Leaf abaxial immunity to powdery mildew in Arabidopsis is conferred by multiple defense mechanisms

Abstract

Powdery mildew (PM) fungi are obligate biotrophic pathogens that only invade plant epidermal cells. There are two epidermal surfaces for any plant leaves: the adaxial (upper) side and the abaxial (lower) side. While both leaf surfaces can be susceptible to adapted PM fungi in many plant species, there have been observations of leaf abaxial immunity in some plant species including Arabidopsis. The genetic basis of such leaf abaxial immunity remains unknown. In this study, we tested a series of Arabidopsis mutants defective in one or more known defense pathways with the adapted PM isolate Golovinomyces cichoracearum (Gc) UCSC1. We found that leaf abaxial immunity was significantly compromised in mutants impaired for both the EDS1/PAD4- and PEN2/PEN3-dependent defenses. Consistently, expression of EDS1-YFP and PEN2-GFP from their respective native promoters in the respective eds1-2 and pen2-1 mutant backgrounds were higher in the abaxial epidermal cells than that in the adaxial epidermal cells. Altogether, our results indicate that leaf abaxial immunity against PM in Arabidopsis is at least partially due to enhanced EDS1/PAD4- and PEN2/PEN3-dependent defenses. Such transcriptionally preprogrammed defense mechanisms may underly leaf abaxial immunity in other plant species such as hemp and may be exploited for engineering adaxial immunity against PM fungi in crop plants.

Reduction of flavonoid content in honeysuckle via Erysiphe lonicerae-mediated inhibition of three essential genes in flavonoid biosynthesis pathways

“…This disease, which has a global distribution, affects nearly all common crops and is a major concern within the plant pathology community due to the severe economic losses it causes annually worldwide ( Lebeda et al., 2024 ; Lu et al., 2024 ; Stack et al., 2024 ; Xue et al., 2024 ). Moreover, research on powdery mildew in certain key crops and model plants has progressed to the stage of investigating immune mechanisms at a molecular level ( Wu et al., 2024 ). Honeysuckle is not immune to powdery mildew, a disease recognized as one of the most devastating to its cultivation, particularly in large-scale production.…”

Spatial regulation of immunity: unmasking the secrets of abaxial immunity to powdery mildew

“…1A ). By flipping and fixing leaf position with tape, Wu et al . (2024) minimized the impact of differences in micro-environmental conditions.…”

“…In this issue, Wu et al . (2024) reported the genetic and molecular mechanisms underpinning the leaf abaxial immunity in Arabidopsis.…”

“…While the abaxial and adaxial leaf surfaces exhibit clear physical distinctions and micro-environmental variations, the extent to which defense signaling pathways contribute to spatial immunity on the abaxial surface remains largely unknown. In this issue, Wu et al (2024) investigated the genetic and molecular mechanisms underlying leaf abaxial immunity in Arabidopsis. Through a comprehensive analysis of diverse Arabidopsis immune mutants, the authors unveiled that abaxial immunity in Arabidopsis arises from more active glucosinolate metabolism and EDS1/PAD4-dependent defense within the abaxial epidermal layer.…”

“…At the phenotypic level, plants exhibit diverse degrees of spatially and temporally distinct immunity to pathogens, a phenomenon observed across various maturation stages and in different organs. An intriguing phenomenon referred to as abaxial immunity highlights a more robust defense against powdery mildew on the lower (abaxial) side of a leaf compared with the upper (adaxial) side ( Wu et al , 2024 ).…”