Picolinic acid spray stimulates the antioxidative metabolism and minimizes impairments on photosynthesis on wheat leaves infected by Pyricularia oryzae

Abstract

Fungal pathogens produce toxins that are important for their pathogenesis and/or aggressiveness towards their hosts. Picolinic acid (PA), a non-host selective toxin, causes lesions on rice leaves resembling those originated from Pyricularia oryzae infection. Considering that non-host selective toxins can be useful for plant diseases control, this study investigated whether the foliar spray with PA on wheat (Triticum aestivum L.) plants, in a non-phytotoxic concentration, could increase their resistance to blast, stimulate the anti-oxidative metabolism, and minimize alterations in photosynthesis. The PA spray at concentrations greater than 0.1 mg ml −1 caused foliar lesions, compromised the photosynthesis and was linked with greater accumulation of hydrogen peroxide (H 2 O 2 ) and superoxide anion radical (O 2 •− ). Fungal mycelial growth, conidia production and germination decreased by PA at 0.3 mg ml −1 . Blast severity was significantly reduced by 59 and 23%, respectively, at 72 and 96 h after inoculation for plants sprayed with PA (0.1 mg ml −1 ) at 24 h before fungal inoculation compared to non-sprayed plants. Reduction on blast symptoms was linked with increases on ascorbate peroxidase (EC 1.superoxide dismutase (EC 1.15.1.1) activities, lower H 2 O 2 and O 2•− accumulation, reduced malondialdehyde production as well as less impairments to the photosynthetic apparatus. A more efficient antioxidative metabolism that rapidly scavenges the reactive oxygen species generated during P. oryzae infection, without dramatically decreasing the photosynthetic performance, was a remarkable effect obtained with PA spray.Abbreviations -A, net CO 2 assimilation rate; APX, ascorbate peroxidase; BS, blast severity; CAT, catalase; C i , internal CO 2 concentration; E, transpiration rate; F m , maximum fluorescence image; F v /F m , variable-to-maximum chlorophyll fluorescence ratio; GPX, glutathione peroxidase; g s , stomatal conductance to water vapor; GST, glutathione-S-transferase; hai, hours after inoculation; H 2 O 2 , hydrogen peroxide; MDA, malondialdehyde; O 2 •− , superoxide anion radical; PA, picolinic acid; POX, peroxidase; q P , coefficient for photochemical quenching; SOD, superoxide dismutase; Y(II), effective photosystem II quantum yield; Y(NO), quantum yield of non-regulated energy dissipation; Y(NPQ), quantum yield of regulated energy dissipation.

Photosynthetic changes in wheat cultivars with contrasting levels of resistance to blast

“…Alterations in A at the asymptomatic phase of P. oryzae infection in rice plants were associated with the non‐host selective toxins released by the fungus that caused profound tissue disintegration and compromised water and photoassimilates translocation to leaf tissues distant from the infection sites (Bastianns, 1991). Leaves of wheat plants sprayed with picolinic acid (concentrations ranging from 0.3 to 5 mg/ml), a non‐host selective toxin produced by P. oryzae , caused significant reductions ranging from 10% to 50% in A and g s coupled to high production of hydrogen peroxide and anion superoxide (Aucique‐Pérez et al., 2019). During the symptomatic phase of blast development in the leaves of wheat plants, there were reductions in A due to lower apparent RuBisCo activity, lower CO 2 inflow from the atmosphere to the carboxylation sites in the leaf tissues, and increase in the respiration rate (Debona et al., 2014; Rios et al., 2017).…”

“…In the present study, the Y(NO) values were higher in the regions surrounding the lesions in the leaves of plants from cultivar GUA at AP and became more evident at ISP and ASP regardless of luminous intensity. Increases in Y(NO) values were detected in the leaves of wheat plants sprayed with picolinic acid (Aucique‐Pérez et al., 2019). According to Bürling et al.…”

“…The fluorescence imaging of Chl a parameters was determined by using the Imaging‐PAM MAXI fluorometer and the software ImagingWIN version 2.32 (Heinz Walz GmbH, Effeltrich, Germany) following the procedures described by Aucique‐Pérez et al. (2019). For semi‐quantitative analyses, six areas of interest (AOI) of 1 cm 2 each were randomly selected in each leaf per replication of each treatment, and the results were averaged.…”

“…High blast severity on wheat leaves caused drastic decreases in the photosynthetic capacity of plants. Experiments demonstrated reductions greater than 50% in net CO 2 assimilation rate ( A ), stomatal conductance to water vapour and transpiration rate in leaves with 30% of blast severity (Aucique‐Pérez et al., 2014, 2017, 2019; Debona et al., 2014). Additionally, these authors proposed that reductions in A in infected leaves by P. oryzae may be accounted for physiological alterations associated with biochemical events in the photosynthetic process.…”

A review on South Asian wheat blast: The present status and future perspective

“…The spray application of PA on rice leaves caused foliar lesions resembling those from P. oryzae infection. However, spraying of wheat leaves with a lower nonphytotoxic concentration of PA (0.1 mg/ml) resulted in less blast symptoms in association with a better photosynthetic performance and an improvement in the antioxidant metabolism (Aucique‐Pérez et al ., 2019). The reduction of blast symptoms was associated with increases in ascorbate peroxidase, catalase, glutathione peroxidase, glutathione reductase, glutathione‐S‐transferase, peroxidase, and superoxide dismutase activities, lower H 2 O 2 and O 2 •− accumulation, and reduced malondialdehyde production, as well as less impairment to the photosynthetic apparatus.…”