Journal of Integrative Agriculture 2021, 20(1): 4–23

Available online at www.sciencedirect.com

ScienceDirect

REVIEW

Crop photosynthetic response to light quality and light intensity

Iram SHAFIQ1, 2*, Sajad HUSSAIN1, 2*, Muhammad Ali RAZA1, 2, Nasir IQBAL1, 2, Muhammad Ahsan
ASGHAR1, 2, Ali RAZA1, 2, FAN Yuan-fang1, 2, Maryam MUMTAZ1, Muhammad SHOAIB3, Muhammad
ANSAR4, Abdul MANAF4, YANG Wen-yu1, 2, YANG Feng1, 2
1
College of Agronomy, Sichuan Agricultural University, Chengdu 611130, P.R.China
2
Sichuan Engineering Research Center for Crop Strip Intercropping, Chengdu 611130, P.R.China
3
College of Resources, Sichuan Agricultural University, Chengdu 611130, P.R.China
4
Department of Agronomy, Pir Mehr Ali Shah Arid Agriculture University Rawalpindi, Punjab 46300, Pakistan

Abstract
Under natural conditions, plants constantly encounter various biotic and abiotic factors, which can potentially restrict plant
growth and development and even limit crop productivity. Among various abiotic factors affecting plant photosynthesis, light
serves as an important factor that drives carbon metabolism in plants and supports life on earth. The two components of
light (light quality and light intensity) greatly affect plant photosynthesis and other plant’s morphological, physiological and
biochemical parameters. The response of plants to different spectral radiations and intensities differs in various species
and also depends on growing conditions. To date, much research has been conducted regarding how different spectral
radiations of varying intensity can affect plant growth and development. This review is an effort to briefly summarize the
available information on the effects of light components on various plant parameters such as stem and leaf morphology and
anatomy, stomatal development, photosynthetic apparatus, pigment composition, reactive oxygen species (ROS) production,
antioxidants, and hormone production.

Keywords: light intensity, light quality, photosynthesis, stomatal development, pigment composition, reactive oxygen species,
antioxidants, plant hormones

1. Introduction

Modern farming, which increases crop yields with the greater

use of chemical fertilizers, pesticides and non-renewable
resources, is presently being called into question as the
Received 6 October, 2019 Accepted 22 March, 2020
Correspondence YANG Feng, Tel: +86-28-86290960, E-mail: issue of food security is increasingly gaining paramount
[email protected]; YANG Wen-yu, E-mail: mssiyangwy@ importance in a world of ever-increasing population and
sicau.edu.cn
* global climate change. The rising need of food necessitates
These authors contributed equally to this study.
the development of crops with optimum growth, higher quality
© 2021 CAAS. Published by Elsevier Ltd. This is an open
and yields, and robust stress resistance, to sustainably feed
access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/). the ever-increasing human population which is expected to
doi: 10.1016/S2095-3119(20)63227-0 rise by 10 billion in next 50 years (Glick 2014; Nowicka et al.
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 5

2018; Vogel and Meyer 2018). usually suffer from low irradiance or shade stress. Shade
Of many abiotic factors, light plays a vital role in agricultural or low-light conditions is a pervasive abiotic stress in
production (Yang et al. 2014) as it is indispensable for agricultural crop production due to light blockage from
photosynthesis, a complex biochemical and biophysical interculture practices such as intercropping (Yang F et al.
process for biomass production, which involves the synthesis 2018b), high plant densities such as those found in forests
of photosynthetic pigments, Calvin cycle and the light-driven and prairies, where a mixture of different species grow in
electron transport (Wang et al. 2013b). Light is perceived by dense conditions (Martinez-Garcia et al. 2010), or due to
plants through different photoreceptors, i.e., phytochromes cloud cover, snow and many other factors (Zhu et al. 2017).
and cryptochromes (Ballaré and Pierik 2017; Mawphlang It is characterized by a reduced amount of photosynthetically
and Kharshiing 2017). The two components of light, light active radiations (PAR) and changes in the spectral
quality (which means the color or wavelength of light) and composition of light (Park and Runkle 2017; Yang F et al.
light intensity greatly affect the structure and function of plant 2018b) (Fig. 1). It not only affects the amount of light
photosynthetic apparatus (Li R et al. 2014; He et al. 2018; received by plants but also alters the plant environmental
Yang F et al. 2018a) as well as growth and yield potential conditions, such as the temperature of air and ground around
(Fan et al. 2018; Yang F et al. 2018a). Earlier studies have the plant, humidity, carbon dioxide (CO2) concentrations,
reported blue light (425–490 nm) and red light (610–700 nm) etc., which are essential for plant growth (Song et al. 2012).
to be the best light spectra for plant photosynthesis, while a Low light conditions substantially affect various agronomic
very low amount of green light (520–610 nm) is absorbed traits of plants (Wang et al. 2012). It negatively affects the
by plants (Pettai et al. 2005; Chang et al. 2016; Yoshida morphology (Wu L et al. 2017), physiology and biochemistry
et al. 2016). Red light (R) contributes to the development of crop plants (Liu et al. 2016), especially photosynthesis
of photosynthetic apparatus and induces transformations in (Yang F et al. 2018a).
the photochromic system, thus, influences morphogenesis Generally, it is observed that lower light intensities or the
(Urbonavičiūtė et al. 2007). Far-red light (FR) is reported shading conditions in intercropping inhibit leaf growth, lead
to contribute minimally to the plant photosynthesis because to thinner leaves with smaller leaf area, thinner palisade
of its poor absorption by leaves and unbalanced excitation tissues and reduced chlorophyll content resulting in lower
of the two photosystems; photosystem I (PSI) and PSII, light-harvesting (Yang et al. 2014; Gong et al. 2015).
leading to low quantum yields (Hill and Bendall 1960; Moreover, stomatal density and conductance are decreased
Duysens and Amesz 1962; McCree 1971; Myers 1971). which results in poor CO2 transport. The electron transfer
While, the blue light is observed to regulate different plant from PSII to PSI is blocked, the amount and activity of
processes such as photosynthesis, stomatal opening, enzymes involved in the Calvin cycle are altered. Reactive
photo-morphogenesis, maturation of chloroplasts, and oxygen species are generated which further disrupt the
biosynthesis of chlorophyll and enzymes (Tibbitts et al. normal functioning of the photosynthetic apparatus. All of
1983; Okamoto et al. 1997; Heo et al. 2002; Urbonavičiūtė this leads to a lower carbon dioxide assimilation rate, and
et al. 2007). Similarly, previous studies show that green a lower net photosynthetic rate and reduced light-saturated
light contributes to plant growth by stimulating carbon net photosynthetic rate (Pnmax). Higher light intensities are
assimilation in lower parts of the plant canopies since it reported to disturb the balance between energy supply
can penetrate deeper in the foliage and crop in comparison and energy consumption in plants. It is well known that the
to red and blue lights (Yorio et al. 2001; Kim et al. 2004a; electron transport and synthesis of ATP and NADPH occur at
Terashima et al. 2005). It has also been observed to much slower rates in comparison to the light-harvesting and
protect light-labile plant defense secondary metabolites energy transfer to PSII (Ruban et al. 2012). In conditions
(Gould et al. 2010) and improve plant defense mechanisms of higher light intensities, the amount of energy absorbed
by triggering and upregulating the expression of specific recurrently overcomes the metabolic energy needed which
genes under biotic or abiotic stress (Zhang and Folta 2012; results in the accumulation of excess energy in thylakoid
Nagendran and Lee 2015). membranes that has the potential to harm PSII. Moreover,
Similarly, extensive research has been conducted it may result in the permanent closure of the PSII reaction
related to the effect of different light intensities on plant centres and cause photo-inhibition (Long et al. 1994; Keren
photosynthesis and other morphological, anatomical, et al. 1997; Jansen et al. 1999). It has been reported earlier
physiological, and biochemical parameters. Plants need that plants growing in higher and lower light intensities have
a specific light intensity for their growth, higher or lower a different composition of photosynthetic pigments, electron
than normal light intensity may inhibit photosynthesis. In carriers, chloroplast ultrastructure, and photosynthetic rates
comparison to higher light intensities, intercropped crops (Boardman 1977; Lichtenthaler et al. 1981; Wild et al. 1986;
6 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

Anderson et al. 1995). photosynthesis and other plant parameters in various

Until now, much research has been conducted in species, which will help us to give an insight of how
context to how different light qualities and intensities affect plants respond and manage their growth in a varying light
plant photosynthesis and other plant parameters either environment (Fig. 2). Moreover, it will aid in increasing our
positively or negatively but to date, no one has compiled understanding of how to manipulate light in ways that can
this information. This review is devoted to briefly compile favor plant growth and enhance yield, thereby optimizing
the information regarding the role of different light qualities, food production and ensuring higher yields and economic
intensities and their positive or negative effects on plant benefits.

Low light intensity Thinner leaves

Greater biomass partitioning
to stem Limited leaf growth Smaller leaf area

Reduced stomatal
Decreased chlorophyll content density
and conductance
Low light harvesting
Poor CO2 transport

ROS production Gas exchange

Chloroplast Photosynthetic
and
membrane enzymes
chlorophyll
composition concentration
fluorescence
Oxidative stress

Protein content Electron transport

Disrupted photosynthetic
apparatus

Lower net photosynthetic rates

Fig. 1 A proposed pathway for how low light intensity results in lower net photosynthetic rates. ROS, reactive oxygen species.

Light intensity Photosynthesis Light quality

Photoreceptor

Receptor
(PHY)B Blue

(CRY)2 Red
Plant response
Far red

Green

Red:far red

Down regulation of photosynthesis

responsible genes under shading (low light)

Fig. 2 Graphical representation of the abstract.

 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 7

2. Plant morphology and anatomy limited light conditions (Terashima and Saeki 1985; Shi
2006). However, in comparison to thicker leaves, the thinner
2.1. Leaf leaves have thinner palisade tissue and less chloroplast,
this structure does not support the transport and dissolution
Shade governs leaf morphology and anatomy. Leaves are of CO2 (Terashima et al. 2001) (Fig. 3). Therefore, thinner
considered as the main organ for plant photosynthesis and leaves are not proficient in photosynthesis and biomass
transpiration, their structure reflects how environmental accumulation (Wu Y et al. 2017). Moreover, plants under
factors influence plants or how plants adapt to the changing shade invest greater biomass partitioning to stem growth
environment. Under normal light conditions, palisade tissue at the expense of leaf expansion. Taken together, these
elongate and increase the area of chloroplast channel findings suggest an inhibited growth of plant leaves under
through which CO2 enters, thereby increasing the leaf lower PAR (Wu Y et al. 2017).
thickness and strengthening the photosynthetic ability Light quality also significantly influences the development
(Terashima et al. 2005; Wu et al. 2016). However, shade of leaf palisade/spongy parenchyma and thus leaf thickness.
or low PAR irradiances result in smaller leaf area (Kim et al. This is observed for Arabidopsis (Weston et al. 2000) and
2005; Kozuka et al. 2005; Fan X X et al. 2013; Gong et al. Alternanthera brasiliana (Macedo et al. 2011). The number
2014) and thinner leaves, which is a common adaptation of mesophyll cells per leaf section and palisade cell length
mechanism in many plant species (Terashima et al. 2005; decreased in response to low R:FR in Phaseolus vulgaris
Kalve et al. 2014; Mishio and Kawakubo 2015; Ballaré and and Solanum tuberosum respectively (Barreiro et al.
Pierik 2017; Bertel et al. 2017; Han et al. 2017; Ajmi et al. 1992; Thiele et al. 1999). The blue light effects on the
2018; Fan et al. 2018). leaf thickness are known to be species dependent. A blue
Most of the scientists believe that thinner leaves have light supplementation to pepper plants grown under red
greater ability to intercept light due to low leaf dry mass light is correlated with an increase of palisade and spongy
per unit area (Valladares and Niinemets 2008; Terashima mesophyll thickness in pepper plants (Schuerger et al.
et al. 2011) and the structural characteristics also aid in 1997). An increase of more than 25% blue light ratio in
increasing the light reflection and scattering in the leaves rapeseed leaves resulted in two cell-layers in the palisade
which helps the plants to maximize light penetration into the tissue, which indicates that blue light has a decisive role in
leaves to increase light absorption for chloroplasts under the development of the palisade tissues (Chang et al. 2016).

Light intensities

Normal PAR Low PAR

Ecological adaptation

Thick leaves Thin leaves

Elongated palisade Greater mesophyll Thinner palisade tissues Less chloroplast

tissues surface area

Area of chloroplast
channel ↑

Poor transport and

dissolution of CO2

CO2

Photosynthetic efficiency and Photosynthetic efficiency and

biomass accumulation ↑ biomass accumulation ↓

Fig. 3 Effect of light intensity on leaf anatomy. The upward and downward arrows in the box represent increase and decrease
respectively. PAR, photosynthetically active radiation.
8 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

In contrast, the addition of blue light decreases leaf thickness low xylem area, low pith and xylem ratio (Liu et al. 2019),
in peach (Rapparini et al. 1999). Johkan et al. (2012) reduced cross-sectional area of stem, stem rind thickness
observed an increased width and length of lettuce leaves and vascular bundle number (Cui et al. 2012).
irradiated with green LED light of higher photosynthetic Low light intensities also alter the expression of genes
photon flux, i.e., 300. involved in shade avoidance response and lignin and
cellulose synthesis. It has been observed in A. thaliana that
2.2. Stem green shade (created by adding a green color filter to the
white light background which reduced PAR to 65 µmol m–2
Generally, under shade conditions, plants have increased s–1, R:FR to 0.19 and blue light photon fluence rate to 2 µmol
stem height, petiole length and decreased stem diameter, m–2 s–1) increased the expression of four genes (XTH16, –17,
as more carbon is allocated to the elongation of stem –19, and –22) which play a role in boosting shade avoidance
and petiole at the expense of leaf and root development responses under low light conditions (Sasidharan et al.
(Gommers et al. 2013; Park and Runkle 2017). Such a 2014). Similarly, in rice plants, reduced expression of genes
structure helps plants in searching for light under shade involved in lignin and cellulose biosynthesis (OsCesA1,
conditions (Smith 1982; Green-Tracewicz et al. 2011; OsCesA3 and OsCesA8) at the stem formation stage is
Casal 2012; Gong et al. 2015; Wu L et al. 2017) (Fig. 4). observed (Wu L et al. 2017). However, more research needs
However, shade results in weaker and slender stems with to be conducted to investigate the expression of the genes
poor mechanical strength (Su et al. 2014). related to the expression of lignin biosynthesis and genetic
The stem strength depends on the contents such as lignin, engineering techniques must be exploited to regulate
cellulose, semi-fiber, sucrose, pectin, starch, etc. (Hussain these genes. The schematic diagram below represents
et al. 2019b, d). Lignin is a complex aromatic polymer in the physiological, anatomical, proteomic, and enzymatic
vascular plants and is an important constituent of the cell changes in the stem of shaded plants (Fig. 6).
wall (Fig. 5) (Weng et al. 2008). It enhances the strength of Light quality also regulates the stem morphological
cell walls by crosslinking with cellulose and hemicellulose and anatomical structures. Since plants mainly absorb
(Li et al. 2009). Low light intensity or shade conditions red and blue lights in comparison to green light, so their
serve as a limiting factor in the biosynthesis of lignin by development and physiology are greatly influenced by
reducing the activities of enzymes, i.e., phenylalanine blue or red light (Terashima et al. 2009). It is known
ammonialyase (PAL), cinnamyl alcohol dehydrogenase that a blue light supplementation in the incident light
(CAD), 4-coumarate:CoA ligase (4CL), and peroxidase influences characteristics such as plant height, number
(POD) involved in it (Koyama et al. 2012; Wang et al. 2012; of nodes per branch and biomass accumulation (Yorio
Wu L et al. 2017). Weaker stems with higher lodging rates et al. 2001). Tomato plants raised in blue light had smaller
resulted in a reduced transport of carbohydrates and dry shoots, reduced number of nodes and internode length
matter production, increased attack by various pests and (Głowacka 2004). In vitro grapes also showed reduced
pathogens, all of this is significantly correlated with yield loss height in response to blue light (Poudel et al. 2008). Similar
(Hussain et al. 2019b, 2020). Moreover, it is observed that results were observed for pines and narcissi (Sarala et al.
lower light intensities alter the thicknesses of mechanical 2007; Woźny and Jerzy 2007). Camptotheca acuminate
tissue layers and vascular bundle sheath cells which are grown under blue and yellow lights resulted in small stem
important for crop lodging resistance at the anatomical height whereas red light promoted plant growth and stem
level (Zhang et al. 2016). Shade results in plants with elongation (Yu et al. 2017). Similar results were reported

2 Trifoliate
Lignin

Angle
Angle
Lignin

Normal light Low light

Normal light Low light

Fig. 5 Biosynthesis of lignin under normal light and low light

Fig. 4 Phenotypic changes of soybean plants under normal conditions. The dark pink color lining shows lignin content in the
light and low light conditions. stem under normal light and low light conditions. Bar=1 000 μm.
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 9

Fig. 6 Diagrammatic scheme to summarize the influence of shade on plant physiological, proteomic, anatomical changes and
enzymatic activities (Hussain et al. 2019c). XTHs, xyloglucan endotransglucosylase/hydrolase proteins; EXP, expansins; PAL,
phenylalanine ammonia-lyase; 4CL, 4-coumarate: CoA ligase; CAD, cinnamyl alcohol dehydrogenase; POD, peroxidase.

for Pelargonium by Appelgren (1991). Furthermore, earlier

Stomata size
research reports that blue light suppresses hypocotyl
elongation while red light induces hypocotyl elongation Stomata size
(McNellis and Deng 1995; Johkan et al. 2010). While
green light is known to induce early stem elongation (Folta
2004; Kim et al. 2004b) and results in decreased biomass
production (Folta and Maruhnich 2007). Normal light Low light

3. Stomatal development
Fig. 7 Stomatal density and size under normal light and low light
conditions (the size and number were larger under the normal
The stomata are known as an important channel for the light stomata than those under low light condition).
process of transpiration, i.e., exchange of water and
gases with the external environment. Light influences
Shade stress might also reduce stomatal opening (Knapp
stomatal conductivity (Timperio et al. 2007). The stomatal
and Smith 1990) as under low light ABA level increases in
development is related to light intensity (Hattori et al. 2007)
guard cells, where they bind to a soluble receptor to trigger
and the stomatal response to fluctuating light intensities
stomatal closure (McCourt and Creelman 2008). The
has been widely studied (Shimazaki et al. 2007; Lawson
activated ABA receptor represses protein phosphatases
et al. 2010; McAusland et al. 2016; Kardiman and Ræbild
that enhances the activity of various enzymes, including
2017; Matthews et al. 2018). Most plants reduce stomatal
respiratory burst oxidases (RBOHs) due to enhanced
density as an adaptation to low light conditions, which is
well observed under natural and controlled conditions (Gay phosphorylation (Mustilli et al. 2002; Park et al. 2009). The
and Hurd 1975; Proietti et al. 1988; Gregoriou et al. 2007; activation of RBOH leads to a transient burst of ROS in
Granado-Yela et al. 2011; Muneer et al. 2014; Yang et al. guard cells (Pei et al. 2000) which opens calcium ion influx
2014; Zheng and Van Labeke 2017; Ajmi et al. 2018) (Fig. 7). channels (Mittler and Blumwald 2015; Minguet-Parramona
Moreover, under lower irradiances, stomatal conductance et al. 2016), that in turn, activate ion efflux channels on the
decreases, which leads to increased levels of intercellular plasma membrane. These changes in the ion concentration
CO2 concentration (Meng et al. 2002; Yang et al. 2011). result in the efflux of water, hence guard cells become flaccid
10 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

leading to stomatal closure (Chen et al. 2010). decreased quantum yield (Fv/Fm), effective quantum yield
The stomatal response to different light spectra varies. of photosystem (PSII), photochemical quenching (qP), and
It is known that phytochromes A and B promote stomatal electron transport rate (ETR) in plants grown under shade
maturation in A. thaliana in response to FR and R light conditions (Hussain et al. 2019c) (Fig. 8). Reductions in
respectively (Kang et al. 2009). A low R:FR or phytochrome photosynthetic rate is reported to occur due to two main
B (PHYB) reduced expression decreases the stomatal reasons; either due to decreased CO2 diffusion into leaves,
density, which results in a decreased stomatal opening that decrease in intercellular CO2 and stomatal conductance, or
can either cause an increase or decrease in CO2 stomatal due to inhibition of photosynthesis by inhibition of the leaf
conductance. Similar results of decreased stomatal density growth and enlargement by controlling the cell proliferation
in response to low R:FR ratio have been reported in (Wu L et al. 2017; Wu et al. 2018). Furthermore, it was
A. thaliana, Citrus insitorum and Oryza sativa (Boccalandro observed that photosynthetic efficiency of rice plants under
et al. 2003; Liu et al. 2012; Distefano et al. 2013). In contrast, low light decreased by 79.84% as compared to that of
stomatal density did not change in leaves of C. communis natural light (Sato and Kim 1980). Earlier research also
(Assmann 1992) indicating that all species do not follow
suggests disrupted photosynthesis due to shade stress
the shade response pattern of Arabidopsis. While, former
at the vegetative stage which blocks electron transport
studies observed no effect of phytochrome B on stomatal
from PSII to PSI, thus reducing the electron transport rate,
development in O. sativa (Liu et al. 2012). The lettuce plants
reducing the amount of ATP produced and the amount or
grown under blue LEDs with high light intensities showed
activity of Rubisco (Yao et al. 2017; Huang et al. 2018).
well-organized guard cells with open stomata, the number
Shade leaves usually have a lower net CO2 assimilation rate
of stomata were observed to be higher and the opening and
(An) (Tateno and Taneda 2007) and is saturated at lower
closing of stomata was also more effective (Muneer et al.
PPFD (Zhang et al. 2004). Plants are known to adjust their
2014). Previous studies observed that stomatal opening
photosynthetic apparatus in response to changes in light
is opposed when given a brief pulse of green light, while
conditions by making changes at molecular level such as
stomata open if the green light is followed by blue light
(Frechilla et al. 2000). Similar observations of this blue- modulation of PSI and PSII antenna size by light intensity;
green effect were recorded by Talbott et al. (2002) in a it is observed that plants grown under high light intensity
diverse suite of plant species that suggested the existence have smaller antenna than those grown in shade (Anderson
of this effect throughout the plant kingdom. In contrast, et al. 1995). Other long-term acclimation responses of the
blue and purple light treatments in tomato reduced the thylakoid membrane to the varying light conditions (quantity
stomatal conductance and increased the intercellular CO2 and quality) include changes in the ratio of PSI and PSII units
concentration which indicates that B and P wavelengths can and inactivation of a subpopulation of PSII reaction centres
reduce the photosynthetic gas exchange of tomato leaves (Melis 1991); it is observed that plants grown under shade
(Yang F et al. 2018a). It is reported that light quality does conditions possess a higher PSII/PSI ratio to compensate
not affect when light intensities are too low as stomata hardly for the reduction in the amount of red light, which is required
open. It was found that low-intensity monochromatic blue
and red lights did not affect the stomatal opening of exposed
sunflower and tobacco leaf discs (Habermann 1973).
Normal light

4. Photosynthetic apparatus

Low light conditions change the photosynthetic apparatus

Low light
of plants by altering the levels of enzymes involved in
carbon-reduction cycle (Wang et al. 2013a), components
of electron transport (Yang F et al. 2018b), proteins (Li
T et al. 2014a), and light-harvesting pigments (Wherley
Low R:FR
et al. 2005) as shown in Fig. 2. It generally results in lower
photosynthetic rates, which is observed in different plant
species (Lichtenthaler et al. 1981; Sarijeva et al. 2007; Fv/Fm Fv´/Fm´ qp

Jiang et al. 2011; Li R et al. 2014; Muneer et al. 2014; Yang

Fig. 8 Chlorophyll fluorescence of the soybean leaves under a
F et al. 2018a). Lower photosynthetic capacity is always
variable light environment. Fv/Fm, the maximum photochemical
accompanied with lower quantity of electrons passing efficiency of PSII; Fv´/Fm´, actual photochemical efficiency; qp,
through PSII (Yao et al. 2017). Earlier findings suggest photochemical quenching. R:FR, red to far red ratio.
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 11

to excite PSII (Osmond et al. 1987). McCree 1971; Inada 1976). Wu et al. (2014) reported a
Over the years, different light conditions have been higher photosynthetic efficiency in tomato plants grown
considered to conduct the physiological studies of under green light in comparison to plants grown under
photosynthesis. A combination of red and blue LEDs with yellow light. Similarly, a better photosynthetic performance
varying light intensities and wavelengths is considered as was observed for sunflower leaves grown under green
an effective source for the photosynthesis (Lin et al. 2013). light mixed with strong white light in comparison to those
The grape cultivar “Italia”, when grown under red light, grown under red light alone (Terashima et al. 2009).
displayed the high net photosynthetic rate and the ratio of This is in line with the physical laws of light quanta, with
Fv/Fm in comparison to control (Wang et al. 2016). In line shorter wavelength photons possessing more energy and
with this, Sæbø et al. (1995), Shimizu et al. (2011) and therefore exciting chlorophylls to an unproductive singlet
Kobayashi et al. (2013) reported red light to be significant for state. Similarly, when lettuce plants were grown under
photosynthetic apparatus development as it might increase high-intensity (≥PPF 300) green LEDs, they showed
starch accumulation in various plant species through normal development like plants grown under fluorescent
inhibiting the translocation of photosynthates out of the lamp, which indicated the fact that green light at higher
leaves. However, Lactuca sativa plants grown under red intensity is available to the plants for morphogenesis and
LEDs showed lower rates of photosynthesis with a decrease photosynthesis while green light of low intensity might
in light intensity (Muneer et al. 2014). Similar results of the penetrate the leaf insufficiently for morphogenesis or
reduced rate of photosynthesis under low light intensity and photosynthesis (Johkan et al. 2012).
red LEDs have also been reported for rice (Matsuda et al.
2004) and wheat (Yano and Fujiwara 2012). Such results 5. Pigment composition
may suggest that vulnerability to a lower photosynthetic rate
might be linked with changes in multiprotein complexes (PSI Low light conditions or shade change the photosynthetic
and PSII) (Muneer et al. 2014; Hussain et al. 2019a). Such pigment composition of plants, i.e., chlorophyll (Chl a, Chl b,
results could also be attributed to lower leaf nitrogen content Chl a+b, and Chl a/b), which are important pigments involved
because of low chlorophyll and carotenoid content (Kim in absorbance, transmittance and conversion of solar energy
et al. 2004a). Yorio et al. (2001) reported that a blue light into electrochemical energy (Liu et al. 2014). Contrasting
supplementation in lettuce grown under red light resulted in views regarding the effect of low irradiance on chlorophyll
higher weight accumulation than that grown under red light content have been reported. Some studies claimed reduced
alone. Blue LEDs in combination with high light intensities chlorophyll contents under shading conditions (Wittmann
are reported to be efficient for biomass production in plants; et al. 2001; Zhu et al. 2017; Fan et al. 2018) (Fig. 9),
lettuce plants, when grown in blue LEDs and high light which is also a typical symptom of oxidative stress, it might
intensity, displayed higher net photosynthetic rate which either due to the photo-oxidation of chlorophyll, deficiency
is indicative of the fact that the plants had a pronounced of chlorophyll synthesis and/or chlorophyll degradation
acclimation of photosystems for CO2 fixation (Muneer (Smirnoff 1993). It has been reported that the modulation of
et al. 2014). A blue light supplementation also leads chlorophyll biosynthesis in response to low light conditions in
to the increased photosynthetic activity of Convallaria A. thaliana is usually regulated by an overall down-regulation
majalis and strawberry plants (Bukhov et al. 1995; Yoshida of genes involved in chlorophyll biosynthesis (McLaren and
et al. 2016). It is reported for spinach leaves that a blue Smith 1978) while to a lesser extent by up-regulation of
light deficiency can result in acclimations of light energy genes associated with chlorophyll degradation (Brouwer
partitioning in PSII and CO2 to high irradiance (Matsuda et al. 2014).
et al. 2008). Considering the effects of green light, the Chlorophyll might also decrease under conditions of
poor absorption of this wavelength by plant leaves is well continuous shading as previous studies confirmed that
explained through the absorption spectra of chlorophylls applying shade for a longer duration or completely providing
or other plant pigments extracted from green leaves the shading condition (i.e., 100% shade) did not lead to
(Terashima et al. 2009). The green wavelength is known the maximum total chlorophyll content (Tran 2018). In
to result in reduced plant photosynthesis (Sun et al. contrast, other researchers reported enhanced chlorophyll
1998) and have negative effects on plant physiology and production in response to lower PAR (Escoubas et al.
development (Folta and Maruhnich 2007). In contrast, 1995; Lichtenthaler and Buschmann 2001; Terashima et al.
earlier research also suggests that green light results in 2001; Sun et al. 2003; Terashima et al. 2005; Gregoriou
high photosynthetic efficiency provided that it is absorbed et al. 2007; Lichtenthaler et al. 2007; Evans et al. 2009;
by the leaves (Bjorkman 1968; Balegh and Biddulph 1970; Melgar et al. 2009), especially the contents of Chl b (Zhu
12 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

Low PAR
Shade tolerant
Chlorophyll genotypes
degradation
Deficiency of
Chlorophyll chlorophyll
photo oxidation synthesis
Chl Chl b
content ↓ content ↑

↓ Light interception ↑

Fig. 9 Contrasting effect of low irradiance on chlorophyll content. Upward and downward arrows refer to increase and decrease
respectively while the red color shows the importance of the parameters with respect to its function. PAR, photosynthetically
active radiations.

et al. 2008, 2017; Li R et al. 2014; Yang F et al. 2018b) C. sativus (Wang et al. 2009; Fan X et al. 2013).
the increase of which could lead to rise in light-interception
under shade stress (Pearcy and Seemann 1990). Zhu et al. 6. Reactive oxygen species (ROS)
(2008) reported that low light-tolerant hybrid rice exhibited a
higher content of Chl b when exposed to low light. Zhu et al. An important biochemical change that occurs in plants in
(2017) reported that purple pak-choi showed an increased response to oxidative stress is the production of reactive
-
Chl b content in the shade treatments at 5 d, however, with oxygen species (ROS) such as superoxide anion (O2 ·),
the extension of shading time (at 15 d), the relative content hydrogen peroxide (H2O2), hydroxyl radical (HO·) and
of chlorophyll decreased over time. It can be inferred that singlet oxygen (1O2) (Smirnoff 1993; Allen 1995; Vranová
chlorophyll content may tend to increase under shading et al. 2002; Apel and Hirt 2004; Miller et al. 2010; McCarthy-
conditions to enhance light harvesting in shade-tolerant Suárez et al. 2011). Low light or shade conditions induce
varieties (Valladares and Niinemets 2008). oxidative stress in plants which increases ROS production
Similar to light intensity, different light spectra also affect and causes lipid peroxidation. The production of ROS under
the plant pigment content. A low R:FR ratio is observed low light intensities or shade stress leads to an increased
to result in decreased foliar chlorophyll content per unit level of photorespiration and enhances the activity of
area in various species such as Citrus insitorum, Solanum mitochondrial electron-transport-chain (mETC) (Blokhina
tuberosum, Trifolium repens, Solanum lycopersican, and et al. 2003; Lawlor and Tezara 2009). Zhu et al. (2017)
Cucumis sativus (Tucker 1981; Thiele et al. 1999; Heraut- observed an increased production of malondialdehyde
Bron et al. 2000; Schittenhelm et al. 2004; Distefano et al. content under low light stress in purple pak-choi
2013). However, tomato plants grown under red light had (B. campestris ssp. Chinensis makino). Similarly, analyses
higher contents of Chl a, b and carotenoid (Yang F et al. of membrane lipid peroxidation in peach fruit showed that
2018a). Similarly, D. versipellis plants grown under red decreasing the light intensity increased the malondialdehyde
colored plastic film had the maximum chlorophyll content (MDA) content with more cell membrane damage (Apel and
(He et al. 2018). Grape cultivars when grown under Hirt 2004; Volkov et al. 2006). Under the conditions of light
supplemental red light also had high chlorophyll content intensities that exceed plant’s photosynthetic capacity when
and Chl a/b ratio (Wang et al. 2016). In contrast, Fan X photosynthesis is unable to utilize all the absorbed energy,
et al. (2013) reported that red light was not conducive for the chloroplast lumen turns acidic, reduces the electron
the synthesis of chlorophyll. Mizuno et al. (2009) found a transport chain, and excitation energy gathers within the
high chlorophyll content in cabbage grown under blue light. chloroplast which could lead to the production of singlet and
Similar results were reported in birch plantlets in vitro (Sæbø triplet forms of chlorophyll and singlet oxygen that are toxic
et al. 1995) and in lettuce and spinach plants (Tibbitts et al. (Ali et al. 2005). The excess excitation energy depletes the
1983) where the highest chlorophyll content was observed NADP+ pool that increases the rate of electron flow from
in blue-light sources compared to red-light sources. Plants the donor side of PSI to oxygen, thereby generating ROS
grown under yellow film resulted in decreased chlorophyll such as superoxide and hydrogen peroxide (Asada 1999).
content (He et al. 2018). Similar effects for yellow light Ivanov et al. (2012) reported an increase in both superoxides
treatment have been reported in Brassica campestris L. and radical and hydrogen peroxide (H2O2) production by the
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 13

photosynthetic electron-transport chain under conditions of between their production and removal which is compatible
high light intensities. The main source of ROS generation in with the optimum functioning of photosynthesis (Foyer
plants is chloroplast (Asada 2000). Since ROS are highly 2018). The increases in the antioxidant defense system
reactive, in the absence of any protective mechanism, under conditions of low irradiances have been well reported
ROS can cause potential damage to cellular and molecular in several studies (Esterbauer and Grill 1978; Anderson
machinery, protein modification and lipid peroxidation, thus et al. 1992; Polle and Rennenberg 1992; Doulis et al. 1993;
disrupting the normal metabolism of the plants leading to Verhoeven et al. 2005) (Fig. 10). Ascorbate-Glutathione
severe yield losses (Ahmed et al. 2009). However, recent pathway (also known as Asada-Halliwell pathway) is the
research has also recognized a positive role of ROS as major pathway of antioxidant defense that mainly detoxifies
essential pro-life signals (Noctor and Foyer 2016; Foyer the H2O2 in the plant cell. Within the antioxidant defencse
et al. 2017). The ROS production is considered essential for system, the AsA-GSH (ascorbate and glutathione) pool
redox sensing, signaling and regulation in the photosynthetic plays the immediate role of minimizing stress effect
cells (Foyer 2018). through scavenging ROS using four key enzymes, e.g.,
Light quality also affects ROS production. Camptotheca ascorbate peroxidase (APX), monodehydroascorbate
acuminata seedlings grown under blue and yellow light reductase (MDHAR), dehydroascorbate reductase (DHAR),
suffered from oxidative damage to lipid membranes due and glutathione reductase (GR) (Latowski et al. 2010;
to higher contents of O2-·, H2O2 and MDA while red light Hasanuzzaman et al. 2011, 2012). Usually, the pathway
reduced the O2-· production rate and H2O2 content as involves SOD giving the frontline protection against ROS
compared to white light (Yu et al. 2017). by converting O2-· to H2O2. Afterward, CAT and APX
scavenge H2O2 to H2O. Glutathione peroxidase and GST
7. Antioxidant enzymes (glutathione S-transferase) also scavenge H2O2 to H2O
with the help of glutathione (GSH) (Hasanuzzaman et al.
Plants produce an elaborate arsenal of antioxidant enzymes 2011). Ghasemzadeh et al. (2010) reported that a lower
such as superoxide dismutase (SOD), POD, catalase (CAT), light intensity of 310 μmol m−2 s−1 enhanced the antioxidant
ascorbate peroxidase (APX), etc., in response to oxidative activity of ginger by increasing total flavonoid content.
stress to not only interrupt the cascades of uncontrolled Similarly, a higher activity of antioxidant enzymes, i.e., SOD,
oxidation by ROS but rather maintain an appropriate balance POD, CAT, and APX was observed in callus culture of the

Generation of
ROS
OH .
1
O2
iss
We
er tion
absorption

b Fenton
Energy

Ha reac reaction
Normal conditions
e– e– + 2H+
O2 O2–· H2O2
SOD
Equilibrium
AOX ROS
Scavenging
and
AOX production ROS

Shade s
tress

AOX

ROS
Antioxidants

Oxidants

Fig. 10 Shade causes oxidative stress. AOX and ROS, antioxidants and reactive oxygen species, respectively.
14 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

olive cult. Arbosana kept in dark conditions (Mohammad Among the endogenous plant hormones, gibberellins (GAs)
et al. 2019). Zhu et al. (2017) found that antioxidant and auxin (indole-3-acetic acid (IAA)) regulate the shade-
activities of guaiacol POD, CAT and SOD increased in the induced differential growth and elongation (Kurepin et al.
shade treatments at 5 d, however, with the extension of 2007a; Lucas and Prat 2014; Yang and Li 2017). When
shading time (at 15 d), the activity of antioxidants decreased plants grow near neighboring vegetation, they perceive
considerably. The increase in antioxidant activity under reductions in R:FR which serves as an early warning
low light intensities might be attributed to reduced leaf signal to the plants and promotes the escape responses
temperature because of the shade as earlier studies proved before the occurrence of shade (Ballaré et al. 1990). A
that low temperature raise the antioxidant activities in plants low R:FR inactivates the phytochromes, stabilizes and
to cope with the negative effects of low temperature (Guy activates the transcription factors called the phytochrome-
and Carter 1984; Adams III and Demmig-Adams 1994; interacting factors (PIFs). The PIF4, PIF5 and PIF7 act in
Burkle and Logan 2003; Lohrmann et al. 2004; Logan et al. collaboration to promote the auxin biosynthesis and result in
2006). However, contrasting views have also been reported stem elongation (Lorrain et al. 2008; Li et al. 2012). Under
by Grace and Logan (1996), Logan et al. (1996, 1998a, conditions of true shade, plants also experience reduced
b), Apel and Hirt (2004), and Callejón-Ferre et al. (2009). levels of blue light which together with low R:FR promote
Apel and Hirt (2004) and Volkov et al. (2006) reported that hypocotyl elongation and phototropic curvature to facilitate
decreasing the light intensity decreased CAT, G-POD and shade escape (Franklin 2016). Earlier findings suggest
APX activity in peach fruit. that a lateral blue light enhances the auxin accumulation on
Similar to light intensity, the effects of variable light the shaded sides of the plant stem that causes the cells to
wavelengths on antioxidant enzymes production in plants elongate more in comparison to the cells on the illuminated
are complex and are most often reported with contrasting side, thus leading to stem curvature (Goyal et al. 2013).
results (Yu et al. 2017). For example, earlier studies In Arabidopsis seedlings, apart from auxin, gibberellic
suggest that a low-energy red light increases the activity of acid and brassinosteroids have also been documented to
antioxidant enzymes as well as the content of low molecular regulate hypocotyl elongation (de Wit et al. 2014; Nozue
weight antioxidants, i.e., carotenoids and UV-absorbing et al. 2015), gibberellic acid and jasmonic acid to regulate
pigments in spinach (Kreslavskii et al. 2012). A short-term petiole elongation (Nozue et al. 2015), abscisic acid to
red light (500 mW cm−2 s−1) was observed to increase the regulate auxiliary bud growth (Reddy et al. 2013) while
peroxidase activity in maize by 50–70% when measured changes in auxin and ethylene levels might restrict root
1 d after exposure (Sharma et al. 1976). The stimulation growth (Růžička et al. 2007; Stepanova et al. 2007). An
of peroxidase activity and another antioxidant in response increase in the auxin to cytokinin ratio in leaf meristem of
to red light could be due to higher transcriptional levels of Arabidopsis exposed to shade inhibits the leaf development
the genes encoding for peroxidase and other enzymes (Carabelli et al. 2007). While lower values of PAR have been
(Kreslavski et al. 2013). Similarly, red and far-infrared reported to promote growth and increase the GA levels in the
light wavelengths were found effectively for the antioxidant hypocotyls and leaves of sunflower (Kurepin et al. 2007b),
activity in pea seedlings and rice hulls (Lee et al. 2003; internodes of bean plants (Beall et al. 1996) and in the
Wu et al. 2007). In contrast, SOD, POD and CAT did not shoots of Arabidopsis (Kurepin et al. 2012). Similarly, shade
increase under red light-grown C. acuminata seedlings significantly increased the IAA and gibberellin contents
rather higher antioxidants were recorded for seedlings while significantly decreased the cytokinin content in young,
grown under blue and yellow lights (Yu et al. 2017). A middle and old leaves of soybean (Wu Y et al. 2017).
blue light supplementation resulted in higher ascorbate To counteract shading, some plants evolve shade
peroxidase activity (APX) in the detached oat leaves tolerance strategies that enable them to survive and
(Mastropasqua et al. 2012). Similar results were recorded reproduce at low light intensities (Gommers et al. 2013) while
in Kalanchoe pinnata by Nascimento et al. (2013). Such other species compete for light, using an escape strategy
results suggest that different light spectra evoke different termed shade avoidance (Casal 2012). Plants initiate shade
antioxidant responses depending on the plant species and avoidance responses (SARs) which are a set of responses
that investigation of suitable light quality is essential for that plants display upon exposure to encroach vegetation
maximal biomass production. (Yang C et al. 2018). It is a complex phenomenon that
involves the modulation of transcriptional and metabolic
8. Hormones networks that favour elongation at the expense of leaf
development and increase apical dominance, thereby
The hormones regulate light dependent changes in plant allowing young and growing tissues to escape from shade
morphogenesis (Islam et al. 2014; Kissoudis et al. 2017). (Franklin 2008; Keuskamp et al. 2010; Casal 2012).
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 15

Moreover, SAR is an important phenomenon in crops oxidative stress, and signal transduction. Annual Review
growing in dense canopies (Boomsma et al. 2009; Carriedo of Plant Biology, 55, 373–399.
et al. 2016). Appelgren M. 1991. Effects of light quality on stem elongation
of Pelargonium in vitro. Scientia Horticulturae, 45, 345–351.
Asada K. 1999. The water-water cycle in chloroplasts:
9. Conclusion/Future prospective
Scavenging of active oxygens and dissipation of excess
photons. Annual Review of Plant Biology, 50, 601–639.
Redesigning photosynthesis for agronomic and horticultural
Asada K. 2000. The water-water cycle as alternative photon
crops through manipulation of slight shade could be
and electron sinks. Philosophical Transactions of the Royal
helpful to reduce the drastic effect of shade stress. Light Society of London (Series B: Biological Sciences), 355,
intensity and quality change the structure and functions of 1419–1431.
photosynthetic apparatus through certain signalling ways Assmann S. 1992. Effects of light quantity and quality during
including phytohormones and biochemical changes (ROS). development on the morphology and stomatal physiology
The role of subcellular protein organizations and protein of Commelina communis. Oecologia, 92, 188–195.
phosphorylation changes under different light spectra needs Balegh S, Biddulph O. 1970. The photosynthetic action
exploration to address the light intensity and quality dilemma. spectrum of the bean plant. Plant Physiology, 46,1–5.
Ballaré C L, Pierik R. 2017. The shade-avoidance syndrome:
Multiple signals and ecological consequences. Plant, Cell
Acknowledgements
& Environment, 40, 2530–2543.
Ballaré C L, Scopel A L, Sánchez R A. 1990. Far-red
The research was supported by the National Natural Science
radiation reflected from adjacent leaves: An early signal
Foundation of China (31571615) and the earmarked fund of competition in plant canopies. Science, 247, 329–332.
for China Agriculture Research System (CARS-04-PS19). Barreiro R, Guiamét J J, Beltrano J, Montaldi E R. 1992.
Regulation of the photosynthetic capacity of primary bean
References leaves by the red:far-red ratio and photosynthetic photon
flux density of incident light. Physiologia Plantarum, 85,
Adams III W W, Demmig-Adams B. 1994. Carotenoid 97–101.
composition and down regulation of photosystem II in three Beall F D, Yeung E C, Pharis R P. 1996. Far-red light stimulates
conifer species during the winter. Physiologia Plantarum, internode elongation, cell division, cell elongation, and
92, 451–458. gibberellin levels in bean. Canadian Journal of Botany,
Ahmed C B, Rouina B B, Sensoy S, Boukhris M, Abdallah F 74, 743–752.
B. 2009. Changes in gas exchange, proline accumulation Bertel C, Schönswetter P, Frajman B, Holzinger A, Neuner G.
and antioxidative enzyme activities in three olive cultivars 2017. Leaf anatomy of two reciprocally non-monophyletic
under contrasting water availability regimes. Environmental mountain plants (Heliosperma spp.): Does heritable
and Experimental Botany, 67, 345–352. adaptation to divergent growing sites accompany the onset
Ajmi A, Vázquez S, Morales F, Chaari A, El-Jendoubi H, of speciation? Protoplasma, 254, 1411–1420.
Abadía A, Larbi A. 2018. Prolonged artificial shade Bjorkman O. 1968. Further studies on differentiation of
affects morphological, anatomical, biochemical and photosynthetic properties in sun and shade ecotypes of
ecophysiological behavior of young olive trees (cv. ”Solidago virgaurea”. Physiologia Plantarum, 21, 84–99.
Arbosana). Scientia Horticulturae, 241, 275–284. Blokhina O, Virolainen E, Fagerstedt K V. 2003. Antioxidants,
Ali M B, Hahn E J, Paek K Y. 2005. Effects of light intensities oxidative damage and oxygen deprivation stress: A review.
on antioxidant enzymes and malondialdehyde content Annals of Botany, 91, 179–194.
during short-term acclimatization on micropropagated Boardman N. 1977. Comparative photosynthesis of sun and
Phalaenopsis plantlet. Environmental and Experimental shade plants. Annual Review of Plant Physiology, 28,
Botany, 54, 109–120. 355–377.
Allen R D. 1995. Dissection of oxidative stress tolerance using Boccalandro H E, Ploschuk E L, Yanovsky M J, Sánchez R
transgenic plants. Plant Physiology, 107, 1049. A, Gatz C, Casal J J. 2003. Increased phytochrome B
Anderson J M, Chow W S, Park Y I. 1995. The grand design of alleviates density effects on tuber yield of field potato crops.
photosynthesis: Acclimation of the photosynthetic apparatus Plant Physiology, 133, 1539–1546.
to environmental cues. Photosynthesis Research, 46, Boomsma C R, Santini J B, Tollenaar M, Vyn T J. 2009. Maize
129–139. morphophysiological responses to intense crowding and
Anderson J V, Chevone B I, Hess J L. 1992. Seasonal variation low nitrogen availability: An analysis and review. Agronomy
in the antioxidant system of eastern white pine needles: Journal, 101, 1426–1452.
Evidence for thermal dependence. Plant Physiology, 98, Brouwer B, Gardeström P, Keech O. 2014. In response to
501–508. partial plant shading, the lack of phytochrome A does not
Apel K, Hirt H. 2004. Reactive oxygen species: Metabolism, directly induce leaf senescence but alters the fine-tuning of
16 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

chlorophyll biosynthesis. Journal of Experimental Botany, and glutathione reductase in needles of Picea abies. Plant
65, 4037–4049. Physiology, 61, 119–121.
Bukhov N, Drozdova I, Bondar V. 1995. Light response curves Evans J R, Kaldenhoff R, Genty B, Terashima I. 2009.
of photosynthesis in leaves of sun-type and shade-type Resistances along the CO2 diffusion pathway inside leaves.
plants grown in blue or red light. Journal of Photochemistry Journal of Experimental Botany, 60, 2235–2248.
and Photobiology (B: Biology), 30, 39–41. Fan X, Zang J, Xu Z, Guo S, Jiao X, Liu X, Gao Y. 2013.
Burkle L A, Logan B A. 2003. Seasonal acclimation of Effects of different light quality on growth, chlorophyll
photosynthesis in eastern Hemlock and Partridgeberry in concentration and chlorophyll biosynthesis precursors of
different light environments. Northeastern Naturalist, 10, non-heading Chinese cabbage (Brassica campestris L.).
1–17. Acta Physiologiae Plantarum, 35, 2721–2726.
Callejón-Ferre A, Manzano-Agugliaro F, Díaz-Pérez M, Fan X X, Xu Z G, Liu X Y, Tang C M, Wang L W, Han X l. 2013.
Carreño-Ortega A, Pérez-Alonso J. 2009. Effect of shading Effects of light intensity on the growth and leaf development
with aluminised screens on fruit production and quality of young tomato plants grown under a combination of red
in tomato (Solanum lycopersicum L.) under greenhouse and blue light. Scientia Horticulturae, 153, 50–55.
conditions. Spanish Journal of Agricultural Research, 7, Fan Y, Chen J, Cheng Y, Raza M A, Wu X, Wang Z, Liu Q,
41–49. Wang R, Wang X, Yong T. 2018. Effect of shading and light
Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, recovery on the growth, leaf structure, and photosynthetic
Ruberti I. 2007. Canopy shade causes a rapid and transient performance of soybean in a maize-soybean relay-strip
arrest in leaf development through auxin-induced cytokinin intercropping system. PLoS ONE, 13, e198159.
oxidase activity. Genes & Development, 21,1863–1868. Folta K M. 2004. Green light stimulates early stem elongation,
Carriedo L G, Maloof J N, Brady S M. 2016. Molecular control antagonizing light-mediated growth inhibition. Plant
of crop shade avoidance. Current Opinion in Plant Biology, Physiology, 135, 1407–1416.
30, 151–158. Folta K M, Maruhnich S A. 2007. Green light: A signal to
Casal J J. 2012. Shade avoidance. The Arabidopsis Book/ slow down or stop. Journal of Experimental Botany, 58,
American Society of Plant Biologists, 10, e0157. 3099–3111.
Chang S X, Li C X, Yao X Y, Chen S, Jiao X L, Liu X Y, Xu Foyer C H. 2018. Reactive oxygen species, oxidative signaling
Z G, Guan R Z. 2016. Morphological, photosynthetic, and the regulation of photosynthesis. Environmental and
and physiological responses of rapeseed leaf to different Experimental Botany, 154, 134–142.
combinations of red and blue lights at the rosette stage. Foyer C H, Ruban A V, Noctor G. 2017. Viewing oxidative stress
Frontiers in Plant Science, 7, 1144. through the lens of oxidative signalling rather than damage.
Chen Z H, Hills A, Lim C K, Blatt M R. 2010. Dynamic Portland Press Limited, 474, 877–833.
regulation of guard cell anion channels by cytosolic free Franklin K A. 2008. Shade avoidance. New Phytologist, 179,
Ca2+ concentration and protein phosphorylation. The Plant 930–944.
Journal, 61, 816–825. Franklin K A. 2016. Photomorphogenesis: Plants feel blue in
Cui H, Jin L, Li B, Zhang J, Zhao B, Dong S, Liu P. 2012. Effects the shade. Current Biology, 26, R1275–R1276.
of shading on stalks morphology, structure and lodging Frechilla S, Talbott L D, Bogomolni R A, Zeiger E. 2000.
of summer maize in field. Scientia Agricultura Sinica, 45, Reversal of blue light-stimulated stomatal opening by green
3497–3505. (in Chinese) light. Plant and Cell Physiology, 41, 71–176.
Distefano G, Cirilli M, Las Casas G, La Malfa S, Continella A, Gay A, Hurd R. 1975. The influence of light on stomatal density
Rugini E, Thomas B, Long G, Gentile A, Muleo R. 2013. in the tomato. New Phytologist, 75, 37–46.
Ectopic expression of Arabidopsis phytochrome B in Troyer Ghasemzadeh A, Jaafar H Z, Rahmat A, Wahab P E M,
citrange affects photosynthesis and plant morphology. Halim M R A. 2010. Effect of different light intensities on
Scientia Horticulturae, 159, 1–7. total phenolics and flavonoids synthesis and anti-oxidant
Doulis A, Hausladen A, Mondy B, Alscher R, Chevone B, activities in young ginger varieties (Zingiber officinale
Hess J, Weiser R. 1993. Antioxidant response and winter Roscoe). International Journal of Molecular Sciences, 11,
hardiness in red spruce (Picea rubens Sarg.). New 3885–3897.
Phytologist, 123, 365–374. Glick B R. 2014. Bacteria with ACC deaminase can promote
Duysens L, Amesz J. 1962. Function and identification of two plant growth and help to feed the world. Microbiological
photochemical systems in photosynthesis. Biochimica et Research, 169, 30–39.
Biophysica Acta, 64, 243–260. Głowacka B. 2004. The effect of blue light on the height
Escoubas J M, Lomas M, LaRoche J, Falkowski P G. 1995. Light and habit of the tomato (Lycopersicon esculentum Mill.)
intensity regulation of cab gene transcription is signaled by transplant. Folia Horticulturae, 16, 3–10.
the redox state of the plastoquinone pool. Proceedings of Gommers C M, Visser E J, St Onge K R, Voesenek L A, Pierik R.
the National Academy of Sciences of the United States of 2013. Shade tolerance: When growing tall is not an option.
America, 92, 10237–10241. Trends in Plant Science, 18, 65–71.
Esterbauer H, Grill D. 1978. Seasonal variation of glutathione Gong W, Jiang C, Wu Y, Chen H, Liu W, Yang W. 2015.
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 17

Tolerance vs. avoidance: Two strategies of soybean (Glycine of colored plastic films on the photosynthetic characteristics
max) seedlings in response to shade in intercropping. and content of active ingredients of Dysosma versipellis.
Photosynthetica, 53, 259–268. Horticulture, Environment, and Biotechnology, 59, 519–528.
Gong W, Qi P, Du J, Sun X, Wu X, Song C, Liu W, Wu Y, Yu Heo J, Lee C, Chakrabarty D, Paek K. 2002. Growth
X, Yong T. 2014. Transcriptome analysis of shade-induced responses of marigold and salvia bedding plants as
inhibition on leaf size in relay intercropped soybean. PLoS affected by monochromic or mixture radiation provided by
ONE, 9, e98465. a light-emitting diode (LED). Plant Growth Regulation, 38,
Gould K S, Dudle D A, Neufeld H S. 2010. Why some stems 225–230.
are red: Cauline anthocyanins shield photosystem II Heraut-Bron V, Robin C, Varlet-Grancher C, Afif D, Guckert
against high light stress. Journal of Experimental Botany, A. 2000. Light quality (red:far-red ratio): Does it affect
61, 2707–2717. photosynthetic activity, net CO2 assimilation, and morphology
Goyal A, Szarzynska B, Fankhauser C. 2013. Phototropism: At of young white clover leaves? Canadian Journal of Botany,
the crossroads of light-signaling pathways. Trends in Plant 77, 1425–1431.
Science, 18, 393–401. Hill R, Bendall F. 1960. Function of the two cytochrome
Grace S C, Logan B A. 1996. Acclimation of foliar antioxidant components in chloroplasts: A working hypothesis. Nature,
systems to growth irradiance in three broad-leaved 186, 136–137.
evergreen species. Plant Physiology, 112, 1631–1640. Huang W, Zhang S B, Liu T. 2018. Moderate photoinhibition
Granado-Yela C, García-Verdugo C, Carrillo K, Rubio de Casas of photosystem II significantly affects linear electron flow in
R, Kleczkowski L A, Balaguer L. 2011. Temporal matching the shade-demanding plant Panax notoginseng. Frontiers
among diurnal photosynthetic patterns within the crown of in Plant Science, 9, 637.
the evergreen sclerophyll Olea europaea L. Plant, Cell & Hussain S, Iqbal N, Brestic M, Raza M A, Pang T, Langham D
Environment, 34, 800–810. R, Safdar M E, Ahmed S, Wen B, Gao Y. 2019a. Changes
Green-Tracewicz E, Page E R, Swanton C J. 2011. Shade in morphology, chlorophyll fluorescence performance and
avoidance in soybean reduces branching and increases Rubisco activity of soybean in response to foliar application
plant-to-plant variability in biomass and yield per plant. of ionic titanium under normal light and shade environment.
Weed Science, 59, 43–49. Science of the Total Environment, 658, 626–637.
Gregoriou K, Pontikis K, Vemmos S. 2007. Effects of reduced Hussain S, Iqbal N, Rahman T, Ting L, Brestic M, Safdar M
irradiance on leaf morphology, photosynthetic capacity, E, Asghar M A, Farooq M U, Shafiq I, Ali A. 2019b. Shade
and fruit yield in olive (Olea europaea L.). Photosynthetica, effect on carbohydrates dynamics and stem strength of
45, 172–181. soybean genotypes. Environmental and Experimental
Guy C, Carter J V. 1984. Characterization of partially purified Botany, 162, 374–382.
glutathione reductase from cold-hardened and nonhardened Hussain S, Iqbal N, Raza M A, Khan M N, Ahmed S, Rahman
spinach leaf tissue. Cryobiology, 21, 454–464. T, Chen P, Wang X, Du X, Liu W, Yang W. 2019c.
Habermann H M. 1973. Evidence for two photoreactions and Distribution and effects of ionic titanium application on
possible involvement of phytochrome in light-dependent energy partitioning and quantum yield of soybean under
stomatal opening. Plant Physiology, 51, 543–548. different light conditions. Photosynthetica, 57, 572–580.
Han S, Chen S, Song A, Liu R, Li H, Jiang J, Chen F. 2017. Hussain S, Iqbal N, Ting P, Khan M N, Liu W, Yang W. 2019d.
Photosynthetic responses of Chrysanthemum morifolium Weak stem under shade reveals the lignin reduction
to growth irradiance: Morphology, anatomy and chloroplast behavior. Journal of Integrative Agriculture, 18, 496–505.
ultrastructure. Photosynthetica, 55, 184–192. Hussain S, Ting L, Nasir I, Brestic M, Ting P, Mumtaz M,
Hasanuzzaman M, Hossain M A, Fujita M. 2011. Nitric oxide Shafiq I, Li S, Wang L, Yang G. 2020. Effects of lignin,
modulates antioxidant defense and the methylglyoxal cellulose, hemicellulose, sucrose and monosaccharaides
detoxification system and reduces salinity-induced damage carbohydrates on soybean physical stem strength and yield
of wheat seedlings. Plant Biotechnology Reports, 5, 353. in intercropping. Photochemical & Photobiological Sciences,
Hasanuzzaman M, Hossain M A, Fujita M. 2012. Exogenous 19, 462–472.
selenium pretreatment protects rapeseed seedlings Inada K. 1976. Action spectra for photosynthesis in higher
from cadmium-induced oxidative stress by upregulating plants. Plant and Cell Physiology, 17, 355–365.
antioxidant defense and methylglyoxal detoxification Islam M A, Tarkowská D, Clarke J L, Blystad D R, Gislerød H
systems. Biological Trace Element Research, 149, R, Torre S, Olsen J E. 2014. Impact of end-of-day red and
248–261. far-red light on plant morphology and hormone physiology
Hattori T, Sonobe K, Inanaga S, An P, Tsuji W, Araki H, Eneji of poinsettia. Scientia Horticulturae, 174, 77–86.
A E, Morita S. 2007. Short term stomatal responses to Ivanov A G, Rosso D, Savitch L V, Stachula P, Rosembert
light intensity changes and osmotic stress in sorghum M, Oquist G, Hurry V, Hüner N P. 2012. Implications of
seedlings raised with and without silicon. Environmental alternative electron sinks in increased resistance of PSII and
and Experimental Botany, 60, 177–182. PSI photochemistry to high light stress in cold-acclimated
He B, Chen Y, Zhang H, Xia C, Zhang Q, Li W. 2018. The effect Arabidopsis thaliana. Photosynthesis Research, 113,
18 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

191–206. Kobayashi K, Amore T, Lazaro M. 2013. Light-emitting diodes

Jansen M A, Mattoo A K, Edelman M. 1999. D1-D2 protein (LEDs) for miniature hydroponic lettuce. Optics and
degradation in the chloroplast: Complex light saturation Photonics Journal, 3, 74.
kinetics. European Journal of Biochemistry, 260, 527–532. Koyama K, Ikeda H, Poudel P R, Goto-Yamamoto N. 2012.
Jiang C D, Wang X, Gao H Y, Shi L, Chow W S. 2011. Systemic Light quality affects flavonoid biosynthesis in young berries
regulation of leaf anatomical structure, photosynthetic of Cabernet Sauvignon grape. Phytochemistry, 78, 54–64.
performance, and high-light tolerance in sorghum. Plant Kozuka T, Horiguchi G, Kim G T, Ohgishi M, Sakai T, Tsukaya
physiology, 155, 1416–1424. H. 2005. The different growth responses of the Arabidopsis
Johkan M, Shoji K, Goto F, Hahida S N, Yoshihara T. thaliana leaf blade and the petiole during shade avoidance
2012. Effect of green light wavelength and intensity on are regulated by photoreceptors and sugar. Plant and Cell
photomorphogenesis and photosynthesis in Lactuca sativa. Physiology, 46, 213–223.
Environmental and Experimental Botany, 75, 128–133. Kreslavski V D, Shirshikova G N, Lyubimov V Y, Shmarev A N,
Johkan M, Shoji K, Goto F, Hashida S, Yoshihara T. 2010. Blue Boutanaev A M, Kosobryukhov A A, Schmitt F J, Friedrich
light-emitting diode light irradiation of seedlings improves T, Allakhverdiev S I. 2013. Effect of preillumination with red
seedling quality and growth after transplanting in red leaf light on photosynthetic parameters and oxidant-/antioxidant
lettuce. HortScience, 45, 1809–1814. balance in Arabidopsis thaliana in response to UV-A.
Kalve S, Fotschki J, Beeckman T, Vissenberg K, Beemster G Journal of Photochemistry and Photobiology (B: Biology),
T. 2014. Three-dimensional patterns of cell division and 127, 229–236.
expansion throughout the development of Arabidopsis Kreslavskii V, Khristin M, Shabnova N, Lyubimov V Y. 2012.
thaliana leaves. Journal of Experimental Botany, 5, Preillumination of excised spinach leaves with red light
6385–6397. increases resistance of photosynthetic apparatus to UV
Kang C Y, Lian H L, Wang F F, Huang J R, Yang H Q. 2009. radiation. Russian Journal of Plant Physiology, 59, 717–723.
Cryptochromes, phytochromes, and COP1 regulate light- Kurepin L V, Emery R N, Pharis R P, Reid D M. 2007a. The
controlled stomatal development in Arabidopsis. The Plant interaction of light quality and irradiance with gibberellins,
Cell, 21, 2624–2641. cytokinins and auxin in regulating growth of Helianthus
Kardiman R, Ræbild A. 2017. Relationship between stomatal annuus hypocotyls. Plant, Cell & Environment, 30, 147–155.
density, size and speed of opening in Sumatran rainforest Kurepin L V, Emery R N, Pharis R P, Reid D M. 2007b.
species. Tree Physiology, 38, 696–705. Uncoupling light quality from light irradiance effects in
Keren N, Berg A, Van Kan P J, Levanon H, Ohad I. 1997. Helianthus annuus shoots: Putative roles for plant hormones
Mechanism of photosystem II photoinactivation and D1 in leaf and internode growth. Journal of Experimental
protein degradation at low light: The role of back electron Botany, 58, 2145–2157.
flow. Proceedings of the National Academy of Sciences of Kurepin L V, Walton L J, Hayward A, Emery R N, Pharis R
the United States of America, 94, 1579–1584. P, Reid D M. 2012. Interactions between plant hormones
Keuskamp D H, Sasidharan R, Pierik R. 2010. Physiological and light quality signaling in regulating the shoot growth
regulation and functional significance of shade avoidance of Arabidopsis thaliana seedlings. Botany, 90, 237–246.
responses to neighbors. Plant Signaling & Behavior, 5, Latowski D, Surówka E, Strzałka K. 2010. Regulatory role of
655–662. components of ascorbate-glutathione pathway in plant
Kim G T, Yano S, Kozuka T, Tsukaya H. 2005. stress tolerance. In: Anjum N, Chan M T, Umar S, eds.,
Photomorphogenesis of leaves: Shade-avoidance and Ascorbate-Glutathione Pathway and Stress Tolerance in
differentiation of sun and shade leaves. Photochemical & Plants. Springer, Dordrecht. pp. 1–53.
Photobiological Sciences, 4, 770–774. Lawlor D W, Tezara W. 2009. Causes of decreased
Kim H H, Goins G D, Wheeler R M, Sager J C. 2004a. Green- photosynthetic rate and metabolic capacity in water-
light supplementation for enhanced lettuce growth under deficient leaf cells: A critical evaluation of mechanisms and
red-and blue-light-emitting diodes. HortScience, 39, integration of processes. Annals of Botany, 103, 561–579.
1617–1622. Lawson T, von Caemmerer S, Baroli I. 2010. Photosynthesis
Kim H H, Goins G D, Wheeler R M, Sager J C. 2004b. Stomatal and stomatal behaviour. In: Progress in Botany 72. Springer,
conductance of lettuce grown under or exposed to different Berlin, Heidelberg. pp. 265–304.
light qualities. Annals of Botany, 94, 691–697. Lee S C, Kim J H, Jeong S M, Kim D R, Ha J U, Nam K, Ahn
Kissoudis C, Seifi A, Yan Z, Islam A T M T, van der Schoot H, D. 2003. Effect of far-infrared radiation on the antioxidant
van de Wiel C, Visser R G, van der Linden C G, Bai Y. 2017. activity of rice hulls. Journal of Agricultural and Food
Ethylene and abscisic acid signaling pathways differentially Chemistry, 51, 4400–4403.
influence tomato resistance to combined powdery mildew Li L, Ljung K, Breton G, Schmitz R J, Pruneda-Paz J, Cowing-
and salt stress. Frontiers in Plant Science, 7, 2009. Zitron C, Cole B J, Ivans L J, Pedmale U V, Jung H S.
Knapp A K, Smith W K. 1990. Stomatal and photosynthetic 2012. Linking photoreceptor excitation to changes in plant
responses to variable sunlight. Physiologia Plantarum, 78, architecture. Genes & Development, 26, 785–790.
160–165. Li R, Wen T, Tang Y, Sun X, Xia C. 2014. Effect of shading on
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 19

photosynthetic and chlorophyll fluorescence characteristics Logan B A, Grace S C, Adams III W W, Demmig-Adams
of soybean. Acta Prataculturae Sinica, 23, 198–206. (in B. 1998b. Seasonal differences in xanthophyll cycle
Chinese) characteristics and antioxidants in Mahonia repens growing
Li T, Heuvelink E, Dueck T, Janse J, Gort G, Marcelis L. 2014. in different light environments. Oecologia, 116, 9–17.
Enhancement of crop photosynthesis by diffuse light: Logan B A, Kornyeyev D, Hardison J, Holaday A S. 2006.
Quantifying the contributing factors. Annals of Botany, The role of antioxidant enzymes in photoprotection.
114, 145–156. Photosynthesis Research, 88, 119–132.
Li X, Yang Y, Yao J, Chen G, Li X, Zhang Q, Wu C. Lohrmann N L, Logan B A, Johnson A S. 2004. Seasonal
2009. FLEXIBLE CULM 1 encoding a cinnamyl-alcohol acclimatization of antioxidants and photosynthesis in
dehydrogenase controls culm mechanical strength in rice. Chondrus crispus and Mastocarpus stellatus, two co-
Plant Molecular Biology, 69, 685–697. occurring red algae with differing stress tolerances. The
Lichtenthaler H, Buschmann C, Döll M, Fietz H J, Bach T, Kozel Biological Bulletin, 207, 225–232.
U, Meier D, Rahmsdorf U. 1981. Photosynthetic activity, Long S P, Humphries S, Falkowski P G. 1994. Photoinhibition
chloroplast ultrastructure, and leaf characteristics of high- of photosynthesis in nature. Annual Review of Plant Biology,
light and low-light plants and of sun and shade leaves. 45, 633–662.
Photosynthesis Research, 2, 115–141. Lorrain S, Allen T, Duek P D, Whitelam G C, Fankhauser
Lichtenthaler H K, Ač A, Marek M V, Kalina J, Urban O. C. 2008. Phytochrome-mediated inhibition of shade
2007. Differences in pigment composition, photosynthetic avoidance involves degradation of growth-promoting bHLH
rates and chlorophyll fluorescence images of sun and transcription factors. The Plant Journal, 53, 312–323.
shade leaves of four tree species. Plant Physiology and de Lucas M, Prat S. 2014. PIFs get BR right: Phytochrome
Biochemistry, 45, 577–588. Interacting Factors as integrators of light and hormonal
Lichtenthaler H K, Buschmann C. 2001. Chlorophylls and signals. New Phytologist, 202, 1126–1141.
carotenoids: Measurement and characterization by UV- Macedo A F, Leal-Costa M V, Tavares E S, Lage C L S, Esquibel
VIS spectroscopy. Current Protocols in Food Analytical M A. 2011. The effect of light quality on leaf production and
Chemistry, 1, F4–F3. development of in vitro-cultured plants of Alternanthera
Lin K H, Huang M Y, Huang W D, Hsu M H, Yang Z W, Yang brasiliana Kuntze. Environmental and Experimental Botany,
C M. 2013. The effects of red, blue, and white light-emitting 70, 43–50.
diodes on the growth, development, and edible quality Martinez-Garcia J F, Galstyan A, Salla-Martret M, Cifuentes-
of hydroponically grown lettuce (Lactuca sativa L. var. Esquivel N, Gallemi M, Bou-Torrent J. 2010. Regulatory
capitata). Scientia Horticulturae, 150, 86–91. components of shade avoidance syndrome. In: Advances in
Liu J, Zhang F, Zhou J, Chen F, Wang B, Xie X. 2012. Botanical Research. Elsevier, Academic Press. pp. 65–116.
Phytochrome B control of total leaf area and stomatal Mastropasqua L, Borraccino G, Bianco L, Paciolla C. 2012.
density affects drought tolerance in rice. Plant Molecular Light qualities and dose influence ascorbate pool size in
Biology, 78, 289–300. detached oat leaves. Plant Science, 183, 57–64.
Liu Q, Xiu W, Chen B, Jie G. 2014. Effects of low light on Matsuda R, Ohashi-Kaneko K, Fujiwara K, Goto E, Kurata K.
agronomic and physiological characteristics of rice including 2004. Photosynthetic characteristics of rice leaves grown
grain yield and quality. Rice Science, 21, 243–251. under red light with or without supplemental blue light. Plant
Liu W, Deng Y, Hussain S, Zou J, Yuan J, Luo L, Yang C, and Cell Physiology, 45, 1870–1874.
Yuan X, Yang W. 2016. Relationship between cellulose Matsuda R, Ohashi-Kaneko K, Fujiwara K, Kurata K. 2008.
accumulation and lodging resistance in the stem of relay Effects of blue light deficiency on acclimation of light energy
intercropped soybean [Glycine max (L.) Merr.]. Field Crops partitioning in PSII and CO2 assimilation capacity to high
Research, 196, 261–267. irradiance in spinach leaves. Plant and Cell Physiology,
Liu W G, Hussain S, Ting L, Zou J, Ren M, Tao Z, Jiang L, Feng 49, 664–670.
Y, Yang W Y. 2019. Shade stress decreases stem strength Matthews J S, Vialet-Chabrand S, Lawson T. 2018. Acclimation
of soybean through restraining lignin biosynthesis. Journal to fluctuating light impacts the rapidity of response and
of Integrative Agriculture, 18, 43–53. diurnal rhythm of stomatal conductance. Plant Physiology,
Logan B, Barker D, Demmig-Adams B, Adams III W. 1996. 176, 1939–1951.
Acclimation of leaf carotenoid composition and ascorbate Mawphlang O I, Kharshiing E V. 2017. Photoreceptor mediated
levels to gradients in the light environment within an plant growth responses: Implications for photoreceptor
Australian rainforest. Plant, Cell & Environment, 19, engineering toward improved performance in crops.
1083–1090. Frontiers in Plant Science, 8, 1181.
Logan B A, Demmig-Adams B, Adams III W W, Grace S C. McAusland L, Vialet-Chabrand S, Davey P, Baker N R, Brendel
1998a. Antioxidants and xanthophyll cycle-dependent O, Lawson T. 2016. Effects of kinetics of light-induced
energy dissipation in Cucurbita pepo L. and Vinca major stomatal responses on photosynthesis and water-use
L. acclimated to four growth PPFDs in the field. Journal of efficiency. New Phytologist, 211, 1209–1220.
Experimental Botany, 49, 1869–1879. McCarthy-Suárez I, Gómez M, Del Río L, Palma J. 2011.
20 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

Role of peroxisomes in the oxidative injury induced by Journal of Molecular Sciences, 15, 4657–4670.
2,4-dichlorophenoxyacetic acid in leaves of pea plants. Mustilli A C, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002.
Biologia Plantarum, 55, 485–492. Arabidopsis OST1 protein kinase mediates the regulation
McCourt P, Creelman R. 2008. The ABA receptors - we report of stomatal aperture by abscisic acid and acts upstream
you decide. Current Opinion in Plant Biology, 11, 474–478. of reactive oxygen species production. The Plant Cell, 14,
McCree K J. 1971. The action spectrum, absorptance and 3089–3099.
quantum yield of photosynthesis in crop plants. Agricultural Myers J. 1971. Enhancement studies in photosynthesis. Annual
Meteorology, 9, 191–216. Review of Plant Physiology, 22, 289–312.
McLaren J, Smith H. 1978. The function of phytochrome in the Nagendran R, Lee Y H. 2015. Green and red light reduces the
natural environment. VI. Phytochrome control of the growth disease severity by Pseudomonas cichorii JBC1 in tomato
and development of Rumex obtusifolius under simulated plants via upregulation of defense-related gene expression.
canopy light environments. Plant, Cell and Environment, Phytopathology, 105, 412–418.
1, 61–67. Nascimento L B, Leal-Costa M V, Coutinho M A, Moreira
McNellis T W, Deng X W. 1995. Light control of seedling N S, Lage C L, Barbi N S, Costa S S, Tavares E S.
morphogenetic pattern. The Plant Cell, 7, 1749. 2013. Increased antioxidant activity and changes in
Melgar J C, Guidi L, Remorini D, Agati G, Degl’innocenti E, phenolic profile of Kalanchoe pinnata (Lamarck) Persoon
Castelli S, Camilla Baratto M, Faraloni C, Tattini M. 2009. (Crassulaceae) specimens grown under supplemental blue
Antioxidant defences and oxidative damage in salt-treated light. Photochemistry and Photobiology, 89, 391–399.
olive plants under contrasting sunlight irradiance. Tree Noctor G, Foyer C H. 2016. Intracellular redox compartmentation
Physiology, 29, 1187–1198. and ROS-related communication in regulation and signaling.
Melis A. 1991. Dynamics of photosynthetic membrane Plant Physiology, 171, 1581–1592.
composition and function. Biochimica et Biophysica Acta Nowicka B, Ciura J, Szymańska R, Kruk J. 2018. Improving
(Bioenergetics), 1058, 87–106. photosynthesis, plant productivity and abiotic stress
Meng L, Chen W, Li L, Xu Z, Liu L, Sun J. 2002. Influence of tolerance - current trends and future perspectives. Journal
low light on stomatal characters in rice leaves. Journal of of Plant Physiology, 231, 415–433.
Shenyang Agricultural University, 33, 87–89. (in Chinese) Nozue K, Tat A V, Devisetty U K, Robinson M, Mumbach M R,
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2010. Reactive Ichihashi Y, Lekkala S, Maloof J N. 2015. Shade avoidance
oxygen species homeostasis and signalling during drought components and pathways in adult plants revealed by
and salinity stresses. Plant, Cell & Environment, 33, phenotypic profiling. PLoS Genetics, 11, e1004953.
453–467. Okamoto K, Yanagi T, Takita S, Tanaka M, Higuchi T, Ushida Y,
Minguet-Parramona C, Wang Y, Hills A, Vialet-Chabrand S, Watanabe H. 1996. Development of plant growth apparatus
Griffiths H, Rogers S, Lawson T, Lew V L, Blatt M R. 2016. using blue and red LED as artificial light source. Acta
An optimal frequency in Ca2+ oscillations for stomatal closure Horticulturae, 440, 111–116.
is an emergent property of ion transport in guard cells. Plant Osmond C B, Kyle D, Arntzen C J. 1987. Amsterdam, 9,
Physiology, 170, 33–42. 123–144.
Mishio M, Kawakubo N. 2015. Variations in leaf morpho- Park S Y, Fung P, Nishimura N, Jensen D R, Fujii H, Zhao Y,
anatomy and photosynthetic traits between sun and shade Lumba S, Santiago J, Rodrigues A, Tsz-fung F C. 2009.
populations of Eurya japonica (Pentaphylacaceae) whose Abscisic acid inhibits type 2C protein phosphatases via
seeds are dispersed by birds across habitats. Plant Species the PYR/PYL family of START proteins. Science, 324,
Biology, 30, 147–158. 1068–1071.
Mittler R, Blumwald E. 2015. The roles of ROS and ABA in Park Y, Runkle E S. 2017. Far-red radiation promotes growth
systemic acquired acclimation. The Plant Cell, 27, 64–70. of seedlings by increasing leaf expansion and whole-plant
Mizuno T, Amaki W, Watanabe H. 2009. Effects of net assimilation. Environmental and Experimental Botany,
monochromatic light irradiation by LED on the growth and 136, 41–49.
anthocyanin contents in leaves of cabbage seedlings. Acta Pearcy R W, Seemann J R. 1990. Photosynthetic induction state
Horticulturae, 907, 179–184. of leaves in a soybean canopy in relation to light regulation
Mohammad S, Khan M A, Ali A, Khan L, Khan M S. 2019. of ribulose-1-5-bisphosphate carboxylase and stomatal
Feasible production of biomass and natural antioxidants conductance. Plant Physiology, 94, 628–633.
through callus cultures in response to varying light Pei Z M, Murata Y, Benning G, Thomine S, Klüsener B, Allen G
intensities in olive (Olea europaea. L.) cult. Arbosana. J, Grill E, Schroeder J I. 2000. Calcium channels activated
Journal of Photochemistry and Photobiology (B: Biology), by hydrogen peroxide mediate abscisic acid signalling in
193, 140–147. guard cells. Nature, 406, 731–734.
Muneer S, Kim E, Park J, Lee J. 2014. Influence of green, Pettai H, Oja V, Freiberg A, Laisk A. 2005. The long-wavelength
red and blue light emitting diodes on multiprotein complex limit of plant photosynthesis. Federation of European
proteins and photosynthetic activity under different light Biochemical Societies, 579, 4017–4019.
intensities in lettuce leaves (Lactuca sativa L.). International Polle A, Rennenberg H. 1992. Field studies on Norway spruce
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 21

trees at high altitudes: II. Defence systems against oxidative Plant Cell, Tissue and Organ Culture, 41, 177–185.
stress in needles. New Phytologist, 121, 635–642. Shimazaki K, Doi M, Assmann S M, Kinoshita T. 2007. Light
Poudel P R, Kataoka I, Mochioka R. 2008. Effect of red-and regulation of stomatal movement. Annual Review of Plant
blue-light-emitting diodes on growth and morphogenesis of Biology, 58, 219–247.
grapes. Plant Cell, Tissue and Organ Culture, 92, 147–153. Shimizu H, Saito Y, Nakashima H, Miyasaka J, Ohdoi K. 2011.
Proietti P, Preziosi P, Tombesi A. 1988. Influence of shading Light environment optimization for lettuce growth in plant
on olive leaf photosynthesis. In: Proceedings of the 2nd factory. IFAC Proceedings Volumes, 44, 605–609.
International Meeting on Mediterranean Tree Crops. Smirnoff N. 1993. The role of active oxygen in the response
Chania, Greece. pp. 334–342. of plants to water deficit and desiccation. New Phytologist,
Rapparini F, Rotondi A, Baraldi R. 1999. Blue light regulation 125, 27–58.
of the growth of Prunus persica plants in a long term Smith H. 1982. Light quality, photoperception, and plant
experiment: Morphological and histological observations. strategy. Annual Review of Plant Physiology, 33, 481–518.
Trees, 14, 169–176. Song R, Kelman D, Johns K, Wright A. 2012. Correlation
Reddy S K, Holalu S V, Casal J J, Finlayson S A. 2013. Abscisic between leaf age, shade levels, and characteristic beneficial
acid regulates axillary bud outgrowth responses to the ratio natural constituents of tea (Camellia sinensis) grown in
of red to far-red light. Plant Physiology, 163, 1047–1058. Hawaii. Food Chemistry, 133, 707–714.
Ruban A V, Johnson M P, Duffy C D. 2012. The photoprotective Stepanova A N, Yun J, Likhacheva A V, Alonso J M. 2007.
molecular switch in the photosystem II antenna. Biochimica Multilevel interactions between ethylene and auxin in
et Biophysica Acta (Bioenergetics), 1817, 167–181. Arabidopsis roots. The Plant Cell, 19, 2169–2185.
Růžička K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Su B, Song Y, Song C, Cui L, Yong T, Yang W. 2014. Growth
Friml J, Benková E. 2007. Ethylene regulates root growth and photosynthetic responses of soybean seedlings to
through effects on auxin biosynthesis and transport- maize shading in relay intercropping system in Southwest
dependent auxin distribution. The Plant Cell, 19, 2197–2212. China. Photosynthetica, 52, 332–340.
Sarala M, Taulavuori K, Taulavuori E, Karhu J, Laine K. Sun B, Dilcher D L, Beerling D J, Zhang C, Yan D, Kowalski E.
2007. Elongation of Scots pine seedlings under blue light 2003. Variation in Ginkgo biloba L. leaf characters across
depletion is independent of etiolation. Environmental and a climatic gradient in China. Proceedings of the National
Experimental Botany, 60, 340–343. Academy of Sciences of the United States of America,
Sarijeva G, Knapp M, Lichtenthaler H K. 2007. Differences in 100, 7141–7146.
photosynthetic activity, chlorophyll and carotenoid levels, Sun J, Nishio J N, Vogelmann T C. 1998. Green light drives
and in chlorophyll fluorescence parameters in green sun CO2 fixation deep within leaves. Plant and Cell Physiology,
and shade leaves of Ginkgo and Fagus. Journal of Plant 39, 1020–1026.
Physiology, 164, 950–955. Talbott L D, Nikolova G, Ortiz A, Shmayevich I, Zeiger E.
Sasidharan R, Keuskamp D H, Kooke R, Voesenek L A, Pierik 2002. Green light reversal of blue-light-stimulated stomatal
R. 2014. Interactions between auxin, microtubules and opening is found in a diversity of plant species. American
XTHs mediate green shade-induced petiole elongation in Journal of Botany, 89, 366–368.
Arabidopsis. PLoS ONE, 9, e90587. Tateno M, Taneda H. 2007. Photosynthetically versatile thin
Sato K, Kim J M. 1980. Relationships between environmental shade leaves: A paradox of irradiance-response curves.
conditions and production and consumption activities of Photosynthetica, 45, 299–302.
individual leaves in the population of rice plant in a paddy Terashima I, Fujita T, Inoue T, Chow W S, Oguchi R. 2009.
field: IV. Leaf positional and seasonal cahnges in the rates Green light drives leaf photosynthesis more efficiently
of net photosynthesis and dark respiration in paddy fields than red light in strong white light: Revisiting the enigmatic
of different plant spacing and fertilization. Japanese Journal question of why leaves are green. Plant and Cell Physiology,
of Crop Science, 49, 263–269. 50, 684–697.
Schittenhelm S, Menge-Hartmann U, Oldenburg E. 2004. Terashima I, Hanba Y T, Tazoe Y, Vyas P, Yano S. 2005.
Photosynthesis, carbohydrate metabolism, and yield of Irradiance and phenotype: Comparative eco-development
phytochrome-B-overexpressing potatoes under different of sun and shade leaves in relation to photosynthetic CO2
light regimes. Crop Science, 44, 131–143. diffusion. Journal of Experimental Botany, 57, 343–354.
Schuerger A C, Brown C S, Stryjewski E C. 1997. Anatomical Terashima I, Hanba Y T, Tholen D, Niinemets Ü. 2011. Leaf
features of pepper plants (Capsicum annuum L.) grown functional anatomy in relation to photosynthesis. Plant
under red light-emitting diodes supplemented with blue or Physiology, 155, 108–116.
far-red light. Annals of Botany, 79, 273–282. Terashima I, Miyazawa S I, Hanba Y T. 2001. Why are sun
Sharma R, Sopory S K, Guha-Mukherjee S. 1976. Phytochrome leaves thicker than shade leaves? - Consideration based
regulation of peroxidase activity in maize. Plant Science on analyses of CO2 diffusion in the leaf. Journal of Plant
Letters, 6, 69–75. Research, 114, 93–105.
Sæbø A, Krekling T, Appelgren M. 1995. Light quality affects Terashima I, Saeki T. 1985. A new model for leaf photosynthesis
photosynthesis and leaf anatomy of birch plantlets in vitro. incorporating the gradients of light environment and of
22 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23

photosynthetic properties of chloroplasts within a leaf. of Proteome Research, 12, 5124–5136.

Annals of Botany, 56, 489–499. Wang S, Wang X, Shi X, Wang B, Zheng X, Wang H, Liu F.
Thiele A, Herold M, Lenk I, Quail P H, Gatz C. 1999. 2016. Red and blue lights significantly affect photosynthetic
Heterologous expression of Arabidopsis phytochrome B in properties and ultrastructure of mesophyll cells in senescing
transgenic potato influences photosynthetic performance grape leaves. Horticultural Plant Journal, 2, 82–90.
and tuber development. Plant Physiology, 120, 73–82. Wang Y, Gao L, Shan Y, Liu Y, Tian Y, Xia T. 2012. Influence
Tibbitts T, Morgan D, Warrington I. 1983. Growth of lettuce, of shade on flavonoid biosynthesis in tea (Camellia sinensis
spinach, mustard, and wheat plants under four combinations (L.) O. Kuntze). Scientia horticulturae, 141, 7–16.
of high-pressure sodium, metal halide, and tungsten Weng J K, Li X, Stout J, Chapple C. 2008. Independent origins
halogen lamps at equal PPFD. Journal of the American of syringyl lignin in vascular plants. Proceedings of the
Society for Horticultural Science, 108, 622–630. National Academy of Sciences of the United States of
Timperio A M, D’amici G M, Barta C, Loreto F, Zolla L. 2007. America, 105, 7887–7892.
Proteomics, pigment composition, and organization of Weston E, Thorogood K, Vinti G, López-Juez E. 2000. Light
thylakoid membranes in iron-deficient spinach leaves. quantity controls leaf-cell and chloroplast development in
Journal of Experimental Botany, 58, 3695–3710. Arabidopsis thaliana wild type and blue-light-perception
Tran T T. 2018. The effect of light exposure on the total mutants. Planta, 211, 807–815.
chlorophyll content, Chl a/b ratio, and Car/Chl ratio in the Wherley B, Gardner D, Metzger J. 2005. Tall fescue
barks of Fraxinus latifolia seedlings. [2019-05-16]. https:// photomorphogenesis as influenced by changes in the
pdxscholar.library.pdx.edu/honorstheses/575 spectral composition and light intensity. Crop Science, 45,
Tucker D. 1981. Phytochrome regulation of leaf senescence in 562–568.
cucumber and tomato. Plant Science Letters, 23, 103–108. Wild A, Höpfner M, Rühle W, Richter M. 1986. Changes in the
Urbonavičiūtė A, Pinho P, Samuolienė G, Duchovskis P, Vitta stoichiometry of photosystem II components as an adaptive
P, Stonkus A, Tamulaitis G, Žukauskas A, Halonen L. response to high-light and low-light conditions during
2007. Effect of short-wavelength light on lettuce growth growth. Zeitschrift für Naturforschung (C), 41, 597–603.
and nutritional quality. Sodininkystė ir Daržininkystė, 26, de Wit M, Lorrain S, Fankhauser C. 2014. Auxin-mediated
157–165. plant architectural changes in response to shade and high
Valladares F, Niinemets Ü. 2008. Shade tolerance, a key temperature. Physiologia Plantarum, 151, 13–24.
plant feature of complex nature and consequences. Wittmann C, Aschan G, Pfanz H. 2001. Leaf and twig
Annual Review of Ecology, Evolution, and Systematics, photosynthesis of young beech (Fagus sylvatica) and aspen
39, 237–257. (Populus tremula) trees grown under different light regime.
Verhoeven A S, Swanberg A, Thao M, Whiteman J. 2005. Basic and Applied Ecology, 2, 145–154.
Seasonal changes in leaf antioxidant systems and Woźny A, Jerzy M. 2007. Effect of light wavelength on growth
xanthophyll cycle characteristics in Taxus × media growing and flowering of narcissi forced under short-day and low
in sun and shade environments. Physiologia Plantarum, quantum irradiance conditions. The Journal of Horticultural
123, 428–434. Science and Biotechnology, 82, 924–928.
Vogel E, Meyer R. 2018. Climate change, climate extremes, Wu L, Zhang W, Ding Y, Zhang J, Cambula E D, Weng F, Liu Z,
and global food production - Adaptation in the agricultural Ding C, Tang S, Chen L. 2017. Shading contributes to the
sector. In: Resilience. Elsevier. pp. 31–49. reduction of stem mechanical strength by decreasing cell
Volkov R A, Panchuk I I, Mullineaux P M, Schöffl F. 2006. Heat wall synthesis in japonica rice (Oryza sativa L.). Frontiers
stress-induced H2O2 is required for effective expression of in Plant Science, 8, 881.
heat shock genes in Arabidopsis. Plant Molecular Biology, Wu M C, Hou C Y, Jiang C M, Wang Y T, Wang C Y, Chen H H,
61, 733–746. Chang H M. 2007. A novel approach of LED light radiation
Vranová E, Inzé D, Van Breusegem F. 2002. Signal transduction improves the antioxidant activity of pea seedlings. Food
during oxidative stress. Journal of Experimental Botany, Chemistry, 101, 1753–1758.
53, 1227–1236. Wu Q, Su N, Shen W, Cui J. 2014. Analyzing photosynthetic
Wang H, Gu M, Cui J, Shi K, Zhou Y, Yu J. 2009. Effects of activity and growth of Solanum lycopersicum seedlings
light quality on CO2 assimilation, chlorophyll-fluorescence exposed to different light qualities. Acta Physiologiae
quenching, expression of Calvin cycle genes and Plantarum, 36, 1411–1420.
carbohydrate accumulation in Cucumis sativus. Journal of Wu Y, Gong W, Wang Y, Yong T, Yang F, Liu W, Wu X, Du J,
Photochemistry and Photobiology (B: Biology), 96, 30–37. Shu K, Liu J. 2018. Leaf area and photosynthesis of newly
Wang L, Deng F, Ren W J, Yang W Y. 2013a. Effects of shading emerged trifoliolate leaves are regulated by mature leaves
on starch pasting characteristics of indica hybrid rice (Oryza in soybean. Journal of Plant Research, 131, 671–680.
sativa L.). PLoS ONE, 8, e68220. Wu Y, Gong W, Yang F, Wang X, Yong T, Yang W. 2016.
Wang L, Liang W, Xing J, Tan F, Chen Y, Huang L, Cheng C Responses to shade and subsequent recovery of soya bean
L, Chen W. 2013b. Dynamics of chloroplast proteome in in maize-soybean relay strip intercropping. Plant Production
salt-stressed mangrove Kandelia candel (L.) Druce. Journal Science, 19, 206–214.
 Iram SHAFIQ et al. Journal of Integrative Agriculture 2021, 20(1): 4–23 23

Wu Y, Gong W, Yang W. 2017. Shade inhibits leaf size by Yorio N C, Goins G D, Kagie H R, Wheeler R M, Sager J
controlling cell proliferation and enlargement in soybean. C. 2001. Improving spinach, radish, and lettuce growth
Scientific Reports, 7, 9259. under red light-emitting diodes (LEDs) with blue light
Shi X D. 2006. Research on the effect of different light stresses supplementation. HortScience, 36, 380–383.
on crop growth. Journal of Anhui Agricultural Sciences, 34, Yoshida H, Mizuta D, Fukuda N, Hikosaka S, Goto E. 2016.
4216. (in Chinese) Effects of varying light quality from single-peak blue and
Yang C, Li L. 2017. Hormonal regulation in shade avoidance. red light-emitting diodes during nursery period on flowering,
Frontiers in Plant Science, 8, 1527. photosynthesis, growth, and fruit yield of everbearing
Yang C, Xie F, Jiang Y, Li Z, Huang X, Li L. 2018. Phytochrome strawberry. Plant Biotechnology, 33, 267–276.
A negatively regulates the shade avoidance response Yu W, Liu Y, Song L, Jacobs DF, Du X, Ying Y, Shao Q, Wu
by increasing auxin/indole acidic acid protein stability. J. 2017. Effect of differential light quality on morphology,
Developmental Cell, 44, 29–41. photosynthesis, and antioxidant enzyme activity in
Yang D, Duan L, Xie H, Li Z, Huang T. 2011. Effect of pre- Camptotheca acuminata seedlings. Journal of Plant Growth
flowering light deficiency on biomass accumulation and Regulation, 36, 148–160.
physiological characteristics of rice. Chinese Journal of Zhang J, Shi L, Shi A, Zhang Q. 2004. Photosynthetic responses
Eco-Agriculture, 19, 347–352. (in Chinese) of four Hosta cultivars to shade treatments. Photosynthetica,
Yang F, Fan Y, Wu X, Cheng Y, Liu Q, Feng L, Chen J, Wang 42, 213–218.
Z, Wang X, Yong T. 2018a. Auxin-to-gibberellin ratio as a Zhang T, Folta K M. 2012. Green light signaling and adaptive
signal for light intensity and quality in regulating soybean response. Plant Signaling & Behavior, 7, 75–78.
growth and matter partitioning. Frontiers in Plant Science, Zhang W, Wu L, Ding Y, Fei W, Wu X, Li G, Liu Z, She T, Dinng
9, 56. C, Wang S. 2016. Top-dressing nitrogen fertilizer rate
Yang F, Feng L, Liu Q, Wu X, Fan Y, Raza M A, Cheng Y, Chen contributes to decrease culm physical strength by reducing
J, Wang X, Yong T. 2018b. Effect of interactions between structural carbohydrate content in japonica rice. Journal of
light intensity and red-to-far-red ratio on the photosynthesis Integrative Agriculture, 15, 992–1004.
of soybean leaves under shade condition. Environmental Zheng L, Van Labeke M C. 2017. Chrysanthemum morphology,
and Experimental Botany, 150, 79–87. photosynthetic efficiency and antioxidant capacity are
Yang F, Huang S, Gao R, Liu W, Yong T, Wang X, Wu X, differentially modified by light quality. Journal of Plant
Yang W. 2014. Growth of soybean seedlings in relay strip Physiology, 213, 66–74.
intercropping systems in relation to light quantity and red:far- Zhu H, Li X, Zhai W, Liu Y, Gao Q, Liu J, Ren L, Chen H, Zhu
red ratio. Field Crops Research, 155, 245–253. Y. 2017. Effects of low light on photosynthetic properties,
Yano A, Fujiwara K. 2012. Plant lighting system with five antioxidant enzyme activity, and anthocyanin accumulation
wavelength-band light-emitting diodes providing photon in purple pak-choi (Brassica campestris ssp. Chinensis
flux density and mixing ratio control. Plant Methods, 8, 46. Makino). PLoS ONE, 12, e0179305.
Yao X, Li C, Li S, Zhu Q, Zhang H, Wang H, Yu C, Martin S K S, Zhu P, Yang S M, Ma J, Li S X, Chen Y. 2008. Effect of shading
Xie F. 2017. Effect of shade on leaf photosynthetic capacity, on the photosynthetic characteristics and yield at later
light-intercepting, electron transfer and energy distribution growth stage of hybrid rice combination. Acta Agronomica
of soybeans. Plant Growth Regulation, 83, 409–416. Sinica, 34, 2003–2009. (in Chinese)

Executive Editor-in-Chief LI Shao-kun

Managing editor WANG Ning