Why plants’ soapy defences against disease don’t always wash

Natural soaps are an important weapon in the armoury that plants deploy to protect against disease attack, but a report today, in the international journal Nature, describes how disease-causing microbes can turn these plant defences to their own advantage. Scientists at the Sainsbury Laboratory (SL)[1] Norwich, UK, have discovered that fungi that attack tomatoes break down the natural soaps that help protect the plant against infection. Even worse for the plant, these breakdown products then interfere with the internal communication system that the plant relies on to actively fight off invaders.

“Our discovery shows that plants face a double whammy from attacks by fungi”, said Dr Anne Osbourn (leader of the research team at the SL). “The first line of defence is transformed into a weapon that makes the plant unable to protect itself against further attack.”

Many plants produce natural soaps (called saponins). These chemicals are toxic to bacteria and fungi and so form part of the plant’s protection against disease [2]. Researchers have known for some years that microbes that can successfully infect saponin-containing plants often produce enzymes that break down the saponins into less toxic chemicals. This enables the invader to breach the plant’s first line of defence.

Working with tomato [3] and tobacco the SL scientists have shown that saponin breakdown products interfere with essential communication processes in the plant. Signalling pathways that would normally set off the alarm system leading to the activation of defence responses are disabled. So in overcoming one line of defence the microbe also disrupts the plant’s ability to trigger its other defence systems.

“A better understanding of how plants and their diseases interact will eventually help scientists and breeders who are trying to breed plants with improved natural disease resistance. The next challenge for us is to find out how the saponin breakdown products interfere with internal plant signalling systems, and to establish how common this phenomenon is”, concludes Dr Osbourn.

[1] The Sainsbury Laboratory has a worldwide reputation for research on molecular plant-microbe interactions. The major aim of the Laboratory is to pursue the fundamental processes involved in the interactions of plants and their microbial pathogens and symbionts. Funding for the Laboratory is primarily through grants from a charitable foundation. In addition grants are obtained from research councils, the European Union and other organizations. The laboratory is located at the John Innes Centre, Norwich, UK, which is an independent, world-leading research centre in plant and microbial science.

[2] Many plants produce saponins that have anti-fungal and anti-bacterial activity. The Solanacae typically contain glycosylated steroidal and/or steroidal glycoalkaloid saponins. The main saponin in tomato (Lycopersicon esculentum) is a-tomatine, which has very strong anti-fungal activity.

The tomato leaf spot fungus (Septoria lycoperscii) will also infect tobacco (Nicotiana benthamiana). S. lycoperscii produces tomatinase, an extracellular enzyme, which hydrolyses glucose from a-tomatine to form b2-tomatine. b2-tomatine has significantly less anti-fungal activity than a-tomatine.

[3] In the early stages of infection tomato leaf spot (Septoria lycoperscii) hyphae enter the plant leaf through the stomata and grow among the mesophyll cells on the inside of the leaf.

However, mutants of S. lycoperscii, which were unable to produce tomatinase, were found to be unable to invade tobacco leaves. Attempted infections with the mutant lines induced severe cell death around the infection site and molecular analysis demonstrated that several genes known to be involved in defence against disease were active. Neither of these responses was seen in infections with the wild type fungus.

When researchers used gene-silencing technology to switch off the STG1 gene in tobacco (which is involved in the signal transmission pathway that leads to disease resistance) they found these plants were susceptible to the mutant lines of S. lycoperscii. This demonstrated that the effect of tomatinase is not simply through de-toxification of a-tomatine, but that there is interference with internal signaling associated with disease resistance.

In subsequent experiments a-tomatine, b2-tomatine or tomatinase were infiltrated into normal tobacco leaves, which were then challenge inoculated with wild type or mutant S. lycopersii. The mutant lines (tomatinase-deficient) were only able to infect leaves that had been infiltrated with b2-tomatine or tomatinase, not a-tomatine. This demonstrated that the interference with host defence is a result of the action of tomatinase and the presence of b2-tomatine.

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