Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores.

Plant volatiles play important roles in signalling between plants and insects, but their role in communication among plants remains controversial. Previous research on plant-plant communication has focused on interactions between neighbouring plants, largely overlooking the possibility that volatiles function as signals within plants. Here, we show that volatiles released by herbivore-wounded leaves of hybrid poplar (Populus deltoides x nigra) prime defences in adjacent leaves with little or no vascular connection to the wounded leaves. Undamaged leaves exposed to volatiles from wounded leaves on the same stem had elevated defensive responses to feeding by gypsy moth larvae (Lymantria dispar L.) compared with leaves that did not receive volatiles. Volatile signals may facilitate systemic responses to localized herbivory even when the transmission of internal signals is constrained by vascular connectivity. Self-signalling via volatiles is consistent with the short distances over which plant response to airborne cues has been observed to occur and has apparent benefits for emitting plants, suggesting that within-plant signalling may have equal or greater ecological significance than signalling between plants.

[1]  M. Marra,et al.  Genomics of hybrid poplar (Populus trichocarpa× deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full‐length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect‐induced defences in poplar , 2006, Molecular ecology.

[2]  J. Schultz,et al.  Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus , 2002, Oecologia.

[3]  I. Raskin,et al.  Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? , 1995, The Plant cell.

[4]  C. Kost,et al.  Priming of indirect defences. , 2006, Ecology letters.

[5]  M. Farag,et al.  (Z)-3-Hexenol induces defense genes and downstream metabolites in maize , 2005, Planta.

[6]  Agrawal Communication between plants: this time it's real. , 2000, Trends in ecology & evolution.

[7]  Richard Karban,et al.  Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. , 2006, Ecology.

[8]  A. Slusarenko,et al.  The Pattern of Systemic Acquired Resistance Induction within the Arabidopsis Rosette in Relation to the Pattern of Translocation1 , 2003, Plant Physiology.

[9]  C. Orians,et al.  Vascular Architecture Generates Fine Scale Variation in Systemic Induction of Proteinase Inhibitors in Tomato , 2000, Journal of Chemical Ecology.

[10]  I. Baldwin,et al.  Fitness costs of induced resistance: emerging experimental support for a slippery concept. , 2002, Trends in plant science.

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

[12]  B. Poinssot,et al.  Priming: getting ready for battle. , 2006, Molecular plant-microbe interactions : MPMI.

[13]  M. Dicke,et al.  Herbivore-Induced Plant Volatiles Mediate In-Flight Host Discrimination by Parasitoids , 2005, Journal of Chemical Ecology.

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

[15]  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.

[16]  G. Laue,et al.  Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush , 2000, Oecologia.

[17]  R. Karban,et al.  Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers , 2006, Oecologia.

[18]  I. Baldwin,et al.  Volatile signaling in plant-plant-herbivore interactions: what is real? , 2002, Current opinion in plant biology.

[19]  I. Baldwin Jasmonate-induced responses are costly but benefit plants under attack in native populations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  I. Baldwin,et al.  Transport of [2-14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris , 1997, Planta.

[21]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Farag,et al.  C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato. , 2002, Phytochemistry.

[23]  B. Lamb,et al.  Surrogate Pheromone Plumes in Three Forest Trunk Spaces: Composite Statistics and Case Studies , 2004 .

[24]  M. Sabelis,et al.  Evolution of herbivore-induced plant volatiles , 2002 .

[25]  Edward E. Farmer,et al.  Surface-to-air signals , 2001, Nature.

[26]  C. Orians Herbivores, Vascular Pathways, and Systemic Induction: Facts and Artifacts , 2005, Journal of Chemical Ecology.

[27]  I. Baldwin,et al.  Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata , 2006, Oecologia.

[28]  J. Thaler Jasmonate-inducible plant defences cause increased parasitism of herbivores , 1999, Nature.

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

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

[31]  I. Baldwin,et al.  Constraints to Herbivore-Induced Systemic Responses: Bidirectional Signaling Along Orthostichies in Nicotiana attenuata , 2003, Journal of Chemical Ecology.

[32]  B. Casper,et al.  MORPHOGENETIC CONSTRAINTS ON PATTERNS OF CARBON DISTRIBUTION IN PLANTS , 1984 .

[33]  J. D. Rhodes,et al.  The pathway for systemic electrical signal conduction in the wounded tomato plant , 1996, Planta.

[34]  J. Bergelson,et al.  Costs of induced responses in plants , 2003 .

[35]  J. Agrell,et al.  Within-plant variation in induced defence in developing leaves of cotton plants , 2005, Oecologia.

[36]  R. Karban,et al.  THE FITNESS CONSEQUENCES OF INTERSPECIFIC EAVESDROPPING BETWEEN PLANTS , 2002 .

[37]  M. Mescher,et al.  Caterpillar-induced nocturnal plant volatiles repel conspecific females , 2001, Nature.

[38]  K. Schmidt Site fidelity in habitats with contrasting levels of nest predation and brood parasitism , 2001 .

[39]  D. F. Rhoades Responses of Alder and Willow to Attack by Tent Caterpillars and Webworms: Evidence for Pheromonal Sensitivity of Willows , 1983 .

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

[41]  M. Sabelis,et al.  Plants are better protected against spider-mites after exposure to volatiles from infested conspecifics , 1992, Experientia.

[42]  M. Held,et al.  Priming by airborne signals boosts direct and indirect resistance in maize. , 2006, The Plant journal : for cell and molecular biology.

[43]  Ted C. J. Turlings,et al.  Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids , 2001 .

[44]  J. Bergelson,et al.  Interplant Communication Revisited , 1995 .

[45]  Marcel Dicke,et al.  Chemical information transfer between wounded and unwounded plants: backing up the future , 2001 .

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

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

[48]  J. Coleman,et al.  Control of systemically induced herbivore resistance by plant vascular architecture , 1993, Oecologia.

[49]  J. Gershenzon,et al.  The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. , 2004, Phytochemistry.

[50]  P. Hasegawa,et al.  Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate. , 1994, The Plant cell.

[51]  J. D. Rhodes,et al.  Evidence for Physically Distinct Systemic Signalling Pathways in the Wounded Tomato Plant , 1999 .

[52]  M. Gordon,et al.  Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[53]  I. Baldwin,et al.  Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[54]  J. Thaler,et al.  Plant Vascular Architecture and Within-Plant Spatial Patterns in Resource Quality Following Herbivory , 2004, Journal of Chemical Ecology.

[55]  I. Baldwin,et al.  Ontogeny Constrains Systemic Protease Inhibitor Response in Nicotiana attenuata , 2001, Journal of Chemical Ecology.

[56]  J. Gershenzon Metabolic costs of terpenoid accumulation in higher plants , 1994, Journal of Chemical Ecology.

[57]  J. Tumlinson,et al.  Airborne signals prime plants against insect herbivore attack. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Bohlmann,et al.  Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (-)-germacrene D synthase, PtdTPS1. , 2004, The Plant journal : for cell and molecular biology.

[59]  J. Lawton,et al.  Rapidly Induced Defenses and Talking Trees: The Devil's Advocate Position , 1985, The American Naturalist.

[60]  R. Karban,et al.  Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants , 2003 .

[61]  J. Ruther,et al.  Plant–Plant Signaling: Ethylene Synergizes Volatile Emission In Zea mays Induced by Exposure to (Z)-3-Hexen-1-ol , 2005, Journal of Chemical Ecology.

[62]  N. Dudareva,et al.  Plant Volatiles: Recent Advances and Future Perspectives , 2006 .

[63]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[64]  J. Schultz,et al.  Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. , 2004, The New phytologist.

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

[66]  J. Schultz,et al.  Rapid Changes in Tree Leaf Chemistry Induced by Damage: Evidence for Communication Between Plants , 1983, Science.

[67]  J. Stratmann Long distance run in the wound response--jasmonic acid is pulling ahead. , 2003, Trends in plant science.