A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1.

The phytopathogenic fungus Alternaria alternata f. sp. lycopersici (AAL) produces toxins that are essential for pathogenicity of the fungus on tomato (Lycopersicon esculentum). AAL toxins and fumonisins of the unrelated fungus Fusarium moniliforme are sphinganine-analog mycotoxins (SAMs), which cause inhibition of sphingolipid biosynthesis in vitro and are toxic for some plant species and mammalian cell lines. Sphingolipids can be determinants in the proliferation or death of cells. We investigated the tomato Alternaria stem canker (Asc) locus, which mediates resistance to SAM-induced apoptosis. Until now, mycotoxin resistance of plants has been associated with detoxification and altered affinity or absence of the toxin targets. Here we show that SAM resistance of tomato is determined by Asc-1, a gene homologous to the yeast longevity assurance gene LAG1 and that susceptibility is associated with a mutant Asc-1. Because both sphingolipid synthesis and LAG1 facilitate endocytosis of glycosylphosphatidylinositol-anchored proteins in yeast, we propose a role for Asc-1 in a salvage mechanism of sphingolipid-depleted plant cells.

[1]  E. M. Wray,et al.  Fumonisin- and AAL-Toxin-Induced Disruption of Sphingolipid Metabolism with Accumulation of Free Sphingoid Bases , 1994, Plant physiology.

[2]  M. Skrzypek,et al.  Suppressor gene analysis reveals an essential role for sphingolipids in transport of glycosylphosphatidylinositol-anchored proteins in Saccharomyces cerevisiae , 1997, Journal of bacteriology.

[3]  S. Clouse,et al.  Rapid purification of host-specific pathotoxins from Alternaria alternata f. sp. lycopersici by solid-phase adsorption on octadecylsilane. , 1985, Journal of chromatography.

[4]  K. Simons,et al.  Neuronal polarity: essential role of protein-lipid complexes in axonal sorting. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Bostock,et al.  Apoptosis: A Functional Paradigm for Programmed Plant Cell Death Induced by a Host-Selective Phytotoxin and Invoked during Development. , 1996, The Plant cell.

[6]  O. Yoder,et al.  Molecular Genetics of Host-Specific Toxins in Plant Disease , 1998, Developments in Plant Pathology.

[7]  M. Gao,et al.  Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. , 1999, The Plant journal : for cell and molecular biology.

[8]  F. Takken,et al.  Genetic and physical analysis of a YAC contig spanning the fungal disease resistance locus Asc of tomato (Lycopersicon esculentum) , 1999, Molecular and General Genetics MGG.

[9]  H. Sambrook.  Molecular cloning : a laboratory manual. Cold Spring Harbor, NY , 1989 .

[10]  D. V. Lynch.  Enzymes of sphingolipid metabolism in plants. , 2000, Methods in enzymology.

[11]  A. Futerman.  Inhibition of sphingolipid synthesis: effects on glycosphingolipid-GPI-anchored protein microdomains. , 1995, Trends in cell biology.

[12]  R. F. Smith,et al.  BCM Search Launcher--an integrated interface to molecular biology data base search and analysis services available on the World Wide Web. , 1996, Genome research.

[13]  Y. Itoh,et al.  AAL-Toxin-Deficient Mutants of Alternaria alternata Tomato Pathotype by Restriction Enzyme-Mediated Integration. , 1997, Phytopathology.

[14]  S. Spiegel,et al.  Sphingolipids--the enigmatic lipid class: biochemistry, physiology, and pathophysiology. , 1997, Toxicology and applied pharmacology.

[15]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[16]  B. Liu,et al.  The Allophycocyanin [alpha] Subunit Gene from Cyanidium caldarium , 1994, Plant physiology.

[17]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[18]  P. Walter,et al.  Two endoplasmic reticulum (ER) membrane proteins that facilitate ER-to-Golgi transport of glycosylphosphatidylinositol-anchored proteins. , 1999, Molecular biology of the cell.

[19]  G. Martin.  Functional analysis of plant disease resistance genes and their downstream effectors. , 1999, Current opinion in plant biology.

[20]  M. Dutton.  Fumonisins, mycotoxins of increasing importance: their nature and their effects. , 1996, Pharmacology & therapeutics.

[21]  D. Gilchrist.  Interaction of the asc locus in f 8 paired lines of tomato with Alternaria alternata f. sp. lycopersici and AAL-toxin , 1987 .

[22]  T. Doering,et al.  Specific requirements for the ER to Golgi transport of GPI-anchored proteins in yeast. , 1997, Journal of cell science.

[23]  H. Abbas,et al.  Susceptibility of Various Crop and Weed Species to AAL-Toxin, a Natural Herbicide , 1995, Weed Technology.

[24]  A. Horváth,et al.  Ceramide synthesis enhances transport of GPI‐anchored proteins to the Golgi apparatus in yeast. , 1994, The EMBO journal.

[25]  D. Franklin,et al.  Cloning and characterization of LAG1, a longevity-assurance gene in yeast. , 1994, The Journal of biological chemistry.

[26]  A. Bacic,et al.  GPI-anchors on arabinogalactan-proteins: implications for signalling in plants , 1998 .

[27]  F. Reggiori,et al.  Biosynthesis of Inositol Phosphoceramides and Remodeling of Glycosylphosphatidylinositol Anchors in Saccharomyces cerevisiae Are Mediated by Different Enzymes* , 1998, The Journal of Biological Chemistry.

[28]  J. Walton,et al.  Host-selective toxins: agents of compatibility. , 1996, The Plant cell.

[29]  G. Bonnema,et al.  An improved method of partially digesting plant megabase DNA suitable for YAC cloning: application to the construction of a 5.5 genome equivalent YAC library of tomato. , 1996, The Plant journal : for cell and molecular biology.

[30]  S. Jazwinski,et al.  Homologs of the yeast longevity gene LAG1 in Caenorhabditis elegans and human. , 1998, Genome research.

[31]  Hong Wang,et al.  Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  F. Ausubel,et al.  A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. , 1993, The Plant journal : for cell and molecular biology.