Priming Seeds with Indole and (Z)-3-Hexenyl Acetate Enhances Resistance Against Herbivores and Stimulates Growth

Appel HM et al (2014) Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. Front Plant Sci 5

Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515

Azooz M (2009) Salt stress mitigation by seed priming with salicylic acid in two faba bean genotypes differing in salt tolerance. Int J Agric Biology 11:343–350

Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L (2014) The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J 80:758–771

Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257

Barsics F, Delory BM, Delaplace P, Francis F, Fauconnier M-L, Haubruge É, Verheggen FJ (2017) Foraging wireworms are attracted to root-produced volatile aldehydes. J Pest Sci 90:69–76

Bate NJ, Rothstein SJ (1998) C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16:561–569

Bentsink L, Koornneef M (2008) Seed dormancy and germination. Arabidopsis Book/American Society of Plant Biologists 6

Bergmann C et al (1993) Stimulation of Orobanche crenata seed germination by (+)-strigol and structural analogues dependence on constitution and configuration of the germination stimulants. J Plant Physiol 142:338–342

Bhattacharyya D, Garladinne M, Lee YH (2015) Volatile indole produced by rhizobacterium Proteus vulgaris JBLS202 stimulates growth of Arabidopsis thaliana through auxin, cytokinin, and brassinosteroid pathways. J Plant Growth Regul 34:158–168

Blom D et al (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058

Brader Gn T, Ev, Palva ET (2001) Jasmonate-Dependent Induction of Indole Glucosinolates in Arabidopsis by Culture Filtrates of the Nonspecific PathogenErwinia carotovora. Plant Physiol 126:849–860. doi:https://doi.org/10.1104/pp.126.2.849

Bradow JM, Connick WJ (1990) Volatile seed germination inhibitors from plant residues. J Chem Ecol 16:645–666

Bruce TJ, Martin JL, Pickett JA, Pye BJ, Smart LE, Wadhams LJ (2003) cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius)(Homoptera: Aphididae). Pest Manage Sci 59:1031–1036

Bucciarelli B, Hanan J, Palmquist D, Vance CP (2006) A standardized method for analysis of Medicago truncatula phenotypic development. Plant Physiol 142:207–219

Buijs G, Vogelzang A, Nijveen H, Bentsink L (2020) Dormancy cycling: translation-related transcripts are the main difference between dormant and non‐dormant seeds in the field. Plant J 102:327–339

Buswell W et al (2018) Chemical priming of immunity without costs to plant growth. New Phytol 218:1205–1216

Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in. Arabidopsis Plant J 53:214–224

Chahtane H, Kim W, Lopez-Molina L (2016) Primary seed dormancy: a temporally multilayered riddle waiting to be unlocked. J Exp Bot 68:857–869. https://doi.org/10.1093/jxb/erw377

Chen H, Zhang J, Neff MM, Hong S-W, Zhang H, Deng X-W, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500

Chen PK, Leather GR (1990) Plant growth regulatory activities of artemisinin and its related compounds. J Chem Ecol 16:1867–1876

Conrath U et al (2006) Priming: getting ready for battle Molecular. Plant-Microbe Interact 19:1062–1071

Cook C, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190

Dervinis C, Frost CJ, Lawrence SD, Novak NG, Davis JM (2010) Cytokinin primes plant responses to wounding and reduces insect performance. J Plant Growth Regul 29:289–296

Dixon K, Merritt D, Flematti G, Ghisalberti E (2009) Karrikinolide–a phytoreactive compound derived from smoke with applications in horticulture. Ecol Restor Agric Act Hort 813:155–170

Dombrecht B et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785. https://doi.org/10.1073/pnas.0308037100

Engelberth J, Engelberth M (2019) The costs of green leaf volatile-induced defense priming: temporal diversity in growth responses to mechanical wounding and insect herbivory. Plants 8:23

Engelberth J, Seidl-Adams I, Schultz JC, Tumlinson JH (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxophytodienoic acid reductases in Zea mays Molecular. Plant-Microbe Interact 20:707–716

Erb M, Veyrat N, Robert CA, Xu H, Frey M, Ton J, Turlings TC (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nat Comm 6:6273. https://doi.org/10.1038/ncomms7273

Farag MA, Fokar M, Zhang HA, Allen RD, Par‚ PW (2005) (Z)-3-Hexenol induces defense genes and downstream metabolites. in maize Planta 220:900–909

Fenner M (2000) Seeds: the ecology of regeneration in plant communities. Cabi

Finch-Savage WE, Leubner‐Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977–977

Flores J, Jurado E, Arredondo A (2006) Effect of light on germination of seeds of Cactaceae from the Chihuahuan Desert México Seed. Sci Res 16:149–155

Frank L, Wenig M, Ghirardo A, van der Krol A, Vlot AC, Schnitzler JP, Rosenkranz M (2021) Isoprene and β-caryophyllene confer plant resistance via different plant internal signalling pathways. Plant Cell Environ 44:1151–1164

Freundlich GE, Shields M, Frost CJ (2021) Dispensing a Synthetic Green Leaf Volatile to Two Plant Species in a Common Garden Differentially Alters Physiological Responses and Herbivory. Agronomy 11:958. doi:https://doi.org/10.3390/agronomy11050958

Friis EM, Crane PR, Pedersen KR (2011) Early flowers and angiosperm evolution. Cambridge University Press

Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498. https://doi.org/10.1111/j.1461-0248.2007.01043.x

Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008a) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824. https://doi.org/10.1104/pp.107.113027

Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008b) Why do distance limitations exist on plant-plant signaling via airborne volatiles? Plant Signal Behav 3:466–468

Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008c) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–734. https://doi.org/10.1104/pp.107.113027

Frost CJ, Nyamdari B, Tsai C-J, Harding SA (2012) The tonoplast-localized sucrose transporter in Populus (PtaSUT4) regulates whole-plant water relations, responses to water stress, and photosynthesis. PLoS ONE 7:e44467

Gao L-L, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol 146:996–1009

Garcia LC, Eubanks MD (2019) Overcompensation for insect herbivory: a review and meta-analysis. Evid Ecol 100:e02585

Gasmi L et al (2019) Can herbivore-induced volatiles protect plants by increasing the herbivores’ susceptibility to natural pathogens? Appl Environ Microbiol 85:e01468–e01418. https://doi.org/10.1128/AEM.01468-18

Gfeller A et al (2013) Characterization of volatile organic compounds emitted by barley (Hordeum vulgare L.) roots and their attractiveness to wireworms. J Chem Ecol 39:1129–1139

Godschalx AL, Stady L, Watzig B, Ballhorn DJ (2016) Is protection against florivory consistent with the optimal defense hypothesis? BMC Plant Biol 16:1–9

Guo R, Shen W, Qian H, Zhang M, Liu L, Wang Q (2013) Jasmonic acid and glucose synergistically modulate the accumulation of glucosinolates in Arabidopsis thaliana. J Exp Bot 64:5707–5719

Gutterman Y (1994) Strategies of seed dispersal and germination in plants inhabiting deserts. Bot Rev 60:373–425

Haas J, Lozano ER, Haida KS, Mazaro SM, de Souza Vismara E, Poppy GM (2018) Getting ready for battle: do cabbage seeds treated with jasmonic acid and chitosan affect chewing and sap-feeding insects? Entomol Exp Appl 166:412–419

Helms AM, De Moraes CM, Tröger A, Alborn HT, Francke W, Tooker JF, Mescher MC (2017) Identification of an insect-produced olfactory cue that primes plant defenses. Nat Comm 8:337

Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biology 67:283–335

Hilker M et al (2015) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 91:1118–1133

Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy, and germination. New Phytol 179:33–54

Hopkins R, Griffiths D, Birch A, McKinlay R (1998) Influence of increasing herbivore pressure on modification of glucosinolate content of swedes (Brassica napus spp. rapifera). J Chem Ecol 24:2003–2019

Hu L, Ye M, Erb M (2019) Integration of two herbivore-induced plant volatiles results in synergistic effects on plant defence and resistance. Plant Cell Environ 42:959–971

Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151

Karban R (2007) Experimental clipping of sagebrush inhibits seed germination of neighbours. Ecol Lett 10:791–797

Kazan K, Manners JM (2013) MYC2: the master in action Molecular plant 6:686–703

Koitabashi R, Suzuki T, Kawazu T, Sakai A, Kuroiwa H, Kuroiwa T (1997) 1,8-Cineole inhibits root growth and DNA synthesis in the root apical meristem of Brassica campestris. L Journal of Plant Research 110:1–6

Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination Curr. Opin Plant Biol 5:33–36

Lawo NC, Weingart GJ, Schuhmacher R, Forneck A (2011) The volatile metabolome of grapevine roots: first insights into the metabolic response upon phylloxera attack. Plant Physiol Biochem 49:1059–1063

Lee J-H, Wood TK, Lee J (2015) Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23:707–718. https://doi.org/10.1016/j.tim.2015.08.001

Levine JM, McEachern AK, Cowan C (2008) Rainfall effects on rare annual plants. J Ecol 96:795–806

Mashiguchi K et al. (2011) The main auxin biosynthesis pathway in (Arabidopsis). Proc Natl Acad Sci USA 108:18512-18517. https://doi.org/10.1073/pnas.1108434108

Maurya AK, Kelly MP, Mahaney SM, Gomez SK (2018) Arbuscular mycorrhizal symbiosis alters plant gene expression and aphid weight in a tripartite interaction. J Plant Interact 13:294–305

Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162

Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense. Signal pathways Phytochemistry 67:2450–2462

Milberg P, Andersson L, Thompson K (2000) Large-seeded species are less dependent on light for germination than small-seeded ones. Seed Sci Res 10:99–104

Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant J 53:197–213

Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

Muller CH, Muller WH, Haines BL (1964) Volatile growth inhibitors produced by aromatic shrubs. Science 143:471–473

Muller WH (1965) Volatile materials produced by Salvia leucophylla: effects on seedling growth and soil bacteria. Bot Gaz 126:195–200

Muller WH, Muller CH (1964) Volatile growth inhibitors produced bySalvia species Bulletin of the Torrey. Botanical Club:327–330

Muscolo A, Panuccio M, Sidari M (2001) The effect of phenols on respiratory enzymes in seed germination. Plant Growth Reg 35:31–35

Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM (2012) Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu Rev Plant Biol 63:107–130

Ninkovic V (2003) Volatile communication between barley plants affects biomass allocation. J Exp Bot 54:1931–1939

Oleszek W (1987) Allelopathic effects of volatiles from some Cruciferae species on lettuce, barnyard grass and wheat growth. Plant Soil 102:271–273

Pake CE, Venable DL (1996) Seed banks in desert annuals: implications for persistence and coexistence in variable. Environ Ecol 77:1427–1435

Palma R, Mutis A, Manosalva L, Ceballos R, Quiroz A (2012) Behavioral and electrophysiological responses of Hylastinus obscurus to volatiles released from the roots of Trifolium pratense L. J soil Sci plant Nutr 12:183–193

Paparella S, Araújo S, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the art and new perspectives. Plant Cell Rep 34:1281–1293

Peñuelas J, Asensio D, Tholl D, Wenke K, Rosenkranz M, Piechulla B, Schnitzler J-P (2014) Biogenic volatile emissions from the soil. Plant Cell Environ 37:1866–1891

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. https://doi.org/10.1016/S1369-5266(02)00251-0

Pickett JA, Khan ZR (2016) Plant volatile-mediated signalling and its application in agriculture: successes and challenges. New Phytol 212:856–870

Preston CA, Laue G, Baldwin IT (2001) Methyl jasmonate is blowing in the wind, but can it act as a plant-plant airborne signal? Biochem Syst Ecol 29:1007–1023

Probert RJ (2000) The role of temperature in the regulation of seed dormancy and germination. Seeds: the ecology of regeneration in plant communities 2:261–292

Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923

Rasmann S et al (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

Reymond P, Bodenhausen N, Van Poecke RM, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147

Reynolds SA, Corbin JD, D’Antonio CM (2001) The effects of litter and temperature on the germination of native and exotic grasses in a coastal California grassland. Madrono:230–235

Rodriguez-Saona C, Frost CJ (2010) New evidence for a multifunctional role of herbivore-induced plant volatiles in defense against herbivores. Plant Signal Behav 5:58–60

Rodriguez-Saona C, Rodriguez-Saona L, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175

Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ, Paul WP, Bais HP (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Communicative & Integrative Biology 3:130–138

Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14:17781–17811

Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69:463–472

Sharifi R, Ryu C-M (2016) Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Front Microbiol 7:196

Simonin KA, Roddy AB (2018) Genome downsizing, physiological novelty, and the global dominance of flowering plants. PLoS Biol 16:e2003706

Smart LE, Martin JL, Limpalaër M, Bruce TJ, Pickett JA (2013) Responses of herbivore and predatory mites to tomato plants exposed to jasmonic acid seed treatment. J Chem Ecol 39:1297–1300

Song G, Ryu C-M (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819

Song GC, Choi HK, Ryu C-M (2015) Gaseous 3-pentanol primes plant immunity against a bacterial speck pathogen, Pseudomonas syringae pv. tomato via salicylic acid and jasmonic acid-dependent signaling pathways in Arabidopsis. Front Plant Sci 6:821

Thaler JS, Fidantsef AL, Bostock RM (2002) Antagonism between jasmonate-and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J Chem Ecol 28:1131–1159

Thelen GC et al (2005) Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecol Lett 8:209–217

Toh S et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385

Tomczak VV, Müller C (2017) Influence of arbuscular mycorrhizal stage and plant age on the performance of a generalist aphid. J Insect Physiol 98:258–266

Tsai C-J, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172:47–62. doi:https://doi.org/10.1111/j.1469-8137.2006.01798.x

Tukey H Jr (1970) The leaching of substances from plants. Annu Rev Plant Physiol 21:305–324

Tyagi S, Mulla SI, Lee K-J, Chae J-C, Shukla P (2018) VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes. Critical reviews in biotechnology 1–20

van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607

Veyrat N, Robert CAM, Turlings TCJ, Erb M (2016) Herbivore intoxication as a potential primary function of an inducible volatile plant signal. J Ecol 104:591–600. doi:https://doi.org/10.1111/1365-2745.12526

Vos I, Verhage A, Schuurink R, Watt L, Pieterse C, Van Wees S (2013) Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid. Front Plant Sci 4. doi:https://doi.org/10.3389/fpls.2013.00539

Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Herbivore-and elicitor-induced resistance in groundnut to Asian armyworm, Spodoptera litura (Fab.)(Lepidoptera: Noctuidae). Plant Signal Behav 6:1769–1777

Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response growth and development. Annals of botany 100:681–697

Wesson G, Wareing P (1969) The role of light in the germination of naturally occurring populations of buried weed seeds. J Exp Bot 20:402–413

Worrall D et al (2012) Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytol 193:770–778

Yang C et al (2016) Seed treatment with salicylic acid invokes defence mechanism of Helianthus annuus against Orobanche cumana. Annals of applied biology 169:408–422

Ye M, Veyrat N, Xu H, Hu L, Turlings TC, Erb M (2018) An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars. Sci Adv 4:eaar4767

Yu S-M, Lee YH (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495

Zhang R, Wang B, Ouyang J, Li J, Wang Y (2008) Arabidopsis indole synthase, a homolog of tryptophan synthase alpha, is an enzyme involved in the trp-independent indole‐containing metabolite biosynthesis. J Integr Plant Biol 50:1070–1077

Zhao Y et al (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112