Horizontal Chromosome Transfer, a Mechanism for the Evolution and Differentiation of a Plant-Pathogenic Fungus

ABSTRACT The tomato pathotype of Alternaria alternata produces host-specific AAL toxin and causes Alternaria stem canker on tomato. A polyketide synthetase (PKS) gene, ALT1, which is involved in AAL toxin biosynthesis, resides on a 1.0-Mb conditionally dispensable chromosome (CDC) found only in the pathogenic and AAL toxin-producing strains. Genomic sequences of ALT1 and another PKS gene, both of which reside on the CDC in the tomato pathotype strains, were compared to those of tomato pathotype strains collected worldwide. This revealed that the sequences of both CDC genes were identical among five A. alternata tomato pathotype strains having different geographical origins. On the other hand, the sequences of other genes located on chromosomes other than the CDC are not identical in each strain, indicating that the origin of the CDC might be different from that of other chromosomes in the tomato pathotype. Telomere fingerprinting and restriction fragment length polymorphism analyses of the A. alternata strains also indicated that the CDCs in the tomato pathotype strains were identical, although the genetic backgrounds of the strains differed. A hybrid strain between two different pathotypes was shown to harbor the CDCs derived from both parental strains with an expanded range of pathogenicity, indicating that CDCs can be transmitted from one strain to another and stably maintained in the new genome. We propose a hypothesis whereby the ability to produce AAL toxin and to infect a plant could potentially be distributed among A. alternata strains by horizontal transfer of an entire pathogenicity chromosome. This could provide a possible mechanism by which new pathogens arise in nature.

Sphingosine-related mycotoxins in plant and animal diseases

The AAL-toxins and fumonisins are a group of chemically related phytotoxic congeners produced by Alternaria alternata f. sp. lycopersici and Fusarium moniliforme, respectively, that also are widespread mycotoxins with important health implications. These mycotoxins, which bear a structural relationship to the sphingoid base, sphingosine, also incite maladies in animals ranging from neoplasms to renal, neural, and hepatic necrosis. A. alternata f. sp. lycopersici causes the Alternaria stem canker disease in tomatoes, while F. moniliforme causes pink ear rot of maize and is associated with post-harvest contamination of many different food staples. These toxins are potent inhibitors of ceramide synthase in plants and animals. Sphingoid bases are mediators of signal transduction leading to neoplasms and necrosis in animals. Significant inhibition of ceramide synthase in microsomal preparations of tomato occurs at 20 nM with an I50 in the range of 35–40 nM for both AAL-toxin, TA, and fumonisin, FB1. In plants, specific alterations of physiological processes associated with cellular response to these toxins appears to be required for cell death. A net decrease in sucrose influx to treated leaves occurs within 4 h of AAL-toxin treatment. Untreated leaves of toxin-resistant and -sensitive isolines of tomato show significant differences in sucrose transport capacity. Exogenous application of sucrose transport inhibitors mimicked AAL-toxin symptoms and enhanced cell death in susceptible lines of tomato. Conversely, the accumulation of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACQ occurred in 1 h and increased rapidly during the next 6 h after exposure to AAL-toxin. ACC accumulation is followed by a burst in ethylene within 12 h. Application of specific inhibitors of ethylene synthesis or ethylene action results in a decrease in toxin-induced cell death. These toxins appear to be useful tools for defining biochemical and molecular features common to induced cell death in both plants and animals. Key words: AAL-toxins, fumonisins, mycotoxins, host-selective toxins, Alternaria stem canker, Alternaria alternata, Fusarium moniliforme.