Crop photosynthetic response to light quality and light intensity

lram SHAFlQ ,Sajad HUSSAlN ,Muhammad Ali RAZA ,Nasir lQBAL ,Muhammad Ahsan ASGHAR ,Ali RAZA ,FAN Yuan-fang ,Maryam MUMTAZMuhammad SHOAlB,Muhammad ANSAR,Abdul MANAF,YANG Wen-yu ,YANG Feng

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.lntroduction

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 issue of food security is increasingly gaining paramount importance in a world of ever-increasing population and global climate change. The rising need of food necessitates the development of crops with optimum growth,higher quality and yields,and robust stress resistance,to sustainably feed the ever-increasing human population which is expected to rise by 10 billion in next 50 years (Glick 2014; Nowickaet al.2018; Vogel and Meyer 2018).

Of many abiotic factors,light plays a vital role in agricultural production (Yanget al.2014) as it is indispensable for photosynthesis,a complex biochemical and biophysical process for biomass production,which involves the synthesis of photosynthetic pigments,Calvin cycle and the light-driven electron transport (Wanget al.2013b). Light is perceived by plants through different photoreceptors,i.e.,phytochromes and cryptochromes (Ballaré and Pierik 2017; Mawphlang and Kharshiing 2017). The two components of light,light quality (which means the color or wavelength of light) and light intensity greatly affect the structure and function of plant photosynthetic apparatus (Li Ret al.2014; Heet al.2018;Yang Fet al.2018a) as well as growth and yield potential(Fanet al.2018; Yang Fet al.2018a). Earlier studies have reported blue light (425-490 nm) and red light (610-700 nm)to be the best light spectra for plant photosynthesis,while a very low amount of green light (520-610 nm) is absorbed by plants (Pettaiet al.2005; Changet al.2016; Yoshidaet al.2016). Red light (R) contributes to the development of photosynthetic apparatus and induces transformations in the photochromic system,thus,influences morphogenesis(Urbonavičiūtėet al.2007). Far-red light (FR) is reported to contribute minimally to the plant photosynthesis because of its poor absorption by leaves and unbalanced excitation of the two photosystems; photosystem I (PSI) and PSII,leading to low quantum yields (Hill and Bendall 1960;Duysens and Amesz 1962; McCree 1971; Myers 1971).While,the blue light is observed to regulate different plant processes such as photosynthesis,stomatal opening,photo-morphogenesis,maturation of chloroplasts,and biosynthesis of chlorophyll and enzymes (Tibbittset al.1983; Okamotoet al.1997; Heoet al.2002; Urbonavičiūtėet al.2007). Similarly,previous studies show that green light contributes to plant growth by stimulating carbon assimilation in lower parts of the plant canopies since it can penetrate deeper in the foliage and crop in comparison to red and blue lights (Yorioet al.2001; Kimet al.2004a;Terashimaet al.2005). It has also been observed to protect light-labile plant defense secondary metabolites(Gouldet al.2010) and improve plant defense mechanisms by triggering and upregulating the expression of specific genes under biotic or abiotic stress (Zhang and Folta 2012;Nagendran and Lee 2015).

Similarly,extensive research has been conducted related to the effect of different light intensities on plant photosynthesis and other morphological,anatomical,physiological,and biochemical parameters. Plants need a specific light intensity for their growth,higher or lower than normal light intensity may inhibit photosynthesis. In comparison to higher light intensities,intercropped crops usually suffer from low irradiance or shade stress. Shade or low-light conditions is a pervasive abiotic stress in agricultural crop production due to light blockage from interculture practices such as intercropping (Yang Fet al.2018b), high plant densities such as those found in forests and prairies,where a mixture of different species grow in dense conditions (Martinez-Garciaet al.2010),or due to cloud cover,snow and many other factors (Zhuet al.2017).It is characterized by a reduced amount of photosynthetically active radiations (PAR) and changes in the spectral composition of light (Park and Runkle 2017; Yang Fet al.2018b) (Fig.1). It not only affects the amount of light received by plants but also alters the plant environmental conditions,such as the temperature of air and ground around the plant,humidity,carbon dioxide (CO2) concentrations,etc.,which are essential for plant growth (Songet al.2012).Low light conditions substantially affect various agronomic traits of plants (Wanget al.2012). It negatively affects the morphology (Wu Let al.2017),physiology and biochemistry of crop plants (Liuet al.2016),especially photosynthesis(Yang Fet al.2018a).

Generally,it is observed that lower light intensities or the shading conditions in intercropping inhibit leaf growth,lead to thinner leaves with smaller leaf area,thinner palisade tissues and reduced chlorophyll content resulting in lower light-harvesting (Yanget al.2014; Gonget al.2015).Moreover,stomatal density and conductance are decreased which results in poor CO2transport. The electron transfer from PSII to PSI is blocked,the amount and activity of enzymes involved in the Calvin cycle are altered. Reactive oxygen species are generated which further disrupt the normal functioning of the photosynthetic apparatus. All of this leads to a lower carbon dioxide assimilation rate,and a lower net photosynthetic rate and reduced light-saturated net photosynthetic rate (Pnmax). Higher light intensities are reported to disturb the balance between energy supply and energy consumption in plants. It is well known that the electron transport and synthesis of ATP and NADPH occur at much slower rates in comparison to the light-harvesting and energy transfer to PSII (Rubanet al.2012). In conditions of higher light intensities,the amount of energy absorbed recurrently overcomes the metabolic energy needed which results in the accumulation of excess energy in thylakoid membranes that has the potential to harm PSII. Moreover,it may result in the permanent closure of the PSII reaction centres and cause photo-inhibition (Longet al.1994; Kerenet al.1997; Jansenet al.1999). It has been reported earlier that plants growing in higher and lower light intensities have a different composition of photosynthetic pigments,electron carriers,chloroplast ultrastructure,and photosynthetic rates(Boardman 1977; Lichtenthaleret al.1981; Wildet al.1986;Andersonet al.1995).

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

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

Fig.2 Graphical representation of the abstract.

2.Plant morphology and anatomy

2.1.Leaf

Shade governs leaf morphology and anatomy. Leaves are considered as the main organ for plant photosynthesis and transpiration,their structure reflects how environmental factors influence plants or how plants adapt to the changing environment. Under normal light conditions,palisade tissue elongate and increase the area of chloroplast channel through which CO2enters,thereby increasing the leaf thickness and strengthening the photosynthetic ability(Terashimaet al.2005; Wuet al.2016). However,shade or low PAR irradiances result in smaller leaf area (Kimet al.2005; Kozukaet al.2005; Fan X Xet al.2013; Gonget al.2014) and thinner leaves,which is a common adaptation mechanism in many plant species (Terashimaet al.2005;Kalveet al.2014; Mishio and Kawakubo 2015; Ballaré and Pierik 2017; Bertelet al.2017; Hanet al.2017; Ajmiet al.2018; Fanet al.2018).

Most of the scientists believe that thinner leaves have greater ability to intercept light due to low leaf dry mass per unit area (Valladares and Niinemets 2008; Terashimaet al.2011) and the structural characteristics also aid in increasing the light reflection and scattering in the leaves which helps the plants to maximize light penetration into the leaves to increase light absorption for chloroplasts under limited light conditions (Terashima and Saeki 1985; Shi 2006). However,in comparison to thicker leaves,the thinner leaves have thinner palisade tissue and less chloroplast,this structure does not support the transport and dissolution of CO2(Terashimaet al.2001) (Fig.3). Therefore,thinner leaves are not proficient in photosynthesis and biomass accumulation (Wu Yet al.2017).Moreover,plants under shade invest greater biomass partitioning to stem growth at the expense of leaf expansion. Taken together,these findings suggest an inhibited growth of plant leaves under lower PAR (Wu Yet al.2017).

Light quality also significantly influences the development of leaf palisade/spongy parenchyma and thus leaf thickness.This is observed forArabidopsis(Westonet al.2000) andAlternanthera brasiliana(Macedoet al.2011). The number of mesophyll cells per leaf section and palisade cell length decreased in response to low R:FR inPhaseolus vulgarisandSolanum tuberosumrespectively (Barreiroet al.1992; Thieleet al.1999). The blue light effects on the leaf thickness are known to be species dependent. A blue light supplementation to pepper plants grown under red light is correlated with an increase of palisade and spongy mesophyll thickness in pepper plants (Schuergeret al.1997). An increase of more than 25% blue light ratio in rapeseed leaves resulted in two cell-layers in the palisade tissue,which indicates that blue light has a decisive role in the development of the palisade tissues (Changet al.2016).In contrast,the addition of blue light decreases leaf thickness in peach (Rappariniet al.1999). Johkanet al.(2012)observed an increased width and length of lettuce leaves irradiated with green LED light of higher photosynthetic photon flux,i.e.,300.

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.

2.2.Stem

Generally,under shade conditions,plants have increased stem height,petiole length and decreased stem diameter,as more carbon is allocated to the elongation of stem and petiole at the expense of leaf and root development(Gommerset al.2013; Park and Runkle 2017). Such a structure helps plants in searching for light under shade conditions (Smith 1982; Green-Tracewiczet al.2011;Casal 2012; Gonget al.2015; Wu Let al.2017) (Fig.4).However,shade results in weaker and slender stems with poor mechanical strength (Suet al.2014).

The stem strength depends on the contents such as lignin,cellulose,semi-fiber,sucrose,pectin,starch,etc.(Hussainet al.2019b,d). Lignin is a complex aromatic polymer in vascular plants and is an important constituent of the cell wall (Fig.5) (Wenget al.2008). It enhances the strength of cell walls by crosslinking with cellulose and hemicellulose(Liet al.2009). Low light intensity or shade conditions serve as a limiting factor in the biosynthesis of lignin by reducing the activities of enzymes,i.e.,phenylalanine ammonialyase (PAL),cinnamyl alcohol dehydrogenase(CAD),4-coumarate:CoA ligase (4CL),and peroxidase(POD) involved in it (Koyamaet al.2012; Wanget al.2012;Wu Let al.2017). Weaker stems with higher lodging rates resulted in a reduced transport of carbohydrates and dry matter production,increased attack by various pests and pathogens,all of this is significantly correlated with yield loss(Hussainet al.2019b,2020). Moreover,it is observed that lower light intensities alter the thicknesses of mechanical tissue layers and vascular bundle sheath cells which are important for crop lodging resistance at the anatomical level (Zhanget al.2016). Shade results in plants with low xylem area,low pith and xylem ratio (Liuet al.2019),reduced cross-sectional area of stem,stem rind thickness and vascular bundle number (Cuiet al.2012).

Low light intensities also alter the expression of genes involved in shade avoidance response and lignin and cellulose synthesis. It has been observed inA.thalianathat green shade (created by adding a green color filter to the white light background which reduced PAR to 65 μmol m-2s-1,R:FR to 0.19 and blue light photon fluence rate to 2 μmol m-2s-1) increased the expression of four genes (XTH16,-17,-19,and-22) which play a role in boosting shade avoidance responses under low light conditions (Sasidharanet al.2014). Similarly,in rice plants,reduced expression of genes involved in lignin and cellulose biosynthesis (OsCesA1,OsCesA3andOsCesA8) at the stem formation stage is observed (Wu Let al.2017). However,more research needs to be conducted to investigate the expression of the genes related to the expression of lignin biosynthesis and genetic engineering techniques must be exploited to regulate these genes. The schematic diagram below represents the physiological,anatomical,proteomic,and enzymatic changes in the stem of shaded plants (Fig.6).

Light quality also regulates the stem morphological and anatomical structures. Since plants mainly absorb red and blue lights in comparison to green light,so their development and physiology are greatly influenced by blue or red light (Terashimaet al.2009). It is known that a blue light supplementation in the incident light influences characteristics such as plant height,number of nodes per branch and biomass accumulation (Yorioet al.2001). Tomato plants raised in blue light had smaller shoots,reduced number of nodes and internode length(Głowacka 2004).In vitrograpes also showed reduced height in response to blue light (Poudelet al.2008). Similar results were observed for pines and narcissi (Saralaet al.2007; Woźny and Jerzy 2007).Camptotheca acuminategrown under blue and yellow lights resulted in small stem height whereas red light promoted plant growth and stem elongation (Yuet al.2017). Similar results were reported for Pelargonium by Appelgren (1991). Furthermore,earlier research reports that blue light suppresses hypocotyl elongation while red light induces hypocotyl elongation(McNellis and Deng 1995; Johkanet al.2010). While green light is known to induce early stem elongation (Folta 2004; Kimet al.2004b) and results in decreased biomass production (Folta and Maruhnich 2007).

Fig.4 Phenotypic changes of soybean plants under normal light and low light conditions.

Fig.5 Biosynthesis of lignin under normal light and low light conditions. The dark pink color lining shows lignin content in the stem under normal light and low light conditions. Bar=1 000 μm.

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.

3.Stomatal development

The stomata are known as an important channel for the process of transpiration,i.e.,exchange of water and gases with the external environment.Light influences stomatal conductivity (Timperioet al.2007). The stomatal development is related to light intensity (Hattoriet al.2007)and the stomatal response to fluctuating light intensities has been widely studied (Shimazakiet al.2007; Lawsonet al.2010; McAuslandet al.2016; Kardiman and Ræbild 2017; Matthewset al.2018). Most plants reduce stomatal density as an adaptation to low light conditions,which is well observed under natural and controlled conditions (Gay and Hurd 1975; Proiettiet al.1988; Gregoriouet al.2007;Granado-Yelaet al.2011; Muneeret al.2014; Yanget al.2014; Zheng and Van Labeke 2017; Ajmiet al.2018) (Fig.7).Moreover,under lower irradiances,stomatal conductance decreases,which leads to increased levels of intercellular CO2concentration (Menget al.2002; Yanget al.2011).Shade stress might also reduce stomatal opening (Knapp and Smith 1990) as under low light ABA level increases in guard cells,where they bind to a soluble receptor to trigger stomatal closure (McCourt and Creelman 2008). The activated ABA receptor represses protein phosphatases that enhances the activity of various enzymes,including respiratory burst oxidases (RBOHs) due to enhanced phosphorylation (Mustilliet al.2002; Parket al.2009). The activation of RBOH leads to a transient burst of ROS in guard cells (Peiet al.2000) which opens calcium ion influx channels (Mittler and Blumwald 2015; Minguet-Parramonaet al.2016),that in turn,activate ion efflux channels on the plasma membrane. These changes in the ion concentration result in the efflux of water,hence guard cells become flaccid leading to stomatal closure (Chenet al.2010).

The stomatal response to different light spectra varies.It is known that phytochromes A and B promote stomatal maturation inA.thalianain response to FR and R light respectively (Kanget al.2009). A low R:FR or phytochrome B (PHYB) reduced expression decreases the stomatal density,which results in a decreased stomatal opening that can either cause an increase or decrease in CO2stomatal conductance. Similar results of decreased stomatal density in response to low R:FR ratio have been reported inA.thaliana,Citrus insitorum and Oryza sativa(Boccalandroet al.2003; Liuet al.2012; Distefanoet al.2013). In contrast,stomatal density did not change in leaves ofC.communis(Assmann 1992) indicating that all species do not follow the shade response pattern ofArabidopsis.While,former studies observed no effect of phytochrome B on stomatal development inO.sativa(Liuet al.2012). The lettuce plants grown under blue LEDs with high light intensities showed well-organized guard cells with open stomata,the number of stomata were observed to be higher and the opening and closing of stomata was also more effective (Muneeret al.2014). Previous studies observed that stomatal opening is opposed when given a brief pulse of green light,while stomata open if the green light is followed by blue light(Frechillaet al.2000). Similar observations of this bluegreen effect were recorded by Talbottet al.(2002) in a diverse suite of plant species that suggested the existence of this effect throughout the plant kingdom. In contrast,blue and purple light treatments in tomato reduced the stomatal conductance and increased the intercellular CO2concentration which indicates that B and P wavelengths can reduce the photosynthetic gas exchange of tomato leaves(Yang Fet al.2018a). It is reported that light quality does not affect when light intensities are too low as stomata hardly 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).

4.Photosynthetic apparatus

Low light conditions change the photosynthetic apparatus of plants by altering the levels of enzymes involved in carbon-reduction cycle (Wanget al.2013a),components of electron transport (Yang Fet al.2018b),proteins (Li Tet al.2014a),and light-harvesting pigments (Wherleyet al.2005) as shown in Fig.2. It generally results in lower photosynthetic rates,which is observed in different plant species (Lichtenthaleret al.1981; Sarijevaet al.2007;Jianget al.2011; Li Ret al.2014; Muneeret al.2014; Yang Fet al.2018a). Lower photosynthetic capacity is always accompanied with lower quantity of electrons passing through PSII (Yaoet al.2017). Earlier findings suggest decreased quantum yield (Fv/Fm),effective quantum yield of photosystem (PSII),photochemical quenching (qP),and electron transport rate (ETR) in plants grown under shade conditions (Hussainet al.2019c) (Fig.8). Reductions in photosynthetic rate is reported to occur due to two main reasons; either due to decreased CO2diffusion into leaves,decrease in intercellular CO2and stomatal conductance,or due to inhibition of photosynthesis by inhibition of the leaf growth and enlargement by controlling the cell proliferation(Wu Let al.2017; Wuet al.2018). Furthermore,it was observed that photosynthetic efficiency of rice plants under low light decreased by 79.84% as compared to that of natural light (Sato and Kim 1980). Earlier research also suggests disrupted photosynthesis due to shade stress at the vegetative stage which blocks electron transport from PSII to PSI,thus reducing the electron transport rate,reducing the amount of ATP produced and the amount or activity of Rubisco (Yaoet al.2017; Huanget al.2018).Shade leaves usually have a lower net CO2assimilation rate(An) (Tateno and Taneda 2007) and is saturated at lower PPFD (Zhanget al.2004). Plants are known to adjust their photosynthetic apparatus in response to changes in light conditions by making changes at molecular level such as modulation of PSI and PSII antenna size by light intensity;it is observed that plants grown under high light intensity have smaller antenna than those grown in shade (Andersonet al.1995). Other long-term acclimation responses of the thylakoid membrane to the varying light conditions (quantity and quality) include changes in the ratio of PSI and PSII units and inactivation of a subpopulation of PSII reaction centres(Melis 1991); it is observed that plants grown under shade conditions possess a higher PSII/PSI ratio to compensate for the reduction in the amount of red light,which is required to excite PSII (Osmondet al.1987).

Over the years,different light conditions have been considered to conduct the physiological studies of photosynthesis. A combination of red and blue LEDs with varying light intensities and wavelengths is considered as an effective source for the photosynthesis (Linet al.2013).The grape cultivar “Italia”,when grown under red light,displayed the high net photosynthetic rate and the ratio ofFv/Fmin comparison to control (Wanget al.2016). In line with this,Sæbøet al.(1995),Shimizuet al.(2011) and Kobayashiet al.(2013) reported red light to be significant for photosynthetic apparatus development as it might increase starch accumulation in various plant species through inhibiting the translocation of photosynthates out of the leaves. However,Lactuca sativaplants grown under red LEDs showed lower rates of photosynthesis with a decrease in light intensity (Muneeret al.2014). Similar results of the reduced rate of photosynthesis under low light intensity and red LEDs have also been reported for rice (Matsudaet al.2004) and wheat (Yano and Fujiwara 2012). Such results may suggest that vulnerability to a lower photosynthetic rate might be linked with changes in multiprotein complexes (PSI and PSII) (Muneeret al.2014; Hussainet al.2019a).Such results could also be attributed to lower leaf nitrogen content because of low chlorophyll and carotenoid content (Kimet al.2004a). Yorioet al.(2001) reported that a blue light supplementation in lettuce grown under red light resulted in higher weight accumulation than that grown under red light alone. Blue LEDs in combination with high light intensities are reported to be efficient for biomass production in plants;lettuce plants,when grown in blue LEDs and high light intensity,displayed higher net photosynthetic rate which is indicative of the fact that the plants had a pronounced acclimation of photosystems for CO2fixation (Muneeret al.2014). A blue light supplementation also leads to the increased photosynthetic activity ofConvallaria majalisand strawberry plants (Bukhovet al.1995; Yoshidaet al.2016). It is reported for spinach leaves that a blue light deficiency can result in acclimations of light energy partitioning in PSII and CO2to high irradiance (Matsudaet al.2008). Considering the effects of green light,the poor absorption of this wavelength by plant leaves is well explained through the absorption spectra of chlorophylls or other plant pigments extracted from green leaves(Terashimaet al.2009). The green wavelength is known to result in reduced plant photosynthesis (Sunet al.1998) and have negative effects on plant physiology and development (Folta and Maruhnich 2007). In contrast,earlier research also suggests that green light results in high photosynthetic efficiency provided that it is absorbed by the leaves (Bjorkman 1968; Balegh and Biddulph 1970;McCree 1971; Inada 1976). Wuet al.(2014) reported a higher photosynthetic efficiency in tomato plants grown under green light in comparison to plants grown under yellow light. Similarly,a better photosynthetic performance was observed for sunflower leaves grown under green light mixed with strong white light in comparison to those grown under red light alone (Terashimaet al.2009).This is in line with the physical laws of light quanta,with shorter wavelength photons possessing more energy and therefore exciting chlorophylls to an unproductive singlet state.Similarly,when lettuce plants were grown under high-intensity (≥PPF 300) green LEDs,they showed normal development like plants grown under fluorescent lamp,which indicated the fact that green light at higher intensity is available to the plants for morphogenesis and photosynthesis while green light of low intensity might penetrate the leaf insufficiently for morphogenesis or photosynthesis (Johkanet al.2012).

5.Pigment composition

Low light conditions or shade change the photosynthetic pigment composition of plants,i.e.,chlorophyll (Chla,Chlb,Chla+b,and Chla/b),which are important pigments involved in absorbance,transmittance and conversion of solar energy into electrochemical energy (Liuet al.2014). Contrasting views regarding the effect of low irradiance on chlorophyll content have been reported. Some studies claimed reduced chlorophyll contents under shading conditions (Wittmannet al.2001; Zhuet al.2017; Fanet al.2018) (Fig.9),which is also a typical symptom of oxidative stress,it might either due to the photo-oxidation of chlorophyll,deficiency of chlorophyll synthesis and/or chlorophyll degradation(Smirnoff 1993). It has been reported that the modulation of chlorophyll biosynthesis in response to low light conditions inA.thalianais usually regulated by an overall down-regulation of genes involved in chlorophyll biosynthesis (McLaren and Smith 1978) while to a lesser extent by up-regulation of genes associated with chlorophyll degradation (Brouweret al.2014).

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.

Chlorophyll might also decrease under conditions of continuous shading as previous studies confirmed that applying shade for a longer duration or completely providing the shading condition (i.e.,100% shade) did not lead to the maximum total chlorophyll content (Tran 2018). In contrast,other researchers reported enhanced chlorophyll production in response to lower PAR (Escoubaset al.1995; Lichtenthaler and Buschmann 2001; Terashimaet al.2001; Sunet al.2003; Terashimaet al.2005; Gregoriouet al.2007; Lichtenthaleret al.2007; Evanset al.2009;Melgaret al.2009),especially the contents of Chlb(Zhuet al.2008, 2017; Li Ret al.2014; Yang Fet al.2018b)the increase of which could lead to rise in light-interception under shade stress (Pearcy and Seemann 1990). Zhuet al.(2008) reported that low light-tolerant hybrid rice exhibited a higher content of Chlbwhen exposed to low light. Zhuet al.(2017) reported that purple pak-choi showed an increased Chlbcontent in the shade treatments at 5 d,however,with the extension of shading time (at 15 d),the relative content of chlorophyll decreased over time. It can be inferred that chlorophyll content may tend to increase under shading conditions to enhance light harvesting in shade-tolerant varieties (Valladares and Niinemets 2008).

Similar to light intensity,different light spectra also affect the plant pigment content. A low R:FR ratio is observed to result in decreased foliar chlorophyll content per unit area in various species such asCitrus insitorum,Solanum tuberosum,Trifolium repens,Solanum lycopersican,andCucumis sativus(Tucker 1981; Thieleet al.1999; Heraut-Bronet al.2000; Schittenhelmet al.2004; Distefanoet al.2013). However,tomato plants grown under red light had higher contents of Chla,band carotenoid (Yang Fet al.2018a). Similarly,D.versipellisplants grown under red colored plastic film had the maximum chlorophyll content(Heet al.2018). Grape cultivars when grown under supplemental red light also had high chlorophyll content and Chla/bratio (Wanget al.2016). In contrast,Fan Xet al.(2013) reported that red light was not conducive for the synthesis of chlorophyll. Mizunoet al.(2009) found a high chlorophyll content in cabbage grown under blue light.Similar results were reported in birch plantletsin vitro(Sæbøet al.1995) and in lettuce and spinach plants (Tibbittset al.1983) where the highest chlorophyll content was observed in blue-light sources compared to red-light sources. Plants grown under yellow film resulted in decreased chlorophyll content (Heet al.2018). Similar effects for yellow light treatment have been reported inBrassica campestrisL.andC.sativus(Wanget al.2009; Fan Xet al.2013).

6.Reactive oxygen species (ROS)

An important biochemical change that occurs in plants in response to oxidative stress is the production of reactive oxygen species (ROS) such as superoxide anion (O2-·),hydrogen peroxide (H2O2),hydroxyl radical (HO·) and singlet oxygen (1O2) (Smirnoff 1993; Allen 1995; Vranováet al.2002; Apel and Hirt 2004; Milleret al.2010; McCarthy-Suárezet al.2011). Low light or shade conditions induce oxidative stress in plants which increases ROS production and causes lipid peroxidation. The production of ROS under low light intensities or shade stress leads to an increased level of photorespiration and enhances the activity of mitochondrial electron-transport-chain (mETC) (Blokhinaet al.2003; Lawlor and Tezara 2009). Zhuet al.(2017)observed an increased production of malondialdehyde content under low light stress in purple pak-choi(B.campestrisssp.Chinensis makino). Similarly,analyses of membrane lipid peroxidation in peach fruit showed that decreasing the light intensity increased the malondialdehyde(MDA) content with more cell membrane damage (Apel and Hirt 2004; Volkovet al.2006). Under the conditions of light intensities that exceed plant’s photosynthetic capacity when photosynthesis is unable to utilize all the absorbed energy,the chloroplast lumen turns acidic,reduces the electron transport chain,and excitation energy gathers within the chloroplast which could lead to the production of singlet and triplet forms of chlorophyll and singlet oxygen that are toxic(Aliet al.2005). The excess excitation energy depletes the NADP+pool that increases the rate of electron flow from the donor side of PSI to oxygen,thereby generating ROS such as superoxide and hydrogen peroxide (Asada 1999).Ivanovet al.(2012) reported an increase in both superoxides radical and hydrogen peroxide (H2O2) production by the photosynthetic electron-transport chain under conditions of high light intensities. The main source of ROS generation in plants is chloroplast (Asada 2000). Since ROS are highly reactive,in the absence of any protective mechanism,ROS can cause potential damage to cellular and molecular machinery,protein modification and lipid peroxidation,thus disrupting the normal metabolism of the plants leading to severe yield losses (Ahmedet al.2009). However,recent research has also recognized a positive role of ROS as essential pro-life signals (Noctor and Foyer 2016; Foyeret al.2017). The ROS production is considered essential for redox sensing,signaling and regulation in the photosynthetic cells (Foyer 2018).

Light quality also affects ROS production.Camptotheca acuminataseedlings grown under blue and yellow light suffered from oxidative damage to lipid membranes due to higher contents of O2-·,H2O2and MDA while red light reduced the O2-· production rate and H2O2content as compared to white light (Yuet al.2017).

7.Antioxidant enzymes

Plants produce an elaborate arsenal of antioxidant enzymes such as superoxide dismutase (SOD),POD,catalase (CAT),ascorbate peroxidase (APX),etc.,in response to oxidative stress to not only interrupt the cascades of uncontrolled oxidation by ROS but rather maintain an appropriate balance between their production and removal which is compatible with the optimum functioning of photosynthesis (Foyer 2018). The increases in the antioxidant defense system under conditions of low irradiances have been well reported in several studies (Esterbauer and Grill 1978; Andersonet al.1992; Polle and Rennenberg 1992; Douliset al.1993;Verhoevenet al.2005) (Fig.10). Ascorbate-Glutathione pathway (also known as Asada-Halliwell pathway) is the major pathway of antioxidant defense that mainly detoxifies the H2O2in the plant cell. Within the antioxidant defencse system,the AsA-GSH (ascorbate and glutathione) pool plays the immediate role of minimizing stress effect through scavenging ROS using four key enzymes,e.g.,ascorbate peroxidase (APX),monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR),and glutathione reductase (GR) (Latowskiet al.2010;Hasanuzzamanet al.2011,2012). Usually,the pathway involves SOD giving the frontline protection against ROS by converting O2-· to H2O2. Afterward,CAT and APX scavenge H2O2to H2O. Glutathione peroxidase and GST(glutathioneS-transferase) also scavenge H2O2to H2O with the help of glutathione (GSH) (Hasanuzzamanet al.2011). Ghasemzadehet al.(2010) reported that a lower light intensity of 310 μmol m-2s-1enhanced the antioxidant activity of ginger by increasing total flavonoid content.Similarly,a higher activity of antioxidant enzymes,i.e.,SOD,POD,CAT,and APX was observed in callus culture of the olive cult.Arbosanakept in dark conditions (Mohammadet al.2019). Zhuet al.(2017) found that antioxidant activities of guaiacol POD,CAT and SOD increased in the shade treatments at 5 d,however,with the extension of shading time (at 15 d),the activity of antioxidants decreased considerably. The increase in antioxidant activity under low light intensities might be attributed to reduced leaf temperature because of the shade as earlier studies proved that low temperature raise the antioxidant activities in plants to cope with the negative effects of low temperature (Guy and Carter 1984; Adams III and Demmig-Adams 1994;Burkle and Logan 2003; Lohrmannet al.2004; Loganet al.2006). However,contrasting views have also been reported by Grace and Logan (1996),Loganet al.(1996,1998a,b),Apel and Hirt (2004),and Callejón-Ferreet al.(2009).Apel and Hirt (2004) and Volkovet al.(2006) reported that decreasing the light intensity decreased CAT,G-POD and APX activity in peach fruit.

Fig.10 Shade causes oxidative stress. AOX and ROS,antioxidants and reactive oxygen species,respectively.

Similar to light intensity,the effects of variable light wavelengths on antioxidant enzymes production in plants are complex and are most often reported with contrasting results (Yuet al.2017). For example,earlier studies suggest that a low-energy red light increases the activity of antioxidant enzymes as well as the content of low molecular weight antioxidants,i.e.,carotenoids and UV-absorbing pigments in spinach (Kreslavskiiet al.2012). A short-term red light (500 mW cm-2s-1) was observed to increase the peroxidase activity in maize by 50-70% when measured 1 d after exposure (Sharmaet al.1976). The stimulation of peroxidase activity and another antioxidant in response to red light could be due to higher transcriptional levels of the genes encoding for peroxidase and other enzymes(Kreslavskiet al.2013). Similarly,red and far-infrared light wavelengths were found effectively for the antioxidant activity in pea seedlings and rice hulls (Leeet al.2003;Wuet al.2007). In contrast,SOD,POD and CAT did not increase under red light-grownC.acuminataseedlings rather higher antioxidants were recorded for seedlings grown under blue and yellow lights (Yuet al.2017). A blue light supplementation resulted in higher ascorbate peroxidase activity (APX) in the detached oat leaves(Mastropasquaet al.2012). Similar results were recorded inKalanchoe pinnataby Nascimentoet al.(2013). Such results suggest that different light spectra evoke different antioxidant responses depending on the plant species and that investigation of suitable light quality is essential for maximal biomass production.

8.Hormones

The hormones regulate light dependent changes in plant morphogenesis (Islamet al.2014; Kissoudiset al.2017).Among the endogenous plant hormones,gibberellins (GAs)and auxin (indole-3-acetic acid (IAA)) regulate the shadeinduced differential growth and elongation (Kurepinet al.2007a; Lucas and Prat 2014; Yang and Li 2017). When plants grow near neighboring vegetation,they perceive reductions in R:FR which serves as an early warning signal to the plants and promotes the escape responses before the occurrence of shade (Ballaréet al.1990). A low R:FR inactivates the phytochromes,stabilizes and activates the transcription factors called the phytochromeinteracting factors (PIFs). The PIF4,PIF5 and PIF7 act in collaboration to promote the auxin biosynthesis and result in stem elongation (Lorrainet al.2008; Liet al.2012). Under conditions of true shade,plants also experience reduced levels of blue light which together with low R:FR promote hypocotyl elongation and phototropic curvature to facilitate shade escape (Franklin 2016). Earlier findings suggest that a lateral blue light enhances the auxin accumulation on the shaded sides of the plant stem that causes the cells to elongate more in comparison to the cells on the illuminated side,thus leading to stem curvature (Goyalet al.2013).InArabidopsisseedlings,apart from auxin,gibberellic acid and brassinosteroids have also been documented to regulate hypocotyl elongation (de Witet al.2014; Nozueet al.2015),gibberellic acid and jasmonic acid to regulate petiole elongation (Nozueet al.2015),abscisic acid to regulate auxiliary bud growth (Reddyet al.2013) while changes in auxin and ethylene levels might restrict root growth (Růžičkaet al.2007; Stepanovaet al.2007). An increase in the auxin to cytokinin ratio in leaf meristem ofArabidopsisexposed to shade inhibits the leaf development(Carabelliet al.2007). While lower values of PAR have been reported to promote growth and increase the GA levels in the hypocotyls and leaves of sunflower (Kurepinet al.2007b),internodes of bean plants (Beallet al.1996) and in the shoots ofArabidopsis(Kurepinet al.2012). Similarly,shade significantly increased the IAA and gibberellin contents while significantly decreased the cytokinin content in young,middle and old leaves of soybean (Wu Yet al.2017).

To counteract shading,some plants evolve shade tolerance strategies that enable them to survive and reproduce at low light intensities (Gommerset al.2013) while other species compete for light,using an escape strategy termed shade avoidance (Casal 2012). Plants initiate shade avoidance responses (SARs) which are a set of responses that plants display upon exposure to encroach vegetation(Yang Cet al.2018). It is a complex phenomenon that involves the modulation of transcriptional and metabolic networks that favour elongation at the expense of leaf development and increase apical dominance,thereby allowing young and growing tissues to escape from shade(Franklin 2008; Keuskampet al.2010; Casal 2012).Moreover,SAR is an important phenomenon in crops growing in dense canopies (Boomsmaet al.2009; Carriedoet al.2016).

9.Conclusion/Future prospective

Redesigning photosynthesis for agronomic and horticultural crops through manipulation of slight shade could be helpful to reduce the drastic effect of shade stress. Light intensity and quality change the structure and functions of photosynthetic apparatus through certain signalling ways including phytohormones and biochemical changes (ROS).The role of subcellular protein organizations and protein phosphorylation changes under different light spectra needs exploration to address the light intensity and quality dilemma.

Acknowledgements

The research was supported by the National Natural Science Foundation of China (31571615) and the earmarked fund for China Agriculture Research System (CARS-04-PS19).