Light-dependent death of maize lls1 cells is mediated by mature chloroplasts

Truman State University, IRK, Missouri, United States
Plant physiology (Impact Factor: 6.84). 01/2003; 130(4):1894-907. DOI: 10.1104/pp.008441
Source: PubMed


We reported previously the isolation of a novel cell death-suppressing gene from maize (Zea mays) encoded by the Lls1 (Lethal leaf spot-1) gene. Although the exact metabolic function of LLS1 remains elusive, here we provide insight into mechanisms that underlie the initiation and propagation of cell death associated with lls1 lesions. Our data indicate that lls1 lesions are triggered in response to a cell-damaging event caused by any biotic or abiotic agent or intrinsic metabolic imbalance--as long as the leaf tissue is developmentally competent to develop lls1 lesions. Continued expansion of these lesions, however, depends on the availability of light, with fluence rate being more important than spectral quality. Double-mutant analysis of lls1 with two maize mutants oil-yellow and iojap, both compromised photosynthetically and unable to accumulate normal levels of chlorophyll, indicated that it was the light harvested by the plant that energized lls1 lesion development. Chloroplasts appear to be the key mediators of lls1 cell death; their swelling and distortion occurs before any other changes normally associated with dying cells. In agreement with these results are indications that LLS1 is a chloroplast-localized protein whose transcript was detected only in green tissues. The propagative nature of light-dependent lls1 lesions predicts that cell death associated with these lesions is caused by a mobile agent such as reactive oxidative species. LLS1 may act to prevent reactive oxidative species formation or serve to remove a cell death mediator so as to maintain chloroplast integrity and cell survival.

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    • "Numerous lesion mimic mutants have been identified and cloned, e.g., acd2, acd11 and lsd1 in Arabidopsis, mlo in barley and Lls1 in maize, that were cloned in the 1990s. These genes encode proteins that regulate plant defense to pathogens and/or cell death (Dietrich et al., 1994, 1997; Buschges et al., 1997; Gray et al., 1997, 2002). In rice, spl7 was the first lesion mimic mutant gene to be cloned and encodes a heat stress transcription factor (Yamanouchi et al., 2002). "
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    • "The Arabidopsis propagative LMM acd1 and its maize orthologue lls1 are deficient in PAO (pheophorbide a oxygenase), the key enzyme of chlorophyll catabolism: these mutants accumulate the phototoxic chlorophyll catabolite pheide a that in a light-dependent manner allows the production of ROS, the presumed diffusible signal responsible for the spread of the lesions (Pružinská, et al., 2003). The first morphological alteration reported in lls1 mutants is the loss of structural integrity of chloroplast and thylakoid membranes in mesophyll cells (Gray et al., 2002), which, by causing the leakage of phototoxic chlorophyll intermediates, determine the propagative cell death (Pružinská et al., 2003). "
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    ABSTRACT: Lesion mimic mutants (LMMs) are a class of mutants in which hypersensitive cell death and defence responses are constitutively activated in the absence of pathogen attack. Various signalling molecules, such as salicylic acid (SA), reactive oxygen species (ROS), nitric oxide (NO), Ca(2+), ethylene, and jasmonate, are involved in the regulation of multiple pathways controlling hypersensitive response (HR) activation, and LMMs are considered useful tools to understand the role played by the key elements of the HR cell death signalling cascade. Here the characterization of an Arabidopsis LMM lacking the function of the FZL gene is reported. This gene encodes a membrane-remodelling GTPase playing an essential role in the determination of thylakoid and chloroplast morphology. The mutant displayed alteration in chloroplast number, size, and shape, and the typical characteristics of an LMM, namely development of chlorotic lesions on rosette leaves and constitutive expression of genetic and biochemical markers associated with defence responses. The chloroplasts are a major source of ROS, and the characterization of this mutant suggests that their accumulation, triggered by damage to the chloroplast membranes, is a signal sufficient to start the HR signalling cascade, thus confirming the central role of the chloroplast in HR activation.
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    • "Recent research has linked chloroplast-produced ROS with hypersensitive response (HR) (Mur et al., 2008). Chloroplast-produced ROS have been shown to be capable of transmitting the spread of woundinduced PCD through maize tissues (Gray et al., 2002). "
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