Arabidopsis GOLD36/MVP1/ERMO3 is required for powdery mildew penetration resistance and proper targeting of the PEN3 transporter

Authors: Underwood, William

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/9/2022
Publication Date: 4/20/2022
Citation: Underwood, W. 2022. Arabidopsis GOLD36/MVP1/ERMO3 is required for powdery mildew penetration resistance and proper targeting of the PEN3 transporter. Molecular Plant-Microbe Interactions. 35:393-400. https://doi.org/10.1094/MPMI-09-21-0240-R.
DOI: https://doi.org/10.1094/MPMI-09-21-0240-R

Interpretive Summary: Plant cells respond to attack by pathogenic microorganisms such as fungi and bacteria with targeted physical and chemical defenses to reinforce the plant cell wall. Delivery of proteins and other cargo involved in this localized defense response is accomplished by redirection of subcellular membrane trafficking toward the site of pathogen detection at the cell surface. Timely delivery of defense cargo is critical for successful pathogen defense, as delays or disruptions in defense-related membrane trafficking result in impaired resistance to pathogens. Although timely reinforcement of the cell wall is critical for successful disease resistance, our knowledge of the mechanisms underlying regulation and redirection of membrane trafficking during pathogen defense is limited. In this study, we report the characterization of a mutant impaired in delivery of an important defense protein to the host-pathogen interface and identification of the gene underlying the defense defect. The results of this study provide new insights into the processes involved in delivery of defense proteins and compounds to sites of pathogen attack for effective disease resistance.

Technical Abstract: The Arabidopsis PENETRATION 3 (PEN3) ATP binding cassette (ABC) transporter contributes to penetration resistance against non-adapted powdery mildew fungi and is targeted to papillae deposited at sites of interaction with the fungus. Timely recruitment of PEN3 and other components of penetration resistance to the host-pathogen interface is important for successful defense against this biotrophic pathogen. We previously carried out a forward genetic screen to identify Arabidopsis mutants that mis-target the PEN3 transporter or fail to accumulate PEN3 at sites of attempted powdery mildew penetration. In this study, we describe PEN3 mis-targeting in the aberrant localization of PEN3 4 (alp4) mutant and identification of the causal gene. In the alp4 mutant, PEN3 accumulates within the endomembrane system in an apparently abnormal endoplasmic reticulum and is not exported into papillae at powdery mildew penetration sites. This targeting defect compromises defenses at the host-pathogen interface, resulting in increased penetration success by a non-adapted powdery mildew. Genetic mapping identified alp4 as an allele of GOLGI DEFECTS 36 (GOLD36), a gene encoding a GDSL-lipase/esterase family protein that is involved in maintaining normal morphology and organization of multiple endomembrane compartments. Genetic complementation confirmed that mutation in GOLD36 is responsible for the PEN3 targeting and powdery mildew penetration resistance defects in alp4. These results reinforce the importance of endomembrane trafficking in resistance to haustorium-forming phytopathogens such as powdery mildew fungi.