Key Components of Different Plant Defense Pathways Are Dispensable for Powdery Mildew Resistance of the Arabidopsis mlo2 mlo6 mlo12 Triple Mutant

Abstract

Loss of function mutations of particular plant MILDEW RESISTANCE LOCUS O (MLO) genes confer durable and broad-spectrum penetration resistance against powdery mildew fungi. Here, we combined genetic, transcriptomic and metabolomic analyses to explore the defense mechanisms in the fully resistant Arabidopsis thaliana mlo2 mlo6 mlo12 triple mutant. We found that this genotype unexpectedly overcomes the requirement for indolic antimicrobials and defense-related secretion, which are critical for incomplete resistance of mlo2 single mutants. Comparative microarray-based transcriptome analysis of mlo2 mlo6 mlo12 mutants and wild type plants upon Golovinomyces orontii inoculation revealed an increased and accelerated accumulation of many defense-related transcripts. Despite the biotrophic nature of the interaction, this included the non-canonical activation of a jasmonic acid/ethylene-dependent transcriptional program. In contrast to a non-adapted powdery mildew pathogen, the adapted powdery mildew fungus is able to defeat the accumulation of defense-relevant indolic metabolites in a MLO protein-dependent manner. We suggest that a broad and fast activation of immune responses in mlo2 mlo6 mlo12 plants can compensate for the lack of single or few defense pathways. In addition, our results point to a role of Arabidopsis MLO2, MLO6, and MLO12 in enabling defense suppression during invasion by adapted powdery mildew fungi.

The powdery mildew-resistant Arabidopsis mlo2 mlo6 mlo12 triple mutant displays altered infection phenotypes with diverse types of phytopathogens

“…Alternatively, or in addition, the lack of compatibility conferred by mlo triple mutants might be too powerful to be disabled by A. laibachii . This would be in line with the results of recent genetic analysis, demonstrating that single or even multiple defence pathways are dispensable for resistance of the mlo2 -5 mlo6 -2 mlo12 -1 triple mutant 54 .…”

Mildew Locus O facilitates colonization by arbuscular mycorrhiza in angiosperms

“…In addition, the increased expression of other MLOs during mycorrhization (Fig. S3a) in M. truncatula suggests that-as for other mlo phenotypes such as powdery mildew resistance (Kuhn et al, 2017) and synergid cell reception )-MLOs act redundantly, with different MLOs potentially contributing unequally across different cell types and developmental stages. It is, therefore, possible that higher-order mutants will have increasingly stronger arbuscular mycorrhizal phenotypes.…”

“…The ancestral function of MLO proteins is unknown, but their presence in green algae suggests that the so-far characterized roles are derivative (Takamatsu, 2004;Jiao et al, 2011). In Arabidopsis thaliana, loss of MLO family members belonging to a separate clade from barley MLO1 confer resistance to powdery mildew in a redundant fashion (Kusch et al, 2016;Kuhn et al, 2017). Interestingly, one of these can complement the Atmlo7 pollen tube reception phenotype, suggesting a conserved biochemical function of MLO proteins .…”

Comparative transcriptome analysis uncovers regulatory roles of long non-coding RNAs involved in resistance to powdery mildew in melon

“…In tomato, the loss-offunction of MLO family gene (SlMLO1) led to high resistance against PM [32]. Besides, in Arabidopsis thaliana, T-DNA insertion mutations in three MLO homologs (AtMLO2, AtMLO6 and AtMLO12) contributed to significant PM resistance, although the mutation in AtMLO2 had a significant effect compared to mutations in other two genes [33]. These studies showed that MLO proteins in plants function as characteristic susceptibility genes (S-genes) and play a negative regulatory role in resisting to PM.…”