Priming of Wheat with the Green Leaf Volatile Z-3-Hexenyl Acetate Enhances Defense against Fusarium graminearum But Boosts Deoxynivalenol Production

Abstract

Priming refers to a mechanism whereby plants are sensitized to respond faster and/or more strongly to future pathogen attack. Here, we demonstrate that preexposure to the green leaf volatile Z-3-hexenyl acetate (Z-3-HAC) primed wheat (Triticum aestivum) for enhanced defense against subsequent infection with the hemibiotrophic fungus Fusarium graminearum. Bioassays showed that, after priming with Z-3-HAC, wheat ears accumulated up to 40% fewer necrotic spikelets. Furthermore, leaves of seedlings showed significantly smaller necrotic lesions compared with nonprimed plants, coinciding with strongly reduced fungal growth in planta. Additionally, we found that F. graminearum produced more deoxynivalenol, a mycotoxin, in the primed treatment. Expression analysis of salicylic acid (SA) and jasmonic acid (JA) biosynthesis genes and exogenous methyl salicylate and methyl jasmonate applications showed that plant defense against F. graminearum is sequentially regulated by SA and JA during the early and later stages of infection, respectively. Interestingly, analysis of the effect of Z-3-HAC pretreatment on SA-and JA-responsive gene expression in hormone-treated and pathogen-inoculated seedlings revealed that Z-3-HAC boosts JA-dependent defenses during the necrotrophic infection stage of F. graminearum but suppresses SA-regulated defense during its biotrophic phase. Together, these findings highlight the importance of temporally separated hormone changes in molding plant health and disease and support a scenario whereby the green leaf volatile Z-3-HAC protects wheat against Fusarium head blight by priming for enhanced JA-dependent defenses during the necrotrophic stages of infection.

Resistance to Fusarium verticillioides and fumonisin accumulation in maize inbred lines involves an earlier and enhanced expression of lipoxygenase (LOX) genes

“…Primed wheat plants with the GLV Z-3-hexenyl acetate (Z-3-HAC) showed reduced fungal spread in subsequent F. graminearum infections, although accumulated higher levels of mycotoxins (Ameye et al, 2015). Moreover Z-3-HAC was responsible for the transition from SA-to JA-dependent defences, occurring at 2 dpi (Ameye et al, 2015). This study showed that wounding (mock-inoculation) triggered genes for GLV production, including…”

“…GLV role in priming, which refers to a sensitization of plants to respond faster and/or more strongly to future herbivore insect attack, was demonstrated in maize (Engelberth et al, 2004), but recently also in wheat against fungal pathogens (Ameye et al, 2015). Primed wheat plants with the GLV Z-3-hexenyl acetate (Z-3-HAC) showed reduced fungal spread in subsequent F. graminearum infections, although accumulated higher levels of mycotoxins (Ameye et al, 2015). Moreover Z-3-HAC was responsible for the transition from SA-to JA-dependent defences, occurring at 2 dpi (Ameye et al, 2015).…”

“…It is known that plant resistance to biotrophic/hemibiotrophic pathogens activated by gene for gene recognition is controlled largely by SA-mediated signalling pathways, while resistance to necrotrophic pathogens is mediated, antagonistically, by the JA and ET signalling pathways (Glazebrook, 2005). It was proven that wheat defence against the hemibiotrophic F. graminearum is sequentially regulated by SA and JA during the early and later stages of infection, respectively (Ameye et al, 2015;Ding et al, 2011). Wheat cultivars at 32 and 72 h post inoculation revealed the existence of a biphasic strategy against F. graminearum: a JA-and ET-mediated defence mechanism was directed against fungal growth and sporulation and induced the transcription in the resistant cultivar of a set of genes encoding antimicrobial peptides, PR proteins as lipid transfer proteins, defensins and thionins and the second mechanism was specifically directed towards fungal mycotoxins and proteases (Gottwald et al, 2012).…”

Early events induced by the toxin deoxynivalenol lead to programmed cell death in Nicotiana tabacum cells

“…The authors demonstrated induction of a suite of defence gene transcripts and proteins in wheat seedlings. Through a priming experiment that enhanced plant defence against F. graminearum in wheat, DON production has also been shown to be boosted [14]. Thus, the effects of DON appear to be complex and the mechanism of toxicity remains poorly understood in plant.…”

Spore Density Determines Infection Strategy by the Plant Pathogenic Fungus Plectosphaerella cucumerina

“…Apart from the hyperstimulation of PTI, necrotrophic fungi typically rely on the production of mycotoxins to induce host necrosis (Christensen and Kolomiets, 2011;Woloshuk and Shim, 2013;Ameye et al, 2015). Future research is required to verify whether the necrotrophic behavior of droplet-inoculated P. cucumerina depends on mycotoxin production and whether such mycotoxin production is stimulated by early immune responses of the host plant.…”