Ethylene Insensitivity Modulates Ozone-Induced Cell Death in Birch

Abstract

We have used genotypic variation in birch (Betula pendula Roth) to investigate the roles of ozone (O 3 )-induced ethylene (ET), jasmonic acid, and salicylic acid in the regulation of tissue tolerance to O 3 . Of these hormones, ET evolution correlated best with O 3 -induced cell death. Disruption of ET perception by transformation of birch with the dominant negative mutant allele etr1-1 of the Arabidopsis ET receptor gene ETR1 or blocking of ET perception with 1-methylcyclopropene reduced but did not completely prevent the O 3 -induced cell death, when inhibition of ET biosynthesis with aminooxyacetic acid completely abolished O 3 lesion formation. This suggests the presence of an ET-signaling-independent but ET biosynthesis-dependent component in the ET-mediated stimulation of cell death in O 3 -exposed birch. Functional ET signaling was required for the O 3 induction of the gene encoding ␤-cyanoalanine synthase, which catalyzes detoxification of the cyanide formed during ET biosynthesis. The results suggest that functional ET signaling is required to protect birch from the O 3 -induced cell death and that a decrease in ET sensitivity together with a simultaneous, high ET biosynthesis can potentially cause cell death through a deficient detoxification of cyanide.The concentration of tropospheric ozone (O 3 ) has increased during the past decades due to human activities, and it has been estimated that in year 2100, 50% of global forest area will be exposed to potentially phytotoxic O 3 concentrations (Fowler et al., 1999). In the leaves of O 3 -sensitive plants, symptoms of high O 3 are observed as rapid lesion formation. Traditionally, formation of reactive oxygen species (ROS), such as superoxide (O 2 ⅐ Ϫ ) and hydrogen peroxide (H 2 O 2 ) from the degradation of O 3 in the apoplast has been thought to alter the integrity of the plasma membrane and thus the integrity of the cell (Laisk et al., 1989; Heath, 1994). However, O 3 also induces an active and controlled apoplastic oxidative burst, the production of O 2 ⅐ Ϫ and H 2 O 2 in the leaves affected, which may initiate programmed cell death analogous to that induced by ROS in an incompatible plant-pathogen interaction (Schraudner et al., 1998;Pellinen et al., 1999Pellinen et al., , 2002Overmyer et al., 2000; Moeder et al., 2002; Wohlgemuth et al., 2002).Activation of ethylene (ET) biosynthesis by induction of the genes encoding 1-aminocyclopropane-1-carboxylate synthase (ACS) is one of the fastest and most obvious biochemical responses to O 3 and has been mechanistically linked to the regulation of O 3 lesion formation (Schlagnhaufer et al., 1997;Tuomainen et al., 1997;Vahala et al., 1998;Overmyer et al., 2000; Moeder et al., 2002). ET is perceived by a two-component His kinase receptor family (Chang et al., 1993a; Hua et al., 1995Hua et al., , 1998Sakai et al., 1998). The ET receptor can be pharmacologically blocked with a competitive inhibitor of ET action, norbornadiene, or with 1-methylcyclopropene (MCP; Serek et al., 1995), which prevents the binding ...

Ozone-Induced Cell Death Mediated with Oxidative and Calcium Signaling Pathways in Tobacco Bel-W3 and Bel-B Cell Suspension Cultures

“…It has been suggested that many of biological actions of O 3 in planta are mediated by stimulated productions of ethylene and salicylic acid. [22][23][24][25] We examined the impacts of ethylene and salicylic acid on the induced cell death (Fig. 10).…”

Impact of Seawater Salinity on Ultrastructure of Chloroplasts and Oleosomes in Relation to Fat Metabolism in Flag Leaf of Two Wheat Cultivars During Grain-filling

“…The membrane stability index (MSI) was determined according to Sairam et al [22]. Membrane leakage was determined according Vahala et al [23].…”

Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus

“…In the etr1 mutant, ethylene binding to the receptor is lost, and because of the dominant nature of the mutant alleles, this renders the plant insensitive to ethylene (18). In species less amenable to mutant screens, including trees, heterologous expression of the Arabidopsis etr1-1 mutant allele has been used to construct ethyleneinsensitive plants to explore the function of endogenous ethylene (19)(20)(21)(22).We have used a transgenic approach to generate ethyleneoverproducing and ethylene-insensitive Populus trees. Together with experiments using the ethylene perception inhibitor 1-methylcyclopropene (1-MCP) (23), our results demonstrate that ethylene stimulates cambial growth by acting through ethylene receptors, and that endogenous ethylene produced in leaning trees is a key regulator for the asymmetrical cambial growth in the TW response.…”

“…In the etr1 mutant, ethylene binding to the receptor is lost, and because of the dominant nature of the mutant alleles, this renders the plant insensitive to ethylene (18). In species less amenable to mutant screens, including trees, heterologous expression of the Arabidopsis etr1-1 mutant allele has been used to construct ethyleneinsensitive plants to explore the function of endogenous ethylene (19)(20)(21)(22).…”