Abstract
Rust fungi are obligate biotrophic pathogens that differentiate a series of specialized cells to establish infection. One of these cells, the haustorium, which serves to absorb nutrients from living host cells, normally develops only in planta. Here, we show that the rust fungus Uromyces fabae (Pers.) Schroet. stimulates volatile emission of its host, broad bean (Vicia faba L.). Volatiles were identified and shown to be perceived by the fungus in in vitro assays that excluded the host. Three of them, nonanal, decanal, and hexenyl acetate promoted the development of haustoria on artificial membranes. In contrast, the terpenoid farnesyl acetate suppressed this differentiation. In assays using whole plants, farnesyl acetate reduced rust disease not only on broad bean but also on several cereals and legumes including soybean. This natural substance was effective against all rusts tested when directly applied to the host. This demonstrated that farnesyl acetate may serve as a powerful novel tool to combat rust fungi including Phakopsora pachyrhizi that currently threatens the production of soybeans world-wide.
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Abbreviations
- HMC:
-
Haustorial mother cell
- GC/MS:
-
Gas chromatography/mass spectrometry
References
Boehm EWA, Wenstrom JC, McLaughlin DJ, Szabo LJ, Roelfs AP, Bushnell WR (1992) An ultrastructural pachytene karyotype for Puccinia graminis f. sp. tritici. Can J Bot 70:401–413
DeBary A (1863) Recherches sur le developpement de quelques champignons parasites. Ann Sci Nat Bot 20:5–148
Deising H, Jungblut PR, Mendgen K (1991) Differentiation-related proteins of the broad bean rust fungus Uromyces viciae-fabae, as revealed by high-resolution two-dimensional polyacrylamide-gel electrophoresis. Arch Microbiol 155:191–198
Donath J, Boland W (1995) Biosynthesis of acyclic homoterpenes: enzyme selectivity and absolute configuration of the nerolidol precursor. Phytochemistry 39:785–790
Epstein L, Nicholson RL (1997) Adhesion of spores and hyphae to plant surfaces. In: Carroll GC, Tudzynski P (eds) The mycota V, part A. Springer, Berlin Heidelberg New York, pp 11–25
Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297
Flaishman MA, Kolattukudy PE (1994) Timing of fungal invasion using host’s ripening hormone as a signal. Proc Natl Acad Sci USA 91:6579–6583
French RC (1992) Volatile chemical germination stimulators of rust and other fungal spores. Mycologia 84:277–288
French RC, Nester SE, Stavely JR (1993) Stimulation of germination of teliospores of Uromyces appendiculatus by volatile aroma compounds. J Agric Food Chem 41:1743–1747
Gold RE, Mendgen K (1983) Activation of teliospore germination in Uromyces appendiculatus var. appendiculatus II. Light and host volatiles. J Phytopathol 108:281–293
Heath MC (1989) In vitro formation of haustoria of the cowpea rust fungus, Uromyces vignae, in the absence of a living plant cell I. Light microscopy. Physiol Mol Plant Pathol 35:357–366
Heath MC (1990) Influence of carbohydrates on the induction of haustoria of the cowpea rust fungus in vitro. Exp Mycol 14:84–88
Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann Bot Lond 80:713–720
Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED (1987) Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235:1659–1662
Holopainen JK (2004) Multiple functions of inducible plant volatiles. Trends Plant Sci 9:529–533
Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668
Kulakiotu EK, Thanassoulopoulos CC, Sfakiotakis EM (2004) Biological control of Botrytis cinerea by volatiles of ‘Isabella’ grapes. Phytopathology 94:924–931
Kunert M, Biedermann A, Koch T, Boland W (2002) Ultrafast sampling and analysis of plant volatiles by a hand-held miniaturised GC with pre-concentration unit: Kinetic and quantitative aspects of plant volatile production. J Sep Sci 25:677–684
Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam KH, Amar O, Lastochkin E, Larkov O, Ravid U, Hiatt W, Gepstein S, Pichersky E (2001) Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol 127:1256–1265
Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7:352–356
Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386
Miles MR, Frederick RD, Hartmann GL (2003) Soybean rust: is the U.S. soybean crop at risk? http://www.apsnet.org/online/feature/rust
Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6:320–326
Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243
Pivonia S, Yang XB (2004) Assessment of the potential year-round establishment of soybean rust throughout the world. Plant Dis 88:523–529
Raguso RA, Roy BA (1998) ‘Floral’ scent production by Puccinia rust fungi that mimic flowers. Mol Ecol 7:1127–1136
Robert C, Bancal MO, Lannou C (2004) Wheat leaf rust uredospore production on adult plants: influence of leaf nitrogen content and Septoria tritici blotch. Phytopathology 94:712–721
Rogers J, Redding J (2004) USDA confirms soybean rust in United States. http://www.usda.gov/wps/portal/!ut/p/_s.7_0_A/7_0_1OB?contentidonly = true&contentid = 2004/11/0498.xml
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932
Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641–667
Staples RC (2000) Research on the rust fungi during the twentieth century. Annu Rev Phytopathol 38:49–69
Staples RC, Hoch HC (1997) Physical and chemical cues for spore germination and appressorium formation by fungal pathogens. In: Carroll GC, Tudzynski P (eds) The mycota V, part A. Springer, Berlin Heidelberg New York, pp 27–40
Stokstad E (2004) Plant pathologists gear up for battle with dread fungus. Science 306:1672–1673
Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci USA 98:8139–8144
Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98:8133–8138
Wiethölter N, Horn S, Reisige K, Beike U, Moerschbacher BM (2003) In vitro differentiation of haustorial mother cells of the wheat stem rust fungus, Puccinia graminis f. sp. tritici, triggered by the synergistic action of chemical and physical signals. Fungal Genet Biol 38:320–326
Acknowledgements
Financial support was provided by the Deutsche Forschungsgemeinschaft. We express our gratitude to Christine Giele and Heinz Vahlenkamp for expert technical assistance. We thank Matthias Hahn and Emily Wheeler for critically reading the manuscript.
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Mendgen, K., Wirsel, S.G.R., Jux, A. et al. Volatiles modulate the development of plant pathogenic rust fungi. Planta 224, 1353–1361 (2006). https://doi.org/10.1007/s00425-006-0320-2
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DOI: https://doi.org/10.1007/s00425-006-0320-2