Optimized Jasmonic Acid Production by Lasiodiplodia theobromae Reveals Formation of Valuable Plant Secondary Metabolites

Abstract

Jasmonic acid is a plant hormone that can be produced by the fungus Lasiodiplodia theobromae via submerged fermentation. From a biotechnological perspective jasmonic acid is a valuable feedstock as its derivatives serve as important ingredients in different cosmetic products and in the future it may be used for pharmaceutical applications. The objective of this work was to improve the production of jasmonic acid by L. theobromae strain 2334. We observed that jasmonic acid formation is dependent on the culture volume. Moreover, cultures grown in medium containing potassium nitrate as nitrogen source produced higher amounts of jasmonic acid than analogous cultures supplemented with ammonium nitrate. When cultivated under optimal conditions for jasmonic acid production, L. theobromae secreted several secondary metabolites known from plants into the medium. Among those we found 3-oxo-2-(pent-2-enyl)-cyclopentane-1-butanoic acid (OPC-4) and hydroxy-jasmonic acid derivatives, respectively, suggesting that fungal jasmonate metabolism may involve similar reaction steps as that of plants. To characterize fungal growth and jasmonic acid-formation, we established a mathematical model describing both processes. This model may form the basis of industrial upscaling attempts. Importantly, it showed that jasmonic acid-formation is not associated to fungal growth. Therefore, this finding suggests that jasmonic acid, despite its enormous amount being produced upon fungal development, serves merely as secondary metabolite.

Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection

“…Constitutive JA Signaling in jao2 Plants Depends on Higher Flux through the JAR1-COI1 Module 12OH-JA accumulation has been commonly observed in different organs and plant species (Miersch et al, 2008), and its importance is now being recognized for plant-microbe interactions. 12OH-JA and other JAs can be synthetized by some fungi (Eng et al, 2016), and a recent report suggested that fungus-produced 12OH-JA attenuates host immunity in rice (Patkar et al, 2015). We detected no 12OH-JA in the B. cinerea-infected aos mutant, which is devoid of any plantderived JA (L. Poirier and T. Heitz, unpublished result), indicating that this fungus does not produce 12OH-JA under our conditions.…”

A fungal catalase reacts selectively with the 13S fatty acid hydroperoxide products of the adjacent lipoxygenase gene and exhibits 13S-hydroperoxide-dependent peroxidase activity

“…We had considered Fg-cat as a candidate for the role of the “missing” AOS activity in fungi, in which case the adjacent 13 S -LOX gene in F. graminearum could provide the appropriate AOS substrate, as suggested as a potential role for the F. oxysporum 13 S -LOX homologue [15]). Many fungi including Fusarium species synthesize jasmonates [45–48] (although we find no evidence concerning F. graminearum ). Notwithstanding the apparent logic, in the course of our extensive analyses we found no evidence of allene oxide synthesis nor cyclopentenone formation from interaction of Fg-cat with either 13 S -HPODE or 13 S -HPOTE, likely dismissing the possibility of its involvement in jasmonate synthesis in F. graminearum .…”

An allene oxide and 12-oxophytodienoic acid are key intermediates in jasmonic acid biosynthesis by Fusarium oxysporum

“…theobromae and members of the Fusarium family remain prototypes for studies of (+)-JA biosynthesis. L. theobromae (strain 2334) can routinely produce 300-500 mg (+)-JA per liter of growth medium and occasionally much more (17)(18)(19). In the fields, L. theobromae causes excessive growth of tropical fruit trees, possibly due to (+)-JA secretion (15,18).…”

“…L. theobromae (strain 2334) can routinely produce 300-500 mg (+)-JA per liter of growth medium and occasionally much more (17)(18)(19). In the fields, L. theobromae causes excessive growth of tropical fruit trees, possibly due to (+)-JA secretion (15,18). Several subspecies of F. oxysporum, which infect garden stock, cabbage, and tulips, are also known to produce (+)-JA, 9,10-dihydro-JA, and their conjugates with isoleucine (15,20).…”