Tomatidine and lycotetraose, hydrolysis products of α‐tomatine by Fusarium oxysporum tomatinase, suppress induced defense responses in tomato cells

Abstract

Many fungal pathogens of tomato produce extracellular enzymes, collectively known as tomatinases, that detoxify the preformed antifungal steroidal glycoalkaloid a-tomatine. Tomatinase from the vascular wilt pathogen of tomato Fusarium oxysporum f. sp. lycopersici cleaves a-tomatine into the aglycon tomatidine (Td) and the tetrasaccharide lycotetraose (Lt). Although modes of action of a-tomatine have been extensively studied, those of Td and Lt are poorly understood. Here, we show that both Td and Lt inhibit the oxidative burst and hypersensitive cell death in suspension-cultured tomato cells. A tomatinase-negative F. oxysporum strain inherently non-pathogenic on tomato was able to infect tomato cuttings when either Td or Lt was present. These results suggest that tomatinase from F. oxysporum is required not only for detoxification of atomatine but also for suppression of induced defense responses of host.

GLYCOALKALOID METABOLISM1 Is Required for Steroidal Alkaloid Glycosylation and Prevention of Phytotoxicity in Tomato

“…Several fungal and bacterial species possess tomatinases that are capable of removing part or even the entire lycotetraose structure from tomatine. By doing so, the toxicity of these substances toward the pathogens is reduced and the damage to the host plant may increase (Sandrock and Vanetten, 1998;Morrissey and Osbourn, 1999;Bouarab et al, 2002;Ito et al, 2004;Oka et al, 2006). Moreover, derivatives of a-tomatine hydrolysis could also mediate suppression of plant defenses (Bouarab et al, 2002;Ito et al, 2004).…”

“…By doing so, the toxicity of these substances toward the pathogens is reduced and the damage to the host plant may increase (Sandrock and Vanetten, 1998;Morrissey and Osbourn, 1999;Bouarab et al, 2002;Ito et al, 2004;Oka et al, 2006). Moreover, derivatives of a-tomatine hydrolysis could also mediate suppression of plant defenses (Bouarab et al, 2002;Ito et al, 2004). a-Tomatine is toxic to several fungi; thus, the reduced levels of a-tomatine we observed in leaf extracts of GAME1-silenced plants may explain the reduced inhibition of germination and growth of the fungal pathogen C. coccodes.…”

Dual Effects of Plant Steroidal Alkaloids on Saccharomycescerevisiae

“…The removal of sugars from saponins is traditionally associated with a reduction in antimi-crobial activity (30). However, ␣-tomatine hydrolysis products are able to suppress induced plant defense responses, indicating that they have other as yet uncharacterized effects on plant cells (7,25). ␣-Tomatine and its hydrolysis products have also been associated with a variety of effects on human health, including toxicity, cholesterol lowering, enhanced immune responses as cancer chemotherapy agents, and protection against pathogenic fungi and other microorganisms (16).…”

Streptomyces scabies87-22 Possesses a Functional Tomatinase

“…Data presented here do not rule out the possibility that tomatinase has a role in suppression of induced plant defenses in some hosts, just as it does in F. oxysporum f. sp. lycopersici and Septoria lycopersici (8,22). Expression analysis of genes involved in induced defense responses of wildtype strain-and ⌬tomA1 strain-inoculated plants will evaluate this hypothesis.…”

“…The toxicity of ␣-tomatine is typically mediated through complexing with sterols in eukaryotic membranes to ultimately cause membrane pores and cell lysis (30,31). In addition to nullification of an antimicrobial compound, tomatinases are able to indirectly suppress the induced plant defense response; this presumably results from plant recognition of by-products from ␣-tomatine hydrolysis (8,22). Despite the obvious advantage for a tomato pathogen to have a tomatinase in its arsenal, tomatinase-null mutants are not impaired in their ability to cause disease on tomato plants (42,46).…”