Secondary plant products causing photosensitization in grazing herbivores: their structure, activity and regulation

Abstract

Photosensitivity in animals is defined as a severe dermatitis that results from a heightened reactivity of skin cells and associated dermal tissues upon their exposure to sunlight, following ingestion or contact with UV reactive secondary plant products. Photosensitivity occurs in animal cells as a reaction that is mediated by a light absorbing molecule, specifically in this case a plant-produced metabolite that is heterocyclic or polyphenolic. In sensitive animals, this reaction is most severe in non-pigmented skin which has the least protection from UV or visible light exposure. Photosensitization in a biological system such as the epidermis is an oxidative or other chemical change in a molecule in response to light-induced excitation of endogenous or exogenously-delivered molecules within the tissue. Photo-oxidation can also occur in the plant itself, resulting in the generation of reactive oxygen species, free radical damage and eventual DNA degradation. Similar cellular changes occur in affected herbivores and are associated with an accumulation of photodynamic molecules in the affected dermal tissues or circulatory system of the herbivore. Recent advances in our ability to identify and detect secondary products at trace levels in the plant and surrounding environment, or in organisms that ingest plants, have provided additional evidence for the role of secondary metabolites in photosensitization of grazing herbivores. This review outlines the role of unique secondary products produced by higher plants in the animal photosensitization process, describes their chemistry and localization in the plant as well as impacts of the environment upon their production, discusses their direct and indirect effects on associated animal systems and presents several examples of well-characterized plant photosensitization in animal systems.

Figure 1.

Type I and II chemical photosensitization. Type I: the activated sensitizer reacts with the acceptor, in a one-electron transfer reaction, to produce a radical ion in both the sensitizer and eventually in the acceptor. The acceptor (substrate) donates an electron to the sensitizer (Sen), resulting in an acceptor radical cation (Substrate+) and a sensitizer radical anion (Sen^•−), but the opposite may also occur, depending on the redox potential of the pair of molecules. In the presence of oxygen, both of these radicals can proceed to produce oxygenated products. Type II reactions: activated sensitizer transfers its excess energy to ground state molecular oxygen, producing excited state singlet oxygen and regenerating the ground-state sensitizer. Singlet oxygen then reacts with the acceptor to produce oxidized metabolites. Reprinted with permission of the author and publisher [24].

Figure 2.

Selected chemical structures of SPPs causing photosensitization in grazing livestock, clockwise from upper left to right. Phytoporphyrin is a microbially produced breakdown product of chlorophyll. Echimidine is produced by Echium plantagineum. Angelicin is produced by Heracleum mantegazzianum. Diosgenin is produced by Panicum virgatum. Chlorophyll A is produced by all green plants. Dehydroretronecine is produced by Senecio spp. Heliotrine is produced by Heliotrope spp. Hypericin is produced by Hyperacum perforatum.

Figure 3.

Modes of delivery to the skin of common photosensitizing compounds affecting domestic livestock in primary or hepatogenic photosensitization.

Figure 4.

Photosensitization in domestic livestock caused by Biserrula pelecinus L. and Tribulus terrestris L. (A) Biserrula pelecinus, a pasture legume crop causing photosensitization in grazing herbivores; (B) Severe photosensitization resulting from ingestion of saponins in Australian sheep grazing Tribulus terrestris, also known as caltrop. Note severe impact on eyes and face with severe dermal lesions and tissue swelling and loss of fleece on face and muzzle. Eyes are swollen and produce significant exudates; (C) Photosensitization in Australian sheep grazing Biserrula pelecinus “Mauro”. Lesions are less severe as grazing occurred for only 72 h. Note similar loss of fleece around the muzzle and swelling around the eyes with crusty exudate. This example also experienced corneal ulceration.