‘Floral’ scent production by Puccinia rust fungi that mimic flowers

Crucifers (Brassicaceae) in 11 genera are often infected by rust fungi in the Puccinia monoica complex. Infection causes a ‘pseudoflower’ to form that is important for attracting insect visitors that sexually outcross the fungus. ‘Pollinator’ attraction is accomplished through visual floral mimicry, the presence of a nectar reward and floral fragrances. Here we used gas chromatography and mass spectrometry to identify and quantify fragrance production by these rust fungi on several Arabis hosts, and by co‐occurring true flowers that share insect visitors. Fungal pseudoflowers produced distinctive floral fragrances composed primarily of aromatic alcohols, aldehydes and esters. Pseudoflower fragrances were chemically similar to noctuid‐moth‐pollinated flowers, such as Cestrum nocturnum and Abelia grandiflora, but were very different from host flowers, host vegetation and the flowers of coblooming, nonhost angiosperms. There was variation in the quantity and composition of fragrance profiles from different fungal species as well as within and among hosts. The evolution of scent chemistry is relatively conservative in these fungi and can be most parsimoniously explained in three steps by combining chemical data with a previously determined rDNA ITS sequence‐based phylogeny. Pseudoflower scent does not appear to represent a simple modification of host floral or vegetative emissions, nor does it mimic the scent of coblooming flowers. Instead, we suspect that the unique fragrances, beyond their function as pollinator attractants, may be important in reducing gamete loss by reinforcing constancy among foraging insects.

[1]  T. Szaro,et al.  Cryptic species in the Puccinia monoica complex , 1998 .

[2]  R. Raguso,et al.  Dynamic headspace analysis of floral volatiles: A comparison of methods , 1998 .

[3]  B. Kropp,et al.  A Study on the Phylogeny of the Dyer's Woad Rust Fungus and Other Species of Puccinia from Crucifers. , 1997, Phytopathology.

[4]  R. Raguso,et al.  Olfactory versus visual cues in a floral mimicry system , 1997, Oecologia.

[5]  B. Roy A PLANT PATHOGEN INFLUENCES POLLINATOR BEHAVIOR AND MAY INFLUENCE REPRODUCTION OF NONHOSTS , 1996 .

[6]  C. Noël-Suberville,et al.  Correlation between fatty acid content and aromatic compound release in fresh blewit (Lepista nuda) , 1996 .

[7]  L. Montanarella,et al.  Headspace Solid-Phase Microextraction Analysis of Volatile Organic Sulfur Compounds in Black and White Truffle Aroma , 1995 .

[8]  J. Schmid,et al.  Molecular organization of the shikimate pathway in higher plants , 1995 .

[9]  R. Dixon,et al.  Stress-Induced Phenylpropanoid Metabolism. , 1995, The Plant cell.

[10]  B. Roy The breeding systems of six species of Arabis (Brassicaceae) , 1995 .

[11]  J. Phillipson,et al.  Anthranilate synthase in microorganisms and plants. , 1995, Phytochemistry.

[12]  J. Shykoff,et al.  Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a venereal disease of plants , 1995 .

[13]  J. Møller,et al.  Asynchronous rhythms in the emission of volatiles from Hesperis matronalis flowers , 1995 .

[14]  Michele R. Dudash,et al.  A model and lexicon for pollen fate , 1994 .

[15]  C. Olsen,et al.  EMISSION OF VOLATILES FROM FLOWERS AND LEAVES OF BRASSICA NAPUS IN SITU , 1994 .

[16]  T. Kawabe,et al.  Production of Benzaldehyde and Benzyl Alcohol by the Mushroom Polyporus tuberaster K2606 , 1994 .

[17]  B. Roy The use and abuse of pollinators by fungi. , 1994, Trends in ecology & evolution.

[18]  B. Roy,et al.  THE EFFECTS OF PATHOGEN-INDUCED PSEUDOFLOWERS AND BUTTERCUPS ON EACH OTHER'S INSECT VISITATION' , 1994 .

[19]  J. Knudsen,et al.  Floral scent in generalistic Angelica (Apiaceae): an adaptive character? , 1994 .

[20]  J. Knudsen,et al.  Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa , 1993 .

[21]  B. Roy,et al.  Floral mimicry by a plant pathogen , 1993, Nature.

[22]  B. Roy PATTERNS OF RUST INFECTION AS A FUNCTION OF HOST GENETIC DIVERSITY AND HOST DENSITY IN NATURAL POPULATIONS OF THE APOMICTIC CRUCIFER, ARABIS HOLBOELLII , 1993, Evolution; international journal of organic evolution.

[23]  A. Erhardt Pollination of the edelweiss, Leontopodium alpinum , 1993 .

[24]  P. Landolt,et al.  Identification of Floral Compounds of Night-Blooming Jessamine Attractive to Cabbage Looper Moths , 1992 .

[25]  P. Landolt,et al.  Lure and Toxicant System for the Cabbage Looper (Lepidoptera: Noctuidae) , 1991 .

[26]  P. Landolt,et al.  Sexual Role Reversal in Mate-Finding Strategies of the Cabbage Looper Moth , 1990, Science.

[27]  H. M. Alexander Epidemiology of anther-smut infection of Silene alba caused by Ustilago violacea: patterns of spore deposition and disease incidence , 1990 .

[28]  T. Talou,et al.  New Trends in Black Truffle Aroma Analysis , 1989 .

[29]  H. M. Alexander,et al.  DISEASE SPREAD AND POPULATION DYNAMICS OF ANTHER-SMUT INFECTION OF SILENE ALBA CAUSED BY THE FUNGUS USTILAGO VIOLACEA , 1988 .

[30]  M. Jacobson,et al.  Phenylacetaldehyde Attracts Moths to Bladder Flower and to Blacklight Traps , 1979 .

[31]  C. Maier Dispersal of Adults of the Black Vine Weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae), in an Urban Area , 1978 .

[32]  J. Visser,et al.  GENERAL GREEN LEAF VOLATILES IN THE OLFACTORY ORIENTATION OF THE COLORADO BEETLE, LEPTINOTARSA DECEMLINEATA , 1978 .

[33]  S. Kinsman,et al.  POLLINATION, FECUNDITY, AND THE DISTRIBUTION OF MOTH-FLOWERED PLANTS. , 1976 .

[34]  T. Mcfadden,et al.  Supplementary Data on Phenylacetaldehyde: an Attractant for Lepidoptera , 1973 .

[35]  C. H. Dodson,et al.  Floral Fragrances and Isolating Mechanisms in the Genus Catasetum (Orchidaceae) , 1972 .

[36]  G. W. Robinson Studies on the Palaeozoic Soils of North Wales. , 1919 .

[37]  R. Croteau,et al.  Origin of Natural Odorants , 1994 .

[38]  R. Buttery,et al.  Volatile compounds of tomato fruit and plant parts: relationship and biogenesis , 1993 .

[39]  M. Morris Sarapiqui Chronicle: A naturalist in Costa Rica , 1993 .

[40]  W. M. Whitten Floral fragrances of Stanhopea (Orchidaceae) , 1992 .

[41]  W. Connick,et al.  Volatiles emitted during the sexual stage of the Canada thistle rust fungus and by thistle flowers , 1991 .

[42]  J. Vidal,et al.  Volatile compounds from aroma of some edible mushrooms: morel (Morchella conica) wood blewitt (Lepista nuda), clouded agaric (Clitocybe nebularis), and false chanterelle (Hygrophoropsis aurantiaca) , 1989 .

[43]  J. Webber,et al.  Insect dissemination of fungal pathogens of trees. , 1989 .

[44]  G. Bergström,et al.  Headspace volatiles of whole plants and macerated plant parts of Brassica and Sinapis , 1988 .

[45]  P. Schreier,et al.  Metabolism of linalool by botrytis cinerea , 1986 .

[46]  Chi-Tang Ho,et al.  Enzymic formation of volatile compounds in Shiitake mushroom (Lentinus edodes sing.) , 1986 .

[47]  D. Armstrong Selective production of ethyl acetate by Candida utilis , 1986 .

[48]  H. Hanssen Sesquiterpene alcohols from Lentinus lepideus , 1985 .

[49]  R. Heaney,et al.  Glucosinolates and their breakdown products in food and food plants. , 1983, Critical reviews in food science and nutrition.

[50]  K. Engel,et al.  Formation of eight-carbon and ten-carbon components in mushrooms (Agaricus campestris) , 1982 .

[51]  L. Nilsson The pollination ecology of Dactylorhiza sambucina (Orchidaceae). , 1980 .

[52]  C. Vance,et al.  Conversion of p-coumaric acid to p-hydroxybenzoic acid by cell free extracts of potato tubers and Polyporus hispidus , 1976 .