Leaf rust induced volatile organic compounds signalling in willow during the infection

Plants are known to emit volatile organic compounds (VOC) in response to various biotic or abiotic stresses. Although the VOC emission in the case of insect attacks is well described, there is only little known about the impact of pathogens on plant emission. In the present study, we used a willow-leaf rust system to describe the effects of a biotrophic fungal infection on the VOC emission pattern of willow leaves. We detected that isoprene emissions from rust-infected leaves decreased threefold compared to control. The total monoterpene emissions did not change although a stress-signalling compound (Z)-β-ocimene showed an increase in infected plants on several days. The infection also increased the emission of sesquiterpenes and lipoxygenase products (LOX) by factors of 175-fold and 10-fold, respectively. The volatile emission signals showed two clear peaks during the experiment. At 6, 7 and 12 days post-infection (dpi), the relative volatile emission signal increased to about sixfold compared to uninfected plants. These time points are directly connected to rust infection since at 6 dpi the first rust pustules appeared on the leaves and at 12 dpi necrosis had developed around several pustules. We present correlations between LOX and sesquiterpene emission signals, which suggest at least two different steps in eliciting the volatile emission.

[1]  S. Rambal,et al.  Impact of drought on seasonal monoterpene emissions from Quercus ilex in southern France , 2002 .

[2]  K. Mendgen,et al.  Rust haustoria: nutrient uptake and beyond. , 2003, The New phytologist.

[3]  Ü. Niinemets,et al.  Modeling the temporal dynamics of monoterpene emission by isotopic labeling in Quercus ilex leaves , 2010 .

[4]  H. Hakola.  Biogenic volatile organic compound (voc) emissions from boreal deciduous trees and their atmospheric chemistry , 2002 .

[5]  G. Pilate,et al.  Histological Aspects of a Hypersensitive Response in Poplar to Melampsora larici-populina. , 1999, Phytopathology.

[6]  M. Heil,et al.  Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature , 2007, Proceedings of the National Academy of Sciences.

[7]  Petri Peltonen,et al.  Epirrita autumnata induced VOC emission of silver birch differ from emission induced by leaf fungal pathogen , 2007, Arthropod-Plant Interactions.

[8]  BVOC Emissions at the Canopy Scale: Micrometeorological Flux Measurements , 1999 .

[9]  J. Holopainen,et al.  Multiple functions of inducible plant volatiles. , 2004, Trends in plant science.

[10]  S. Rambal,et al.  Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex. , 2002, Physiologia plantarum.

[11]  K. Heinsoo,et al.  Rust severity in bioenergy willow plantations treated with additional nutrients , 2009 .

[12]  J. Tumlinson,et al.  In vivo Volatile Emissions from Peanut Plants Induced by Simultaneous Fungal Infection and Insect Damage , 2004, Journal of Chemical Ecology.

[13]  F. Wilson,et al.  Symptoms of pests, rust and other disorders on leaves of willow fertilised with wastewater, urine or sewage sludge , 2008 .

[14]  W. M. Dawson,et al.  Short rotation coppice willow in Northern Ireland since 1973: development of the use of mixtures in the control of foliar rust (Melampsora spp.) , 1998 .

[15]  Joshua S. Yuan,et al.  Smelling global climate change: mitigation of function for plant volatile organic compounds. , 2009, Trends in ecology & evolution.

[16]  R. Staples.  Research on the Rust Fungi During the Twentieth Century. , 2000, Annual review of phytopathology.

[17]  W. Boland,et al.  Volatiles modulate the development of plant pathogenic rust fungi , 2006, Planta.

[18]  M. C. Heath.  Signalling between Pathogenic Rust Fungi and Resistant or Susceptible Host Plants , 1997 .

[19]  J. Oakey,et al.  Interaction of methyl jasmonate, wounding and fungal elicitation during sesquiterpene induction in Hyoscyamus muticus in root cultures , 1998, Plant Cell Reports.

[20]  A. Grover,et al.  Molecular Biology, Biotechnology and Genomics of Flooding-Associated Low O2 Stress Response in Plants , 2006 .

[21]  J. Ponche,et al.  The biogenic volatile organic compounds emission inventory in France: application to plant ecosystems in the Berre-Marseilles area (France). , 2006, The Science of the total environment.

[22]  L. Vierling,et al.  Volatile organic compound emission rates from mixed deciduous and coniferous forests in Northern Wisconsin, USA , 1999 .

[23]  J. Peñuelas,et al.  Seasonal patterns of non-terpenoid C6-C10 VOC emission from seven Mediterranean woody species. , 2001, Chemosphere.

[24]  Katrin Heinsoo,et al.  Relation between leaf rust (Melampsora epitea) severity and the specific leaf area in short rotation coppice willows , 2010, European Journal of Plant Pathology.

[25]  C. Kost,et al.  Herbivore-induced, indirect plant defences. , 2005, Biochimica et biophysica acta.

[26]  H. Hakola,et al.  Variation of the VOC emission rates of birch species during the growing season , 2001 .

[27]  E. J. van Henten,et al.  Health monitoring of plants by their emitted volatiles: trichome damage and cell membrane damage are detectable at greenhouse scale , 2009 .

[28]  Rainer Steinbrecher,et al.  Temporal and spatial variation of forest VOC emissions in Germany in the decade 1994-2003 , 2006 .

[29]  Y. Hiratsuka,et al.  Illustrated genera of rust fungi. , 1960 .

[30]  A. Schüßler,et al.  Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi , 2006, Nature.

[31]  H. El-Sheikh,et al.  Efficacy of fungal rust disease on willow plant in Egypt. , 2009 .

[32]  A. Séguin,et al.  Transcriptome profiling in hybrid poplar following interactions with Melampsora rust fungi. , 2009, Molecular plant-microbe interactions : MPMI.

[33]  J. Holopainen,et al.  Real-time monitoring of herbivore induced volatile emissions in the field. , 2010, Physiologia plantarum.

[34]  J. Flexas,et al.  Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. , 2009, Journal of experimental botany.

[35]  J. Tumlinson,et al.  Systemic induction of volatile release in cotton: How specific is the signal to herbivory? , 2005, Planta.

[36]  J. Holopainen,et al.  Emission of herbivore‐induced volatile terpenoids from two hybrid aspen (Populus tremula×tremuloides) clones under ambient and elevated ozone concentrations in the field , 2007 .

[37]  Tuomas Laurila,et al.  The hydrocarbon emission rates of tea-leafed willow (Salix phylicifolia), silver birch (Betula pendula) and European aspen (Populus tremula) , 1998 .

[38]  R. Jansen,et al.  Release of lipoxygenase products and monoterpenes by tomato plants as an indicator of Botrytis cinerea-induced stress. , 2009, Plant biology.

[39]  Ian T. Baldwin,et al.  Volatile Signaling in Plant-Plant Interactions: "Talking Trees" in the Genomics Era , 2006, Science.

[40]  P. Wincker,et al.  Transcript Profiling of Poplar Leaves upon Infection with Compatible and Incompatible Strains of the Foliar Rust Melampsora larici-populina1[W] , 2007, Plant Physiology.

[41]  Corinne Robert,et al.  Wheat leaf photosynthesis loss due to leaf rust, with respect to lesion development and leaf nitrogen status. , 2004, The New phytologist.