Dose-responses for solar radiation exposure reveal high sensitivity of microbial decomposition to changes in plant litter quality that occur during photodegradation.

Plant litter decomposition is a key process for carbon (C) turnover in terrestrial ecosystems. Sunlight has been shown to cause and accelerate C release in semiarid ecosystems, yet the dose-response relationships for these effects have not been evaluated. We conducted a two-phase experiment where plant litter of three species was subjected to a broad range of cumulative solar radiation (CSR) exposures under field conditions. We then evaluated the relationships between CSR exposure and abiotic mass loss, litter quality and the subsequent biotic decomposition and microbial activity in litter. Dose-response relationships demonstrated that CSR exposure was modestly correlated with abiotic mass loss but highly significantly correlated with lignin degradation, saccharification, microbial activity and biotic decay of plant litter across all species. Moreover, a comparison of these dose-response relationships suggested that small reductions in litter lignin due to exposure to sunlight may have large consequences for biotic decay. These results provide strong support for a model that postulates a critical role for lignin photodegradation in the mechanism of photofacilitation and demonstrate that, under natural field conditions, biotic degradation of plant litter is linearly related with the dose of solar radiation received by the material before coming into contact with decomposer microorganisms.

Linkages between stratospheric ozone, UV radiation and climate change and their implications for terrestrial ecosystems.

Exposure of plants and animals to ultraviolet-B radiation (UV-B; 280-315 nm) is modified by stratospheric ozone dynamics and climate change. Even though stabilisation and projected recovery of stratospheric ozone is expected to curtail future increases in UV-B radiation at the Earth's surface, on-going changes in climate are increasingly exposing plants and animals to novel combinations of UV-B radiation and other climate change factors (e.g., ultraviolet-A and visible radiation, water availability, temperature and elevated carbon dioxide). Climate change is also shifting vegetation cover, geographic ranges of species, and seasonal timing of development, which further modifies exposure to UV-B radiation. Since our last assessment, there has been increased understanding of the underlying mechanisms by which plants perceive UV-B radiation, eliciting changes in growth, development and tolerances of abiotic and biotic factors. However, major questions remain on how UV-B radiation is interacting with other climate change factors to modify the production and quality of crops, as well as important ecosystem processes such as plant and animal competition, pest-pathogen interactions, and the decomposition of dead plant matter (litter). In addition, stratospheric ozone depletion is directly contributing to climate change in the southern hemisphere, such that terrestrial ecosystems in this region are being exposed to altered patterns of precipitation, temperature and fire regimes as well as UV-B radiation. These ozone-driven changes in climate have been implicated in both increases and reductions in the growth, survival and reproduction of plants and animals in Antarctica, South America and New Zealand. In this assessment, we summarise advances in our knowledge of these and other linkages and effects, and identify uncertainties and knowledge gaps that limit our ability to fully evaluate the ecological consequences of these environmental changes on terrestrial ecosystems.

Soybean resistance to stink bugs (Nezara viridula and Piezodorus guildinii) increases with exposure to solar UV-B radiation and correlates with isoflavonoid content in pods under field conditions.

Solar UV-B radiation (280-315 nm) has a significant influence on trophic relationships in natural and managed ecosystems, affecting plant-insect interactions. We explored the effects of ambient UV-B radiation on the levels of herbivory by stink bugs (Nezara viridula and Piezodorus guildinii) in field-grown soybean crops. The experiments included two levels of UV-B radiation (ambient and attenuated UV-B) and four soybean cultivars known to differ in their content of soluble leaf phenolics. Ambient UV-B radiation increased the accumulation of the isoflavonoids daidzin and genistin in the pods of all cultivars. Soybean crops grown under attenuated UV-B had higher numbers of unfilled pods and damaged seeds than crops grown under ambient UV-B radiation. Binary choice experiments with soybean branches demonstrated that stink bugs preferred branches of the attenuated UV-B treatment. We found a positive correlation between percentage of undamaged seeds and the contents of daidzin and genistin in pods. Our results suggest that constitutive and UV-B-induced isoflavonoids increase plant resistance to stink bugs under field conditions.

Beneficial effects of solar UV-B radiation on soybean yield mediated by reduced insect herbivory under field conditions.

Ultraviolet-B radiation (UV-B: 280-315 nm) has damaging effects on cellular components and macromolecules. In plants, natural levels of UV-B can reduce leaf area expansion and growth, which can lead to reduced productivity and yield. UV-B can also have important effects on herbivorous insects. Owing to the successful implementation of the Montreal Protocol, current models predict that clear-sky levels of UV-B radiation will decline during this century in response to ozone recovery. However, because of climate change and changes in land use practices, future trends in UV doses are difficult to predict. In the experiments reported here, we used an exclusion approach to study the effects of solar UV-B radiation on soybean crops, which are extensively grown in many areas of the world that may be affected by future variations in UV-B radiation. In a first experiment, performed under normal management practices (which included chemical pest control), we found that natural levels of UV-B radiation reduced soybean yield. In a second experiment, where no pesticides were applied, we found that solar UV-B significantly reduced insect herbivory and, surprisingly, caused a concomitant increase in crop yield. Our data support the idea that UV-B effects on agroecosystems are the result of complex interactions involving multiple trophic levels. A better understanding of the mechanisms that mediate the anti-herbivore effect of UV-B radiation may be used to design crop varieties with improved adaptation to the cropping systems that are likely to prevail in the coming decades in response to agricultural intensification.

Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense.

Ultraviolet B (UV-B) radiation, a very small fraction of the daylight spectrum, elicits changes in plant secondary metabolism that have large effects on plant-insect interactions. The signal transduction pathways that mediate these specific effects of solar UV-B are not known. We examined the role of jasmonate signaling by measuring responses to UV-B in wild-type and transgenic jasmonate-deficient Nicotiana attenuata plants in which a lipoxygenase gene (NaLOX3) was silenced (as-lox). In wild-type plants, UV-B failed to elicit the accumulation of jasmonic acid (JA) or the bioactive JA-isoleucine conjugate but amplified the response of jasmonate-inducible genes, such as trypsin proteinase inhibitor (TPI), to wounding and methyl jasmonate, and increased the accumulation of several phenylpropanoid derivatives. Some of these phenolic responses (accumulation of caffeoyl-polyamine conjugates) were completely lacking in as-lox plants, whereas others (accumulation of rutin and chlorogenic acid) were similar in both genotypes. In open field conditions, as-lox plants received more insect damage than wild-type plants, as expected, but the dramatic increase in resistance to herbivory elicited by UV-B exposure, which was highly significant in wild-type plants, did not occur in as-lox plants. We conclude that solar UV-B (1) uses jasmonate-dependent and -independent pathways in the elicitation of phenolic compounds, and (2) increases sensitivity to jasmonates, leading to enhanced expression of wound-response genes (TPI). The lack of UV-B-induced antiherbivore protection in as-lox plants suggests that jasmonate signaling plays a central role in the mechanisms by which solar UV-B increases resistance to insect herbivores in the field.

Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuata and Nicotiana longiflora.

BACKGROUND AND AIMS: Plants exposed to solar ultraviolet-B radiation (UV-B, 280-315 nm) frequently suffer less insect herbivory than do plants that receive attenuated levels of UV-B. This anti-herbivore effect of solar UV-B exposure, which has been documented in several ecosystems, is in part mediated by changes in plant tissue quality. Exposure to UV-B can modify the abundance of a number of secondary metabolites, including phenolic compounds with potential impacts on insect herbivores. The aim of this study is to assess the potential anti-herbivore role of UV-B-induced phenolic compounds by comparing the phenolic profiles induced by UV-B and simulated insect herbivory in two wild species of the genus Nicotiana. METHODS: Plants grown under field and glasshouse conditions were exposed to contrasting levels of UV-B. Half of the plants of the attenuated UV-B treatment were given a simulated herbivory treatment, where leaves were mechanically damaged and immediately treated with oral secretions of Manduca sexta caterpillars. This treatment is known to mimic the impact of real herbivory on the expression of plant defences in Nicotiana. Phenolic profiles induced by UV-B and simulated herbivory were characterized using high-performance liquid chromatography-mass spectrometry (HPLC-MS). KEY RESULTS: UV-B induced the accumulation of several UV-absorbing phenolic compounds that are known to play a significant role in UV-B screening. Interestingly, there was a significant convergence in the phenolic profiles induced by UV-B and simulated herbivory: chlorogenic acid and dicaffeoylspermidine isomers, in particular, displayed a similar pattern of response to these stimuli. In contrast, rutin, the only flavonoid that accumulated in significant quantities in the experiments, was only induced by UV-B. CONCLUSIONS: The results suggest that the anti-herbivory effect induced by UV-B may be mediated at least in part by the accumulation of phenylpropanoid derivatives that are similar to those induced by the plant in response to insect herbivory.

Remote sensing of future competitors: impacts on plant defenses.

Far-red radiation (FR) reflected by green tissues is a key signal that plants use to detect the proximity of future competitors. Perception of increased levels of FR elicits a suite of responses collectively known as the shade-avoidance syndrome, which includes increased stem elongation, production of erect leaves, and reduced lateral branching. These responses improve the access to light for plants that occur in crowded populations. Responses to the proximity of competitors are known to affect the susceptibility to disease and predation in several organisms, including social animals. However, the impacts of warning signals of competition on the expression of defenses have not been explicitly investigated in plants. In the experiments reported here, we show that reflected FR induced a dramatic down-regulation of chemical defenses in wild tobacco (Nicotiana longiflora). FR altered the expression of several defense-related genes, inhibited the accumulation of herbivore-induced phenolic compounds, and augmented the performance of the specialist herbivore Manduca sexta. Complementary studies with tomato suggested that the effects of FR on defenses are mediated by the photoreceptor phytochrome B. The central implication of these results is that shade-intolerant species such as wild tobacco and tomato activate functional changes that affect their ability to cope with herbivore attack in response to phytochrome signals of future competition, even in the absence of real competition for resources. These findings suggest that competition overshadowed herbivory during the evolution of this group of species and add a new axis to the definition of the shade-avoidance syndrome.

Solar ultraviolet-B radiation alters the attractiveness of Arabidopsis plants to diamondback moths (Plutella xylostella L.): impacts on oviposition and involvement of the jasmonic acid pathway.

Solar ultraviolet-B radiation (UV-B) can have large impacts on the interactions between plants and herbivorous insects. Several studies have documented effects of UV-B-induced changes in plant tissue quality on the feeding performance of insect larvae. In contrast, the effects of UV-B-induced plant responses on the behavior of adult insects have received little attention. We carried out a series of field and glasshouse experiments using the model plant Arabidopsis thaliana L. and the crucifer-specialist insect Plutella xylostella L. (diamondback moth) to investigate the effects of UV-B on natural herbivory and plant-insect interactions. Natural herbivory under field conditions was less severe on plants exposed to ambient UV-B than on plants grown under filters that attenuated the UV-B component of solar radiation. This reduced herbivory could not be accounted for by effects of UV-B on larval feeding preference and performance, as P. xylostella caterpillars did not respond to changes in plant quality induced by UV-B. In contrast, at the adult stage, the insects presented clear behavioral responses: P. xylostella moths deposited significantly more eggs on plants grown under attenuated UV-B levels than on plants exposed to ambient UV-B. The deterring effect of UV-B exposure on insect oviposition was absent in jar1-1, a mutant with impaired jasmonic acid (JA) sensitivity, but it was conserved in mutants with altered ethylene signaling. The jar1-1 mutant also presented reduced levels of UV-absorbing phenolic compounds than the other genotypes that we tested. Our results suggest that variations in UV-B exposure under natural conditions can have significant effects on insect herbivory by altering plant traits that female adults use as sources of information during the process of host selection for oviposition. These effects of natural UV-B on plant quality appear to be mediated by activation of signaling circuits in which the defense-related hormone JA plays a functional role.

Solar UV-B radiation affects leaf quality and insect herbivory in the southern beech tree Nothofagus antarctica.

We examined the effects of solar ultraviolet-B (UV-B) radiation on plant-insect interactions in Tierra del Fuego (55 degrees S), Argentina, an area strongly affected by ozone depletion because of its proximity to Antarctica. Solar UV-B under Nothofagus antarctica branches was manipulated using a polyester plastic film to attenuate UV-B (uvb-) and an Aclar film to provide near-ambient UV-B (uvb+). The plastic films were placed on both north-facing (i.e., high solar radiation in the Southern Hemisphere) and south-facing branches. Insects consumed 40% less leaf area from north- than from south-facing branches, and at least 30% less area from uvb+ branches than from uvb- branches. The reduced herbivory on leaves from uvb+ branches occurred for both branch orientations. Leaf mass per area increased and relative water content decreased on north- versus south-facing branches, while no differences were apparent between the UV-B treatments. Solar UV-B did lead to lower gallic acid concentration and higher flavonoid aglycone concentration in uvb+ leaves relative to uvb- leaves. Both the flavonoid aglycone and quercetin-3-arabinopyranoside were higher on north-facing branches. In laboratory preference experiments, larvae of the dominant insect in the natural community, Geometridae "Brown" (Lepidoptera), consumed less area from field-grown uvb+ leaves than from uvb- leaves in 1996-97, but not in 1997-98. Correlation analyses suggested that the reduction in insect herbivory in the field under solar UV-B may be mediated in part by the UV-B effects on gallic acid and flavonoid aglycone.

Convergent responses to stress. Solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora.

The effects of solar ultraviolet (UV)-B (280-315 nm) on plants have been studied intensively over the last 2 decades in connection with research on the biological impacts of stratospheric ozone depletion. However, the molecular mechanisms that mediate plant responses to solar (ambient) UV-B and their interactions with response mechanisms activated by other stressors remain for the most part unclear. Using a microarray enriched in wound- and insect-responsive sequences, we examined expression responses of 241 genes to ambient UV-B in field-grown plants of Nicotiana longiflora Cav. Approximately 20% of the sequences represented on the array showed differential expression in response to solar UV-B. The expression responses to UV-B had parallels with those elicited by simulated Manduca sexta herbivory. The most obvious similarities were: (a) down-regulation of several photosynthesis-related genes, and (b) up-regulation of genes involved in fatty acid metabolism and oxylipin biosynthesis such as HPL (hydroperoxide lyase), alpha-DIOX (alpha-dioxygenase), LOX (13-lipoxygenase), and AOS (allene oxide synthase). Genes encoding a WRKY transcription factor, a ferredoxin-dependent glutamate-synthase, and several other insect-responsive genes of unknown function were also similarly regulated by UV-B and insect herbivory treatments. Our results suggest that UV-B and caterpillar herbivory activate common regulatory elements and provide a platform for understanding the mechanisms of UV-B impacts on insect herbivory that have been documented in recent field studies.

Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors.

Based on research to date, we can state some expectations about terrestrial ecosystem response as several elements of global climate change develop in coming decades. Higher plant species will vary considerably in their response to elevated UV-B radiation, but the most common general effects are reductions in height of plants, decreased shoot mass if ozone reduction is severe, increased quantities of some phenolics in plant tissues and, perhaps, reductions in foliage area. In some cases, the common growth responses may be lessened by increasing CO2 concentrations. However, changes in chemistry of plant tissues will generally not be reversed by elevated CO2. Among other things, changes in plant tissue chemistry induced by enhanced UV-B may reduce consumption of plant tissues by insects and other herbivores, although occasionally consumption may be increased. Pathogen attack on plants may be increased or decreased as a consequence of elevated UV-B, in combination with other climatic changes. This may be affected both by alterations in plant chemistry and direct damage to some pathogens. Water limitation may decrease the sensitivity of some agricultural plants to UV-B, but for vegetation in other habitats, this may not apply. With global warming, the repair of some types of UV damage may be improved, but several other interactions between warming and enhanced UV-B may occur. For example, even though warming may lead to fewer killing frosts, with enhanced UV-B and elevated CO2 levels, some plant species may have increased sensitivity to frost damage.

Solar ultraviolet-B radiation affects plant-insect interactions in a natural ecosystem of Tierra del Fuego (southern Argentina).

We examined the effects of solar ultraviolet-B radiation (UVB) on plant-herbivore interactions in native ecosystems of the Tierra del Fuego National Park (southern Argentina), an area of the globe that is frequently under the Antarctic "ozone hole" in early spring. We found that filtering out solar UVB from the sunlight received by naturally-occurring plants of Gunnera magellanica, a creeping perennial herb, significantly increased the number of leaf lesions caused by chewing insects. Field surveys suggested that early-season herbivory was principally due to the activity of moth larvae (Lepidoptera: Noctuidae). Manipulative field experiments showed that exposure to solar UVB changes the attractiveness of G. magellanica leaf tissue to natural grazers. In a laboratory experiment, locally caught moth caterpillars tended to eat more tissue from leaves grown without UVB than from leaves exposed to natural UVB during development; however, the difference between treatments was not significant. Leaves grown under solar UVB had slightly higher N levels than leaves not exposed to UVB; no differences between UVB treatments in specific leaf mass, relative water content, and total methanol-soluble phenolics were detected. Our results show that insect herbivory in a natural ecosystem is influenced by solar UVB, and that this influence could not be predicted from crude measurements of leaf physical and chemical characteristics and a common laboratory bioassay.