Abstract
Ficus species have adapted to diverse environments and pests by developing physical or chemical protection strategies. Physical defences are based on the accumulation of minerals such as calcium oxalate crystals, amorphous calcium carbonates and silica that lead to tougher plants. Additional cellular structures such as non-glandular trichomes or laticifer cells make the leaves rougher or sticky upon injury. Ficus have also established structures that are able to produce specialized metabolites (alkaloids, terpenoids, and phenolics) or proteins (proteases, protease inhibitors, oxidases, and chitinases) that are toxic to predators. All these defence mechanisms are distributed throughout the plant and can differ depending on the genotype, the stage of development or the environment. In this review, we present an overview of these strategies and discuss how these complementary mechanisms enable effective and flexible adaptation to numerous hostile environments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abu-Mustafa EA, El-Tawil BAH, Fayez MBE (1963) Constituents of local plants—IV. Ficus carica L., F. sycomorus L. and F. salicifolia L. leaves. Phytochemistry 3:701–703. https://doi.org/10.1016/S0031-9422(00)82968-4
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. https://doi.org/10.1146/annurev.ecolsys.110308.120307
Ahmad S, Rao H, Akhtar M et al (2011) Phytochemical composition and pharmacological prospectus of Ficus benghalensis Linn. (Moraceae)—a review. J Med Plants Res 5:6393–6400. https://doi.org/10.5897/JMPR11.455
Alam P, Siddiqui N, Basudan O et al (2015) Comparative profiling of biomarker psoralen in antioxidant active extracts of different species of genus Ficus by validated HPTLC method. Afr J Tradit Complement Altern Med 12:57. https://doi.org/10.4314/ajtcam.v12i1.9
Al-Khdhairawi AAQ, Krishnan P, Mai C-W et al (2017) A bis-benzopyrroloisoquinoline alkaloid incorporating a cyclobutane core and a chlorophenanthroindolizidine alkaloid with cytotoxic activity from Ficus fistulosa var. tengerensis. J Nat Prod 80:2734–2740. https://doi.org/10.1021/acs.jnatprod.7b00500
Anstett MC (2001) Unbeatable strategy, constraint and coevolution, or how to resolve evolutionary conflicts: the case of the fig/wasp mutualism. Oikos 95:476–484. https://doi.org/10.1034/j.1600-0706.2001.950313.x
Athnasios AK, El-Kholy IE-S, Soliman G, Shaban M (1962) Constituents of leaves of Ficus carica, L. 1. Isolation of psoralen, bergapten, psi-taraxasterol, and beta-sitosterol. J Chem Soc Resumed 4253–4264. https://doi.org/10.1039/jr9620004253
Bai S, Dong C, Li B, Dai H (2013) A PR-4 gene identified from Malus domestica is involved in the defense responses against Botryosphaeria dothidea. Plant Physiol Biochem 62:23–32. https://doi.org/10.1016/j.plaphy.2012.10.016
Basset Y, Novotny V (1999) Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biol J Linn Soc 67:477–499. https://doi.org/10.1111/j.1095-8312.1999.tb01943.x
Bauer P, Elbaum R, Weiss IM (2011) Calcium and silicon mineralization in land plants: transport, structure and function. Plant Sci 180:746–756. https://doi.org/10.1016/j.plantsci.2011.01.019
Baumgartner B, Erdelmeier CAJ, Wright AD et al (1990) An antimicrobial alkaloid from Ficus septica. Phytochemistry 29:3327–3330. https://doi.org/10.1016/0031-9422(90)80209-Y
Baur R, Binder S, Benz G (1991) Nonglandular leaf trichomes as short-term inducible defense of the grey alder, Alnus incana (L.), against the chrysomelid beetle, Agelastica alni L. Oecologia 87:219–226. https://doi.org/10.1007/BF00325259
Bayoudh C, Elair M, Labidi R et al (2017) Efficacy of tissue culture in virus elimination from caprifig and female fig varieties (Ficus carica L.). Plant Pathol J 33:288–295. https://doi.org/10.5423/PPJ.OA.10.2016.0205
Beier RC, Oertli EH (1983) Psoralen and other linear furocoumarins as phytoalexins in celery. Phytochemistry 22:2595–2597. https://doi.org/10.1016/0031-9422(83)80173-3
Berenbaum MR (2002) Postgenomic chemical ecology: from genetic code to ecological interactions. J Chem Ecol 28:873–896. https://doi.org/10.1023/A:1015260931034
Bhutani K, Sharma G, Ali M (1987) Plant based antiamoebic drugs; part I. Antiamoebic activity of phenanthroindolizidine alkaloids; common structural determinants of activity with emetine. Planta Med 53:532–536. https://doi.org/10.1055/s-2006-962803
Bonamonte D, Foti C, Lionetti N et al (2010) Photoallergic contact dermatitis to 8-methoxypsoralen in Ficus carica. Contact Dermat 62:343–348. https://doi.org/10.1111/j.1600-0536.2010.01713.x
Borges RM, Bessière J-M, Ranganathan Y (2013) Diel variation in fig volatiles across syconium development: making sense of scents. J Chem Ecol 39:630–642. https://doi.org/10.1007/s10886-013-0280-5
Broadway RM, Duffey SS (1986) Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exiqua. J Insect Physiol 32:827–833. https://doi.org/10.1016/0022-1910(86)90097-1
Burtoloso A, Bertonha A, Rosset I (2013) Synthesis of alkaloids: recent advances in the synthesis of phenanthroindolizidine alkaloids. Curr Top Med Chem 14:191–199. https://doi.org/10.2174/1568026613666131213154633
Buttery BR, Boatman SG (1976) Water deficits and flow of latex. Soil water measurement, plant responses, and breeding for drought resistance, United Kingdom Edition. Academic Press, London, pp 233–289
Caporale G, Dall’Acqua F, Marciani S, Capozzi A (1970) Studies on the Biosynthesis of Psoralen and Bergapten in the Leaves of Ficus carica. Z Für Naturforschung B 25:700–703. https://doi.org/10.1515/znb-1970-0709
Chamont S (2014) Ficus carica. Les maladies et ravageurs. In: Ephytia. http://ephytia.inra.fr/fr/C/18200/Hypp-encyclopedie-en-protection-des-plantes-Les-maladies-et-ravageurs. Accessed 17 Sep 2018
Chang M-S, Yang Y-C, Kuo Y-C et al (2005) Furocoumarin glycosides from the leaves of Ficus ruficaulis merr. var. antaoensis. J Nat Prod 68:11–13. https://doi.org/10.1021/np0401056
Chantarasuwan B, Baas P, van Heuven B-J et al (2014) Leaf anatomy of Ficus subsection Urostigma (Moraceae). Bot J Linn Soc 175:259–281. https://doi.org/10.1111/boj.12165
Chen L-W, Cheng M-J, Peng C-F, Chen I-S (2010) Secondary metabolites and antimycobacterial activities from the roots of Ficus nervosa. Chem Biodivers 7:1814–1821. https://doi.org/10.1002/cbdv.200900227
Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–234. https://doi.org/10.2307/1942495
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. https://doi.org/10.1126/science.230.4728.895
Cruaud A, Rønsted N, Chantarasuwan B et al (2012) An extreme case of plant–insect codiversification: figs and fig-pollinating wasps. Syst Biol 61:1029–1047. https://doi.org/10.1093/sysbio/sys068
Damu AG, Kuo P-C, Shi L-S et al (2005) Phenanthroindolizidine alkaloids from the stems of Ficus septica. J Nat Prod 68:1071–1075. https://doi.org/10.1021/np050095o
Damu A, Kuo P-C, Shi L-S et al (2009) Cytotoxic phenanthroindolizidine alkaloids from the roots of Ficus septica. Planta Med 75:1152–1156. https://doi.org/10.1055/s-0029-1185483
Dardalhon M, de Massy B, Nicolas A, Averbeck D (1998) Mitotic recombination and localized DNA double-strand breaks are induced after 8-methoxypsoralen and UVA irradiation in Saccharomyces cerevisiae. Curr Genet 34:30–42. https://doi.org/10.1007/s002940050363
de Freitas CDT, Sousa Nogueira FC, Vasconcelos IM et al (2011) Osmotin purified from the latex of Calotropis procera: biochemical characterization, biological activity and role in plant defense. Plant Physiol Biochem 49:738–743. https://doi.org/10.1016/j.plaphy.2011.01.027
Debib A, Tir-Touil A, Mothana RA et al (2014) Phenolic content, antioxidant and antimicrobial activities of two fruit varieties of Algerian Ficus carica L.: antioxidant and antimicrobial activity of Algerian figs. J Food Biochem 38:207–215. https://doi.org/10.1111/jfbc.12039
Dussourd DE (2017) Behavioral sabotage of plant defenses by insect folivores. Annu Rev Entomol 62:15–34. https://doi.org/10.1146/annurev-ento-031616-035030
Dussourd DE, Denno RF (1991) Deactivation of plant defense: correspondence between insect behavior and secretory canal architecture. Ecology 72:1383–1396. https://doi.org/10.2307/1941110
Dussourd DE, Denno RF (1994) Host range of generalist caterpillars: trenching permits feeding on plants with secretory canals. Ecology 75:69–78. https://doi.org/10.2307/1939383
Dussourd DE, Eisner T (1987) Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237:898–901. https://doi.org/10.1126/science.3616620
Dussourd DE, Hoyle AM (2000) Poisoned plusiines: toxicity of milkweed latex and cardenolides to some generalist caterpillars. Chemoecology 10:11–16. https://doi.org/10.1007/PL00001810
Edreva A (2005) Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol 31:105–124
Elbeaino T, Digiaro M, Martelli GP (2011) Complete sequence of Fig fleck-associated virus, a novel member of the family Tymoviridae. Virus Res 161:198–202. https://doi.org/10.1016/j.virusres.2011.07.022
El-Sakhawy F, Kassem H, Abou-Hussein D et al (2016) Phytochemical investigation of the bioactive extracts of the leaves of Ficus cyathistipula Warb. Z Für Naturforschung C 71:141–154. https://doi.org/10.1515/znc-2015-0274
FAO (2016) FAOSTAT Database. In: Food Agric. Organ. U. N. http://www.fao.org/faostat/en/#data. Accessed 13 July 2018
Farrell BD, Dussourd DE, Mitter C (1990) Escalation of plant defense: do latex and resin canals spur plant diversification? Am Nat 138:881–900. https://doi.org/10.1086/285258
Felton GW, Gatehouse JA (1996) Antinutritive plant defence mechanisms. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Springer, Dordrecht, pp 373–416
Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore, Spodoptera exigua. J Insect Physiol 38:277–285. https://doi.org/10.1016/0022-1910(92)90128-Z
Finley DS (1999) Patterns of calcium oxalate crystals in young tropical leaves: a possible role as an anti-herbivory defense. Rev Biol Trop 47:27–31
Foster AS (1956) Plant idioblasts: remarkable examples of cell specialization. Protoplasma 46:184–193. https://doi.org/10.1007/BF01248877
Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annu Rev Plant Biol 56:41–71. https://doi.org/10.1146/annurev.arplant.56.032604.144106
Gal A, Weiner S, Addadi L (2010) The stabilizing effect of silicate on biogenic and synthetic amorphous calcium carbonate. J Am Chem Soc 132:13208–13211. https://doi.org/10.1021/ja106883c
Gal A, Brumfeld V, Weiner S et al (2012) Certain biominerals in leaves function as light scatterers. Adv Mater 24:OP77–OP83. https://doi.org/10.1002/adma.201104548
Gautam P, Lal B, Tripathi R et al (2016) Role of silica and nitrogen interaction in submergence tolerance of rice. Environ Exp Bot 125:98–109. https://doi.org/10.1016/j.envexpbot.2016.02.008
Ghana S, Suleman N, Compton SG (2017) Style length variation in male and female figs: development, inheritance, and control of pollinator oviposition. Entomol Exp Appl 162:41–50. https://doi.org/10.1111/eea.12533
Gibernau M, Buser HR, Frey JE, Hossaert-McKey M (1997) Volatile compounds from extracts of figs of Ficus carica. Phytochemistry 46:241–244. https://doi.org/10.1016/S0031-9422(97)00292-6
Guo Q, Du G, He H et al (2016) Two nematicidal furocoumarins from Ficus carica L. leaves and their physiological effects on pine wood nematode (Bursaphelenchus xylophilus). Nat Prod Res 30:1969–1973. https://doi.org/10.1080/14786419.2015.1094804
Hagel J, Yeung E, Facchini P (2008) Got milk? The secret life of laticifers. Trends Plant Sci 13:631–639. https://doi.org/10.1016/j.tplants.2008.09.005
He K, Iyer KR, Hayes RN et al (1998) Inactivation of cytochrome P450 3A4 by bergamottin, a component of grapefruit juice. Chem Res Toxicol 11:252–259. https://doi.org/10.1021/tx970192k
Hebeish A, Fouda MMG, Hamdy IA et al (2008) Preparation of durable insect repellent cotton fabric: limonene as insecticide. Carbohydr Polym 74:268–273. https://doi.org/10.1016/j.carbpol.2008.02.013
Hilder VA, Gatehouse AM, Sheerman SE et al (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–163. https://doi.org/10.1038/330160a0
Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot 96:1027–1046. https://doi.org/10.1093/aob/mci255
Hoffmann-Sommergruber K (2002) Pathogenesis-related (PR)-proteins identified as allergens. Biochem Soc Trans 30:930–935. https://doi.org/10.1042/bst0300930
Hosomi A, Miwa Y, Furukawa M, Kawaradani M (2012) Growth of fig varieties resistant to ceratocystis canker following infection with Ceratocystis fimbriata. J Jpn Soc Hortic Sci 81:159–165. https://doi.org/10.2503/jjshs1.81.159
Hudgins JW, Krekling T, Franceschi VR (2003) Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defense mechanism? New Phytol 159:677–690. https://doi.org/10.1046/j.1469-8137.2003.00839.x
Hunt JW, Dean AP, Webster RE et al (2008) A novel mechanism by which silica defends grasses against herbivory. Ann Bot 102:653–656. https://doi.org/10.1093/aob/mcn130
Huynh QK, Borgmeyer JR, Zobel JF (1992) Isolation and characterization of a 22 kDa protein with antifungal properties from maize seeds. Biochem Biophys Res Commun 182:1–5. https://doi.org/10.1016/S0006-291X(05)80103-2
Jaina R, Jain SC, Bhagchandani T, Yadav N (2013) New furanocoumarins and other chemical constituents from Ficus carica root heartwood. Z Für Naturforschung C 68:3–7. https://doi.org/10.1515/znc-2013-1-201
Janzen DH (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51. https://doi.org/10.1146/annurev.es.10.110179.000305
Jeong M-R, Kim H-Y, Cha J-D (2009) Antimicrobial activity of methanol extract from Ficus carica leaves against oral bacteria. J Bacteriol Virol 39:97–102. https://doi.org/10.4167/jbv.2009.39.2.97
Jun LI, Tian Y, Sun B et al (2012) Analysis on volatile constituents in leaves and fruits of Ficus carica by GC–MS. Chin Herb Med 4:63–69. https://doi.org/10.3969/j.issn.1674-6384.2012.01.010
Kim JS, Kim YO, Ryu HJ et al (2003) Isolation of stress-related genes of rubber particles and latex in fig tree (Ficus carica) and their expressions by abiotic stress or plant hormone treatments. Plant Cell Physiol 44:412–414. https://doi.org/10.1093/pcp/pcg058
Kim YS, Park SJ, Lee EJ et al (2008) Antibacterial compounds from rose bengal-sensitized photooxidation of β-caryophyllene. J Food Sci 73:C540–C545. https://doi.org/10.1111/j.1750-3841.2008.00879.x
Kitajima S, Aoki W, Shibata D et al (2018) Comparative multi-omics analysis reveals diverse latex-based defense strategies against pests among latex-producing organs of the fig tree (Ficus carica). Planta 247:1423–1438. https://doi.org/10.1007/s00425-018-2880-3
Klimko M, Truchan M (2006) Morphological variability of the leaf epidermis in selected taxa of the genus Ficus L. (Moraceae) and its taxonomic implication. Acta Soc Bot Pol 75:309–324. https://doi.org/10.5586/asbp.2006.038
Koenigs LL, Trager WF (1998) Mechanism-based inactivation of P450 2A6 by furanocoumarins. Biochemistry 37:10047–10061. https://doi.org/10.1021/bi980003c
Kon S, Whitaker JR (1965) Separation and partial characterization of the peroxidases of Ficus glabrata Latex. J Food Sci 30:977–985. https://doi.org/10.1111/j.1365-2621.1965.tb01873.x
Konno K (2011) Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 72:1510–1530. https://doi.org/10.1016/j.phytochem.2011.02.016
Konno K, Hirayama C, Nakamura M et al (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37:370–378. https://doi.org/10.1046/j.1365-313X.2003.01968.x
Koricheva J, Nykänen H, Gianoli E (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:E64–E75. https://doi.org/10.1086/382601
Korth KL, Doege SJ, Park S-H et al (2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol 141:188–195. https://doi.org/10.1104/pp.106.076737
Kramer DE, Whitaker JR (1964) Ficus enzymes II. Properties of the proteolytic enzymes from the latex of Ficus carica variety Kadota. J Biol Chem 239:2178–2183
Krieger C, Roselli S, Kellner-Thielmann S et al (2018) The CYP71AZ P450 subfamily: a driving factor for the diversification of coumarin biosynthesis in apiaceous plants. Front Plant Sci 9:820. https://doi.org/10.3389/fpls.2018.00820
Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado Potato Beetle. Biotechnol Lett 28:593–599. https://doi.org/10.1007/s10529-006-0022-7
Lazreg Aref H, Gaaliche B, Fekih A et al (2011) In vitro cytotoxic and antiviral activities of Ficus carica latex extracts. Nat Prod Res 25:310–319. https://doi.org/10.1080/14786419.2010.528758
Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15. https://doi.org/10.1086/407484
Lewinsohn TM (1991) The geographical distribution of plant latex. Chemoecology 2:64–68. https://doi.org/10.1007/BF01240668
Li W, Schuler MA, Berenbaum MR (2003) Diversification of furanocoumarin-metabolizing cytochrome P450 monooxygenases in two papilionids: specificity and substrate encounter rate. Proc Natl Acad Sci 100:14593–14598. https://doi.org/10.1073/pnas.1934643100
Li H, Hu T, Wang K et al (2006) Total synthesis and antiviral activity of enantioenriched (+)-deoxytylo-phorinine. Lett Org Chem 3:806–810. https://doi.org/10.2174/157017806779117067
Liu Y, Ahn J-E, Datta S et al (2005) Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol 139:1545–1556. https://doi.org/10.1104/pp.105.066837
Liu F, Yang Z, Zheng X et al (2011) Nematicidal coumarin from Ficus carica L. J Asia Pac Entomol 14:79–81. https://doi.org/10.1016/j.aspen.2010.10.006
Liu M, Zhou F, Pan X et al (2018) Specificity of herbivore-induced responses in an invasive species, Alternanthera philoxeroides (alligator weed). Ecol Evol 8:59–70. https://doi.org/10.1002/ece3.3615
Lynn KR, Clevette-Radford NA (1987) Acid phosphatases from latices of Euphorbiaceae. Phytochemistry 26:655–657. https://doi.org/10.1016/S0031-9422(00)84760-3
Macedo M, Oliveira C, Oliveira C (2015) Insecticidal activity of plant lectins and potential application in crop protection. Molecules 20:2014–2033. https://doi.org/10.3390/molecules20022014
Mamoucha S, Fokialakis N, Christodoulakis NS (2016) Leaf structure and histochemistry of Ficus carica (Moraceae), the fig tree. Flora Morphol Distrib Funct Ecol Plants 218:24–34. https://doi.org/10.1016/j.flora.2015.11.003
Marrelli M, Menichini F, Statti GA et al (2012) Changes in the phenolic and lipophilic composition, in the enzyme inhibition and antiproliferative activity of Ficus carica L. cultivar Dottato fruits during maturation. Food Chem Toxicol 50:726–733. https://doi.org/10.1016/j.fct.2011.12.025
Marrelli M, Statti GA, Tundis R et al (2014) Fatty acids, coumarins and polyphenolic compounds of Ficus carica L. cv. Dottato: variation of bioactive compounds and biological activity of aerial parts. Nat Prod Res 28:271–274. https://doi.org/10.1080/14786419.2013.841689
Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291. https://doi.org/10.1111/j.1365-2656.2008.01472.x
Massey FP, Ennos AR, Hartley SE (2007a) Grasses and the resource availability hypothesis: the importance of silica-based defences. J Ecol 95:414–424. https://doi.org/10.1111/j.1365-2745.2007.01223.x
Massey FP, Roland Ennos A, Hartley SE (2007b) Herbivore specific induction of silica-based plant defences. Oecologia 152:677–683. https://doi.org/10.1007/s00442-007-0703-5
Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue. Plant Physiol 88:936–942. https://doi.org/10.1104/pp.88.3.936
McKenzie EHC (1986) New plant disease record in New Zealand: fig rust (Cerotelium fici) on Ficus carica. N Z J Agric Res 29:707–710. https://doi.org/10.1080/00288233.1986.10430467
McNaughton SJ, Tarrants JL (1983) Grass leaf silicification: natural selection for an inducible defense against herbivores. Proc Natl Acad Sci 80:790–791. https://doi.org/10.1073/pnas.80.3.790
Melchers LS, Apotheker-de Groot M, van der Knaap JA et al (1994) A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J 5:469–480. https://doi.org/10.1046/j.1365-313X.1994.05040469.x
Meyen J (1839) Matériaux pour servir à l’histoire du développement des diverses parties dans les plantes. In: Annales des Sciences Naturelles. Botanique. Crochard, 1869, Paris, pp 257–279
Mohamed SA, Abdel-Aty AM, Belal Hamed M et al (2011) Ficus sycomorus latex: a thermostable peroxidase. Afr J Biotechnol 10:17532–17543. https://doi.org/10.5897/AJB11.2375
Müller J, Clauss M, Codron D et al (2014) Growth and wear of incisor and cheek teeth in domestic rabbits (Oryctolagus cuniculus) fed diets of different abrasiveness. J Exp Zool Part Ecol Genet Physiol 321:283–298. https://doi.org/10.1002/jez.1864
Neal JJ, Wu D (1994) Inhibition of insect cytochromes P450 by furanocoumarins. Pestic Biochem Physiol 50:43–50. https://doi.org/10.1006/pest.1994.1056
Niderman T, Genetet I, Bruyère T et al (1995) Pathogenesis-related PR-1 proteins are antifungal. Plant Physiol 108:17–27. https://doi.org/10.1104/pp.108.1.17
Novotny V, Miller SE, Baje L et al (2010) Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest: plant-herbivore food webs in tropical forest. J Anim Ecol 79:1193–1203. https://doi.org/10.1111/j.1365-2656.2010.01728.x
Ojala T, Remes S, Haansuu P et al (2000) Antimicrobial activity of some coumarin containing herbal plants growing in Finland. J Ethnopharmacol 73:299–305. https://doi.org/10.1016/S0378-8741(00)00279-8
Ojo OA, Ajiboye BO, Ojo AB et al (2014) Phytochemical, proximate analysis and mineral composition of aqueous crude extract of Ficus asperifolia Miq. J Adv Med Life Sci 1:1–4. https://doi.org/10.5281/zenodo.1000388
Oliveira AP, Valentão P, Pereira JA et al (2009) Ficus carica L.: metabolic and biological screening. Food Chem Toxicol 47:2841–2846. https://doi.org/10.1016/j.fct.2009.09.004
Oliveira AP, Silva LR, Ferreres F et al (2010a) Chemical assessment and in vitro antioxidant capacity of Ficus carica latex. J Agric Food Chem 58:3393–3398. https://doi.org/10.1021/jf9039759
Oliveira AP, Silva LR, Guedes de Pinho P et al (2010b) Volatile profiling of Ficus carica varieties by HS-SPME and GC–IT–MS. Food Chem 123:548–557. https://doi.org/10.1016/j.foodchem.2010.04.064
Oliveira AP, Baptista P, Andrade PB et al (2012) Characterization of Ficus carica L. cultivars by DNA and secondary metabolite analysis: is genetic diversity reflected in the chemical composition? Food Res Int 49:710–719. https://doi.org/10.1016/j.foodres.2012.09.019
Pathak MA, Daniels F Jr, Fitzpatrick TB (1962) The presently known distribution of furocoumarins (psoralens) in plants. J Investig Dermatol 39:225–239. https://doi.org/10.1038/jid.1962.106
Patil Vikas V, Bhangale SC, Patil VR (2010) Evaluation of anti-pyretic potential of Ficus carica leaves. Evaluation 2:48–50
Peraza-Sánchez SR, Chai H-B, Shin YG et al (2002) Constituents of the leaves and twigs of Ficus hispida. Planta Med 68:186–188. https://doi.org/10.1055/s-2002-20257
Peumans WJ, Van Damme EJM (1995) Lectins as plant defense proteins. Plant Physiol 109:347–352. https://doi.org/10.1104/pp.109.2.347
Pierantoni M, Tenne R, Rephael B et al (2018) Mineral deposits in Ficus leaves: morphologies and locations in relation to function. Plant Physiol 176:1751–1763. https://doi.org/10.1104/pp.17.01516
Prychid CJ, Rudall PJ, Gregory M (2003) Systematics and biology of silica bodies in monocotyledons. Bot Rev 69:377–440. https://doi.org/10.1663/0006-8101(2004)069[0377:SABOSB]2.0.CO;2
Roberts WK, Selitrennikoff CP (1988) Plant and bacterial chitinases differ in antifungal activity. J Gen Microbiol 134:169–176. https://doi.org/10.1099/00221287-134-1-169
Roberts DM, Gallapatthy G, Dunuwille A, Chan BS (2016) Pharmacological treatment of cardiac glycoside poisoning: cardenolide poisoning. Br J Clin Pharmacol 81:488–495. https://doi.org/10.1111/bcp.12814
Roselli S, Olry A, Vautrin S et al (2017) A bacterial artificial chromosome (BAC) genomic approach reveals partial clustering of the furanocoumarin pathway genes in parsnip. Plant J 89:1119–1132. https://doi.org/10.1111/tpj.13450
Rubnov S, Kashman Y, Rabinowitz R et al (2001) Suppressors of cancer cell proliferation from Fig (Ficus carica) resin: isolation and structure elucidation. J Nat Prod 64:993–996. https://doi.org/10.1021/np000592z
Ruiz N, Ward D, Saltz D (2002) Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defence? Funct Ecol 16:99–105. https://doi.org/10.1046/j.0269-8463.2001.00594.x
Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28:425–449. https://doi.org/10.1146/annurev.py.28.090190.002233
Saeed MA, Sabir AW (2002) Irritant potential of triterpenoids from Ficus carica leaves. Fitoterapia 73:417–420. https://doi.org/10.1016/S0367-326X(02)00127-2
Schaller A, Stintzi A, Rivas S et al (2018) From structure to function—a family portrait of plant subtilases. New Phytol 218:901–915. https://doi.org/10.1111/nph.14582
Schlumbaum A, Mauch F, Vögeli U, Boller T (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324:365–367. https://doi.org/10.1038/324365a0
Sethi A, McAuslane HJ, Rathinasabapathi B et al (2009) Enzyme induction as a possible mechanism for latex-mediated insect resistance in romaine lettuce. J Chem Ecol 35:190–200. https://doi.org/10.1007/s10886-009-9596-6
Sgarbieri VC, Gupte SM, Kramer DE, Whitaker JR (1964) Ficus enzymes I. Separation of the proteolytic enzymes of Ficus carica and Ficus glabrata latices. J Biol Chem 239:2170–2177
Sirisha N, Sreenivasulu M, Sangeeta K, Chetty CM (2010) Antioxidant properties of Ficus species—a review. Int J PharmTech Res 2:2174–2182
Skalicka-Wozniak K, Los R, Glowniak K, Malm A (2009) Volatile compounds in fruits of Peucedanum cervaria (Lap.) L. Chem Biodivers 6:1087–1092. https://doi.org/10.1002/cbdv.200800236
Smith DL, Watt WM (1986) Distribution of lithocysts, trichomes, hydathodes and stomata in leaves of Pilea cadierei Gagnep. & Guill. (Urticaceae). Ann Bot 58:155–166. https://doi.org/10.1093/oxfordjournals.aob.a087193
Smyth TJP, Ramachandran V, Brooks P, Smyth WF (2012) Investigation of antibacterial phytochemicals in the bark and leaves of Ficus coronata by high-performance liquid chromatography-electrospray ionization-ion trap mass spectrometry (HPLC-ESI-MSn) and ESI-MSn. Electrophoresis 33:713–718. https://doi.org/10.1002/elps.201100302
Solomon A, Golubowicz S, Yablowicz Z et al (2006) Antioxidant activities and anthocyanin content of fresh fruits of common Fig (Ficus carica L.). J Agric Food Chem 54:7717–7723. https://doi.org/10.1021/jf060497h
Son J-H, Jin H, You H-S et al (2017) Five cases of phytophotodermatitis caused by fig leaves and relevant literature review. Ann Dermatol 29:86–90. https://doi.org/10.5021/ad.2017.29.1.86
Sosnovsky Y (2016) Sucking herbivore assemblage composition on greenhouse Ficus correlates with host plant leaf architecture. Arthropod Plant Interact 10:55–69. https://doi.org/10.1007/s11829-015-9408-6
Stintzi A, Heitz T, Prasad V et al (1993) Plant ‘pathogenesis-related’ proteins and their role in defense against pathogens. Biochimie 75:687–706. https://doi.org/10.1016/0300-9084(93)90100-7
Strömberg CAE, Di Stilio VS, Song Z (2016) Functions of phytoliths in vascular plants: an evolutionary perspective. Funct Ecol 30:1286–1297. https://doi.org/10.1111/1365-2435.12692
Taira T, Ohdomari A, Nakama N et al (2005) Characterization and antifungal activity of Gazyumaru (Ficus microcarpa) latex chitinases: both the chitin-binding and the antifungal activities of class I chitinase are reinforced with increasing ionic strength. Biosci Biotechnol Biochem 69:811–818. https://doi.org/10.1271/bbb.69.811
Takahashi T, Okiura A, Saito K, Kohno M (2014) Identification of phenylpropanoids in fig (Ficus carica L.) leaves. J Agric Food Chem 62:10076–10083. https://doi.org/10.1021/jf5025938
Takahashi T, Okiura A, Kohno M (2017) Phenylpropanoid composition in fig (Ficus carica L.) leaves. J Nat Med 71:770–775. https://doi.org/10.1007/s11418-017-1093-6
Teixeira DM, Patão RF, Coelho AV, da Costa CT (2006) Comparison between sample disruption methods and solid–liquid extraction (SLE) to extract phenolic compounds from Ficus carica leaves. J Chromatogr A 1103:22–28. https://doi.org/10.1016/j.chroma.2005.11.047
Teixeira DM, Canelas VC, do Canto AM et al (2009) HPLC-DAD quantification of phenolic compounds contributing to the antioxidant activity of Maclura pomifera, Ficus carica and Ficus elastica extracts. Anal Lett 42:2986–3003. https://doi.org/10.1080/00032710903276646
Terras F, Schoofs H, Thevissen K et al (1993) Synergistic enhancement of the antifungal activity of wheat and barley thionins by radish and oilseed rape 2S albumins and by barley trypsin inhibitors. Plant Physiol 103:1311–1319. https://doi.org/10.1104/pp.103.4.1311
Traw BM, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532. https://doi.org/10.1007/s00442-002-0924-6
Ummu-Hani B, Noraini T (2013) The structure of cystoliths in selected taxa of the genus Ficus L. (Moraceae) in Peninsular Malaysia. AIP Conf Proc 1571:372–376. https://doi.org/10.1063/1.4858686
Van Damme EJM, Peumans WJ, Barre A, Rougé P (1998) Plant lectins: a composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Crit Rev Plant Sci 17:575–692. https://doi.org/10.1080/07352689891304276
Vaya J, Mahmood S (2006) Flavonoid content in leaf extracts of the fig (Ficus carica L.), carob (Ceratonia siliqua L.) and pistachio (Pistacia lentiscus L.). BioFactors 28:169–175. https://doi.org/10.1002/biof.5520280303
Volf M, Hrcek J, Julkunen-Tiitto R, Novotny V (2015) To each its own: differential response of specialist and generalist herbivores to plant defence in willows. J Anim Ecol 84:1123–1132. https://doi.org/10.1111/1365-2656.12349
Volf M, Segar ST, Miller SE et al (2018) Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus. Ecol Lett 21:83–92. https://doi.org/10.1111/ele.12875
Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96:675–679. https://doi.org/10.1104/pp.96.3.675
Wahler D, Gronover CS, Richter C et al (2009) Polyphenoloxidase silencing affects latex coagulation in Taraxacum species. Plant Physiol 151:334–346. https://doi.org/10.1104/pp.109.138743
Wang T, Jiao J, Gai Q-Y et al (2017) Enhanced and green extraction polyphenols and furanocoumarins from Fig (Ficus carica L.) leaves using deep eutectic solvents. J Pharm Biomed Anal 145:339–345. https://doi.org/10.1016/j.jpba.2017.07.002
Ward D, Spiegel M, Saltz D (1997) Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. J Chem Ecol 23:333–346. https://doi.org/10.1023/B:JOEC.0000006363.34360.9d
Weddell HA (1854) Sur les cystolithes ou concrétions calcaires des Urticées et d’autres végétaux. In: Annales des Sciences Naturelles. Botanique. Masson, 1854, Paris, pp 267–272
Wu CC, Kuo-Huang LL (1997) Calcium crystals in the leaves of some species of Moraceae. Bot Bull Acad Sin 38:97–104
Wu P-L, Rao KV, Su C-H et al (2002) Phenanthroindolizidine alkaloids and their cytotoxicity from the leaves of Ficus septica. Heterocycles 57:2401–2408. https://doi.org/10.3987/COM-02-9615
Xiang H, Chen J (2004) Interspecific variation of plant traits associated with resistance to herbivory among four species of Ficus (Moraceae). Ann Bot 94:377–384. https://doi.org/10.1093/aob/mch153
Yap VA, Loong B-J, Ting K-N et al (2015) Hispidacine, an unusual 8,4′-oxyneolignan-alkaloid with vasorelaxant activity, and hispiloscine, an antiproliferative phenanthroindolizidine alkaloid, from Ficus hispida Linn. Phytochemistry 109:96–102. https://doi.org/10.1016/j.phytochem.2014.10.032
Yap VA, Qazzaz ME, Raja VJ et al (2016) Fistulopsines A and B antiproliferative septicine-type alkaloids from Ficus fistulosa. Phytochem Lett 15:136–141. https://doi.org/10.1016/j.phytol.2015.12.007
Yarosh EA, Nikonov GK (1973) The coumarins of the genus Ficus. Chem Nat Compd 9:255–256. https://doi.org/10.1007/BF00563357
Yoshihara T, Sogawa K, Pathak MD et al (1980) Oxalic acid as a sucking inhibitor of the brown planthopper in rice (Delphacidae, Homoptera). Entomol Exp Appl 27:149–155. https://doi.org/10.1111/j.1570-7458.1980.tb02959.x
Zangerl AR, Berenbaum MR (1990) Furanocoumarin induction in wild parsnip—genetics and populational variation. Ecology 71:1933–1940. https://doi.org/10.2307/1937601
Zaynoun ST, Aftimos BG, Ali LA et al (1984) Ficus carica; isolation and quantification of the photoactive components. Contact Dermat 11:21–25. https://doi.org/10.1111/j.1600-0536.1984.tb00164.x
Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858. https://doi.org/10.1104/pp.107.112177
Zumwalt JG, Neal JJ (1993) Cytochromes P450 from Papilio polyxenes: adaptations to host plant allelochemicals. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 106:111–118. https://doi.org/10.1016/0742-8413(93)90261-I
Acknowledgements
The authors acknowledge the JSPS Overseas Research Fellowships (R.M.) and the “Impact Biomolecules” project of the “Lorraine Université d’Excellence” (Investissements d’avenir—ANR) for financial support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Villard, C., Larbat, R., Munakata, R. et al. Defence mechanisms of Ficus: pyramiding strategies to cope with pests and pathogens. Planta 249, 617–633 (2019). https://doi.org/10.1007/s00425-019-03098-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-019-03098-2