode infec- light irradiation, suggesting that tryptophan and phenylpropanoid path-
tion under red light in watermelon leaves (Yang et al., 2019). The ways are integral part of the red light-induced resistance against B. oryzae
description of the molecular roles of these genes needs further study. (Parada, Mon-nai, Ueno, Kihara, & Arase, 2015). The effect of red light
The nocturnal effects of red light on the relation of SA-JA in other cases illumination to elevate levels of other antimicrobial compounds in plants
remained also unclear. to combat fungal infections was also reported. The red light treatment
triggered the accumulation of antimicrobial trans-piceid in “Kyoho” and
resveratrol in “Campbell Early” grapevine leaves after 24 h of the applica-
6.4 | Changes in antiviral and antimicrobial tion under B. cinerea infection (Ahn et al., 2015). In addition, antimicrobial
compounds stilbene biosynthetic enzymes were also up-regulated and showed two
differential peaks at 12 and 48 h in ‘Campbell Early’ grapevine leaves
Although the positive effect of red light on SA-mediated PR1 expression under red light (Ahn et al., 2015). Therefore, these compounds could be
was observed in all biotic stress relation, similar data regarding other also essential in plant defence.
PEST AND DISEASE MANAGEMENT BY RED LIGHT 3205

6.5 | Hypersensitive response and cell death light treatment significantly reduced the colony number of P. syringae
regulation pv. tomato on infected Arabidopsis leaves after 2 and 4 days of infec-
tion compared with white light treatment (Islam et al., 2008). Red light
The red light exposure not only inhibits the infection development by treatment decreased hypha formation and spore germination of
inducing defence signalling mechanisms but it also attenuates or B. cinerea (Islam et al., 1998), C. acutatum (Yu et al., 2013),
delays programmed cell death in the infected organs and plants to Podosphaera pannosa (Suthaparan et al., 2010), P. xanthii (Suzuki
inhibit the diffusion of the pathogen. Continuous red light treatment et al., 2018) and S. fuligine (Wang et al., 2010) compared to white light.
for 96 h delayed the hypersensitive response in tobacco leaves infil- Interestingly, others found that red light irradiation did not affect the
trated with P. syringae pv. tomato. As a consequence of attenuated spore germination and appressorium formation of B. oryzae after 24 h
hypersensitive response, lower electrolyte leakage and RUBISCO con- of inoculation as compared with white light (Arase, Parada, Kihara, &
tent were measured. Attenuation of programmed cell death markers Ueno, 2017). In contrast to these findings, the adverse effects of red
such as DNA degradation and accumulation of nucleases, cysteine light on muskmelon seedlings were described (Jing et al., 2018):
proteinases in red-light-exposed leaves in comparison with those Red light significantly increased the disease index and colony number
leaves that were exposed to white light was also observed (Moyano of P. xanthii per leaf after 12 days. However, it can be concluded that
et al., 2020). In addition, red light significantly inhibited A. alternata these effects can depend on the infectious agents, genotype and the
AM-toxin-induced necrosis within 36 h in apple (Malus pumila Mill. mode of the red light application (e.g., duration and intensity).
var. domestica Schneid.) leaf (Tabira et al., 1989). Moreover, red light
treatment for 24 h before A. tenuissima infection suppressed lesion
development in detached leaves of broad bean (Rahman, Honda, & 7 | C O N C LU D I N G R E M A R K S A N D F U T U R E
Arase, 2003). The development of necrotic lesions by B. cinerea was PERSPECTI V ES
significantly reduced after 48 h of infection when the leaves were illu-
minated with the red light. In addition, this treatment decreased the Despite the fact that more comprehensive studies about the protec-
germination and hypha formation ability of B. cinerea spores (Islam, tive effect of red light in plants against pathogen infections have been
Honda, & Arase, 1998; Khanam, Kihara, et al., 2005; Khanam, Ueno, conducted in the past 20 years, there are many gaps in the knowledge
et al., 2005). Later, it was observed that the application of photosyn- of red light connected signalling under different biotic stressors. We
thesis inhibitor (3-[3,4-dichlorophenyl]-1,1-dimethyl urea) suppressed reviewed the current status of the physiological, biochemical and
the red light-induced resistance in broad bean leaflets. Altogether, molecular aspects of red light-regulated defence mechanisms in differ-
these results indicate the presence of a red light-induced resistance ent plant species, genotypes and organs, and we discussed interac-
mechanism against B. cinerea and dependence of the mechanism on tions between plants and pathogens, such as viruses, bacteria, fungi
host plant photosynthesis (Rahman, Honda, Islam, & Arase, 2002). and nematodes, especially focusing the role of ROS metabolism and
Corynespora cassiicola is primarily found in tropical and subtropical phytohormones, especially SA under red light treatments.
regions and causes severe leaf spot disease in various plant species, Numerous studies have already proved that the application of red
including cucumber plants (Dixon, Schlub, Pernezny, & light increases biotic stress tolerance and improves plant growth and
Datnoff, 2009). Rahman et al. (2010) found that red light treatment development, especially at night. Nocturnal red light exposure
significantly suppressed C. cassiicola-induced lesion formation within increases endogenous defence hormone levels, especially those of SA,
24 days in leaves of intact cucumber plants, providing a potential and the expression of their related genes and transcription factors,
strategy to protect cucumber plants against this fungal pathogen such as WRKYs and bZIPs (Figure 4). However, red light induces other
under greenhouse conditions. Moreover, the formation of blast transcription factors, regulating the biosynthesis of defence hormones
lesions caused by M. oryzae was significantly inhibited after 24-hours- and their relation with clock genes remains obscured. In addition,
long red light treatment in intact rice leaves (Shirasawa et al., 2012). based on electrolyte leakage measurements, the beneficial effects of
Pre-treatment of pigeonpea (Cajanus cajan L. Millsp.) seedlings with red light in plant defence mechanism are manifested in the presence
red light showed a protective effect against fungal pathogens in the of various biotic stressors, such as viruses, bacteria, fungi and nema-
early plant developmental stage: 12- and 24-hours-long red light todes, through the alleviation of membrane damage. The reduced oxi-
exposure reduced disease wilt of Fusarium udum (Bansod, Sakhare, dative stress response and lipid peroxidation and enhanced
Deshmukh, & Moharil, 2017). This finding suggests that red light detoxification and antioxidant capacity confirmed the positive effects
treatment could be effective against fungal pathogens during early of red light treatments. Moreover, increased photosynthetic efficiency
plant development. and higher accumulation of defence-related compounds, such as poly-
phenol, flavonoid, chlorophyll and anthocyanin contents, also verified
the beneficial effects of red light in infected plant organs. However,
6.6 | Effects on phytopathogens most of the discussed studies were conducted on detached plant
organs, especially on leaves, which provide a reliable in vitro model
Red light exerts a remarkable protective effect on the surface of host plant system to study plant–pathogen interactions (Köhl, Kolnaar, &
plants against bacterial and fungal infections. It was observed that red Ravensberg, 2019). Compounds involved in cell signalling, defence-
3206
ET AL.
GALLE

related enzymes and metabolites are produced by plants at different AC KNOW LEDG EME NT S
levels in vitro and in situ. Moreover, the long-term effects of infection This work was supported by the grants from the National Research,
and systemic acquired resistance, which is regulated by various phyto- Development and Innovation Office of Hungary – NKFIH
hormones, especially SA, cannot be investigated in detached leaves (FK 124871) and the University of Szeged Open Access Fund (5376).
in vitro because several parts of the intact plant, which could be sites L.G. and L.T. are financed by the FK 134343 and PD 134284 projects
of significant synthesis of defence-related compounds, are missing of Hungarian National Research, Development and Innovation
(Fu & Dong, 2013; Kachroo & Robin, 2013). Therefore, understanding (NKFIH) Office, respectively. Research of L.G. and P.P. has been
the mode of action of red light under pathogen infection is essential supported by the János Bolyai Research Scholarship of the Hungarian
to achieving optimal in situ disease control. Testing the effects of sup- Academy of Sciences. The present work of L.G. and P.P. was
plemented or nocturnal red light on intact plants under biotic stress supported by the ÚNKP-20-5 - New National Excellence Programme
conditions can support the development of novel plant or crop pro- of the Ministry for Innovation and Technology from the source of the
tection strategies. Furthermore, studying the impact of lighting tech- National Research, Development and Innovation Fund.
niques, such as conventional lighting or inter-lighting, on intact plants
can also contribute to realizing these aims. AUTHOR CONTRIBU TIONS
On the basis of the reviewed papers, it can be concluded that the All authors contributed to the writing and revising of the manuscript.
application of only red light, especially at night, elevated endogenous
SA levels and activated SA signalling in plants independently of biotic CONFLICTS OF INTEREST
stressors. However, significant differences in hormone levels and SA The authors declare no conflict of interest.
signalling were observed in various plant species and organs, such as
leaves, hypocotyls and roots. Changes in SA levels in these organs, DATA AVAILABILITY STAT EMEN T
especially in leaves, could be crucial for plants to survive a severe Data sharing not applicable to this article as no datasets were gener-
infection. However, the type of biotic stressors (e.g., biotrophic or ated or analysed during the current study.
necrotrophic herbivory) can also modulate the complexity of plant
defence responses. Therefore, the application of red light as an envi- OR CID
ronmentally friendly technology can prime SA under biotic stress
r
Péter Poo https://orcid.org/0000-0002-4539-6358
without any chemical treatments. In addition, further analyses on SA-
mediated signalling and other defence hormones, such as the JA- RE FE RE NCE S
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