Jason J. Wargent

UVR8 in Arabidopsis thaliana regulates multiple aspects of cellular differentiation during leaf development in response to ultraviolet B radiation

Responses specific to ultraviolet B (UV-B) wavelengths are still poorly understood, both in terms of initial signalling and effects on morphogenesis. Arabidopsis thaliana UV RESISTANCE LOCUS8 (UVR8) is the only known UV-B specific signalling component, but the role of UVR8 in leaf morphogenesis is unknown. The regulatory effects of UVR8 on leaf morphogenesis at a range of supplementary UV-B doses were characterized, revealing both UVR8-dependent and independent responses to UV irradiation. Inhibition of epidermal cell division in response to UV-B is largely independent of UVR8. However, overall leaf growth under UV-B irradiation in wild-type plants is enhanced compared with a uvr8 mutant because of a UVR8-dependent compensatory increase of cell area in wild-type plants. UVR8 was also required for the regulation of endopolyploidy in response to UV-B, and the uvr8 mutant also has a lower density of stomata than the wild type in the presence of UV-B, indicating that UVR8 has a regulatory role in other developmental events. Our findings show that, in addition to regulating UV-protective gene expression responses, UVR8 is involved in controlling aspects of leaf growth and morphogenesis. This work extends our understanding of how UV-B response is orchestrated at the whole-plant level.

Multiple Roles for UV RESISTANCE LOCUS8 in Regulating Gene Expression and Metabolite Accumulation in Arabidopsis under Solar Ultraviolet Radiation

Summary: Under natural sunlight, this study demonstrates multiple and complex roles for the UV-B photoreceptor UV RESISTANCE LOCUS 8 in the acclimation of Arabidopsis plants to UV radiation. Photomorphogenic responses triggered by low fluence rates of ultraviolet B radiation (UV-B; 280–315 nm) are mediated by the UV-B photoreceptor UV RESISTANCE LOCUS8 (UVR8). Beyond our understanding of the molecular mechanisms of UV-B perception by UVR8, there is still limited information on how the UVR8 pathway functions under natural sunlight. Here, wild-type Arabidopsis (Arabidopsis thaliana) and the uvr8-2 mutant were used in an experiment outdoors where UV-A (315–400 nm) and UV-B irradiances were attenuated using plastic films. Gene expression, PYRIDOXINE BIOSYNTHESIS1 (PDX1) accumulation, and leaf metabolite signatures were analyzed. The results show that UVR8 is required for transcript accumulation of genes involved in UV protection, oxidative stress, hormone signal transduction, and defense against herbivores under solar UV. Under natural UV-A irradiance, UVR8 is likely to interact with UV-A/blue light signaling pathways to moderate UV-B-driven transcript and PDX1 accumulation. UVR8 both positively and negatively affects UV-A-regulated gene expression and metabolite accumulation but is required for the UV-B induction of phenolics. Moreover, UVR8-dependent UV-B acclimation during the early stages of plant development may enhance normal growth under long-term exposure to solar UV.

From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production

Largely because of concerns regarding global climate change, there is a burgeoning interest in the application of fundamental scientific knowledge in order to better exploit environmental cues in the achievement of desirable endpoints in crop production. Ultraviolet (UV) radiation is an energetic driver of a diverse range of plant responses and, despite historical concerns regarding the damaging consequences of UV-B radiation for global plant productivity as related to stratospheric ozone depletion, current developments representative of a range of organizational scales suggest that key plant responses to UV-B radiation may be exploitable in the context of a sustainable contribution towards the strengthening of global crop production, including alterations in secondary metabolism, enhanced photoprotection, up-regulation of the antioxidative response and modified resistance to pest and disease attack. Here, we discuss the prospect of this paradigm shift in photobiology, and consider the linkages between fundamental plant biology and crop-level outcomes that can be applied to the plant UV-B response, in addition to the consequences for related biota and many other facets of agro-ecosystem processes.

Tri-trophic consequences of UV-B exposure: plants, herbivores and parasitoids

In this paper we demonstrate a UV-B-mediated link between host plants, herbivores and their parasitoids, using a model system consisting of a host plant Brassica oleracea, a herbivore Plutella xylostella and its parasitoid Cotesia plutellae. Ultraviolet-B radiation (UV-B) is a potent elicitor of a variety of changes in the chemistry, morphology and physiology of plants and animals. Recent studies have demonstrated that common signals, such as jasmonic acid (JA), play important roles in the mechanisms by which plants respond to UV-B and to damage by herbivores. Plant responses elicited by UV-B radiation can affect the choices of ovipositing female insects and the fitness of their offspring. This leads to the prediction that, in plants, the changes induced as a consequence of UV damage will be similar to those elicited in response to insect damage, including knock-on effects upon the next trophic level, predators. In our trials female P. xylostella oviposited preferentially on host plants grown in depleted UV-B conditions, while their larvae preferred to feed on tissues from UV-depleted regimes over those from UV-supplemented ones. Larval feeding patterns on UV-supplemented tissues met the predictions of models which propose that induced defences in plants should disperse herbivory; feeding scars were significantly smaller and more numerous – though not significantly so – than those on host plant leaves grown in UV-depleted conditions. Most importantly, female parasitoids also showed a clear pattern of preference when given the choice between host plants and attendant larvae from the different UV regimes; however, in the case of the female parasitoids, the choice was in favour of potential hosts foraging on UV-supplemented tissues. This study demonstrates the potential for UV-B to elicit a variety of interactions between trophic levels, most likely mediated through effects upon host plant chemistry.

Ultraviolet Radiation as a Limiting Factor in Leaf Expansion and Development

Reductions in leaf growth are a commonly observed response to ultraviolet radiation, but the underlying mechanisms remain poorly defined. This study examined the response of leaves exposed to a UV environment across a range of organizational scales, including leaf expansion rate, epidermal cell size and number, biomechanical properties, leaf–water relations and activity of cell‐wall peroxidases. Two experimental approaches were used; Lettuce (Lactuca sativa L.) plants were propagated under (a) supplementary UV‐B (9 kJ m−2 day−1) in controlled environment (CE) conditions, and (b) field conditions, where plants were placed under three horticultural films with differing UV transmissions. In both experiments, UV‐B caused the greatest reductions in leaf expansion and final leaf size, with some reductions attributable to UV‐A wavelengths. In supplementary UV‐B conditions, adaxial cell size was reduced, while in field plants, both cell size and cell number were lower in an increased UV environment, as was the case with abaxial cells in CE plants. Although leaf turgor and leaf extensibility were not affected by UV wavelengths, breaking strain of leaf tissue was decreased under supplementary UV‐B. Cell‐wall peroxidase activity was increased in both supplementary UV conditions and in the field, where only a zero UV environment showed no upregulation of cell‐wall peroxidase.

The use of wavelength-selective plastic cladding materials in horticulture: understanding of crop and fungal responses through the assessment of biological spectral weighting functions.

Abstract Plant responses to light spectral quality can be exploited to deliver a range of agronomically desirable end points in protected crops. This can be achieved using plastics with specific spectral properties as crop covers. We have studied the responses of a range of crops to plastics that have either (a) increased transmission of UV compared with standard horticultural covers, (b) decreased transmission of UV or (c) increased the ratio of red (R) : far-red (FR) radiation. Both the UV-transparent and R : FR increasing films reduced leaf area and biomass, offering potential alternatives to chemical growth regulators. The UV-opaque film increased growth, but while this may be useful in some crops, there were trade-offs with elements of quality, such as pigmentation and taste. UV manipulation may also influence disease control. Increasing UV inhibited not only the pathogenic fungus Botrytis cinerea but also the disease biocontrol agent Trichoderma harzianum. Unlike B. cinerea, T. harzianum was highly sensitive to UV-A radiation. These fungal responses and those for plant growth in the growth room and the field under different plastics are analyzed in terms of alternative biological spectral weighting functions (BSWF). The role of BSWF in assessing general patterns of response to UV modification in horticulture is also discussed.

Increased exposure to UV-B radiation during early development leads to enhanced photoprotection and improved long-term performance in Lactuca sativa

Plant responses to solar UV radiation are numerous and have often been considered from a perspective of negative outcomes for plant productivity. In this study, we used two experimental approaches consisting of: (1) field-based spectrally modifying filters in addition to (2) controlled indoor exposure to UV-B, to examine the effects of UV radiation on growth and photosynthetic performance of lettuce (Lactuca sativa L.) seedlings. Various aspects of growth were affected in plants grown under a UV-inclusive environment compared to a UV-depleted environment, including reductions in leaf expansion, increases in leaf thickness and the rate of net photosynthesis. After transplantation to a uniform field environment, lettuce plants initially propagated under the UV-inclusive environment exhibited higher harvestable yields than those from a UV-depleted environment. In controlled conditions, photosynthetic rates were higher in plants grown in the presence of UV-B radiation, and relative growth of plants pre-acclimatized to UV-B was also increased, in addition to higher maximum photochemical efficiency of photosystem II (PSII) (F(v) /F(m) ) following subsequent exposure to high photosynthetically active radiation (PAR) and temperature stress. Our findings are discussed within the context of sustainability in agriculture and the paradigm shift in photobiology which such beneficial responses to UV radiation could represent.

Ecological responses to UV radiation: interactions between the biological effects of UV on plants and on associated organisms

Solar ultraviolet (UV)-B radiation (280-315 nm) has a wide range of effects on terrestrial ecosystems, yet our understanding of how UV-B influences the complex interactions of plants with pest, pathogen and related microorganisms remains limited. Here, we report the results of a series of experiments in Lactuca sativa which aimed to characterize not only key plant responses to UV radiation in a field environment but also consequential effects for plant interactions with a sap-feeding insect, two model plant pathogens and phylloplane microorganism populations. Three spectrally modifying filters with contrasting UV transmissions were used to filter ambient sunlight, and when compared with our UV-inclusive filter, L. sativa plants grown in a zero UV-B environment showed significantly increased shoot fresh weight, reduced foliar pigment concentrations and suppressed population growth of green peach aphid (Myzus persicae). Plants grown under a filter which allowed partial transmission of UV-A radiation and negligible UV-B transmission showed increased density of leaf surface phylloplane microbes compared with the UV-inclusive treatment. Effects of UV treatment on the severity of two plant pathogens, Bremia lactucae and Botrytis cinerea, were complex as both the UV-inclusive and zero UV-B filters reduced the severity of pathogen persistence. These results are discussed with reference to known spectral responses of plants, insects and microorganisms, and contrasted with established fundamental responses of plants and other organisms to solar UV radiation, with particular emphasis on the need for future integration between different experimental approaches when investigating the effects of solar UV radiation.

The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B

The UV-B photoreceptor UVR8 regulates expression of genes in response to UV-B, some encoding chloroplast proteins, but the importance of UVR8 in maintaining photosynthetic competence is unknown. The maximum quantum yield of PSII (Fv/Fm) and the operating efficiency of PSII (ΦPSII) were measured in wild-type and uvr8 mutant Arabidopsis thaliana. The importance of specific UVR8-regulated genes in maintaining photosynthetic competence was examined using mutants. Both Fv/Fm and ΦPSII decreased when plants were exposed to elevated UV-B, in general more so in uvr8 mutant plants than wild-type. UV-B increased the level of psbD-BLRP (blue light responsive promoter) transcripts, encoding the PSII D2 protein. This increase was mediated by the UVR8-regulated chloroplast RNA polymerase sigma factor SIG5, but SIG5 was not required to maintain photosynthetic efficiency at elevated UV-B. Levels of the D1 protein of PSII decreased markedly when plants were exposed to elevated UV-B, but there was no significant difference between wild-type and uvr8 under conditions where the mutant showed increased photoinhibition. The results show that UVR8 promotes photosynthetic efficiency at elevated levels of UV-B. Loss of the DI polypeptide is probably important in causing photoinhibition, but does not entirely explain the reduced photosynthetic efficiency of the uvr8 mutant compared to wild-type.

Fungal endophyte infection of ryegrass reprograms host metabolism and alters development

Summary Beneficial associations between plants and microbes play an important role in both natural and agricultural ecosystems. For example, associations between fungi of the genus Epichloë, and cool‐season grasses are known for their ability to increase resistance to insect pests, fungal pathogens and drought. However, little is known about the molecular changes induced by endophyte infection. To study the impact of endophyte infection, we compared the expression profiles, based on RNA sequencing, of perennial ryegrass infected with Epichloë festucae with noninfected plants. We show that infection causes dramatic changes in the expression of over one third of host genes. This is in stark contrast to mycorrhizal associations, where substantially fewer changes in host gene expression are observed, and is more similar to pathogenic interactions. We reveal that endophyte infection triggers reprogramming of host metabolism, favouring secondary metabolism at a cost to primary metabolism. Infection also induces changes in host development, particularly trichome formation and cell wall biogenesis. Importantly, this work sheds light on the mechanisms underlying enhanced resistance to drought and super‐infection by fungal pathogens provided by fungal endophyte infection. Finally, our study reveals that not all beneficial plant–microbe associations behave the same in terms of their effects on the host.