Phenol-Oxidizing Peroxidases Contribute to the Protection of Plants from Ultraviolet Radiation Stress^{<a href="#FN1" rid="FN1" class=" fn">1</a>}

Abstract

UV-B (280–315 nm) radiation is a minor component of the solar spectrum, yet it has the potential to disproportionately affect metabolic processes in humans, animals, plants, and microorganisms. In plants, UV-B can potentially interfere with growth, development, photosynthesis, flowering, pollination, and transpiration (Rozema et al., 1997; Jansen et al., 1998). The molecular targets of UV-driven photomodification and photosensitisation reactions (Greenberg et al., 1997) include nucleotides, aminoacids, lipids, and pigments (Jordan, 1996). The UV-driven inactivation of photosystem II (PSII) has attracted considerable attention. PSII is a protein pigment complex, the core of which is formed by the D1 and D2 proteins (Barber et al., 1997). Degradation of the D1 and D2 reaction center proteins is driven by UV-B fluence rates as low as 1 μmol m ^{s (}Jansen et al., 1996a). Many UV effects are abated in the presence of a background of visible radiation (Cen and Bornman, 1990). However, UV-driven D1-D2 degradation is strongly accelerated in the presence of visible radiation (Jansen et al., 1996a). The acceleration is likely to reflect increased UV absorbance of a photosensitizer charged during photosynthetic electron flow, vis-à-vis the uncharged species (Babu et al., 1999). The increase in inactivated PSII centers can be measured as a decrease in oxygen evolution or variable chlorophyll fluorescence (Greenberg et al., 1997). In this study, we have exploited the UV sensitivity of PSII to study the processes that underlie tolerance to broadband UV radiation.

Many of the detrimental UV-B effects on PSII, as well as other targets, are readily observed under laboratory conditions but are difficult to detect in field experiments (Fiscus and Booker, 1995; Rozema et al., 1997; Jansen et al., 1998). A failure to take into consideration naturally occurring tolerance mechanisms is likely to contribute to the discrepancy between laboratory and field studies (Jansen et al., 1998). Repair and acclimation responses are readily induced in response to UV exposure in many species. A typical repair mechanism is the light-dependent photoreactivation by photolyases, resulting in the restoration of UV-damaged DNA to its native form (Britt, 1996). Acclimation responses include increased oxygen radical scavenging activity (Strid et al., 1994; Rao et al., 1996), and the accumulation of soluble UV-screening flavonoids (Cen and Bornman, 1990; Olsson et al., 1999). In addition, polyamines, waxes, and specific alkaloids may contribute to UV tolerance (Jansen et al., 1998). Levels of UV tolerance differ considerably between genera, species, and even closely related cultivars. Efficient protection from UV radiation effects is particularly found among plants that thrive in areas of high UV-B-like lower latitudes or higher altitudes (Sullivan et al., 1992).

Long-term UV acclimation involves increased UV tolerance as well as changes in plant architecture and secondary metabolism. UV-induced changes in plant morphology include increased leaf thickness, altered leaf shape, increased axillary branching, smaller internodes, and decreased plant height (Ziska et al., 1993; Teramura and Sullivan, 1994; Greenberg et al., 1997; Jansen et al., 1998). Some of these responses could involve a specific UV photoreceptor (Ballaré et al., 1995; Greenberg et al., 1997) and may be of greater importance for plant productivity than direct UV effects on photosynthesis (Barnes et al., 1990; Teramura and Sullivan, 1994). UV effects on secondary metabolism include accumulation of phenolic compounds like flavonoids, cinnamate esters, lignin, and tannin (Rozema et al., 1997). A particular difficulty in the analysis of long-term UV acclimation phenomena is distinguishing adaptive responses from UV-B-induced damage. Despite the ecophysiological importance of UV acclimation, little is known about the molecular-physiological mechanisms underlying this response.

We previously demonstrated differences in UV tolerance among a collection of Spirodela punctata G.F.W. Meyer ecotypes (duckweed family; Lemnaceae; Jansen et al., 1999). A constitutively UV-tolerant ecotype (760) was found to be able to sustain PSII activity and biomass accumulation if exposed to UV-B radiation, relative to a UV-sensitive ecotype (203). Protection was found not to be particularly wavelength specific, but rather it covered the broad wavelength area of the UV-A, UV-B, and UV-C bands (Jansen et al., 1999). However, UV-tolerant plants were not protected against other abiotic stresses, including excessive fluences of photosynthetically active radiation (PAR), heat, or chilling. Tolerance in S. punctata could not be correlated with well-characterized UV adaptation responses like increased accumulation of bulk, soluble UV-screening pigments in the epidermis, or increased oxygen radical scavenging activity (Jansen et al., 1999). In this paper, we show that a UV-tolerant S. punctata ecotype (760) contains significantly more free indole-3-acetic acid (IAA) than a UV-sensitive ecotype (203). Parallel work on Lemna gibba mutants indicated that UV tolerance is related to IAA catabolism, rather than to IAA levels. Class III phenolic peroxidases have been implicated in the degradation of the major endogenous auxin, IAA, as well as the cross-linking of various UV-B-absorbing phenolics. The hypothesis that the activity of phenolic peroxidases can, simultaneously, contribute to UV tolerance as well as auxin catabolism was tested in a direct manner using transgenic tobacco (Nicotiana sylvestris) plants altered in their peroxidase levels. Increased peroxidase activity was found to be correlated with increased UV tolerance and decreased IAA levels. Thus, we conclude that peroxidases play a role in UV protection.

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LITERATURE CITED