Light quality as a driver of photosynthetic apparatus development

Abstract

Light provides energy for photosynthesis and also acts as an important environmental signal. During their evolution, plants acquired sophisticated sensory systems for light perception and light-dependent regulation of their growth and development in accordance with the local light environment. Under natural conditions, plants adapted by using their light sensors to finely distinguish direct sunlight and dark in the soil, deep grey shade under the upper soil layer or litter, green shade under the canopy and even lateral green reflectance from neighbours. Light perception also allows plants to evaluate in detail the weather, time of day, day length and thus the season. However, in artificial lighting conditions, plants are confronted with fundamentally different lighting conditions. The advent of new light sources - light-emitting diodes (LEDs), which emit narrow-band light - allows growing plants with light of different spectral bands or their combinations. This sets the task of finding out how light of different quality affects the development and functioning of plants, and in particular, their photosynthetic apparatus (PSA), which is one of the basic processes determining plant yield. In this review, we briefly describe how plants perceive environment light signals by their five families of photoreceptors and by the PSA as a particular light sensor, and how they use this information to form their PSA under artificial narrow-band LED-based lighting of different spectral composition. We consider light regulation of the biosynthesis of photosynthetic pigments, photosynthetic complexes and chloroplast ATP synthase function, PSA photoprotection mechanisms, carbon assimilation reactions and stomatal development and function.

Keywords: LED lighting; Light quality; Photosynthetic apparatus regulation; Photosynthetic carbon assimilation; Photosynthetic pigment synthesis; Stomata.

Fig. 1

The scheme of the photosynthetic apparatus components and their interactions. Chlorophyll (Chl) and carotenoids (Car) are synthesised in plastids by nuclear coded enzymes (Yuan et al. ; Sun et al. 2018) and used for photosynthetic pigment-protein complex assembly. Electron transport chain (ETC) consists of the two photosystems, PSII and PSI, cytochrome b₆f complex (b₆f) and mobile electron carriers: plastoquinone pool (PQH₂/PQ) in the thylakoid membrane, plastocyanin (PC) in the lumen and ferredoxin (Fd) in the stroma. Light harvesting antennae, LHCII and LHCI, help to harvest light for PSII and PSI, respectively. Linear electron transport through ETC from H₂O to NADPH provides H⁺ cross-membrane transport and produces the proton gradient. ATP synthase uses this gradient energy for ATP synthesis. Calvin cycle of carbon assimilation from CO₂ to sugars consumes NADPH and ATP, produced by ETC. Generated trioses may be stored transiently in the chloroplast as starch or are exported and transported to other organs as sucrose and other sugars (Raines 2003). A part of the mobile pool of LHCII can disconnect from PSII with the help of serine/threonine kinase STN7 and PsbS subunit and move to PSI or dissipate absorbed light energy to heat (red curly arrows). Violaxanthin de-epoxidase (VDE) converts violaxanthin to zeaxanthin which quenches light energy in LHCII and PSII minor antennae. The major light input targets for photosynthetic apparatus formation, function and regulation are marked with red lightning symbols. Pigment-protein complexes containing Chls and Cars capture light for photosynthesis. Photoreceptors percept light and regulate gene expression and cell metabolism. In particular, photoreceptors control stomata development and opening. The light-dependent step in the Chl biosynthesis pathway is also marked

Fig. 2

Photoregulation of chlorophyll (Chl) biosynthesis by blue (B), red (R), green (G), ultraviolet A (UV-A) and B (UV-B) light. Light-activated UV-B receptor (UVR8), cryptochromes (crys) and phytochromes (phys) inhibit COP1-based E3-ubiquitin-ligase and thus rescue HY5 transcription factor from proteolysis. Light-activated phys also inhibit PIF transcription factors. HY5 induces and PIFs repress Chl biosynthesis-related nuclear genes. Photoreceptor Zeitlupe (ztl) controls some of these genes via regulation of circadian clock. Chl biosynthesis depends on local lipid membrane composition. R and G promote lipid peroxidation (POL) in thylakoid membranes, probably via imperfectly formed PSA, which produces an excessive ROS amount. Dashed arrow — unknown mechanism, probably negative influence. Carotenoids (Cars) modulate Chl synthesis, because proper functioning of some Chl synthesis enzymes also needs the presence of carotenoids in their environment. Double line matches regulation on transcription level

Fig. 3

Photoregulation of carotenoid (Car) biosynthesis by blue (B), red (R), ultraviolet A (UV-A) and B (UV-B) light. Light-activated UV-B receptor (UVR8), cryptochromes (crys) and phytochromes (phys) inhibit COP1-based E3-ubiquitin-ligase and thus rescue HY5 transcription factor from proteolysis. Light-activated phys also inhibit PIF1 transcription factor. Phytoene synthase (PSY), the first and main rate-determining enzyme in the carotenoid biosynthesis pathway, is regulated by HY5 and PIF1 on the transcription level. Violaxanthin de-epoxidase (VDE) transcription is activated by HY5 as well. Low temperature increases HY5 binding with VDE and PSY promoters (Stanley and Yuan 2019). Light-dependent photosynthetic electron transport chain (ETC) decreases pH in lumen, increasing VDE activity. In addition, ETC differently changes the balance of reduced and oxidised plastoquinones (PQs): photosystem II (PSII) and plastidial NADH dehydrogenase (NDH) reduce PQ, and photosystem I (PSI) and plastidial terminal oxidase (PTOX) oxidise PQH₂. Desaturases (two desaturases, phytoene desaturase and ζ-carotene desaturase, catalyse four desaturations from phytoene to lycopene) use oxidised plastoquinone as an electron acceptor for the desaturation reactions (Ruiz-Sola and Rodríguez-Concepción 2012). Zeaxanthin (Zea) is a major Car for photodamage protection in the photosynthetic apparatus. Zea level depends both on the activity of β-carotene hydroxylase, which converts β-carotene to zeaxanthin in the common Car biosynthetic pathway, and on the activity of VDE, which converts violaxanthin back to zeaxanthin (Stanley and Yuan 2019). Light quality regulates the expression of both these enzymes, and light, via lumen acidification, activates VDE post-translationally. Gene names in italics and double lines — regulation at transcription level, regular — regulation at post-translation level — protein level and/or activity

Fig. 4

Light-dependent components of non-photochemical quenching (NPQ) of chlorophyll a fluorescence. Photoregulation of NPQ by blue (B), red (R), green (G) and white (W) light. Photosynthetic electron transport chain (ETC) affects NPQ via lumen acidification (↓pH_lumen) and via change of plastoquinone redox state (↑PQH₂/PQ). Lumen acidification promotes PsbS protein protonation following disconnection of LHCII trimers from PSII and energy dissipation — this is the qE component of NPQ. Lumen acidification also promotes protonation and activation of the violaxanthin de-epoxidase (VDE) following violaxanthin (Viol) to zeaxanthin (Zea) conversion and energy dissipation by Zea — this is the qZ component of NPQ. Reduced plastoquinones via cytochrome b₆f complex activate the serine/threonine kinase STN7, which phosphorylates the mobile antenna LHCII and thus induces its dissociation from PSII and relocation from granal to stromal thylakoids, reducing energy transfer to PSII — this is the qT component of NPQ. Light-induced destruction of PSII (primarily D1 protein) is responsible for the photoinhibition component qI. The qH component of NPQ is connected with the PSII antenna, and its mechanism is yet to be elucidated (dashed arrow). High-intensity (↑I) blue light induces chloroplast avoidance response, decreasing light absorption by Chls. However, the contribution of this process to NPQ and the existence of qM component are questionable (dashed arrow). Several protein effectors of NPQ (PSBS, VDE and PETA for cytf subunit of cytochrome b₆f complex) are regulated by light at the transcriptional level, and the light of different quality induces these genes differently (shown based on data from Trojak and Skowron 2021). The mechanism of light regulation of VDE expression is shown in Fig. 3. Gene names in italics and double lines — regulation at transcription level, regular — regulation at post-translation level — protein level and/or activity

Fig. 5

Photoregulation of stomatal development which determines protodermal cell divisions and resulting stomatal index and stomatal density at epidermis by ultraviolet A (UV-A) and B (UV-B), blue (B), green (G), red (R), and far red (FR) light. a Light spectral ranges and the groups of photoreceptors that participate in the regulation of stomatal pattern. UV-B light acts via UVR8 photoreceptor and via nonspecific absorption by various cell components, regulating stomatal development in an opposite manner. Blue light via phots and crys, red light via phyB and far red light via phyA increase stomatal index. Photosynthetic apparatus (PSA) in underlying mesophyll regulates stomatal index and stomatal density via photosynthetic products and/or carbon dioxide concentration changes. b Key components of the most well-studied signalling pathways involved in photoregulation of stomatal development. Photoreceptors phyA, phyB and crys (cry1/2) act in concert to promote light-induced stomatal development via COP1 (E3-ubiquitin ligase), YDA (MAPK kinase kinase, heading MAPK kinase cascade) and transcription factors (SPCH, MUTE and FAMA — closely related bHLH transcription factors, which regulate consecutive steps in the differentiation pathway of stomata), critical for the development of stomata from the protodermal cell. YDA might be positively regulated by COP1 through yet unknown mechanisms (dashed arrow) and inhibits downstream transcription factors probably via their targeting by phosphorylation. PIF4 transcription factor represses SPCH expression, and phyB, inhibiting PIF4, derepresses SPCH, increasing stomatal development. Besides, light promotes ANGUSTIFOLIA3 (AN3) at transcriptional and post-translational levels, likely through the photoreceptor-mediated pathways (crys and probably phys as well), which then downregulates the expression of COP1 and YDA (Wei et al. 2020). Light-green rectangular matches promoting, and pink rectangular matches restricting conditions for photosynthesis. Double line matches regulation on transcription level

Fig. 6

Photoregulation of stomatal opening which determines stomatal conductance and transpiration rate by ultraviolet A (UV-A) and B (UV-B), blue (B), green (G), red (R) and far-red (FR) light. Light spectral ranges, the groups of photoreceptors and key components in their signalling pathways regulating stomatal opening. UV-B light acts via UVR8 photoreceptor and via nonspecific absorption by various cell components, regulating stomatal opening in an opposite manner, depending on light intensity: high UV-B light (↑I) induces stomatal closure and low UV-B light (↓I) induces stomatal opening. UVR8 closure signalling contains COP1–HY5 module and ethylene, and both closure pathways converge on H₂O₂ and nitric oxide (NO) production. Photoactivated crys act via COP1 as well. Photoactivated phots act via activation of the AHA2 (Arabidopsis H⁺-ATPase 2) in plasma membrane, following ion and water fluxes across plasma membrane and accumulation in vacuoles. phots also induce starch degradation to malate and its accumulation in vacuoles. Photosynthetic apparatus (PSA) in guard cells generates soluble sugars (also accumulating in vacuoles) and energy for all these transmembrane translocators. PSA in mesophyll produces sugars imported into guard cells and decreases intercellular CO₂ concentration, which triggers stomata to open. Blue/UV-A light via ZTL and its entrainment of circadian clock forms circadian rhythms of CO₂ fixation and stomatal opening. The thickness of arrows approximately symbolises relative intensity of the response. Light-green rectangular matches promoting and pink rectangular matches restricting conditions for photosynthesis