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

Abstract

1 plant ABA biosynthetic pathway to inhibit seed 2 germination. 3 4 Running title: Cross-kingdom activity of the fungal metabolite pyrenophoric acid 5 B on seed germination. 6 7 Word count: 3565 words 43 44 45 3 Highlight:The fungus Pyrenophora semeniperda produces pyrenophoric acid 46 B, a small molecule that exploits the plant ABA biosynthetic 47 pathway to reduce seed germination, increasing its reproductive 48 success. 49 50 51 Abstract 52 53Pyrenophoric acid (P-Acid), P-Acid B and P-Acid C are three phytotoxic 54 sesquiterpenoids produced by the ascomycete seed pathogen Pyrenophora semeniperda, 55 a fungus proposed as a mycoherbicide for biocontrol of cheatgrass, an extremely invasive 56 weed. When tested in cheatgrass bioassays these metabolites were able to delay seed 57 germination, with P-Acid B being the most active compound. Here, we have investigated 58 the cross-kingdom activity of P-Acid B and its mode of action and found that it activates 59 the ABA signaling pathway in order to inhibit seedling establishment. P-Acid B inhibits 60 seedling establishment in wild-type Arabidopsis thaliana while several mutants affected 61 in the early perception as well as in downstream ABA signaling components were 62 insensitive to the fungal compound. However, in spite of structural similarities between 63 ABA and P-Acid B, the latter is not able to activate the PYR/PYL family of ABA 64 receptors. Instead, we have found that P-Acid B uses the ABA biosynthesis pathway at 65 the level of alcohol dehydrogenase ABA2 to reduce seedling establishment. We propose 66 that the fungus Pyrenophora semeniperda manipulates plant ABA biosynthesis as a 67 4 strategy to reduce seed germination, increasing its ability to cause seed mortality and 68 thereby increase its fitness through higher reproductive success. 69 70 71 Rodriguez PL. 2012. Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiology 158, 970-980. Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL. 2005. A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. . 2015. Abscisic acid analogs as chemical probes for dissection of abscisic acid responses in Arabidopsis thaliana. Phytochemistry 113, 96-107.