mlo-Based Resistance: An Apparently Universal “Weapon” to Defeat Powdery Mildew Disease

Abstract

Loss-of-function mutations of one or more of the appropriate Mildew resistance locus o (Mlo) genes are an apparently reliable "weapon" to protect plants from infection by powdery mildew fungi, as they confer durable broad-spectrum resistance. Originally detected as a natural mutation in an Ethiopian barley landrace, this so-called mlo-based resistance has been successfully employed in European barley agriculture for nearly four decades. More recently, mlo-mediated resistance was discovered to be inducible in virtually every plant species of economic or scientific relevance. By now, mlo resistance has been found (as natural mutants) or generated (by induced mutagenesis, gene silencing, and targeted or nontargeted gene knock-out) in a broad range of monocotyledonous and dicotyledonous plant species. Here, we review features of mlo resistance in barley, discuss approaches to identify the appropriate Mlo gene targets to induce mlo-based resistance, and consider the issue of pleiotropic effects often associated with mlo-mediated immunity, which can harm plant yield and quality. We portray mlo-based resistance as an apparently universal and effective weapon to defeat powdery mildew disease in a multitude of plant species.

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

“…Besides typically short-lived isolate-specific immunity, loss-of-function mutations in specific members of the MILDEW RESISTANCE LOCUS O ( MLO ) gene family provide stable protection against these pathogens (Jørgensen, 1992; Brown, 2015; Kusch et al, 2016). This durable, broad-spectrum type of immunity is conserved amongst monocots and dicots, including several important crop plants (Jørgensen, 1992; Bai et al, 2007; Humphry et al, 2011; Wang et al, 2014; Berg et al, 2015; Acevedo-Garcia et al, 2016; Kusch et al, 2016; Kusch and Panstruga, 2017). Employment of mlo mutant plants in agriculture was pioneered by mutations in a single Mlo gene in diploid barley (Jørgensen, 1992).…”

Recognition of Verticillium effector Ave1 by tomato immune receptor Ve1 mediates Verticillium resistance in diverse plant species

“…Indeed, loss-of-function of the Mildew resistance locus o (Mlo) in barley was found to confer recessively inherited broad-spectrum resistance against powdery mildew (Jørgensen, 1992). Barley Mlo is a plasma membrane-localized protein that is required for pathogen invasion 7 (Humphry et al, 2006;Kusch and Panstruga, 2017). Notably, mlo-mediated powdery mildew resistance has also been described in other plant species, including A. thaliana, tomato, pea, wheat, apple, grapevine, pepper, rose, tobacco, cucumber and melon (Kusch and Panstruga, 2017).…”

“…Barley Mlo is a plasma membrane-localized protein that is required for pathogen invasion 7 (Humphry et al, 2006;Kusch and Panstruga, 2017). Notably, mlo-mediated powdery mildew resistance has also been described in other plant species, including A. thaliana, tomato, pea, wheat, apple, grapevine, pepper, rose, tobacco, cucumber and melon (Kusch and Panstruga, 2017). Other successful examples of recessive resistance genes are the eukaryotic translation elongation initiation factor genes eif4e and eif4g, conferring potyvirus resistance in lettuce, melon, tomato, pepper, barley, pea and rice (Wang and Krishnaswamy, 2012), and rice xa13, xa25 and Os11N3 (also named as OsSWEET11, OsSWETT13 and OsSWEET14, respectively), conferring bacterial blight resistance against X. oryzae pv.…”

Nonhost wild lettuce as a donor for resistance to downy mildew in cultivated lettuce

“…Such a gain-of-function mutation is not very likely to occur, consequently resistance through S gene mutation is potentially durable. One well-known example is recessive mutation of the Mlo gene in many plant species, which was originally detected as a natural mutation in barley (Kusch and Panstruga 2017). Mutation of the Mlo gene prevents haustorial formation and confers durable broad-spectrum powdery mildew resistance.…”

“…The mutant phenotype shows a decreased infection. Loss-of-function mutations in S genes, such as Mlo (Kusch and Panstruga 2017), can lead to a generally recessive resistance to the pathogen, reminiscent of NHR.…”