The fungal sesquiterpenoid pyrenophoric acid B uses the plant ABA biosynthetic pathway to inhibit seed germination

Abstract

Pyrenophoric acid (P-Acid), P-Acid B, and P-Acid C are three phytotoxic sesquiterpenoids produced by the ascomycete seed pathogen Pyrenophora semeniperda, a fungus proposed as a mycoherbicide for biocontrol of cheatgrass, an extremely invasive weed. When tested in cheatgrass bioassays, these metabolites were able to delay seed germination, with P-Acid B being the most active compound. Here, we have investigated the cross-kingdom activity of P-Acid B and its mode of action, and found that it activates the abscisic acid (ABA) signaling pathway in order to inhibit seedling establishment. P-Acid B inhibits seedling establishment in wild-type Arabidopsis thaliana, while several mutants affected in the early perception as well as in downstream ABA signaling components were insensitive to the fungal compound. However, in spite of structural similarities between ABA and P-Acid B, the latter is not able to activate the PYR/PYL family of ABA receptors. Instead, we have found that P-Acid B uses the ABA biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to reduce seedling establishment. We propose that the fungus P. semeniperda manipulates plant ABA biosynthesis as a strategy to reduce seed germination, increasing its ability to cause seed mortality and thereby increase its fitness through higher reproductive success.

Phytotoxic Secondary Metabolites from Fungi

“…Three metabolites showed phytotoxic activity by reducing coleoptile elongation of cheatgrass seedlings [ 209 , 210 ]. Among three metabolites, pyrenophoric acid B ( 314 ) was the most phytotoxic to use the abscisic acid (ABA) biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to reduce seed germination of cheatgrass [ 211 ].…”

Stagonolides J and K and Stagochromene A, Two New Natural Substituted Nonenolides and a New Disubstituted Chromene-4,5-dione Isolated from Stagonospora cirsii S-47 Proposed for the Biocontrol of Sonchus arvensis

“…They are isolated from fungi (ascaulitoxin, pinolidoxin, putaminoxin, spirostaphylotrichins, macrocidins, and others, − and more recently, pyrenophoric acids, colletochlorins E and F, cochliotoxin, and phaeosphaeride A − ) and by allelopathic plants as inuloxins A–D and α-costic acid obtained from Dittrichia viscosa (syn. Inula viscosa ). , For some potential herbicidal metabolites, the absolute configuration was assigned as an important feature that has an impact on the biological activity. − Furthermore, some studies were carried out to further characterize their biological activity, , the structure–activity relationships, , the mode of action, − and their total enantioselective synthesis. , …”

Bioactive Metabolite Production in the Genus Pyrenophora (Pleosporaceae, Pleosporales)

“…It was demonstrated that it uses the ABA biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to achieve this inhibition. This result suggested that P. semeniperda may manipulate plant ABA biosynthesis in the seed as a strategy to reduce germination, increasing its ability to cause seed mortality and thereby increase its fitness through higher reproductive success [92].…”

“…Pyrenophoric acid B (30, Figure 3) P. semeniperda Phytotoxic to Arabidopsis thaliana and B. tectorum [91,92] Pyrenophoric acid C (31, Figure 3 Triticone D (15, Figure 2)…”