Polyphenolic Allelochemicals from the Aquatic Angiosperm Myriophyllum spicatumInhibit Photosystem II

Abstract

Myriophyllum spicatum (Haloragaceae) is a highly competitive freshwater macrophyte that produces and releases algicidal and cyanobactericidal polyphenols. Among them, ␤-1,2,3-tri-O-galloyl-4,6-(S)-hexahydroxydiphenoyl-d-glucose (tellimagrandin II) is the major active substance and is an effective inhibitor of microalgal exoenzymes. However, this mode of action does not fully explain the strong allelopathic activity observed in bioassays. Lipophilic extracts of M. spicatum inhibit photosynthetic oxygen evolution of intact cyanobacteria and other photoautotrophs. Fractionation of the extract provided evidence for tellimagrandin II as the active compound. Separate measurements of photosystem I and II activity with spinach (Spinacia oleracea) thylakoid membranes indicated that the site of inhibition is located at photosystem II (PSII). In thermoluminescence measurements with thylakoid membranes and PSII-enriched membrane fragments M. spicatum extracts shifted the maximum temperature of the B-band (S 2 Q B Ϫ recombination) to higher temperatures. Purified tellimagrandin II in concentrations as low as 3 m caused a comparable shift of the B-band. This demonstrates that the target site of this inhibitor is different from the Q B -binding site, a common target of commercial herbicides like 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Measurements with electron paramagnetic resonance spectroscopy suggest a higher redox midpoint potential for the non-heme iron, located between the primary and the secondary quinone electron acceptors, Q A and Q B . Thus, tellimagrandin II has at least two modes of action, inhibition of exoenzymes and inhibition of PSII. Multiple target sites are a common characteristic of many potent allelochemicals. Allelopathy (sensu;Molisch, 1937) is considered an effective trait of submerged aquatic angiosperms (Wium-Andersen, 1987; Gross, 1999, and refs. therein) to counteract the usually strong competition for light and carbon with other primary producers, especially phytoplankton and epiphytes (SandJensen and Søndergaard, 1981). Allelopathically active compounds known from terrestrial plants generally act as natural herbicides and often have multiple effects on the metabolism of target organisms (Einhellig, 2001). Some have even been explored as natural substitutes for commercial herbicides (Duke et al., 2000). Few studies have, however, targeted the mode of action of allelochemicals from aquatic angiosperms.Several allelochemicals isolated from cyanobacteria or higher plants specifically inhibit photosynthesis of target organisms (Einhellig et al., 1993;Gonzalez et al., 1997;Smith and Doan, 1999). This results in a lower primary production and might consequently cause slower growth of competing photoautotrophs. To prove effects on primary production, the radiocarbon assay (fixation of radioactive labeled 14 C) has been frequently used, e.g. with extracts from Zostera marina (Harrison and Durance, 1985) and Chara globularis (Wium-Andersen et al., 1983). More detailed studies involved separate measureme...

Importance of Nutrient Competition and Allelopathic Effects in Suppression of the Green Alga Scenedesmus obliquus by the Macrophytes Chara, Elodea and Myriophyllum

“…There exist, however, good correlations between F PSII and the rate of C-fixation in algae and algal growth rate (Hofstraat et al, 1994;Geel, 1997). Furthermore, the hydrolyzable polyphenols released by Myriophyllum might also inhibit F PSII (Ko¨rner & Nicklisch, 2002;Leu et al, 2002). However, the results of the current study could not confirm this.…”

Searching for allelopathic effects of submerged macrophytes on phytoplankton—state of the art and open questions

“…The hydrolysable polyphenols in M. spicatum comprise all those activities (Choi et al, 2002;Leu et al, 2002;Walenciak et al, 2002). The cyclic sulphur compounds considered responsible for allelopathic activity in Chara have insecticidal properties (Anthoni et al, 1982;Jacobsen & Pedersen, 1983).…”

Allelopathy of Aquatic Autotrophs

“…Extracts and exudates from Myriophyllum spicatum inhibit photosynthesis of various cyanobacteria, chlorophytes, and diatoms (Körner and Nicklisch, 2002;Leu et al, 2002). Using dialysis membranes and controlling for nutrient competition, Körner and Nicklisch (2002) showed that M. spicatum causes species-specific effects in a range of cyanobacteria, chlorophytes, and diatoms and inhibits both growth and PSII in natural relevant concentrations.…”

“…Using dialysis membranes and controlling for nutrient competition, Körner and Nicklisch (2002) showed that M. spicatum causes species-specific effects in a range of cyanobacteria, chlorophytes, and diatoms and inhibits both growth and PSII in natural relevant concentrations. The mechanism of interference with PSII was studied in detail by Leu et al (2002). Lipophilic extracts and purified tellimagrandin I1 interfered with photosynthetic electron transport of the cyanobacterium Anabaena sp.…”