The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens

Abstract

SummaryDefence against pathogens in Arabidopsis is orchestrated by at least three signalling molecules: salicylic acid (SA), jasmonic acid (JA) and ethylene (ET). The hrl1 (hypersensitive response-like lesions 1) mutant of Arabidopsis is characterized by spontaneous necrotic lesions, accumulation of reactive oxygen species, constitutive expression of SA-and ET/JA-responsive defence genes, and enhanced resistance to virulent bacterial and oomycete pathogens. Epistasis analyses of hrl1 with npr1, etr1, coi1 and SAdepleted nahG plants revealed novel interactions between SA and ET/JA signalling pathways in regulating defence gene expression and cell death. RNA gel-blot analysis of RNA isolated separately from the lesion + and the lesion ± leaves of double mutants of hrl1 revealed different signalling requirements for the expression of defence genes in these tissues. Expression of the ET/JA-responsive PDF1.2 gene was markedly reduced in hrl1 npr1 and in SA-depleted hrl1 nahG plants. In hrl1 nahG plants, expression of PDF1.2 was regulated by benzathiadiazole in a concentration-dependent manner: induced at low concentration and suppressed at high concentration. The hrl1 etr1 plants lacked systemic PR-1 expression, and exhibited compromised resistance to virulent Pseudomonas syringae and Peronospora parasitica. Inhibiting JA responses in hrl1 coi1 plants lead to exaggerated cell death and severe stunting of plants. Finally, the hrl1 mutation lead to elevated expression of AtrbohD, which encodes a major subunit of the NADPH oxidase complex. Our results indicate that defence gene expression and resistance against pathogens in hrl1 is regulated synergistically by SA and ET/JA defence pathways.

Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem

“…(3) The AtrbohD mutant produces significantly more ET than the wild type even 24 h after the inoculation. (4) Lesion-free leaves of the hrl1 lesion-mimic mutant exhibit higher transcriptional rbohD induction than leaves actually displaying lesions (Devadas et al, 2002). (5) Most interestingly, as has been pointed out in two recent papers, pathogen-or host-associated molecular pattern elicitors such as flagellin (flg22) or oligogalacturonides do induce a rapid, transient, RBOHDdependent oxidative burst in Arabidopsis leaves detected by chemiluminescence or xylenol orange methods (Zhang et al, 2007;Galletti et al, 2008).…”

“…Veinal necrosis and preceding accumulation of H 2 O 2 in turnip mosaic virus-infected Landsberg erecta Arabidopsis plants were dependent on the increased formation of SA and ET . SA and ET are also necessary for constitutive transcriptional activation of the rbohD gene in two different Arabidopsis lesion-mimic mutants (Devadas et al, 2002;Bouchez et al, 2007). Torres et al (2005) reported dramatically enhanced cell death in the lsd1 AtrbohD double mutant as a result of SA or BTH treatment in comparison with SA-or BTH-treated lsd1 or AtrbohD single mutant.…”

“…A, An Arabidopsis cell spatially distant from a germinating A. brassicicola conidium is elicited either by low concentration of fungal toxin or by oligosaccharide chitin fragments (Miya et al, 2007;Wan et al, 2008), leading to elevated endogenous SA and ET levels. B, Increasing cellular SA and ET concentrations induce moderate RBOHD activity (Devadas et al, 2002;Bouchez et al, 2007). The resulting mild generation of ROS inhibits the accumulation of SA and ET and suppresses cell death.…”

“…Many Arabidopsis lesion-mimic mutants showed elevated SA and ROS production as well as continuous expression of defense mechanisms (Lorrain et al, 2003). SA was also necessary for the constitutive transcriptional activation of the Arabidopsis NADPH oxidase rbohD in the hrl1 lesion-mimic mutant (Devadas et al, 2002). A mutation in the isochorismate synthase gene of the SA biosynthetic pathway (eds16; identical with ics1 or sid2) suppressed uncontrolled cell death in the lsd1 AtrbohD double mutant.…”

Arabidopsis RADICAL-INDUCED CELL DEATH1 Belongs to the WWE Protein–Protein Interaction Domain Protein Family and Modulates Abscisic Acid, Ethylene, and Methyl Jasmonate Responses

“…Conversely, mutant phenotypes indicate that PR1 expression is induced by SA and inhibited by JA (Turner et al, 2002). In the hypersensitive response-like lesions1 mutant, induction of PR1 expression requires both SA and ET, and induction of PDF1.2 expression requires all three hormones SA, ET, and JA (Devadas et al, 2002), indicating further levels of complexity in hormone interactions. Hence, it is likely that the timing, location, and levels of the various hormones determine the interaction (antagonistic or synergistic) and output responses.…”