Overexpression of barley BAX inhibitor 1 induces breakdown of mlo -mediated penetration resistance to Blumeria graminis

Abstract

Cell death regulation is linked to pathogen defense in plants and animals. Execution of apoptosis as one type of programmed cell death in animals is irreversibly triggered by cytochrome c release from mitochondria via pores formed by BAX proteins. This type of programmed cell death can be prevented by expression of BAX inhibitor 1 (BI-1), a membrane protein that protects cells from the effects of BAX by an unknown mechanism. In barley, a homologue of the mammalian BI-1 is expressed in response to inoculation with the barley powdery mildew fungus Blumeria graminis f.sp. hordei (Bgh). We found differential expression of BI-1 in response to Bgh in susceptible and resistant plants. Chemical induction of resistance to Bgh by soil drench treatment with 2,6-dichloroisonicotinic acid led to down-regulation of the expression level of BI-1. Importantly, single-cell transient overexpression of BI-1 in epidermal leaf tissue of susceptible barley cultivar Ingrid led to enhanced accessibility, resulting in a higher penetration efficiency of Bgh on BI-1-transformed cells. In Bgh-resistant mlo5 genotypes, which do not express the negative regulator of defense and cell death MLO, overexpression of BI-1 almost completely reconstituted susceptibility to fungal penetration. We suggest that BI-1 is a regulator of cellular defense in barley sufficient to substitute for MLO function in accessibility to fungal parasites.

Blufensin1Negatively Impacts Basal Defense in Response to Barley Powdery Mildew

“…mlo-mediated resistance during papillae formation is extremely effective, although in the rare case when penetration does occur, Bgh colonization of the leaf tissue proceeds normally (Jørgensen, 1994). Similarly, overexpression of the barley homolog of BI-1 in epidermal cells generates supersusceptibility (Hü ckelhoven et al, 2003). BI-1 was found to negatively regulate the penetration resistance mediated by mlo and almost restored the penetration efficiency (PE) of Bgh to wild-type levels (Hü ckelhoven et al, 2003).…”

“…Edr1, AtWRKY58, HvWRKY1/2, and BAX inhibitor-1 (BI-1) are examples of well-characterized negative regulators in the known signal and transcriptional activation cascades. By contrast, genes such as the Mlo negative regulator of penetration resistance and several lesion-mimic mutants, such as lsd1, have only recently been characterized with regard to regulatory roles and importance during defense (Bü schges et al, 1997;Frye et al, 2001;Hü ckelhoven et al, 2003;Wang et al, 2006;Shen et al, 2007). Although the former group of genes direct our attention to the complexity and redundancy of the regulatory network of plant defense, the latter set of genes are expanding our understanding of nonhost resistance, biotrophy, and the formation and/or progression of necrosis.…”

“…Several gain-of-function and loss-of-function mutants have revealed genes associated with basal defense and effector-triggered immunity (Bü schges et al, 1997;Frye et al, 2001;Hü ckelhoven et al, 2003;Behn et al, 2004;Jones and Dangl, 2006;Wang et al, 2006;Shen et al, 2007). Many of these genes have been shown to have important roles in overlapping pathways, suggesting a complex interconnected network of regulation.…”

Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death suppressor

“…43 Kim et al 44,45 reported that binding of barley MLO to CaM (HvCaM3) is required for this Mlo-mediated defense response. Interestingly, Hü ckelhoven et al 15 found that barley BI-1 overexpression resulted in breakdown of the penetration resistance to B. graminis in the barley mlo mutant, suggesting that BI-1 and Mlo may have similar functions in plant defense responses. The observation that Mlo binds to HvCaM3 led Ihara-Ohori et al 46 to study CaM-binding ability of AtBI-1.…”

“…and their expression levels are usually enhanced during aging (senescence) and under stress conditions, suggesting that BI-1 function is physiologically associated with cell death control and/or stress management. [12][13][14][15][16][17][18][19][20] In fact, numerous studies by transgenic approaches have revealed that overexpression of plant BI-1 resulted in attenuation of cell death induced by biotic stresses (pathogens) and abiotic stresses such as heat, cold, drought, salt and chemical-induced oxidative stresses, which induce massive accumulation of ROS before cell death activation. [16][17][18][19][20] Interestingly, it was shown that elevated intracellular ROS levels by Bax expression was not abrogated in AtBI-1 (Arabidopsis BI-1) overexpressing Arabidopsis plants, although plant cell death was strongly attenuated.…”