Arabidopsis MLO2 is a negative regulator of sensitivity to extracellular reactive oxygen species

Abstract

The atmospheric pollutant ozone (O ) is a strong oxidant that causes extracellular reactive oxygen species (ROS) formation, has significant ecological relevance, and is used here as a non-invasive ROS inducer to study plant signalling. Previous genetic screens identified several mutants exhibiting enhanced O sensitivity, but few with enhanced tolerance. We found that loss-of-function mutants in Arabidopsis MLO2, a gene implicated in susceptibility to powdery mildew disease, exhibit enhanced dose-dependent tolerance to O and extracellular ROS, but a normal response to intracellular ROS. This phenotype is increased in a mlo2 mlo6 mlo12 triple mutant, reminiscent of the genetic redundancy of MLO genes in powdery mildew resistance. Stomatal assays revealed that enhanced O tolerance in mlo2 mutants is not caused by altered stomatal conductance. We explored modulation of the mlo2-associated O tolerance, powdery mildew resistance, and early senescence phenotypes by genetic epistasis analysis, involving mutants with known effects on ROS sensitivity or antifungal defence. Mining of publicly accessible microarray data suggests that these MLO proteins regulate accumulation of abiotic stress response transcripts, and transcript accumulation of MLO2 itself is O responsive. In summary, our data reveal MLO2 as a novel negative regulator in plant ROS responses, which links biotic and abiotic stress response pathways.

Plant immunity in signal integration between biotic and abiotic stress responses

“…Loss of the integral membrane protein MLO confers powdery mildew resistance and oxidative stress tolerance, in part through SA (Acevedo-Garcia et al, 2014;Cui et al, 2018). Enhanced…”

“…Tansley review New Phytologist immunity in mlo plants, however, can be uncoupled from ROS accumulation and tolerance, which are closely associated with callose deposition and cell death, resembling premature senescence (Cui et al, 2018). Moreover, ol-2 (mlo) resistance in tomato is ABA-dependent (Seifi et al, 2014) and retained under salt stress .…”

Reactive Oxygen Species as Mediators of Gametophyte Development and Double Fertilization in Flowering Plants

“…The synergid-expressed mildew resistance locus o (MLO) gene NORTIA (NTA, also known as MLO7) also participates in pollen tube reception, with nta mutants displaying pollen tube overgrowth (Kessler et al, 2010). Other members of the MLO gene family play a role in powdery mildew infection and have been proposed to negatively regulate localized ROS production at powdery mildew penetration sites and to play a role in modulating the threshold for ROS-induced cell death (Cui et al, 2018). The biochemical function of NTA is not known, but it accumulates in the Golgi during synergid differentiation and then at the filiform apparatus during pollen tube reception (Jones et al, 2017), consistent with a possible role in regulating the synergid response to extracellular ROS in the micropyle.…”

Cucumber Mildew Resistance Locus O Interacts with Calmodulin and Regulates Plant Cell Death Associated with Plant Immunity

“…The results of genetic epistasis analyses suggest that pathogen-responsive callose deposition has been detected in Atmlo2 mutant plants [18]. Arabidopsis MLO2 is a negative regulator of plant ROS responses to biotic stress [19]. In cucumber transgenic cotyledons, the transcription level of HR-associated genes is negatively regulated by CsMLO1 expression [15].…”