Light intensity and quality are among the most critical environmental factors for crop physiology and biochemistry. Crop plants produce smaller and thinner leaves under low light conditions than corresponding leaves in full sunlight conditions. However, shading environments increased the plant height and lodging rate which hinders the transportation of nutrients, water, and photosynthetic products and ultimately causes huge losses to agriculture production. On the other hand, prolonged exposure of plants to high fluxes of solar light also disturbs the balance between absorbed light energy and capacity of its photochemical utilization resulting in photoinhibition of and eventually in damage to plants.
Sunlight damages photosynthetic machinery, primarily photosystem II (PSII), and causes photoinhibition that can limit plant photosynthetic activity, growth and productivity. The extent of photoinhibition is associated with a balance between the rate of photodamage and its repair. PSII has three functional domains: (i) the antenna of chlorophyll (Chl) and other pigments which absorb and transfer photon energy to (ii) the reaction center where the excited state electron from a special pair of Chl a molecules (P680) is transferred to a series of electron acceptors, the exceptionally strong oxidizing power of P680 drives (iii) the extraction of electrons from water within the oxygen evolving complex (OEC). PSII ultimately supplies biology with the electrons required for the conversion of inorganic molecules into the organic molecules that serve as the building blocks for life.
Photosystem II (PSII) of photosynthesis catalyzes one of the most challenging reactions in nature, the light driven oxidation of water and release of molecular oxygen. PSII couples the sequential four step oxidation of water and two step reduction of plastoquinone to single photon photochemistry with charge accumulation centers on both its electron donor and acceptor sides. Photon capture, excitation energy transfer, and trapping occur on a much faster time scale than the subsequent electron transfer and charge accumulation steps. A balance between excitation of PSII and the use of the absorbed energy to drive electron transport is essential. If the absorption of light energy increases and/or the sink capacity for photosynthetically derived electrons decreases, potentially deleterious side reactions may occur, including the production of reactive oxygen species.
- The PSII proteins (particularly D1) and
surrounding lipid milieu are prone to photodamage by reactive oxygen
species (ROS) under conditions of heightened excitation pressure.
- Electron transfer can either be donor side
inhibited, as when electrons are not available from water to re-reduce the
P680+ radical, or acceptor side inhibited, when electrons
are trapped on QA or QB due to saturated
forward electron transfer away from excited state P680.
- The very high redox potential (+1.2–1.4 V)
of the long lived P680+ radical can drive detrimental
oxidation reactions in the surrounding photosynthetic apparatus when the
donor side is inhibited.
- Incomplete oxidation of water by the OEC is
associated with the formation of H2O2, which can be
oxidized to the superoxide radical (O2•−) by TyrZ or
reduced to the hydroxyl radical (HO•) by manganese released
from the Mn4Ca cluster.
- Acceptor side inhibition promotes reverse
electron transfer from QA to Pheo for charge recombination
of the Pheo− P680+ radical pair. This back
reaction results in a radical pair in the singlet state 1Pheo−
1P680+, which can be converted to the triplet radical
pair 3Pheo− 3P680+. Under conditions
of a more negative QA/QA− midpoint
redox potential, charge recombination of the triplet radical pair (3Pheo−
3P680+) results in the formation of triplet excited state
P680 (3P680*).
- The triplet excitation energy from 3P680*
is readily transferred to the triplet ground state of molecular oxygen (3O2)
forming damaging singlet oxygen (1O2), which can
ultimately lead to the production of other ROS.
- Singlet oxygen can also form in the PSII
antenna complex if there is intersystem crossing of singlet excited state
Chl (1Chl*) to triplet excited state chlorophyll (3Chl*).
- The strong coupling between Chl and carotenoids
typically found in the membrane integral LHC complexes, such as LHCII,
results in excitation energy transfer from 3Chl* to
carotenoid forming the triplet excited carotenoid which relaxes harmlessly
emitting heat.
- Production of ROS by PSII leads not only to PSII-
and thylakoid-specific damage but also oxidative degradation and
damage on a whole cell scale.
- Irreversible photodamage to PSII leads to the
formation of a photoinactivated PSII, requiring lengthy and costly repair
processes, principally via the degradation and de novo
synthesis of the D1 proteins.
- The deleterious effects of ROS are stopped by
either dissipating the excess excitation energy before it is transferred
to molecular oxygen, or by cleaning up ROS species before extensive damage
can incur, via the activity of ROS scavengers and antioxidants.
- High excitation pressure can stem from daily
and seasonal transitions in incident sunlight intensity, and from other
environmental factors that affect photosynthetic electron sink capacity
such as salt, nutrient, temperature, pathogen, or
desiccation stress.
- If the rate of D1 turnover can't keep up with
the rate of PSII photoinactivation, there is a net loss in functional
PSII, a condition described as photoinhibition.
Plants have developed a large number of photoprotective mechanisms to prevent photoinhibition and oxidative stress caused by excess or fluctuating light conditions. Absorption of light depends on leaf angle, sun elevation in the sky, the finite width of the sun's disc, changes in special distribution of Q through the canopy, multiple reflections of Q within the canopy, and the arrangement of leaves in the canopy. Most plants have characteristic angles such as Upright in desert, high latitude trees and crowded plants; Prostrate in cold and icy winds areas.
Similarly, four key groups of photoprotective pigments are known that play a crucial role in photoprotection viz. mycosporine-like amino acids, phenolic compounds (including phenolic acids, flavonols, and anthocyanins), alkaloids (betalains), and carotenoids. The accumulation of UV-absorbing compounds (mycosporine-like amino acids and phenolics in lower and higher plants, respectively) is a ubiquitous mechanism of adaptation to and protection from the damage by high fluxes of solar radiation developed by photoautotrophic organisms at the early stages of their evolution.
Mycosporine-like amino acids (MAA)
Many lower plants, including red and green algae and dinoflagellates accumulate mycosporine like amino acids (MAA), the compounds resembling water-soluble mycosporines initially discovered in fungi MAA have molar extinction coefficients in the range 24–50/(mM cm). These compounds possess no measurable fluorescence and do not form free-radical products upon irradiation. Due to a low quantum yield of triplet formation, it is unlikely than MAA could exert a photodynamic effect via 1O2 generation. MAA were reported to be efficient 1O2 quenchers. Thus, mycosporine glycine in its ground state prevented photodamage of some bacteria by photosensitizer-generated 1O2.
Phenolic compounds
Phenolic compounds were found in every plant species and, to the date, more than 100 000 phenolic species are known. These compounds are characterized by an extreme diversity of chemical structure in plants. Phenolic compounds are synthesized mostly in chloroplasts or cytoplasm and, after glycosylation, they are transported to and accumulated mainly in the vacuoles. Many Phenols possess a strong antiradical activity in vitro. Various Phenols serve a plethora of protective functions in plants. The molar absorption coefficients of the most of Phenols are within the range of 10–35/(mM cm). In the case of flavonols common for plants (quercetin and kaempferol glycosides), the in vivo tautomerization induces more profound bathochromic shifts of their long-wave absorption maxima. Betalains. This is an individual group of water-soluble nitrogen-containing compounds (alkaloids) of limited occurrence within flowering plants. Two classes of betalains are distinguished: purple-to-rose betacyanins and yellowish betaxanthins. These classes of betalains are formed by conjugation of betalamic acid chromophore with cyclodioxiphenylalanine or other amino acids, respectively Betalains also occur in plants as glycosides, acylglycosides or more complex forms: the esters with ferulic acid and flavonol conjugates synthesized as a result of UV irradiation. Absorption spectra of betacyanins are characterized by a broad band with the maximum near 593–543 nm; a bathochromic shift to 550 nm is possible as a result of intramolecular copigmentation. The spectra of betaxanthins feature three main bands with the maxima near 217, 262, and 546–471 nm. Betalains are free-radical scavengers, more efficient at alkaline and neutral pH. Betalains are suggested to fulfill the function of Anthocyanin in the species lacking the latter but accumulating high amounts of betalains.
Carotenoids
Carotenoids are the accessory pigments ubiquitous in photoautotrophs; they participate in light-harvesting, fulfill photoprotective function, and stabilize the pigment–protein complexes of the PSA. They are the terpenoid compounds formed via condensation of eight isoprenoid monomers. Yellow-to-orange carotenoids are formed as a result of the stepwise desaturation of their colorless precursors. In higher plants, they could be synthesized in the dark but their quantity and composition are controlled by blue-light and UV receptors. Their molar absorption coefficient in the maximum located in the blue-green region of the spectrum could be as high as 180/(mM cm). The major carotenoids of higher plants include β-carotene and a number of xanthophylls such as lutein, neoxanthin, violaxanthin, antheraxanthin, and zeaxanthin. Carotenoids are potent scavengers of free radicals, including free-radical forms of oxygen. Certain Carotenoids undergo cyclic transformations known as xanthophyll cycles, which yield the carotenoids species capable of efficient thermal dissipation of the excitation energy of Chl preventing the photodamage to the PSA.
Leaf Movement
Leaf movement is also affected by ambient growth conditions, such as light intensity, temperature, and water and nutrient availability. The heliotropism displays two forms: (i) diaheliotropism (the leaf lamina becomes oriented at an angle perpendicular to the direction of light); and (ii) paraheliotropism (the leaf lamina becomes oriented at an angle parallel to the direction of light). Paraheliotropism is associated with minimizing the absorption of solar radiation and avoids absorbing excessive light energy for photosynthesis. Interruption of the diurnal heliotropic leaf movement causes acceleration of photoinhibition in Phaseolus vulgaris. Leaf movement might also act to avoid inhibition of the repair of photodamaged PSII by reducing ROS production associated with excess light absorption by the photosynthetic pigments and electron transport reactions to O2 at PSI and PSII.
Chloroplast movement
Chloroplasts also change their position in the cell to optimize the intensity of light for photosynthesis in plants, ferns, mosses and green algae. Chloroplasts gather at cell walls perpendicular to the direction of the light to capture weak light efficiently (accumulation response). By contrast, under strong light, chloroplasts gather at cell walls parallel to the direction of the light to avoid the absorption of excessive light (avoidance response) and to maximize absorption of CO2 from the intercellular air spaces. CHUP1 (Chloroplast unusual positioning1) protein that is located on the chloroplast outer envelope also plays indispensable role.
Sources
Shunichi Takahashi, Murray R. Badger, Photoprotection in plants: a new light on photosystem II damage, Trends in Plant Science,Volume 16, Issue 1, 2011, Pages 53-60, ISSN 1360-1385, https://doi.org/10.1016/j.tplants.2010.10.001.
Feng L, Raza MA, Li Z, Chen Y, Khalid MHB, Du J, Liu W, Wu X, Song C, Yu L, Zhang Z, Yuan S, Yang W and Yang F (2019) The Influence of Light Intensity and Leaf Movement on Photosynthesis Characteristics and Carbon Balance of Soybean. Front. Plant Sci. 9:1952. doi: 10.3389/fpls.2018.01952.
Takahashi, Shunichi & Badger, Murray. (2010). Photoprotection in Plants: A new Light on Photosystem II Damage. Trends in plant science. 16. 53-60. 10.1016/j.tplants.2010.10.001.