Abstract
Main conclusion
In flowers multiple secretory systems cooperate to deliver specialized metabolites to support specific roles in defence and pollination. The collective roles of cell types, enzymes, and transporters are discussed.
Abstract
The interplay between reproductive strategies and defense mechanisms in flowering plants has long been recognized, with trade-offs between investment in defense and reproduction predicted. Glandular trichomes and secretory cavities or ducts, which are epidermal and internal structures, play a pivotal role in the secretion, accumulation, and transport of specialized secondary metabolites, and contribute significantly to defense and pollination. Recent investigations have revealed an intricate connection between these two structures, whereby specialized volatile and non-volatile metabolites are exchanged, collectively shaping their respective ecological functions. However, a comprehensive understanding of this profound integration remains largely elusive. In this review, we explore the secretory systems and associated secondary metabolism primarily in Asteraceous species to propose potential shared mechanisms facilitating the directional translocation of these metabolites to diverse destinations. We summarize recent advances in our understanding of the cooperativity between epidermal and internal secretory structures in the biosynthesis, secretion, accumulation, and emission of terpenes, providing specific well-documented examples from pyrethrum (Tanacetum cinerariifolium). Pyrethrum is renowned for its natural pyrethrin insecticides, which accumulate in the flower head, and more recently, for emitting an aphid alarm pheromone. These examples highlight the diverse specializations of secondary metabolism in pyrethrum and raise intriguing questions regarding the regulation of production and translocation of these compounds within and between its various epidermal and internal secretory systems, spanning multiple tissues, to serve distinct ecological purposes. By discussing the cooperative nature of secretory structures in flowering plants, this review sheds light on the intricate mechanisms underlying the ecological roles of terpenes in defense and pollination.
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Data availability
The datasets generated or analysed during this study are available from the corresponding author on reasonable request.
References
Adebesin F, Widhalm JR, Boachon B, Lefevre F, Pierman B, Lynch JH, Alam I, Junqueira B, Benke R, Ray S, Porter JA, Yanagisawa M, Wetzstein HY, Morgan JA, Boutry M, Schuurink RC, Dudareva N (2017) Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter. Science 356:1386–1388
Agrawal AA, Hastings AP (2019) Plant defense by latex: ecological genetics of inducibility in the milkweeds and a general review of mechanisms, evolution, and implications for agriculture. J Chem Ecol 45:1004–1018
Agrawal AA, Konno K (2009) Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40:311–331
Amrehn E, Heller A, Spring O (2014) Capitate glandular trichomes of Helianthus annuus (Asteraceae): ultrastructure and cytological development. Protoplasma 251:161–167
Amrehn E, Aschenbrenner A, Heller A, Spring O (2016) Localization of sesquiterpene lactone biosynthesis in cells of capitate glandular trichomes of Helianthus annuus (Asteraceae). Protoplasma 253:447–455
Andreucci AC, Ciccarelli D, Desideri I, Pagni AM (2008) Glandular hairs and secretory ducts of Matricaria chamomilla (Asteraceae): morphology and histochemistry. Ann Bot Fenn 45:11–18
Appezzato-da-Glória B, Da Costa FB, Da Silva VC, Gobbo-Neto L, Rehder VLG, Hayashi AH (2012) Glandular trichomes on aerial and underground organs in Chrysolaena species (Vernonieae - Asteraceae): structure, ultrastructure and chemical composition. Flora 207:878–887
Aschenbrenner AK, Horakh S, Spring O (2013) Linear glandular trichomes of Helianthus (Asteraceae): morphology, localization, metabolite activity and occurrence. AOB Plants 5:plt28
Bantho S, Naidoo Y, Dewir YH (2020) The secretory scales of Combretum erythrophyllum (Combretaceae): Micromorphology, ultrastructure and histochemistry. S Afr J Bot 131:104–117
Barros TCD, Marinho CR, Pedersoli GD, Paulino JV, Teixeira SP (2017) Beyond pollination: diversity of secretory structures during flower development in different legume lineages. Acta Bot Bras 31:358–373
Batista MF, De Souza LA (2017) Flower structure in ten Asteraceae species: considerations about the importance of morpho-anatomical features at species and tribal level. Braz J Bot 40:265–279
Bezerra LDA, Mangabeira PAO, de Oliveira RA, Costa LCDB, Da Cunha M (2018) Leaf blade structure of Verbesina macrophylla (Cass.) F. S. Blake (Asteraceae): ontogeny, duct secretion mechanism and essential oil composition. Plant Bio (stuttgart, Germany) 20:433–443
Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Koley A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci 109:20124–20129
Bombo AB, Appezzato-da-Glória B, Aschenbrenner A, Spring O (2016) Capitate glandular trichomes in Aldama discolor (Heliantheae - Asteraceae): morphology, metabolite profile and sesquiterpene biosynthesis. PLANT BIO 18:455–462
Bouwmeester H (2019) Dissecting the pine tree green chemical factory. J Exp Bot 70:4–6
Cabrita P (2018) Resin flow in conifers. J Theor Biol 453:48–57
Chalvin C, Drevensek S, Dron M, Bendahmane A, Boualem A (2020) Genetic control of glandular trichome development. Trends Plant Sci 25:477–487
Chow JK, Akhtar Y, Isman MB (2005) The effects of larval experience with a complex plant latex on subsequent feeding and oviposition by the cabbage looper moth: Trichoplusia ni (Lepidoptera: Noctuidae). Chemoecology 15:129–133
Ciccarelli D, Garbari F, Pagni AM (2008) The flower of Myrtus communis (Myrtaceae): secretory structures, unicellular papillae, and their ecological role. Flora 203:85–93
Demissie ZA, Tarnowycz M, Adal AM, Sarker LS, Mahmoud SS (2019) A lavender ABC transporter confers resistance to monoterpene toxicity in yeast. Planta 249:139–144
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ’cry for help’. Trends Plant Sci 15:167–175
Fahn A (1988) Secretory tissues in vascular plants. New Phytol 108:229–257
Gani U, Vishwakarma RA, Misra P (2021) Membrane transporters: the key drivers of transport of secondary metabolites in plants. Plant Cell Rep 40:1–18
Gershenzon J, McConkey M, Croteau R (2002) Biochemical and molecular regulation of monoterpene accumulation in peppermint (Mentha × piperita). J Herbs Spices Med Plants 9:153–156
Gibson RW, Pickett JA (1983) Wild potato repels aphids by release of aphid alarm pheromone. Nature 302:608–609
Giuliani C, Ascrizzi R, Lupi D, Tassera G, Santagostini L, Giovanetti M, Flamini G, Fico G (2018) Salvia verticillata: linking glandular trichomes, volatiles and pollinators. Phytochemistry 155:53–60
Giuliani C, Giovanetti M, Lupi D, Mesiano MP, Barilli R, Ascrizzi R, Flamini G, Fico G (2020) Tools to tie: flower characteristics, VOC emission profile, and glandular trichomes of two Mexican Salvia species to attract bees. Plants-Basel 9:1645
Glas J, Schimmel B, Alba J, Escobar-Bravo R, Schuurink R, Kant M (2012) Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci 13:17077–17103
Goodger JQD, Cao B, Jayadi I, Williams SJ, Woodrow IE (2009) Non-volatile components of the essential oil secretory cavities of Eucalyptus leaves: discovery of two glucose monoterpene esters, cuniloside B and froggattiside A. Phytochemistry 70:1187–1194
Goodger JQ, Heskes AM, Mitchell MC, King DJ, Neilson EH, Woodrow IE (2010) Isolation of intact sub-dermal secretory cavities from Eucalyptus. Plant Methods 6:20
Goodger JQD, Mitchell MC, Woodrow IE (2013) Differential patterns of mono- and sesquiterpenes with leaf ontogeny influence pharmaceutical oil yield in Eucalyptus polybractea R.T. Baker Trees 27:511–521
Goodger JQD, Senaratne SL, Nicolle D, Woodrow IE (2018) Differential metabolic specialization of foliar oil glands in Eucalyptus brevistylis Brooker (Myrtaceae). Tree Physiol 38:1451–1460
Goodger JQD, Sargent D, Humphries J, Woodrow IE (2021) Monoterpene synthases responsible for the terpene profile of anther glands in Eucalyptus polybractea R.T. Baker (Myrtaceae). Tree Physiol 41:849–864
Göpfert JC, Heil N, Conrad J, Spring O (2005) Cytological development and sesquiterpene lactone secretion in capitate glandular trichomes of sunflower. Plant Biol 7:148–155
Guo J, Yuan Y, Liu Z, Zhu J (2013) Development and structure of internal glands and external glandular trichomes in Pogostemon cablin. PLoS ONE 8:e77862
Haratym W, Weryszko-Chmielewska E, Konarska A (2020) Microstructural and histochemical analysis of aboveground organs of Centaurea cyanus used in herbal medicine. Protoplasma 257:285–298
Heinrich G, Pfeifhofer HW, Stabentheiner E, Sawidis T (2002) Glandular hairs of Sigesbeckia jorullensis Kunth (Asteraceae): morphology, histochemistry and composition of essential oil. Ann Bot-London 89:459–469
Hu H, Li J, Delatte T, Vervoort J, Gao L, Verstappen F, Xiong W, Gan J, Jongsma MA, Wang C (2018) Modification of chrysanthemum odour and taste with chrysanthemol synthase induces strong dual resistance against cotton aphids. Plant Biotechnol J 16:1434–1445
Huang J, McAuslane HJ, Nuessly GS (2005) Resistance in lettuce to Diabrotica balteata (Coleoptera: Chrysomelidae): the roles of latex and inducible defense. Environ Entomol 32:9–16
Huchelmann A, Boutry M, Hachez C (2017) Plant glandular trichomes: natural cell factories of high biotechnological interest. Plant Physiol 175:6–22
Hwang HS, Adhikari PB, Jo HJ, Han JY, Choi YE (2020) Enhanced monoterpene emission in transgenic orange mint (Mentha × piperita f. citrata) overexpressing a tobacco lipid transfer protein (NtLTP1). Planta 252:44
Jachuła J, Konarska A, Denisow B (2018) Micromorphological and histochemical attributes of flowers and floral reward in Linaria vulgaris (Plantaginaceae). Protoplasma 255:1763–1776
Jaime R, Rey PJ, Alcántara JM, Bastida JM (2013) Glandular trichomes as an inflorescence defence mechanism against insect herbivores in Iberian columbines. Oecologia 172:1051–1060
Joachim C, Weisser WW (2013) Real-time monitoring of (E)-β-farnesene emission in colonies of the pea aphid, Acyrthosiphon pisum, under lacewing and ladybird predation. J Chem Ecol 39:1254–1262
Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854
Khare D, Choi H, Huh SU, Bassin B, Kim J, Martinoia E, Sohn KH, Paek K, Lee Y (2017) Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. Proc Natl Acad Sci 114:5712–5720
Kikuta Y, Ueda H, Nakayama K, Katsuda Y, Ozawa R, Takabayashi J, Hatanaka A, Matsuda K (2011) Specific regulation of pyrethrin biosynthesis in chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol 52:588–596
Kikuta Y, Ueda H, Takahashi M, Mitsumori T, Yamada G, Sakamori K, Takeda K, Furutani S, Nakayama K, Katsuda Y, Hatanaka A, Matsuda K (2012) Identification and characterization of a GDSL lipase-like protein that catalyzes the ester-forming reaction for pyrethrin biosynthesis in Tanacetum cinerariifolium—a new target for plant protection. Plant J 71:183–193
Koley S, Grafahrend-Belau E, Raorane ML, Junker BH (2020) The mevalonate pathway contributes to monoterpene production in peppermint. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Kortbeek RWJ, van der Gragt M, Bleeker PM (2019) Endogenous plant metabolites against insects. Eur J Plant Pathol 154:67–90
Krings M, Kellogg DW, Kerp H, Taylor TN (2003) Trichomes of the seed fern Blanzyopteris praedentata: implications for plant-insect interactions in the Late Carboniferous. Bot J Linn Soc 141:133–149
Kromer K, Kreitschitz A, Kleinteich T, Gorb SN, Szumny A (2016) Oil secretory system in vegetative organs of three Arnica taxa: essential oil synthesis, distribution and accumulation. Plant Cell Physiol 57:1020–1037
Lange BM (2015) The evolution of plant secretory structures and emergence of terpenoid chemical diversity. Annu Rev Plant Biol 66:139–159
Lange BM, Turner GW (2013) Terpenoid biosynthesis in trichomes-current status and future opportunities. Plant Biotechnol J 11:2–22
Lange BM, Ketchum REB, Croteau RB (2001) Isoprenoid biosynthesis. Metabolite profiling of peppermint oil gland secretory cells and application to herbicide target analysis. Plant Physiol 127:305–314
Li W, Zhou F, Pichersky E (2018) Jasmone hydroxylase, a key enzyme in the synthesis of the alcohol moiety of pyrethrin insecticides. Plant Physiol 177:1498–1509
Li J, Hu H, Mao J, Yu L, Stoopen G, Wang M, Mumm R, de Ruijter NCA, Dicke M, Jongsma MA, Wang C (2019) Defense of pyrethrum flowers: repelling herbivore and recruiting carnivore by producing aphid alarm pheromone. New Phytol 223:1607–1620
Li W, Lybrand DB, Xu H, Zhou F, Last RL, Pichersky E (2020) A trichome-specific, plastid-localized Tanacetum cinerariifolium nudix protein hydrolyzes the natural pyrethrin pesticide biosynthetic intermediate trans-chrysanthemyl diphosphate. Front Plant Sci 11:482
Li J, Halitschke R, Li D, Paetz C, Su H, Heiling S, Xu S, Baldwin IT (2021a) Controlled hydroxylations of diterpenoids allow for plant chemical defense without autotoxicity. Science 371:255–260
Li J, Hu H, Chen Y, Xie J, Li J, Zeng T, Wang M, Luo J, Zheng R, Jongsma MA, Wang C (2021b) Tissue specificity of (E)-β-farnesene and germacrene D accumulation in pyrethrum flowers. Phytochemistry 187:112768
Liao P, Maoz I, Shih M, Lee JH, Huang X, Morgan JA, Dudareva N (2023) Emission of floral volatiles is facilitated by cell-wall non-specific lipid transfer proteins. Nat Commun 14:330
Liu C, Srividya N, Parrish AN, Yue W, Shan M, Wu Q, Lange BM (2018) Morphology of glandular trichomes of Japanese catnip (Schizonepeta tenuifolia Briquet) and developmental dynamics of their secretory activity. Phytochemistry 150:23–30
Liu Y, Jing S, Luo S, Li S (2019) Non-volatile natural products in plant glandular trichomes: chemistry, biological activities and biosynthesis. Nat Prod Rep 36:626–665
Livingston SJ, Quilichini TD, Booth JK, Wong DCJ, Rensing KH, Laflamme Yonkman J, Castellarin SD, Bohlmann J, Page JE, Samuels AL (2019) Cannabis glandular trichomes alter morphology and metabolite content during flower maturation. Plant J 101:37–56
Lybrand DB, Xu H, Last RL, Pichersky E (2020) How plants synthesize pyrethrins: safe and biodegradable insecticides. Trends Plant Sci 22:1240–1251
Maes L, Van Nieuwerburgh FCW, Zhang Y, Reed DW, Pollier J, Vande Casteele SRF, Inzé D, Covello PS, Deforce DLD, Goossens A (2011) Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol 189:176–189
Majdi M, Liu Q, Karimzadeh G, Malboobi MA, Beekwilder J, Cankar K, Vos RD, Todorović S, Simonović A, Bouwmeester H (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry 72:1739–1750
Marinho CR, Souza CD, Barros TC, Teixeira SP (2014) Scent glands in legume flowers. Plant Biol 16:215–226
Morimoto M (2019) Chemical defense against insects in Heterotheca subaxillaris and three Orobanchaceae species using exudates from trichomes. Pest Manag Sci 75:2474–2481
Muravnik LE, Shavarda AL (2012) Leaf glandular trichomes in Empetrum nigrum: morphology, histochemistry, ultrastructure and secondary metabolites. Nord J Bot 30:470–481
Muravnik LE, Kostina OV, Shavarda AL (2016) Glandular trichomes of Tussilago Farfara (Senecioneae, Asteraceae). Planta 244:737–752
Muravnik LE, Kostina OV, Mosina AA (2019) Glandular trichomes of the leaves in three Doronicum species (Senecioneae, Asteraceae): morphology, histochemistry, and ultrastructure. Protoplasma 256:789–803
Naidoo Y, Karim T, Heneidak S, Sadashiva CT, Naidoo G (2012) Glandular trichomes of Ceratotheca triloba (Pedaliaceae): morphology, histochemistry and ultrastructure. Planta 236:1215–1226
Naidoo Y, Rikisahedew JJ, Dewir YH, Ali AA, Rihan HZ (2021) Foliar micromorphology, ultrastructure and histochemical analyses of Tagetes minuta L. leaves. Micron 150:103125
Olofsson L, Lundgren A, Brodelius PE (2012) Trichome isolation with and without fixation using laser microdissection and pressure catapulting followed by RNA amplification: expression of genes of terpene metabolism in apical and sub-apical trichome cells of Artemisia annua L. Plant Sci 183:9–13
Olsson ME, Olofsson LM, Lindahl A, Lundgren A, Brodelius M, Brodelius PE (2009) Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70:1123–1128
Palmer-Young EC, Farrell IW, Adler LS, Milano NJ, Egan PA, Junker RR, Irwin RE, Stevenson PC (2019) Chemistry of floral rewards: intra- and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecol Monogr 89:e1335
Parachnowitsch AL, Manson JS (2015) The chemical ecology of plant-pollinator interactions: recent advances and future directions. Curr Opin Insect Sci 8:41–46
Pasqua G, Monacelli B, Manfredini C, Loreto F, Perez G (2002) The role of isoprenoid accumulation and oxidation in sealing wounded needles of Mediterranean pines. Plant Sci 163:355–359
Peter GF (2018) Breeding and engineering trees to accumulate high levels of terpene metabolites for plant defense and renewable chemicals. Front Plant Sci 9:1672
Pickard WF (2007) Laticifers and secretory ducts: two other tube systems in plants. New Phytol 177:877–888
Pierman B, Toussaint F, Bertin A, Lévy D, Smargiasso N, De Pauw E, Boutry M (2017) Activity of the purified plant ABC transporter NtPDR1 is stimulated by diterpenes and sesquiterpenes involved in constitutive and induced defenses. J Biol Chem 292:19491–19502
Prasifka JR (2015) Variation in the number of capitate glandular trichomes in wild and cultivated sunflower germplasm and its potential for use in host plant resistance. Plant Genetic Resour 13:68–74
Prasifka JR, Spring O, Conrad J, Cook LW, Palmquist DE, Foley ME (2015) Sesquiterpene lactone composition of wild and cultivated sunflowers and biological activity against an insect pest. J Agr Food Chem 63:4042–4049
Pütter KM, van Deenen N, Unland K, Prüfer D, Gronover CS (2017) Isoprenoid biosynthesis in dandelion latex is enhanced by the overexpression of three key enzymes involved in the mevalonate pathway. BMC Plant Biol 17:88
Raghu K, Naidoo Y, Dewir YH (2019) Secretory structures in the leaves of Hibiscus sabdariffa L. S Afr J Bot 121:16–25
Ramirez AM, Stoopen G, Menzel TR, Gols R, Bouwmeester HJ, Dicke M, Jongsma MA (2012) Bidirectional secretions from glandular trichomes of pyrethrum enable immunization of seedlings. Plant Cell 24:4252–4265
Ramirez A, Saillard N, Yang T, Franssen M, Bouwmeester H, Jongsma M (2013a) Biosynthesis of sesquiterpene lactones in pyrethrum (Tanacetum cinerariifolium). PLoS ONE 5:e65030
Ramirez AM, Yang T, Bouwmeester HJ, Jongsma MA (2013b) A trichome-specific linoleate lipoxygenase expressed during pyrethrin biosynthesis in pyrethrum. Lipids 48:1005–1015
Reddy VA, Li C, Nadimuthu K, Tjhang JG, Jang I, Rajani S (2021) Sweet basil has distinct synthases for eugenol biosynthesis in glandular trichomes and roots with different regulatory mechanisms. Int J Mol Sci 22:681
Riddick EW, Simmons AM (2014) Do plant trichomes cause more harm than good to predatory insects? Pest Manag Sci 70:1655–1665
Riffell JA (2017) Plant defense-time is everything. Curr Biol 27:339–363
Robert JA, Madilao LL, White R, Yanchuk A, King J, Bohlmann J (2010) Terpenoid metabolite profiling in Sitka spruce identifies association of dehydroabietic acid, (+)-3-carene and terpinolene with resistance against white pine weevil. Botany 88:810–820
Sashida Y, Nakata H, Shimomura H, Kagaya M (1983) Sesquiterpene lactones from pyrethrum flowers. Phytochemistry 22:1219–1222
Sasse J, Schlegel M, Borghi L, Ullrich F, Lee M, Liu G, Giner J, Kayser O, Bigler L, Martinoia E, Kretzschmar T (2016) Petunia hybrida PDR2 is involved in herbivore defense by controlling steroidal contents in trichomes. Plant Cell Environ 39:2725–2739
Savage JA, Clearwater MJ, Haines DF, Klein T, Mencuccini M, Sevanto S, Turgeon R, Zhang C (2016) Allocation, stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology? Plant Cell Environ 39:709–725
Schiebe C, Hammerbacher A, Birgersson G, Witzell J, Brodelius PE, Gershenzon J, Hansson BS, Krokene P, Schlyter F (2012) Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia 170:183–198
Schmiderer C, Grassi P, Novak J, Weber M, Franz C (2008) Diversity of essential oil glands of clary sage (Salvia sclarea L., Lamiaceae). Plant Bio (stuttg) 10:433–440
Schuurink R, Tissier A (2020) Glandular trichomes: micro-organs with model status? New Phytol 225:2251–2266
Soetaert SS, Van Neste CM, Vandewoestyne ML, Head SR, Goossens A, Van Nieuwerburgh FC, Deforce DL (2013) Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua. BMC Plant Biol 13:220
Tekin M, Kartal C (2016) Comparative anatomical investigations on six endemic Tanacetum (Asteraceae) taxa from turkey. Pak J Bot 4:1501–1515
Therezan R, Kortbeek R, Vendemiatti E, Legarrea S, de Alencar SM, Schuurink RC, Bleeker P, Peres LEP (2021) Introgression of the sesquiterpene biosynthesis from Solanum habrochaites to cultivated tomato offers insights into trichome morphology and arthropod resistance. Planta 254:11
Thieme T, Dixon AFG (2015) Is the response of aphids to alarm pheromone stable? J Appl Entomol 139:741–746
Tomas J, Gil L, Llorens-Molina JA, Cardona C, García MT, Llorens L (2019) Biogenic volatiles of rupicolous plants act as direct defenses against molluscs: the case of the endangered Clinopodium rouyanum. Flora 258:151428
Tozin LRDS, Mayo Marques MO, Maria Rodrigues T (2017) Herbivory by leaf-cutter ants changes the glandular trichomes density and the volatile components in an aromatic plant model. AOB Plants 9:plx57
Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol 136:4215–4227
Turner GW, Gershenzon J, Croteau RB (2000) Development of Peltate glandular Trichomes of peppermint. Plant Physiol (bethesda) 124:665–680
Turner GW, Parrish AN, Zager JJ, Fischedick JT, Lange BM (2018) Assessment of flux through oleoresin biosynthesis in epithelial cells of loblolly pine resin ducts. J Exp Bot 70:217–230
Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ (2012) Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochem Molec 42:155–163
Wang B, Dong W, Li H, Onofrio CD, Bai P, Chen R, Yang L, Wu J, Wang X, Wang B, Ai D, Knoll W, Pelosi P, Wang G (2021) Molecular basis of (E)-β-farnesene-mediated aphid location in the predator Eupeodes corollae. Curr Biol 32:1–12
Widhalm JR, Jaini R, Morgan JA, Dudareva N (2015) Rethinking how volatiles are released from plant cells. Trends Plant Sci 20:545–550
Widhalm JR, Shih M, Morgan JA, Dudareva N (2023) Two-way communication: volatile emission and uptake occur through the same barriers. Mol Plant 16:1–3
Xu H, Moghe GD, Wiegert-Rininger K, Schilmiller AL, Barry CS, Last RL, Pichersky E (2018) Coexpression analysis identifies two oxidoreductases involved in the biosynthesis of the monoterpene acid moiety of natural pyrethrin insecticides in Tanacetum cinerariifolium. Plant Physiol 176:524–537
Xu H, Li W, Schilmiller AL, van Eekelen H, de Vos R, Jongsma MA, Pichersky E (2019) Pyrethric acid of natural pyrethrin insecticide: complete pathway elucidation and reconstitution in Nicotiana benthamiana. New Phytol 223:751–765
Yazaki K, Arimura G, Ohnishi T (2017) “Hidden” terpenoids in plants: their biosynthesis, localization and ecological roles. Plant Cell Physiol 58:1615–1621
Zager JJ, Lange BM (2018) Assessing flux distribution associated with metabolic specialization of glandular trichomes. Trends Plant Sci 23:638–647
Zhang Y, Wang D, Li H, Bai H, Sun M, Shi L (2023) Formation mechanism of glandular trichomes involved in the synthesis and storage of terpenoids in lavender. BMC Plant Biol 23:1–6
Zhao J, Dixon RA (2010) The “ins” and “outs” of flavonoid transport. Trends Plant Sci 15:72–80
Zhou W, Kugler A, McGale E, Haverkamp A, Knaden M, Guo H, Beran F, Yon F, Li R, Lackus N, Kollner TG, Bing J, Schuman MC, Hansson BS, Kessler D, Baldwin IT, Xu S (2017) Tissue-specific emission of (E)-α-bergamotene helps resolve the dilemma when pollinators are also herbivores. Curr Biol 27:1336–1341
Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97
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This work was financially supported in China by the China Postdoctoral Science Foundation (2019M662679 and 2018M640720), the National Key Research and Development Project (2019YFD1001500), National Natural Science Foundation of China (31902051) and the fundamental Research Funds for the Central Universities (2662019FW016).
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JJL wrote the initial draft; JJL, HSF and JL performed the experiments and drew the figures; HH, MQW, TZ, JWL, MJ and CYW revised the manuscript. All authors read and approved the final manuscript.
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Li, J., Hu, H., Fu, H. et al. Exploring the co-operativity of secretory structures for defense and pollination in flowering plants. Planta 259, 41 (2024). https://doi.org/10.1007/s00425-023-04322-w
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DOI: https://doi.org/10.1007/s00425-023-04322-w