Fungal and bacterial oxylipins are signals for intra- and inter-cellular communication within plant disease

Abstract

Lipids are central at various stages of host-pathogen interactions in determining virulence and modulating plant defense. Free fatty acids may act as substrates for oxidizing enzymes [e.g., lipoxygenases (LOXs) and dioxygenases (DOXs)] that synthesize oxylipins. Fatty acids and oxylipins function as modulators of several pathways in cell-to-cell communication; their structural similarity among plant, fungal, and bacterial taxa suggests potential in cross-kingdom communication. We provide a prospect of the known role of fatty acids and oxylipins in fungi and bacteria during plant-pathogen interactions. In the pathogens, oxylipin-mediated signaling pathways are crucial both in development and host infection. Here, we report on case studies suggesting that oxylipins derived from oleic, linoleic, and linolenic acids are crucial in modulating the pathogenic lifestyle in the host plant. Intriguingly, overlapping (fungi-plant/bacteria-plant) results suggest that different inter-kingdom pathosystems use similar lipid signals to reshape the lifestyle of the contenders and occasionally determine the outcome of the challenge.

Keywords: Aspergillus spp; Fusarium spp; Olea europaea L.; Xylella fastidiosa; Zea mays (L); lipids; oxylipins.

Figure 1

Fungal oxylipins. Oleic acid (18:1) can be oxidized by LDS enzyme and converted in hydroperoxyoctanoic acid (HPOMEs); other enzymes (e.g. isomerases) convert HPOME in hydroxyoctanoic acid (HOME), and di-hydroxyoctanoic acid (diHOME). Linoleic acid (18:2) can be oxidized by LOX enzyme and converted in hydroperoxyoctadecadienoic acid (HPODE); other enzymes (e.g. reductases) convert HPODE in hydroxyoctadecadienoic acid (HODE), and di-hydroxyoctadecadienoic acid (diHODE). Linoleic acid (18:2) is also the substrate of LDS that catalyzes the conversion in hydroperoxyoctadecadienoic acid (HPODE); other enzymes (e.g. epoxidases) convert HPODE in hydroxyoctadecadienoic acid (HODE), di-hydroxyoctadecadienoic acid (diHODE), and epoxyoctadecenoic acids (EPOME). LOX enzyme acts upon α/δ-Linolenic acid (18:3) to generate hydroperoxyoctadecatrienoic acid (HPOTE); HPOTE is the substrate of other enzymes to generate hydroxyoctadecatrienoic acid (HOTE) and di-hydroxyoctadecatrienoic acid (diHOTE). Arachidonic acid (20:4) can be oxidized by LOX and converted in hydroperoxyeicosatetraenoic acid (HPETE); HPETE is the substrate of hydroxyeicosatetraenoic acid (HETE), di-hydroxyeicosatetraenoic acid (diHETE). COX enzyme convert the arachidonic acid (20:4) in prostaglandins (PGs).

Figure 2

Oxylipin functions. Linoleic acid-derived oxylipins are described for Aspergillus spp., Fusarium spp., and maize. For Aspergillus spp., the main signaling process mediated by lipoxygenases (LOX) and linoleate diol synthases (LDS) is reported, for Fusarium spp. is described the LDS involvement, and for maize the LOX-mediated functions. Linolenic acid oxylipins derived from LOX activity shared the same functions in Aspergillus spp. and Fusarium spp.

Figure 3

Hypothetical model involving oxylipins as signals in X. fastidiosa–host interaction. At the begin of host–bacteria interaction, the host does not recognize the presence of the pathogen, the bacterium modulates the planktonic-biofilm by itself, thought DFS-QS and ODS, and accumulates mainly DOX-oxylipins. Later, the plant recognizes the pathogen, activates the defense response, and triggers plant LOX-oxylipins. The bacterial pathogen switches in the “acquisition phase” by DSF-QS and ODS, accumulating mainly LOX-oxylipins. The bacterium–host interaction stimulates the bacteria biofilming, vector acquisition, and extensive vascular blockage plants, favored by a LOX oxylipins pathway in response to as an adaptive strategy to cope with harsh environmental conditions and to establish pathogenic insult with their host.