Abstract
In Chap. 6, we discussed leaf traits that are related to reflection or avoidance of high radiation loads in high-light environments. Many plants lack these adaptations, and absorb potentially damaging levels of radiation. In this chapter, we discuss some of the negative effects of excess radiation and the physiological mechanisms by which some plants avoid damage (Sect. 7.2.1). Effects of ultraviolet radiation and plant mechanisms to avoid or repair damage are treated in Sect. 7.2.2. Finally, we discuss some effects of both high and low temperatures in Sect. 7.3.
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7.1 Introduction
In Chap. 6, we discussed leaf traits that are related to reflection or avoidance of high radiation loads in high-light environments. Many plants lack these adaptations, and absorb potentially damaging levels of radiation. In this chapter, we discuss some of the negative effects of excess radiation and the physiological mechanisms by which some plants avoid damage (Sect. 7.2.1). Effects of ultraviolet radiation and plant mechanisms to avoid or repair damage are treated in Sect. 7.2.2. Finally, we discuss some effects of both high and low temperatures in Sect. 7.3.
7.2 Radiation
7.2.1 Effects of Excess Irradiance
Species that are adapted to shade often have a restricted capacity to acclimate to a high irradiance. Unacclimated plants have a low capacity to use the products of the light reactions for carbon fixation, and tend to be damaged by high irradiance levels, because the energy absorbed by the photosystems exceeds the energy that can be used by carbon-fixation reactions. The excess energy can give rise to the production of reactive oxygen species (ROS) (i.e. toxic, reactive oxygen-containing molecules that rapidly lose an electron) and radicals (molecules with unpaired electrons) that break down membranes and chlorophyll (photodamage) (Sect. 2.3.3). Acclimated plants have protective mechanisms that avoid this photodamage. For example, the energy absorbed by the light-harvesting complex may be lost as heat through reactions associated with the xanthophyll cycle . When the cycle converts violaxanthin to zeaxanthin or antheraxanthin, nonradiative mechanisms dissipate energy (Sect. 2.3.3.1). When zeaxanthin is present and the thylakoid lumen is acidic, excess light energy is lost as heat. Chlorophyll fluorescence analysis can detect this non-photochemical quenching of excess light energy (Box 2.4; Sect. 2.3.1).
7.2.2 Effects of Ultraviolet Radiation
Effects of ultraviolet (UV) radiation on plants have been studied for more than a century. The finding that the stratospheric UV-screening ozone layer has been substantially depleted due to human activities, however, has increased interest in this topic. Ozone in the Earth’s atmosphere prevents all of the UV-C (<280 nm) and most of the UV-B (280–320 nm) radiation from reaching the Earth’s surface (Fig. 7.1). Due to differences in optical density of the atmosphere, the UV radiation reaching the Earth is least at sea level in polar regions, and greatest at high altitude and low latitude (e.g., the Andes). Cloud cover greatly reduces solar UV irradiance.
7.2.2.1 Damage by UV
Many compounds in plant cells absorb photons in the UV region (Fig. 7.1); the most destructive actions of UV include effects on nucleic acids. DNA is by far the most sensitive nucleic acid. Upon absorption of UV, polymers of pyrimidine bases, termed cyclobutane-pyrimidine dimers , are formed, which leads to loss of biological activity. Although RNA and proteins also absorb UV radiation, much higher doses are required for inactivation to occur, possibly due to their higher concentration in the cell compared with that of DNA. ROS play a role in mediating effects of UV-B: membranes are damaged due to lipid peroxidation (Jansen et al. 1998; Verdaguer et al. 2017).
Algae and bacteria are considerably more sensitive to UV-B radiation than are leaves of higher plants, due to less shielding of their DNA. Higher plants that are sensitive to solar UV show a reduction in photosynthetic capacity, leaf expansion, and height; they tend to have thicker leaves, which are often curled, and increased axillary branching. Although part of the reduced leaf expansion may be the result of reduced photosynthesis, it also involves direct effects on cell division (Caldwell 1981), with both effects leading to reductions in plant growth and productivity. There may be additional effects on plant development, e.g., on leaf epidermal cell size and leaf elongation in Deschampsia antarctica (Antarctic hair grass) (Ruhland and Day 2000).
7.2.2.2 Protection Against UV: Repair or Prevention
Damage incurred by DNA due to UV absorption can be repaired at the molecular level by splitting the pyrimidine dimers, in plants as well as other eukaryotes including humans (Molinier 2017; Elliott et al. 2018). Identification, followed by excision of the lesions from a DNA molecule and replacement by an undamaged patch using the other strand as a template has also been demonstrated. Plants remove UV photoproducts from their genomic DNA through a dual-incision mechanism that is nearly identical to that in humans and other eukaryotes (Canturk et al. 2016). Scavenging of ROS can also alleviate UV-B stress; levels of key antioxidants (glutathione and ascorbate) and enzymes that detoxify ROS [e.g., superoxide dismutase (SOD) and ascorbate peroxidase] are upregulated in response to UV-B (Fig. 7.2; Janssens et al. 1998).
Plants can minimize UV exposure by having steeply inclined leaves, especially at lower latitudes and by reflecting or absorbing UV in the epidermis (Barnes et al. 2015). Epidermal cells may selectively absorb UV, because of the presence of phenolic compounds (specific flavonoids) (Martz et al. 2007). A UV-B photoreceptor (UVR8) senses UV-B, and this triggers the accumulation of UV-absorbing pigments, but not changes in plant morphology (Coffey et al. 2017). In wild populations of Betula pubescens (white birch) in a large climatic transect in Finland, concentrations of quercetin derivatives are positively correlated with latitude (Fig. 7.3). By contrast, the concentrations of apigenin and naringenin derivatives are negatively correlated with latitude. These compound-specific latitudinal gradients compensate each other, resulting in no changes in the concentration of total flavonoids (Stark et al. 2008). Since the antioxidant capacity of quercetin derivatives is greater than that of other flavonoids, the qualitative change reflects acclimation or adaptation to strong light in the north. Along an elevation gradient in Hawaii spanning 2600–3800 m, leaf epidermal UV-A transmittance is strongly correlated with elevation and relative biologically effective UV-B in the exotic Verbascum thapsus (common mullein); however, transmittance is consistently low, and does not vary with elevation in the native Vaccinium reticulatum (ohelo 'ai) (Barnes et al. 2017). UV radiation is the primary factor driving the variation in leaf phenolics across Chinese grasslands (Chen et al. 2013). The concentration of UV-protecting compounds can change rapidly, even on a diurnal basis (Barnes et al. 2015).
In addition to flavonoids , sinapate esters of phenolics provide some protection against UV in Brassicaceae [e.g., Arabidopsis thaliana (thale cress)] (Sheahan 1996; Dean et al. 2014). The most effective location for compounds to screen UV is in the cell walls of epidermal cells , rather than in their vacuoles, where phenolics may also accumulate. The epidermis of evergreens transmits, on average, approximately 4% of the incident UV, and it does not allow penetration beyond 32 μm, as opposed to, on average, 28% and 75 μm, respectively, for leaves of deciduous plants (Day 1993). Conifer needles screen UV-B far more effectively, because the absorbing compounds are located in the cell walls as well as inside their epidermal cells. The epidermis of herbaceous species is relatively ineffective at UV-B screening, because UV-B may still penetrate through the epidermal cell walls, even if their vacuoles contain large amounts of UV-absorbing phenolics (Day et al. 1994). Polyamines , waxes, and specific alkaloids may also contribute to UV tolerance, either because they absorb UV , or because they act as scavengers of ROS (Frohnmeyer and Staiger 2003).
Exposure of Phaseolus vulgaris (common bean) to elevated levels of UV-B enhances nodulation, which is affected by flavonoids (Sect. 12.3.3) (Pinto et al. 2002). Leaf phenolic concentrations in Eriophorum russeolum (cotton grass) are increased at high levels of UV-B. At the end of the growing season, the proportion of total soluble phenolics is greater in leaves exposed to enhanced UV-A and UV-B radiation than in control leaves, but the phenolic composition is not affected (Martz et al. 2011). In Epilobium angustifolium (willow herb), there is no UV effect. Since both these species are reindeer (Rangifer tarandus tarandus) forage plants , there might be a shift in preference in favor of Epilobium angustifolium, but there is no information to support this suggestion.
7.3 Effects of Extreme Temperatures
7.3.1 How Do Plants Avoid Damage by Free Radicals at Low Temperature?
Variation in growth potential at different temperatures may reflect the rate of photosynthesis per unit leaf area, as discussed in Sect. 2.7. A common effect of chilling is photooxidation , which occurs because the biophysical reactions of photosynthesis are far less temperature-sensitive than are the biochemical ones. Chlorophyll continues to absorb light at low temperatures, but the energy cannot be transferred to the normal electron-accepting components with sufficient speed to avoid photoinhibition (Raven, 2011). One mechanism by which cold-acclimated plants avoid photooxidation is to increase the components of the xanthophyll cycle (García-Plazaola et al. 2015), just as observed at excess radiation (Sect. 2.3.3.1). This prevents the formation of ROS ; radicals may form when oxygen is reduced to superoxide (Apel and Hirt 2004; Mittler 2017). The xanthophyll cycle is widespread among plants, however, and other mechanisms also protect the photosynthetic apparatus of cold-adapted species, especially if low temperatures coincide with high levels of irradiance, such as at high altitude.
Once ROS are formed, they must be scavenged to avoid their damaging effect. Upon exposure to oxidative stress, some ROS are produced in nonacclimated plants which induce the expression of genes encoding enzymes involved in the synthesis of phenolic antioxidants (Mittler 2017). High-alpine species contain higher concentrations of a range of antioxidants, such as ascorbic acid (vitamin C), α-tocopherol (vitamin E), and the tripeptide glutathione (Wildi and Lütz 1996). Their concentrations increase with increasing altitude (Fig. 7.4). The higher level of antioxidants in the high-altitude plants enables them to cope with multiple stresses, including lower, early-morning temperature, higher level of irradiance at peak times, or higher levels of UV-B . The concentrations of antioxidants also show a diurnal pattern, with highest values at midday and lower ones at night. Superoxide dismutase (SOD) and catalase are major enzymes that are involved in avoiding damage by ROS (Mittler 2017). SOD catalyzes the conversion of superoxide to hydrogen peroxide (H2O2), and catalase converts H2O2 to water and oxygen.
7.3.2 Heat-Shock Proteins
A sudden rise in temperature, close to the lethal temperature, induces the formation of mRNAs encoding heat-shock proteins (Parcellier et al. 2003). Some of the genes encoding heat-shock proteins are homologous with those from animals; in fact, heat-shock proteins were first discovered in Drosophila . Some of these proteins are only produced after exposure to high temperatures; others are also found after exposure to other extreme environmental conditions (e.g., low temperature, water stress, high light, and drought). There is some evidence that an increase in membrane fluidity specifically enhances the expression of genes encoding heat-shock proteins (Xiong et al. 2002).
Heat-shock proteins may be involved in the protection of the photosynthetic apparatus and prevent photooxidation. Some act as molecular chaperones to prevent irreversible aggregation of stress-labile proteins (Santhanagopalan et al. 2015). Chaperones are involved in arranging the tertiary structure of proteins. Heat-shock proteins are formed both after a sudden increase in temperature, and upon a more gradual and moderate rise in temperature, although not to the same extent. This class of proteins is, therefore, probably also involved in the tolerance of milder degrees of heat stress (Parcellier et al. 2003).
7.3.3 Are Isoprene and Monoterpene Emissions an Adaptation to High Temperatures?
There is increasing evidence that plants, especially some tree species and ferns, can cope with rapidly changing leaf temperatures through the production of the low-molecular-mass hydrocarbon: isoprene and monoterpenes (Dani et al. 2014). Around Sydney in Australia, these hydrocarbons account for the haze in the Blue Mountains (Nelson 2001). Isoprene (2-methyl-1,3-butadiene) is the single most abundant biogenic, nonmethane hydrocarbon entering the atmosphere due to emission by plants in both temperate and tropical ecosystems, and the reason for these high emission rates have puzzled scientists for a long time (Sharkey et al. 2008). Many isoprene-emitting species lose about 15% of fixed carbon as isoprene, with extreme values up to 50%. Global isoprene emissions from plants to the atmosphere amount to 180–450 1012 g carbon per year, more than any other volatile organic carbon lost from plants (Lichtenthaler, 2007). There should be sufficient evolutionary pressure to eliminate this process, if it serves no function. The finding that emissions increase at high temperature and under water stress has stimulated research into a role in coping with high leaf temperatures. The change in isoprene-emission capacity through the canopy is similar to the change in xanthophyll cycle intermediates which suggests that isoprene and monoterpene emission may be the plant’s protection against excess heat, just as the xanthophyll cycle protects against excess light (Loreto and Velikova 2001) (Sect. 2.3.3.1). In the presence of realistic concentrations of isoprene or monoterpenes, leaves are, indeed, protected against high-temperature damage of photosynthesis (Fig. 7.5; Sharkey et al. 2008).
How hot do leaves normally get, if they are not protected in one way or another? Leaves of Quercus alba (white oak) at the top of the canopy can reach a temperature of as much as 14 °C above air temperature, and their temperature may drop by 8 °C within minutes (Singsaas and Sharkey 1998). Using isoprene may be an effective way of changing membrane properties rapidly enough to track leaf temperature. In plants that are not subject to such high temperatures or changes in leaf temperature, slower and less wasteful methods may be more effective.
7.3.4 Chilling Injury and Chilling Tolerance
Many (sub)tropical plants grow poorly at or are damaged by temperatures between 10 and 20 °C. This type of damage is quite different from frost damage, which occurs at subzero temperatures, and is generally described as chilling injury. Different parts of the plant may differ in their sensitivity to low temperatures, and this may vary with age. Low-temperature conditioning alleviates Prunus persica (peach) fruit chilling injury, resulting in a faster rate of ethylene production and a more rapid flesh softening as a result of higher expression of ethylene biosynthetic genes and a series of cell wall hydrolases (Wang et al. 2017). Reduced internal browning of fruit is observed in conditioned plants, with lower transcript levels of polyphenol oxidase and peroxidase. Conditioned fruits also show increased lipid desaturation. Conditioning is a special case of cold acclimation.
The physiological cause of low-temperature damage varies among species and plant organs. The following factors play a role:
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Changes in membrane fluidity;
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Changes in the activity of membrane-bound enzymes and processes, such as electron transport in chloroplasts and mitochondria, and in compartmentation;
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Loss of activity of low-temperature sensitive enzymes;
Chilling tolerance correlates with a high proportion of cis-unsaturated fatty acids in the phosphatidyl-glycerol molecules of chloroplast membranes. Evidence for this comes from work with Nicotiana tabacum (tobacco) plants transformed with glycerol-3-phosphate acyltransferase from either a cold-tolerant species or a cold-sensitive one. Overexpression of the enzyme from the cold-tolerant species increases cold-tolerance, whereas the tobacco plants become more sensitive to cold stress when overexpressing the enzyme from cold-sensitive plants. Cold sensitivity of the transgenic tobacco plants correlates with the extent of fatty acid unsaturation in phosphatidylglycerol which is due to different selectivities for the saturated and cis-unsaturated fatty acids of the enzyme from contrasting sources (Bartels and Nelson 1994).
Heat-shock proteins are expressed at low temperatures (Sabehat et al. 1998), and these probably function in much the same way as discussed in Sect. 7.3.2.
7.3.5 Carbohydrates and Proteins Conferring Frost Tolerance
Plants exposed to sub-zero temperatures face unique challenges that threaten their survival. The growth of ice crystals in the extracellular space can cause cellular dehydration, plasma-membrane rupture, and eventually cell death (Livingston et al. 2018). Additionally, some pathogenic bacteria cause tissue damage by initiating ice crystal growth at high sub-zero temperatures through the use of ice-nucleating proteins, thus providing access to nutrients from lysed cells (Bredow et al. 2018). Frost damage only occurs at subzero temperatures, when the formation of ice crystals within cells causes damage to membranes and organelles, and dehydration of cells; ice crystals that form outside of cells (e.g., in cell walls) generally cause little damage. Cold tolerance correlates with the concentration of soluble carbohydrates in the cells (Ögren 1997; Shin et al. 2015). These carbohydrates play a role in cryoprotection (Pommerrenig et al. 2018). Differences in cold tolerance between Picea abies (Norway spruce), Pinus contorta (lodgepole pine), and Pinus sylvestris (Scots pine), following exposure of hardened needles to 5.5 °C, are closely correlated with their carbohydrate concentration. Picea abies maintains high sugar concentrations by having larger reserves to start with and slower rates of respiration, which decline more rapidly when sugars are depleted (Ögren 1997; Ögren et al. 1997).
Many plants that naturally occur in temperate climates go through an annual cycle of frost hardening and dehardening , with maximum freezing tolerance occurring during winter (Ögren 2001). In many woody plants, short days signal the initiation of cold acclimation, which is mediated by ABA. Freezing tolerance is accompanied by bud dormancy, which is also induced by short days. Despite evidence for gibberellins as negative regulators in growth cessation, and ABA and ethylene in bud formation, understanding of the roles that plant growth regulators play in controlling the activity-dormancy cycle is still very fragmentary (Cooke et al. 2012). In herbaceous plants, frost hardening occurs by exposure to low, nonfreezing temperatures. Antifreeze activity has been detected in more than 60 plant species, and antifreeze proteins have been purified from 15 of these, including gymnosperms, dicots, and monocots (Gupta and Deswal 2014). Their main function is inhibition of ice crystal growth, rather than the lowering of freezing temperatures (Fig. 7.6; Bravo and Griffith 2005; Bredow and Walker 2017). Specific antifreeze proteins accumulate in the apoplast of Secale cereale (winter rye) and other frost-resistant species. These proteins have the unusual ability to bind to and inhibit the growth of ice crystals (Doxey et al. 2006). Ice-binding surfaces for a diverse range of antifreeze proteins clearly discriminates them from other structures in the Protein Data Bank. Knockdown of ice-binding proteins in Brachypodium distachyon (false broom) demonstrates their role in freeze protection (Bredow et al. 2016). Antifreeze proteins that accumulate in several places in the apoplast of rye have no specific cryoprotective activity; rather, they interact directly with ice and reduce freezing injury by slowing the growth and recrystallization of ice (Griffith et al. 2005).
Exposure of Triticum aestivum (wheat) to low temperature induces a dehydrin ; dehydrins are a class of proteins that are related to the products of late embryogenesis abundant genes, which we discussed in Sect. 5.8.3 (Close 1996). In Picea obovata (Siberian spruce), two dehydrins first appear late in the acclimation process, and they remain at detectable levels throughout the period of maximum low-temperature tolerance (Kjellsen et al. 2013). Different dehydrins likely have separate but overlapping functions in establishing and maintaining extreme low-temperature tolerance. Upon cold-acclimation, a specific glycoprotein (cryoprotectin) accumulates in leaves of Brassica oleracea (cabbage) which protects thylakoids from nonacclimated leaves, both of cabbage and of other species such as Spinacia oleracea (spinach) (Sieg et al. 1996). Cryoprotectin is a plant lipid-transfer protein homologue (Hincha 2002). Plant non-specific lipid-transfer proteins are small, basic proteins present that are involved in key processes such as the stabilization of membranes (Liu et al. 2015). They are also active in plant defense (Sect. 13.2).
7.4 Global Change and Future Crops
Plants are frequently exposed to potential harmful radiation and adverse temperatures. Some of the protective mechanisms in plants are universal (e.g., the carotenoids of the xanthophyll cycle that protect against excess radiation). All plants also have mechanisms to avoid effects of UV radiation and repair UV damage. There is a wide variation among species, however, in the extent of the avoidance and probably also in the capacity to repair the damage. The rapid depletion of the stratospheric UV-screening ozone layer, due to human activities, imposes a selective force on plants to cope with UV.
Toxic ROS are produced when the dark reactions of photosynthesis cannot cope with the high activity of the light reactions. This may occur under high-light conditions, in combination with extreme temperatures. The xanthophyll cycle can prevent some of the potential damage. Isoprene production likely provides additional protection of leaves at high temperatures. Specific proteins and carbohydrates offer protection against temperature extremes. Further ecophysiological research on these compounds and on the regulation of genes that encode their production may help us develop crop varieties that have a greater capacity to cope with extreme temperatures. Such plants will be highly desirable for agriculture in those parts of the world where extreme temperatures are a major factor limiting crop productivity.
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Lambers, H., Oliveira, R.S. (2019). Plant Energy Budgets: Effects of Radiation and Temperature. In: Plant Physiological Ecology. Springer, Cham. https://doi.org/10.1007/978-3-030-29639-1_7
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Publisher Name: Springer, Cham
Print ISBN: 978-3-030-29638-4
Online ISBN: 978-3-030-29639-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)