Synthesis of Phytoalexins in Sorghum as a Site-Specific Response to Fungal Ingress

Snyder, Beth; Nicholson, Ralph L.

doi:10.1126/science.248.4963.1637

Cited by 321 publications

(204 citation statements)

References 17 publications

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“…Previous work in a range of other plant-microbe interactions suggests that a stereotypic cellular polarisation and secretion process occurs at the cell periphery. For example, the epidermal cells of Sorghum leaves respond to attempted penetration of the hemibiotroph Colletotrichum graminicola with focal accumulation of coloured vesicles containing the antifungal 3-deoxcyanthocyanidin flavonoid phytoalexins apigeninidin and luteolinidin [30,31]. Shikonin, a red naphthoquinone derivative, is a secondary metabolite that has antimicrobial activity that specifically occurs in boraginaceous plants such as Lithospermum erythrorhizon [32].…”

Section: Snare Proteins and The First Line Of Defence Against Fungal mentioning

confidence: 99%

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Schulze‐Lefert

2004

Current Opinion in Plant Biology

124

101

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New findings challenge the traditional view of the plant cell wall as passive structural barrier to invasion by fungal microorganisms. A surveillance system for cell wall integrity appears to sense perturbation of the cell wall structure upon fungal attack and is interconnected with known plant defence signalling pathways. Biotrophic fungi might manipulate this surveillance system for the establishment of biotrophy. The attempts of fungi to invade also induce a sub-cellular polarisation in attacked cells, which activates an ancient vesicle-associated resistance response that possibly enables the focal transport of regulatory cargo and the secretion of toxic cargo. The underlying resistance machinery might have been subverted by biotrophic fungi for pathogenesis. IntroductionPenetration through the plant cell wall represents an Achilles heel in the pathogenesis of most biotrophic fungi and marks a lifestyle transition from extra-cellular to invasive growth. Modification of the plant cell wall was recognised for the first time as potential resistance mechanism almost 80 years ago following work in which 78 plant species and varieties were challenged with Alternaria spp. and other leaf-spotting fungi [1]. The termination of fungal pathogenesis at the cell wall was commonly associated with wall 'thickenings' and the formation of local additions or 'callosities' in the paramural space (i.e. the space between the cell wall and the plasma membrane). Formation of these cell wall appositions (CWAs) or papillae is usually accompanied by a co-localised accumulation of phenolics and reactive oxygen species [2][3][4][5][6]. The complex process of sub-cellular cell wall remodelling is tightly linked to the rapid disassembly and subsequent focal reassembly of the plant cytoskeleton at fungal entry sites, which is indicative of a pathogen-triggered cell polarisation [6][7][8][9]. There has been a long-standing controversy, however, over whether CWAs function in disease resistance or facilitate the entry of fungal pathogens into host cells by providing a structural collar for the intruder. New molecular genetic data from Arabidopsis and barley have indeed revealed that molecular processes at and in CWAs have Janus-faced functions, that is, functions for fungal pathogenesis and in resistance responses. Focal vesicle transport and vesicle fusion events that are dependent on SNAP (soluble N-ethylmaleimide-sensitive-factor-association protein) receptor (SNARE) proteins at the plasma membrane emerge as potential common underlying mechanisms that might be interconnected with a poorly understood cell wall integrity surveillance system. In this review, I discuss the seemingly paradoxical functions of these processes in establishing the biotrophic lifestyle and in disease resistance at the cell periphery.Linking cell wall structure to biotic stress signalling Callose, a (1!3)-b-D-glucan, has long been known to be synthesised and deposited rapidly at CWAs upon microbial attack. This polymer was thought to contribute to a physical barrie...

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Section: Snare Proteins and The First Line Of Defence Against Fungal mentioning

confidence: 99%

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Schulze‐Lefert

2004

Current Opinion in Plant Biology

124

101

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“…Phytoalexins are low-molecular-weight antimicrobial compounds produced by plants in response to infection or stress (Nicholson & Hammerschmidt, 1992 ;VanEtten et al, 1994 ;Smith 1996). In sorghum leaf tissue, these phytoalexins first appear in the cells which are being invaded, where they accumulate in inclusions in the cytoplasm (Snyder & Nicholson, 1990 ;Snyder et al, 1991). The inclusions migrate to the site of attempted penetration, become pigmented, lose their spherical shape and ultimately release their contents into the cytoplasm, killing the cell and restricting further development of the pathogen.…”

Section: mentioning

confidence: 99%

“…The inclusions migrate to the site of attempted penetration, become pigmented, lose their spherical shape and ultimately release their contents into the cytoplasm, killing the cell and restricting further development of the pathogen. The accumulation of 3-deoxyanthocyanidin phytoalexins is a site-specific response localized around the site of attempted fungal penetration (Nicholson et al, 1987(Nicholson et al, , 1988Snyder & Nicholson, 1990). The accumulation of the phytoalexins occurs much more rapidly in infected cells of resistant cultivars than in susceptible cultivars, preventing the proliferation of fungal hyphae throughout the tissue (Wharton & Julian, 1996).…”

Section: mentioning

confidence: 99%

Temporal synthesis and radiolabelling of the sorghum 3‐deoxyanthocyanidin phytoalexins and the anthocyanin, cyanidin 3‐dimalonyl glucoside

Wharton

Nicholson

2000

New Phytologist

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Sorghum (Sorghum bicolor) synthesizes a complex mixture of 3-deoxyanthocyanidin phytoalexins in response to inoculation with the non-pathogenic fungus Bipolaris maydis. The anthocyanin cyanidin 3-dimalonyl glucoside, is also synthesized naturally in response to light. To determine the order and time of appearance of these compounds, etiolated sorghum mesocotyls were inoculated with B. maydis and tissue extracts were analysed by photodiode array-HPLC every 2 h for the first 24 h and at 48 h post inoculation (hpi). Uninoculated and inoculated etiolated mesocotyls were also allowed to incorporate L-[U-"%C] phenylalanine. Apigeninidin appeared at 10 hpi, followed by luteolinidin and apigeninidin 5-O-arabinoside at 14 hpi. Luteolinidin 5-methylether was not detected until 18 hpi and apigeninidin 7-methylether not until 20 hpi. The concentrations of the primary phytoalexins, apigeninidin, luteolinidin and apigeninidin 5-O-arabinoside, rose steadily between 12 and 24 hpi, and the levels of apigeninidin and luteolinidin were approximately equivalent by 24 hpi. However, between 24 and 48 hpi luteolinidin and luteolinidin 5-methylether accumulated rapidly so that by 48 hpi the amounts of luteolinidin and luteolinidin 5-methylether had increased approximately twofold. Radiolabelling also showed that "%C was incorporated into the 3-deoxyanthocyanidins and cyanidin 3-dimalonyl glucoside. Several other unidentified phenolic compounds also accumulated radioactivity.

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“…For example, flavonols are essential for male fertility in maize, petunia, and tobacco (Nicotiana tabacum; Mo et al, 1992;Ylstra et al, 1992), but not in Arabidopsis (Burbulis et al, 1996;Ylstra et al, 1996). Isoflavonoids are the major phytoalexins in legumes (Dixon and Steele, 1999), whereas similar roles are played by 3-deoxyanthocyanidins in sorghum Sorghum bicolor) and other grasses (Snyder and Nicholson, 1990). The flexibility of this and other secondary metabolic pathways suggests that the selective pressures upon genes encoding enzymes involved in secondary metabolism are quite variable.…”

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confidence: 99%

Functional Conservation of Plant Secondary Metabolic Enzymes Revealed by Complementation of Arabidopsis Flavonoid Mutants with Maize Genes

2001

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Mutations in the transparent testa (tt) loci abolish pigment production in Arabidopsis seed coats. The TT4, TT5, and TT3 loci encode chalcone synthase, chalcone isomerase, and dihydroflavonol 4-reductase, respectively, which are essential for anthocyanin accumulation and may form a macromolecular complex. Here, we show that the products of the maize (Zea mays) C2, CHI1, and A1 genes complement Arabidopsis tt4, tt5, and tt3 mutants, restoring the ability of these mutants to accumulate pigments in seed coats and seedlings. Overexpression of the maize genes in wild-type Arabidopsis seedlings does not result in increased anthocyanin accumulation, suggesting that the steps catalyzed by these enzymes are not rate limiting in the conditions assayed. The expression of the maize A1 gene in the flavonoid 3Ј hydroxylase Arabidopsis tt7 mutant resulted in an increased accumulation of pelargonidin. We conclude that enzymes involved in secondary metabolism can be functionally exchangeable between plants separated by large evolutionary distances. This is in sharp contrast to the notion that the more relaxed selective constrains to which secondary metabolic pathways are subjected is responsible for the rapid divergence of the corresponding enzymes.

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Synthesis of Phytoalexins in Sorghum as a Site-Specific Response to Fungal Ingress

Cited by 321 publications

References 17 publications

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Temporal synthesis and radiolabelling of the sorghum 3‐deoxyanthocyanidin phytoalexins and the anthocyanin, cyanidin 3‐dimalonyl glucoside

Functional Conservation of Plant Secondary Metabolic Enzymes Revealed by Complementation of Arabidopsis Flavonoid Mutants with Maize Genes

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