Trends in Plant Science
Volume 10, Issue 10, October 2005, Pages 503-509
Journal home page for Trends in Plant Science

Sulfur metabolism: a versatile platform for launching defence operations

This review is dedicated to Ahlert Schmidt (University of Hannover) on the occasion of his 65th birthday.
https://doi.org/10.1016/j.tplants.2005.08.006Get rights and content

Sulfur-containing defence compounds (SDCs) are crucial for the survival of plants under biotic and abiotic stress. SDCs include elemental sulfur (S0), H2S, glutathione, phytochelatins, various secondary metabolites and sulfur-rich proteins. Their constitutive and/or stress-induced formation is intimately dependent on demand-driven sulfate uptake and assimilation. Here, we highlight the complex network of plant SDCs and report on recent breakthroughs in our understanding of sulfur assimilation and how its regulation impinges on SDC function. These new insights have led us to revisit the hypothesis of ‘sulfur-induced resistance’, which claimed a prominent role for ‘extra’ sulfur nutrition in the defence potential of plants.

Section snippets

Sulfur nutrition-dependent stress resistance in plants: outline of the basic concept

Sulfur (S) is an essential macronutrient. It is taken up as sulfate and is assimilated into cysteine, an amino acid at the cross roads of primary metabolism, protein synthesis and the formation of low Mr sulfur-containing defence compounds (SDCs) (Figure 1). Sulfate also becomes activated to form phosphoadenosine phosphosulfate, the S-donor for sulfonation reactions. Parallel to S-assimilation ‘dissimilatory’ reactions, such as the release of H2S from cysteine 1, 2, possibly contribute to

Functional profiles of individual SDC groups: strong and weak candidates

Evidence for the direct effects of single SDCs on defence capacity is strong in some cases but remains controversial in others. Constitutively formed SDCs (belonging to the phytoanticipins) are important for defence against first infections, whereas pathogen-induced SDCs [e.g. phytoalexins and some sulfur-rich protein (SRP) isoforms] strongly contribute to induced resistance. Although, in general, SDCs are not designed for pathogen-specific defence operations, they are also likely to impact on

Regulation and compartmentation of SDC synthesis: orchestrating defence in space and time

SDC synthesis appears to be under complex control, involving not only a multitude of endogenous and exogenous signals, but also regulation at different levels ranging from transcriptional to post-translational mechanisms. The control of GSH synthesis and compartmentation will serve as an example. GSH is synthesized in two sequential ATP-dependent steps, catalysed by γ-glutamylcysteine synthetase (GSH1) and glutathione synthetase (GSH2). A recent study using Arabidopsis thaliana has revealed

Engineering individual SDCs: lessons from transgenic approaches

Because increased formation of SDCs could provide an improved protection against biotic and/or abiotic stress, attempts have been made to engineer SDC content. Transformation with either bacterial (E. coli 56, 57) or plant (Arabidopsis [58]) GSH1-constructs (encoding cytosolic or plastidic GSH1), or GR-constructs [59], all driven by the 35S-promoter, have yielded transgenic plants with moderately increased GSH content. Some of these plants exhibited increased stress tolerance, but results have

Demand-driven control of sulfate uptake and assimilation under biotic and abiotic stress: sensing S-depletion

The adaptation of sulfate uptake and assimilation under stress exposure is assumed to be a crucial determinant for SDC-based defence operations. Recently, several groups have performed microarray analysis to monitor the complexity of transcriptome and metabolome responses to S-starvation 5, 6, 7, 63. In these experiments, S-limitation was imposed externally by reducing or completely omitting sulfate in the nutrient medium. A general observation was that, as expected, genes for S-assimilation

Pinning down the molecular basis for a unique role of sulfur nutrition in plant defence: future perspectives

Since the 1980s, atmospheric S-depositions have declined drastically and, together with the renunciation of S-containing fertilizers and the higher S-demand of high-yielding crops, has led to widespread macroscopic S-deficiency in Western Europe. At the 9th International Rapeseed Congress in 1995, Ewald Schnug and colleagues reported on the seminal observation that supplementary S-fertilization reduced the incidence of fungal pathogens on Brassica crops. An SDC-mediated ‘Sulfur-Induced

Acknowledgements

Research in our laboratory was supported by a grant from the DFG to T.R. (FOR383). Additional support from the KWS SAAT AG, Einbeck, and the SÜDZUCKER AG, Mannheim, is gratefully acknowledged. We are grateful to the members of the German Plant Sulfur Group (funded by the DFG FOR383) for many fruitful discussions, and to Rüdiger Hell and Silvia Haneklaus for critical reading of the manuscript.

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