Tuesday, March 01, 2005

UV-B Radiation Stress in Plants


Our nearest star, the sun, emits short wavelength radiation that is incident on the earth’s atmosphere. Most of the radiation in the atmosphere is infrared radiation (700-3000 nm, 67% of the photons) and visible light (400-700 nm, 28%; Nobel, 1983). Ultraviolet radiation (UV, 200-400 nm), on the other hand, reaches the atmosphere in smaller amounts (5% of the photons). The biologically most hazardous part of UV radiation, i.e. UV-C (200-280 nm) and UV-B (280-320 nm) below 290 nm, are completely absorbed by the stratospheric ozone (O3) layer and by other oxygen molecules in the atmosphere (Frederick, 1993). In addition, the ozone layer absorbs some longer-wave UV-B and UV-A radiation (320-400 nm) (Fig. 1). Consequently, of the photons at the earth’s surface, only about 2% are in the ultraviolet range (Nobel, 1983). However, of the total solar energy reaching the earth’s surface, UV-B radiation comprises about 1.5% and UV-A radiation about 6.4% (Frederick et al., 1989). The intensity of UV-B radiation, in particular, is affected by the thickness of the ozone layer, which in turn varies periodically as a consequence of natural processes such as seasons, winds and solar cycles. In addition, latitude, time of year and time of day determine the length of the path of a UV-B photon through the absorptive ozone layer (Caldwell et al., 1980). 

Fig 1. Ultraviolet spectrum 

On average, the ozone concentration in the stratosphere is low, i.e. about ten ozone molecules per million molecules of air; and it is highly dynamic because the ozone molecules are created and destroyed continuously. However, since the 1970’s, human activities have disrupted the natural balance between synthesis and breakdown of ozone. Depletion of the ozone layer has repeatedly been reported to occur over Antarctica, but in the 1990’s there were also frequent occurrences of major spring-time ozone depletion over the Arctic. It has been found that the main man-made compounds responsible for enhancing ozone breakdown are the chlorofluorocarbons (CFC) (Fig. 2) and nitrogen oxides. Recently, it was also found that the increasing concentrations of greenhouse gases result in stratospheric cooling, thus creating suitable conditions for breakdown of ozone molecules. Therefore, the most recent predictions based on stratospheric chemistry and climate-change models estimate that in the northern areas (60-90° N), compared with the long-term means, the maximum springtime UV-B radiation will increase up to 50-60% in 2010-2020. 

Fig 2. Chlorine atoms induce the decomposition of two ozone molecules into three oxygen molecules in a net chain reaction in which the chlorine atoms are regenerated so that decomposition of ozone continues. 

Effect of UV-B radiation in plants

Elevated levels of UV-B radiation will have many direct and indirect effects on plants (Fig. 3). Even present-day levels of UV-B radiation affect the growth and development of plants. The direct effects of UV-B radiation on plant cells are mostly damaging, because UV-B photons have enough energy to create lesions in important UV-B-absorbing biomolecules such as nucleic acids and proteins. It is known that the photoproducts of DNA formed by UV-B radiation, cyclobutane pyrimidine dimers and pyrimidine (6-4) pyrimidone and (6-4) photoproducts, are all toxic and mutagenic. In addition, the altered DNA and RNA structures may interfere with transcription and replication; and therefore protein synthesis may be slowed down during UV-B stress. In order to avoid the effects of DNA damage, plants have efficient systems for DNA repair, including photoreactivation and excision repair, which are involved in restoring the structure of genetic material during exposure to UV-B radiation. However, the indirect effects of UV-B on plant cells can also be damaging: UV-B radiation may cause oxidative damage in chlorophylls and polyunsaturated lipids by increasing the formation of free radicals and peroxides (Jordan, 1996). To prevent oxidative damage, cells contain antioxidants, e.g., phenolic compounds, that scavenge the free radicals. Phenolic compounds have variable antioxidant properties; and several studies have shown that during UV-B exposure, the production of compounds with efficient antioxidant structures, such as additional hydroxyl groups on ring B of the flavonoid skeleton, is favoured. Plant cells also contain enzymes, e.g., superoxide dismutase (SOD) and catalase, which scavenge superoxide radicals and protect the cells against H2O2, respectively. 

Fig. 3. Effects of UV-B radiation on plant system.

Signal transduction and gene expression 

In addition to damaging plant cell components, UV-B radiation often exerts its effects through altered patterns of gene activity; e.g., the effects of UV-B radiation on photosynthesis, UV-B-screening phenolics, growth, reproductive processes, plant form and timing of life phases, are all caused by altered gene action. The mechanisms by which plants perceive UV-B radiation are not fully understood, but it has been suggested that direct absorption of UV-B by DNA could result in the formation of a “signal” that regulates the transcription of genes.

Signal transduction pathway in relation to UV-B radiation stress. Reactive oxygen species (ROS) increase in response to UV-B and are an important component in the regulation of both up-regulated and down-regulated genes. The nature and origin of the ROS involved in the early part of UV-B induced signalling pathways have been investigated in Arabidopsis thaliana. The increase in PR-1 transcript and decrease in light harvesting chlorophyll binding gene (Lhcb) transcript in response to UV-B exposure was shown to be mediated through pathways involving hydrogen peroxide (H2O2) derived from superoxide (O2•-). In contrast, the up-regulation of PDF1.2 transcript was mediated through a pathway involving O2•-- directly. The origins of the ROS were also shown to be distinct and to involve NADPH oxidase and peroxidase(s). The upregulation of CHS by UV-B was not affected by ROS scavengers, but was reduced by inhibitors of nitric oxide synthase (NOS) or NO scavengers. Together these results suggest that UV-B exposure leads to the generation of ROS, from multiple sources, and NO, through increased NOS activity, giving rise to parallel signalling pathways mediating responses of specific genes to UV-B radiation (Fig. 4).
In addition, it has been hypothesized that in plant cells, specific UV-B photoreceptor-mediated signalling processes regulate gene expression. However, the characteristics of a UV-B photoreceptor and how the signals are transduced after UV-B perception, are not yet known.
In addition to the increase in ROS other known signal transduction intermediates increase their levels. These include salicyclic acid (SA), jasmonic acid (JA) and ethylene. Using Arabidopsis mutants that are insensitive to SA, JA and ethylene (NahG, jar 1 and etr 1-1 respectively), clear differences in gene activity response have been demonstrated. For instance, an increase in expression of the two pathogen-related genes PR-1 and PDF1.2 are depended on SA and ethylene or JA and ethylene respectively. In contrast, down-regulation of RNA transcripts for photosynthetic proteins was independent of all three compounds. Furthermore, although ROS is involved in down-regulation of RNA for photosynthetic proteins, the chloroplast signal may not be involved.There are at least three separate signal transduction pathways involved in UV-B gene regulation and substantial “cross-talk” must take place.
A unique response of plants to UV-B radiation relates to the property of high photosynthetically active radiation (PAR) to ameliorate its damaging impact. The interaction of UV-B and PAR was initially discovered at the physiological level, but Jordan et al., (1992) demonstrated that high PAR also reduced down-regulation of gene expression. This ‘protection’ against UV-B damage did not involve synthesis of protective pigments, but was related to the function of the photosynthetic apparatus itself. The photosynthetic system can act as a photoreceptor and specific wavelengths can change chloroplast gene expression. Research conducted by Jordan et al., (1994) on etiolated tissue is also indicative of a strong link between the development of the photosynthetic apparatus and UV-B-induced gene expression. The connections between UV-B radiation and photosynthesis, and the signal transduction pathways that lead to modification of gene expression are yet to be comprehended.

Fig.4.  Schematic illustration of signal transduction pathways induced by UV-B radiation

It was found that in genetically modified tobacco (Nicotiana sylvestris) increased activity of the anionic peroxidase correlated with increased tolerance to UV radiation as well as decreased levels of free auxin indicating that phenol-oxidizing peroxidases concurrently contribute to UV protection as well as the control of leaf and plant architecture.  

Caldwell, C.R. 1993. Ultraviolet-induced photodegradation of cucumber (Cucumis sativus L.) microsomal and soluble protein tryptophanyl residues in vitro. Plant Physiology 101:947-953.

Frederick, J.E. 1993. Ultraviolet sunlight reaching the Earth’s surface: a review of recent research. Photochemistry and Photobiology 57:175-178.

Nobel, P.S. 1983. Biophysical Plant Physiology and Ecology. Freeman & Co., New York, pp.185-238.

Jordan, B.R. 1996. The effects of ultraviolet-B radiation on plants: a molecular perspective. In: Callow, J.A. (editor). Advances in Botanical Research, Vol 22. Academic Press, New York, pp. 97-162.

Jordan, B.R., P. James and S.A-H. Mackerness. (1998). Factors affecting UV-B induced changes in Arabidopsis thaliana gene expression: role of development, protective pigments and the chloroplast signal. Plant & Cell Physiolog, 39: 769-778.

Jordan, B.R., J. He, W.S. Chow and J.M. Anderson. Changes in mRNA levels and polypeptide subunits of ribulose bisphosphate carboxylase in response to supplemental UVB radiation. Plant, Cell and Environment 15: 91-98, 1992.