Host perception and signal transduction studies in wild‐type Blumeria graminis f. sp. hordei and a quinoxyfen‐resistant mutant implicate quinoxyfen in the inhibition of serine esterase activity

Abstract

Quinoxyfen is a potent and effective fungicide, hitherto considered to control powdery mildew disease by perturbing signal transduction during early germling differentiation. The aim of this paper is to understand the mode of action of quinoxyfen by comparing the perception of host-derived signals and signal relay in a wild-type Blumeria graminis f. sp. hordei EM Marchal (Bgh) (WT/IM82) and a quinoxyfen-resistant field isolate (QR/2B11). QR/2B11 germinates more promiscuously on host-like and artificial surfaces than the quinoxyfen-sensitive WT/IM82. The pivotal role of host cuticle deprivation in the formation of hooked appressorial germ tubes (hAGTs) in WT/IM82 and a dramatic drop in germling differentiation in the presence of the mildewicide are demonstrated. QR/2B11 strain shows a dependence on host cuticle-like features for hAGT formation but no significant difference between germling differentiation in the presence or absence of quinoxyfen. PKC-inhibitor Ro 318220 induces morphological changes similar to those seen in quinoxyfen-treated germlings. PKC1 transcript accumulation is equivalently upregulated by quinoxyfen in QR/2B11 and WT/IM82 strains, but Bgh cutinase CUT1 transcript is 8 times more abundant in QR/2B11 conidia than in WT/IM82 conidia. Quinoxyfen inhibits serine esterase activity in WT/IM82, but not in QR/2B11. Collectively, these data suggest that quinoxyfen interferes with the perception of host-derived signals required for full germling differentiation, and that QR/2B11 bypasses the need for such signals. Moreover, quinoxyfen appears to target serine esterase activity, with a downstream perturbation in signal transduction; this represents the first demonstrable biochemical difference between the quinoxyfen-resistant and -sensitive isolates.