Marcel A. K. Jansen

Higher plants and UV-B radiation: balancing damage, repair and acclimation

Abstract Although UV-B is a minor component of sunlight, it has a disproportionately damaging effect on higher plants. Ultraviolet-sensitive targets include DNA, proteins and membranes, and these must be protected for normal growth and development. DNA repair and secondary metabolite accumulation during exposure to UV-B have been characterized in considerable detail, but little is known about the recovery of photosynthesis, induction of free-radical scavenging and morphogenic changes. A future challenge is to elucidate how UV-B-exposed plants balance damage, repair, acclimation and adaptation responses in a photobiologically dynamic environment.

Different stresses, similar morphogenic responses: integrating a plethora of pathways

Exposure of plants to mild chronic stress can cause induction of specific, stress-induced morphogenic responses (SIMRs). These responses are characterized by a blockage of cell division in the main meristematic tissues, an inhibition of elongation and a redirected outgrowth of lateral organs. Key elements in the ontogenesis of this phenotype appear to be stress-affected gradients of reactive oxygen species (ROS), antioxidants, auxin and ethylene. These gradients are present at the the organismal level, but are integrated on the cellular level, affecting cell division, cell elongation and/or cell differentiation. Our analysis of the literature indicates that stress-induced modulation of plant growth is mediated by a plethora of molecular interactions, whereby different environmental signals can trigger similar morphogenic responses. At least some of the molecular interactions that underlie morphogenic responses appear to be interchangeable. We speculate that this complexity can be viewed in terms of a thermodynamic model, in which not the specific pathway, but the achieved metabolic state is biologically conserved.

The cellular redox state in plant stress biology – A charging concept

Different redox-active compounds, such as ascorbate, glutathione, NAD(P)H and proteins from the thioredoxin superfamily, contribute to the general redox homeostasis in the plant cell. The myriad of interactions between redox-active compounds, and the effect of environmental parameters on them, has been encapsulated in the concept of a cellular redox state. This concept has facilitated progress in understanding stress signalling and defence in plants. However, despite the proven usefulness of the concept of a redox state, there is no single, operational definition that allows for quantitative analysis and hypothesis testing.

UV-B-Induced Secondary Plant Metabolites - Potential Benefits for Plant and Human Health

Epidemiological studies have revealed an inverse association between the consumption of fruit, vegetables, and herbs and the risk of both cancer and cardiovascular disease. This protective effect is mostly due to secondary metabolites present in plant tissues. During the last decade, it has become increasingly clear that UV-B radiation is an important regulator of plant secondary metabolism. Low, ecologically-relevant UV-B levels trigger distinct changes in the accumulation of, among others, phenolic compounds, carotenoids and glucosinolates. Fundamental understanding of plant UV-B perception and responses opens up new opportunities for crop manipulation. Thus, targeted low dosage UV-B radiation treatments as emerging technology may be used to generate fruit, vegetables, and herbs enriched with secondary plant metabolites for either fresh consumption or as a source for functional foods and nutraceuticals, resulting in increased ingestion of these health-promoting substances. The UV-B induced accumulation of secondary plant metabolites is likely to have evolved as a plant defense response against harmful UV-B radiation. However, UV-B induced secondary metabolites also alter other trophic interactions, for example by altering plant herbivore resistance. Thus, UV-B driven metabolic changes in the plants secondary metabolism have benefits for both ends of the bio-based food chain, i.e., for plants themselves as well as for humans.

Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance.

Chlorogenic acid (CGA) is one of the most abundant phenolic compounds in tomato (Solanum lycopersicum). Hydroxycinnamoyl CoA quinate transferase (HQT) is the key enzyme catalysing CGA biosynthesis in tomato. We have studied the relationship between phenolic accumulation and UV-susceptibility in transgenic tomato plants with altered HQT expression. Overall, increased CGA accumulation was associated with increased UV-protection. However, the genetic manipulation of HQT expression also resulted in more complex alterations in the profiles of phenolics. Levels of rutin were relatively high in both HQT gene-silenced and HQT-overexpressing plants raised in plant growth tunnels. This suggests plasticity in the flux along different branches of phenylpropanoid metabolism and the existence of regulatory mechanisms that direct the flow of phenolic precursors in response to both metabolic parameters and environmental conditions. These changes in composition of the phenolic pool affected the relative levels of UV-tolerance. We conclude that the capability of the phenolic compounds to protect against potentially harmful UV radiation is determined both by the total levels of phenolics that accumulate in leaves as well as by the specific composition of the phenolic profile.

Re‐interpreting plant morphological responses to UV‐B radiation

There is a need to reappraise the effects of UV-B radiation on plant morphology in light of improved mechanistic understanding of UV-B effects, particularly elucidation of the UV RESISTANCE LOCUS 8 (UVR8) photoreceptor. We review responses at cell and organismal levels, and explore their underlying regulatory mechanisms, function in UV protection and consequences for plant fitness. UV-induced morphological changes include thicker leaves, shorter petioles, shorter stems, increased axillary branching and altered root:shoot ratios. At the cellular level, UV-B morphogenesis comprises changes in cell division, elongation and/or differentiation. However, notwithstanding substantial new knowledge of molecular, cellular and organismal UV-B responses, there remains a clear gap in our understanding of the interactions between these organizational levels, and how they control plant architecture. Furthermore, despite a broad consensus that UV-B induces relatively compact architecture, we note substantial diversity in reported phenotypes. This may relate to UV-induced morphological changes being underpinned by different mechanisms at high and low UV-B doses. It remains unproven whether UV-induced morphological changes have a protective function involving shading and decreased leaf penetration of UV-B, counterbalancing trade-offs such as decreased photosynthetic light capture and plant-competitive abilities. Future research will need to disentangle seemingly contradictory interactions occurring at the threshold UV dose where regulation and stress-induced morphogenesis overlap.

Calcium increases the yield of somatic embryos in carrot embryogenic suspension cultures

An upward shift in the concentration of calcium present in the medium during somatic embryogenesis increased the number of embryos produced approximately two-fold. This was observed when embryogenic suspension cells grown in 2,4-D medium with the normal calcium concentration of 10−3 M were transferred to hormone-free medium containing 10−2 M calcium and when embryogenic suspension cells grown in 2,4-D medium containing 10−4 M calcium were transferred to hormone-free medium with 10−3 M calcium. At calcium concentrations between 6·10−3 and 10−2 M globular stage somatic embryos were found in cultures supplemented with 2·10−6 M of 2,4-D indicating that elevated calcium counteracts the inhibitory effect of 2,4-D on somatic embryogenesis. No qualitative changes were found in the pattern of extracellular polypeptides as a result of growth and embryogenesis in media with different calcium concentrations.

UV-B radiation: from generic stressor to specific regulator

Solar UV-B radiation (280–315 nm) has long been recognized as having a rather diverse environmental role. UV-B mediated-damage and degenerative reactions have been extensively documented. However, the environmental role of UV-B radiation is far broader, encompassing regulation of plant metabolism and morphology (Wargent et al. 2009a, Ballaré et al. 2011), UV-driven photosynthesis of vitamin D3 in human skin (Juzeniene et al. 2011, Norval et al. 2011), provision of informational cues for pollinating insects (Eisner et al. 1969, Indtso et al. 2007), for guiding foraging animals with UV vision towards plants using reflectance or absorption of the UV radiation (Honkavaara et al. 2002, Hogg et al. 2011, Werner et al. 2012), and facilitating mate-choice for spiders through UV-B reflectance (Li et al. 2008). However, the literature on plant UV-B radiation effects has for decades been dominated by reports on UV-B mediated damage, with few studies reporting positive UV-B radiation effects. Indeed, many of the early (1980s–2000s) studies of plant responses to increased UV-B radiation, prompted by reports of stratospheric ozone layer depletion, conveyed the message that UV-B radiation simply causes growth retardation, macroscopic damage and oxidative stress (Caldwell et al. 1994, Searles et al. 2001). These negative effects have been extensively reviewed and comprise damaging effects on DNA, photosynthetic performance and a range of other cellular targets, but were mainly carried out under highly unnatural growth conditions with relatively few studies approaching relevant ambient conditions (for a review see Searles et al. 2001). Perceptions of the biological impact of UV-B radiation on plants have, however, changed dramatically during the last few years. The emphasis has shifted from damage and stress to information and specific regulation, and this has led to a re-appraisal of the environmental role of UV-B radiation. This conceptual change was driven by major advances in the manipulation of UV-B radiation both in the laboratory and the field, as well as further understanding of molecular UV-B perception and physiology (Jenkins 2009, Heijde and Ulm 2012). The manuscripts in this special issue reflect this new understanding of the role of UV-B radiation by plant scientists, and result from discussions between researchers at the first COST-Action UV4Growth network meeting, held in February 2011 in Szeged, Hungary, which focused on bringing together researchers working across the different organisational scales.

Developmental Variability of Photooxidative Stress Tolerance in Paraquat-Resistant Conyza

Paraquat-resistant hairy fleabane (Conyza bonariensis L. Cronq.) has been extensively studied, with some contention. A single, dominant gene pleiotropically controls levels of oxidant-detoxifying enzymes and tolerance to many photooxidants, to photoinhibition, and possibly to other stresses. The weed forms a rosette on humid short days and flowers in dry long days and, thus, needs plasticity to photooxidant stresses. In a series of four experiments over 20 months, the resistant and susceptible biotypes were cultured in constant 10-h low-light short days at 25[deg]C. Resistance was measured as recovery from paraquat. The concentration required to achieve 50% inhibition of the resistant biotype was about 30 times that of the susceptible one just after germination, increased to >300 times that of the susceptibles at 10 weeks of growth, and then decreased to 20-fold, remaining constant except for a brief increase while bolting. Resistance increased when plants were induced to flower by long days. The levels of plastid superoxide dismutase and of glutathione reductase were generally highest in resistant plants compared to those of the susceptibles at the times of highest paraquat resistance, but they were imperceptibly different from the susceptible type at the times of lower paraquat resistance. Photoinhibition tolerance measured as quantum yield of oxygen evolution at ambient temperatures was highest when the relative amounts of enzymes were highest in the resistant biotype. Resistance to photoinhibition was not detected by chlorophyll a fluorescence. Enzyme levels, photoinhibition tolerance, and paraquat resistance all increased during flowering in both biotypes. Imperceptibly small increases in enzyme levels would be needed for 20-fold resistance, based on the moderate enzyme increases correlated with 300-fold resistance. Thus, it is feasible that either these enzymes play a role in the first line of defense against photooxidants, or another, yet unknown mechanism(s) facilitate(s) the lower level of resistance, or the enzymes and unknown mechanisms act together.

The phytohormone auxin is a component of the regulatory system that controls UV-mediated accumulation of flavonoids and UV-induced morphogenesis

In plants, ultraviolet (UV)-B acclimation is a complex, dynamic process that plays an essential role in preventing UV-B damage to targets such as DNA and the photosynthetic machinery. In this study we tested the hypothesis that the phytohormone auxin is a component of the regulatory system that controls both UV-mediated accumulation of flavonoids and UV-induced morphogenesis. We found that the leaf area of Arabidopsis thaliana Col-0 plants raised under a low dose of UV radiation (0.56 kJ m(-2) daily dose) was, on average, decreased by 23% relative to plants raised in the absence of UV-B, and this was accompanied by a decrease (P = 0.063) in free auxin in young leaf tissues. Compared to Col-0, both the auxin influx mutant axr4-1 and the auxin biosynthesis mutant nit1-3 displayed significantly stronger morphogenic responses, i.e. relative decreases in leaf area were greater for these two mutants. UV exposure also induced accumulation of flavonoids. In Col-0, increases in the concentrations of specific kaempferol derivatives ranged from 2.1- to 19-fold. Thus, UV induces complex changes in flavonoid-glycosylation patterns. Compared to Col-0, three auxin mutants displayed significantly different flavonoid profiles. Thus, based on mutant analysis, it is concluded that the phytohormone auxin plays a role in UV acclimation by regulating flavonoid concentration, flavonoid-glycosylation pattern and by controlling UV-induced morphogenic responses.