Maize death acids, 9-lipoxygenase–derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators

Abstract

Plant damage promotes the interaction of lipoxygenases (LOXs) with fatty acids yielding 9-hydroperoxides, 13-hydroperoxides, and complex arrays of oxylipins. The action of 13-LOX on linolenic acid enables production of 12-oxo-phytodienoic acid (12-OPDA) and its downstream products, termed “jasmonates.” As signals, jasmonates have related yet distinct roles in the regulation of plant resistance against insect and pathogen attack. A similar pathway involving 9-LOX activity on linolenic and linoleic acid leads to the 12-OPDA positional isomer, 10-oxo-11-phytodienoic acid (10-OPDA) and 10-oxo-11-phytoenoic acid (10-OPEA), respectively; however, physiological roles for 9-LOX cyclopentenones have remained unclear. In developing maize (Zea mays) leaves, southern leaf blight (Cochliobolus heterostrophus) infection results in dying necrotic tissue and the localized accumulation of 10-OPEA, 10-OPDA, and a series of related 14- and 12-carbon metabolites, collectively termed “death acids.” 10-OPEA accumulation becomes wound inducible within fungal-infected tissues and at physiologically relevant concentrations acts as a phytoalexin by suppressing the growth of fungi and herbivores including Aspergillus flavus, Fusarium verticillioides, and Helicoverpa zea. Unlike previously established maize phytoalexins, 10-OPEA and 10-OPDA display significant phytotoxicity. Both 12-OPDA and 10-OPEA promote the transcription of defense genes encoding glutathione S transferases, cytochrome P450s, and pathogenesis-related proteins. In contrast, 10-OPEA only weakly promotes the accumulation of multiple protease inhibitor transcripts. Consistent with a role in dying tissue, 10-OPEA application promotes cysteine protease activation and cell death, which is inhibited by overexpression of the cysteine protease inhibitor maize cystatin-9. Unlike jasmonates, functions for 10-OPEA and associated death acids are consistent with specialized roles in local defense reactions.

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

“…4B). This indicates that other products of this metabolic pathway, including previously identified death acids (Christensen et al, 2015) and the as yet uncharacterized oxylipins with mass-to-charge ratio 238 and 240 that were detected in our GC-MS assays (Supplemental Table S6), continue to be produced in response to aphid feeding. Recent research suggests that oxylipins other than jasmonic acid can have defense signaling functions in maize (Constantino et al, 2013) or direct nutritive effects on aphids (Nalam et al, 2012).…”

Discovery, Biosynthesis and Stress-Related Accumulation of Dolabradiene-Derived Defenses in Maize

“…1), are part of a complex repertoire of defense-related specialized metabolites, such as phenylpropanoids, oxylipins, benzoxazinoids, and volatile terpenoids (Schnee et al, 2006;Köllner et al, 2008a;Santiago and Malvar, 2010;Ahmad et al, 2011;Huffaker et al, 2011;Schmelz et al, 2011;Christensen et al, 2015;Richter et al, 2016;Wouters et al, 2016). Inducible zealexin and kauralexin production contributes to defense, both aboveground and belowground, against pathogenic fungi, including Fusarium, Aspergillus, and Colletotrichum spp.…”

Accumulation of 9- and 13-KODEs in response to jasmonic acid treatment and pathogenic infection in rice

“…22) In maize (Zea mays) leaves, southern leaf blight (Cochliobolus heterostrophus) infection resulted in the localized accumulation of 10-oxo-11-phytodienoic acid (10-OPDA), 10-oxo-11-phytoenoic acid (10-OPEA), and a series of related 14-and 12-carbon metabolites. 23) Because these compounds are toxic to both pathogens and plants, they play roles as both phytoalexins and signal molecules that induce cell death in plant tissues. Both 12-OPDA and 10-OPEA promote the transcription of defense genes.…”