Why plant volatile analysis needs bioinformatics--detecting signal from noise in increasingly complex profiles.

Plant volatile analysis may be the oldest form of what now is called plant "metabolomic" analysis. A wide array of volatile organic compounds (VOCs), such as alkanes, alcohols, isoprenoids, and esters, can be collected simultaneously from the plant headspace, either within the laboratory or in the field. Increasingly faster and more sensitive analysis techniques allow detection of an ever-growing number of compounds in decreasing concentrations. However, the myriads of data becoming available from such experiments do not automatically increase our ecological and evolutionary understanding of the roles these VOCs play in plant-insect interactions. Herbivores and parasitoids responding to changes in VOC emissions are able to perceive minute changes within a complex VOC background. Plants modified in genes involved in VOC synthesis may be valuable for the evaluation of changes in plant-animal interactions compared to tests with synthetic compounds, as they allow changes to be made within the context of a more complex profile. We argue that bioinformatics is an essential tool to integrate statistical analysis of plant VOC profiles with insect behavioural data. The implementation of statistical techniques such as multivariate analysis (MVA) and meta-analysis is of the utmost importance to interpreting changes in plant VOC mixtures. MVA focuses on differences in volatile patterns rather than in single compounds. Therefore, it more closely resembles the information processing in insects that base their behavioural decisions on differences in VOC profiles between plants. Meta-analysis of different datasets will reveal general patterns pertaining to the ecological role of VOC in plant-insect interactions. Successful implementation of bioinformatics in VOC research also includes the development of MVA that integrate time-resolved chemical and behavioural analyses, as well as databases that link plant VOCs to their effects on insects.

[1]  A. Soria,et al.  Antifeedant effects and chemical composition of essential oils from different populations of Lavandula luisieri L. , 2006 .

[2]  W. Lewis,et al.  Exploitation of Herbivore-Induced Plant Odors by Host-Seeking Parasitic Wasps , 1990, Science.

[3]  J. H. Tumlinson,et al.  Herbivore-infested plants selectively attract parasitoids , 1998, Nature.

[4]  J. Koricheva,et al.  Meta‐analysis of Trade‐offs among Plant Antiherbivore Defenses: Are Plants Jacks‐of‐All‐Trades, Masters of All? , 2004, The American Naturalist.

[5]  Keith Chamberlain,et al.  Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior , 2006, Proceedings of the National Academy of Sciences.

[6]  M. Sabelis,et al.  Olfactory responses of the vine weevil, Otiorhynchus sulcatus, to tree odours , 2002 .

[7]  T. Holopainen,et al.  Emission of non-methane volatile organic compounds (VOCs) from boreal peatland microcosms - effects of ozone exposure , 2005 .

[8]  A. Aharoni,et al.  Volatile science? Metabolic engineering of terpenoids in plants. , 2005, Trends in plant science.

[9]  M. Mescher,et al.  Volatile Chemical Cues Guide Host Location and Host Selection by Parasitic Plants , 2006, Science.

[10]  J. H. Tumlinson,et al.  Volatile Semiochemicals Released from Undamaged Cotton Leaves (A Systemic Response of Living Plants to Caterpillar Damage) , 1996, Plant physiology.

[11]  M. Konstantopoulou,et al.  Chemical Composition of Corn Leaf Essential Oils and Their Role in the Oviposition Behavior of Sesamia nonagrioides Females , 2004, Journal of Chemical Ecology.

[12]  L. Vet.  From Chemical to Population Ecology: Infochemical Use in an Evolutionary Context , 2004, Journal of Chemical Ecology.

[13]  Junji Takabayashi,et al.  Herbivory-induced volatiles elicit defence genes in lima bean leaves , 2000, Nature.

[14]  T. C. Turlings,et al.  In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. , 2005, Chemical senses.

[15]  I. Baldwin,et al.  Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced defenses in Nicotiana attenuata , 2001, Oecologia.

[16]  Maurice W. Sabelis,et al.  Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? , 1988 .

[17]  Robert Verpoorte,et al.  Metabolomic differentiation of Cannabis sativa cultivars using 1H NMR spectroscopy and principal component analysis. , 2004, Journal of natural products.

[18]  R. Dixon,et al.  Plant metabolomics: large-scale phytochemistry in the functional genomics era. , 2003, Phytochemistry.

[19]  G. Poppy,et al.  Genetic manipulation of natural enemies: can we improve biological control by manipulating the parasitoid and/or the plant? , 2004 .

[20]  N. Tinbergen.  On aims and methods of Ethology , 2010 .

[21]  M. Baalen,et al.  The evolution of direct and indirect plant defence against herbivorous arthropods , 1999 .

[22]  W. J. Lewis,et al.  Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors. , 2003, Chemical senses.

[23]  W. J. Lewis,et al.  Associative learning of complex odours in parasitoid host location. , 2003, Chemical senses.

[24]  M. Dicke,et al.  Identification of Volatiles That Are Used in Discrimination Between Plants Infested with Prey or Nonprey Herbivores by a Predatory Mite , 2004, Journal of Chemical Ecology.

[25]  J. Vivanco,et al.  Proton-Transfer-Reaction Mass Spectrometry as a New Tool for Real Time Analysis of Root-Secreted Volatile Organic Compounds in Arabidopsis1 , 2004, Plant Physiology.

[26]  Á. Guerrero,et al.  Olfactory Responses of Plutella xylostella Natural Enemies to Host Pheromone, Larval Frass, and Green Leaf Cabbage Volatiles , 2004, Journal of Chemical Ecology.

[27]  J. Gershenzon,et al.  The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. Kley,et al.  EMISSION OF VOLATILE ORGANIC COMPOUNDS FROM OZONE‐EXPOSED PLANTS , 1999 .

[29]  Julia Koricheva,et al.  Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis , 2004 .

[30]  J. Loon,et al.  Insect-plant biology: from physiology to evolution. , 1998 .

[31]  M. Dicke,et al.  Jasmonic Acid and Herbivory Differentially Induce Carnivore-Attracting Plant Volatiles in Lima Bean Plants , 1999, Journal of Chemical Ecology.

[32]  G. Poppy,et al.  Gene Flow from GM Plants: Poppy/Gene , 2007 .

[33]  J. V. van Loon,et al.  Attraction of Colorado Potato Beetle to Herbivore-Damaged Plants During Herbivory and After Its Termination , 1997, Journal of Chemical Ecology.

[34]  Richard M. Caprioli,et al.  Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature , 2022 .

[35]  J. Peñuelas,et al.  Response to Pichersky et al.: Plant volatile isoprenoids and their opportunistic functions , 2006 .

[36]  M. Hilker,et al.  The significance of background odour for an egg parasitoid to detect plants with host eggs. , 2005, Chemical senses.

[37]  J. Takabayashi,et al.  Developmental stage of herbivorePseudaletia separata affects production of herbivore-induced synomone by corn plants , 1995, Journal of Chemical Ecology.

[38]  J. J. Jansen,et al.  ASCA: analysis of multivariate data obtained from an experimental design , 2005 .

[39]  A. Nissinen,et al.  Response of Plutella xylostella and its Parasitoid Cotesia plutellae to Volatile Compounds , 2005, Journal of Chemical Ecology.

[40]  H. Alborn,et al.  Induction of Volatile Emissions in Maize by Different Larval Instars of Spodoptera littoralis , 2004, Journal of Chemical Ecology.

[41]  J. Harvey.  Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness , 2000 .

[42]  Marcel Dicke,et al.  Parasitoid‐plant mutualism: parasitoid attack of herbivore increases plant reproduction , 2000 .

[43]  Jörg-Peter Schnitzler,et al.  Practical approaches to plant volatile analysis. , 2006, The Plant journal : for cell and molecular biology.

[44]  R. Raguso.  Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. , 2004, Current opinion in plant biology.

[45]  A. Aharoni,et al.  Genetic Engineering of Terpenoid Metabolism Attracts Bodyguards to Arabidopsis , 2005, Science.

[46]  G. Poppy,et al.  Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae , 2006 .

[47]  M. Hunter.  A breath of fresh air: beyond laboratory studies of plant volatile–natural enemy interactions , 2002 .

[48]  T. M. Bezemer,et al.  Linking aboveground and belowground interactions via induced plant defenses. , 2005, Trends in ecology & evolution.

[49]  M. Sabelis,et al.  Does it pay plants to advertise for bodyguards? Towards a cost-benefit analysis of induced synomone production , 1989 .

[50]  M. Hunter.  Maternal effects and the population dynamics of insects on plants , 2002 .

[51]  L. Brussaard,et al.  Food Preference of Wireworms Analyzed with Multinomial Logit Models , 2003, Journal of Insect Behavior.

[52]  D. Ober.  Seeing double: gene duplication and diversification in plant secondary metabolism. , 2005, Trends in plant science.

[53]  C. Kost,et al.  Herbivore‐induced plant volatiles induce an indirect defence in neighbouring plants , 2006 .

[54]  R. Firn,et al.  On the evolution of plant secondary chemical diversity , 1991 .

[55]  T. Nishioka,et al.  Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. , 2000, Plant & cell physiology.

[56]  J. Peñuelas,et al.  Caterpillars of Euphydryas aurinia (Lepidoptera: Nymphalidae) feeding on Succisa pratensis leaves induce large foliar emissions of methanol. , 2005, The New phytologist.

[57]  H. Jeleń,et al.  Application of headspace—solid phase microextraction and multivariate analysis for plant oils differentiation , 2003 .

[58]  Thomas Mitchell-Olds,et al.  Plant evolutionary genomics. , 2002, Current opinion in plant biology.

[59]  Patrik R. Jones,et al.  Resistance to an Herbivore Through Engineered Cyanogenic Glucoside Synthesis , 2001, Science.

[60]  Ted C. J. Turlings,et al.  Recruitment of entomopathogenic nematodes by insect-damaged maize roots , 2005, Nature.

[61]  Christine Woodcock,et al.  Insect host location: a volatile situation. , 2005, Trends in plant science.

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

[63]  S. Dorn,et al.  New insights in analysing parasitoid attracting synomones: early volatile emission and use of stir bar sorptive extraction , 2005, CHEMOECOLOGY.

[64]  M. Dicke,et al.  Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods , 2003 .

[65]  F. Loreto,et al.  Physiological responses of forest trees to heat and drought. , 2006, Plant biology.

[66]  P. Klinkhamer,et al.  Conflicting interests of plants and the natural enemies of herbivores. , 2000 .

[67]  J. Peñuelas,et al.  Response to Firn and Jones: Volatile isoprenoids, a special case of secondary metabolism , 2006 .

[68]  Louise E. M. Vet,et al.  How To Hunt for Hiding Hosts: the Reliability-Detectability Problem in Foraging Parasitoids , 1990 .

[69]  J. Peñuelas,et al.  Opportunistic emissions of volatile isoprenoids. , 2005, Trends in plant science.

[70]  Jens Rohloff,et al.  Volatile profiling of Arabidopsis thaliana - putative olfactory compounds in plant communication. , 2005, Phytochemistry.

[71]  Bruce A. McPheron,et al.  Interactions Among Three Trophic Levels: Influence of Plants on Interactions Between Insect Herbivores and Natural Enemies , 1980 .

[72]  O. Tzakou,et al.  Volatile metabolites from Salvia fruticosa as antifungal agents in soilborne pathogens. , 2003, Journal of agricultural and food chemistry.

[73]  M. Dicke,et al.  beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[74]  R. Firn,et al.  Do we need a new hypothesis to explain plant VOC emissions? , 2006, Trends in plant science.

[75]  R. Firn,et al.  Response to Pichersky et al.: Correcting a misconception about the screening hypothesis , 2006 .

[76]  J. V. van Loon,et al.  GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species , 2002, CHEMOECOLOGY.

[77]  Guy M. Poppy,et al.  Comparison of Glass Vessels and Plastic Bags for Enclosing Living Plant Parts for Headspace Analysis , 2006, Journal of Chemical Ecology.

[78]  T. Hartmann.  Diversity and variability of plant secondary metabolism: a mechanistic view , 1996 .

[79]  F. Marion-Poll,et al.  High Genetic Variability of Herbivore-Induced Volatile Emission within a Broad Range of Maize Inbred Lines1 , 2004, Plant Physiology.

[80]  J. Gershenzon,et al.  Biochemistry of Plant Volatiles1 , 2004, Plant Physiology.

[81]  J. Peñuelas,et al.  Isoprenoids: an evolutionary pool for photoprotection. , 2005, Trends in plant science.

[82]  A. Cortesero,et al.  Systemic Release of Herbivore-Induced Plant Volatiles by Turnips Infested by Concealed Root-Feeding Larvae Delia radicum L. , 2002, Journal of Chemical Ecology.

[83]  J. Gershenzon,et al.  Plant volatiles: a lack of function or a lack of knowledge? , 2006, Trends in plant science.

[84]  Age K. Smilde,et al.  Multilevel component analysis of time-resolved metabolic fingerprinting data , 2005 .

[85]  Yury Tikunov,et al.  A Novel Approach for Nontargeted Data Analysis for Metabolomics. Large-Scale Profiling of Tomato Fruit Volatiles1[w] , 2005, Plant Physiology.

[86]  Sáez.  Volatile oil variability in Thymus serpylloides ssp. gadorensis growing wild in Southeastern Spain. , 2001, Biochemical systematics and ecology.

[87]  W. Boland,et al.  Effects of Feeding Spodoptera littoralis on Lima Bean Leaves. II. Continuous Mechanical Wounding Resembling Insect Feeding Is Sufficient to Elicit Herbivory-Related Volatile Emission , 2005, Plant Physiology.