Skip to main content
SpringerLink
Log in

Diversity and evolution of secretory structures in Sapindales

  • Structural Botany - Review Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

A Correction to this article was published on 08 February 2022

This article has been updated

Abstract

Sapindales comprise nine families with a mainly tropical distribution and include numerous species of high economic importance. Members of this order are known for the production of chemical constituents with medicinal properties, such as antioxidant, anti-inflammatory, and antimicrobial activity, as well as species with insecticidal properties. Such diversity of chemical compounds is attributed to a variety of secretory structures, which may occur in both vegetative and reproductive organs. During the past decades, tremendous progress has been made in anatomical and analytical chemistry studies, which has led to the next level of knowledge regarding the secretory structures of Sapindales. This comprehensive review embraces the most important data of the secretory structures of Sapindales: ducts, cavities, laticifers, floral and extrafloral nectaries, osmophores, colleters, idioblasts, and trichomes. Our review comprises structural, functional, and evolutionary aspects of these glands, which are fundamental for further studies of the diversification within Sapindales.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

Change history

References

  • Acevedo-Rodriguez P (1993a) A revision of Lophostigma (Sapindaceae). Syst Bot 18:379–388

    Article  Google Scholar 

  • Acevedo-Rodríguez P (1993b) Systematics of Serjania (Sapindaceae). Part I: a revision of Serjania sect. Platycoccus. Mem N Y Bot Gard 67:1–93

    Google Scholar 

  • Acevedo-Rodríguez P, van Welzen PC, Adema F, van der Ham RWJM (2011) Sapindaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Volume X. Flowering plants. Eudicots. Sapindales, Cucurbitales, Myrtales. Springer, Berlin, pp 357–407

  • Acevedo-Rodríguez P, Wurdack KJ, Ferrucci MS et al (2017) Generic relationships and classification of Tribe Paullinieae (Sapindaceae) with a new concept of Supertribe Paulliniodae. Syst Bot 42:96–114

    Article  Google Scholar 

  • Agarwal M, Gupta S (2008) Wood anatomy of Sapindales. Bishen Singh Mahendra Pal Singh, Dehra Dun

  • Aguilar-Ortigoza CS, Sosa V (2004) The evolution of toxic phenolic compounds in a group of Anacardiaceae genera. Taxon 53:357–364

    Article  Google Scholar 

  • Aguilar-Ortigoza CS, Sosa V, Aguilar-Ortigoza M (2003) Toxic phenols in various Anacardiaceae species. Econ Bot 57:354–364

    Article  CAS  Google Scholar 

  • Alves GGN (2015) Estudos estruturais como subsídio à taxonomia de Simaba Aubl. (Simaroubaceae). Master Thesis, Universidade de São Paulo, São Paulo

  • Alves IABS, Miranda HM, Soares LAL, Randau KP (2014) Simaroubaceae family: botany, chemical composition and biological activities. Rev Bras Farmacogn 24:481–501

    Article  CAS  Google Scholar 

  • Alves GGN, El Ottra JHL, Devecchi MF, Demarco D, Pirani JR (2017) Structure of the flower of Simaba (Simaroubaceae) and its anatomical novelties. Bot J Linn Soc 183:162–176

    Google Scholar 

  • Alves GGN, Fonseca LHM, Devecchi MF, El Ottra JHL, Demarco D, Pirani JR (2021) What reproductive traits tell us about the evolution and diversification of the Tree-of-Heaven family, Simaroubaceae. Braz J Bot 6:66

    Google Scholar 

  • Amini T, Zare H, Assadi M (2008) Acer mazandaranicum (Aceraceae), a new species from Northern Iran. Iran J Bot 14:81–86

    Google Scholar 

  • Andrade CRB, Martins FM, Brandão HN, Alves CK, Freitas-Silva L (2020) Leaf anatomy and histochemistry of secretory structures of Zanthoxylum caribaeum Lam. (Rutaceae). Braz J Bot 43:961–968

    Article  Google Scholar 

  • Andreeva AV, Kutuzov MA, Evans DE, Hawes CR (1998) The structure and function of Golgi apparatus: a hundred years of questions. J Exp Bot 49:1281–1291

    Article  CAS  Google Scholar 

  • APG (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  • Appelhans MS, Smets E, Razafimandimbison SG, Haevermans T, van Marle EJ, Couloux A, Rabarison H, Randrianarivelojosia M, Keßler PJA (2011) Phylogeny, evolutionary trends and classification of the Spathelia-Ptaeroxylon clade: morphological and molecular insights. Ann Bot 107:1259–1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aragão GF, Cunha MC, Nogueira P, Gomes TL, Barros V (2008) Analgesic and anti-inflammatory activities of the isomeric mixture of alpha- and beta-amyrin from Protium heptaphyllum (Aubl.) March. J Herbal Pharmacother 7:31–47

    Article  Google Scholar 

  • Avalos AA, Lattar EC, Galati BG, Ferrucci MS (2017) Nectary structure and ultrastructure in two floral morphs of Koelreuteria elegans subsp. formosana (Sapindaceae). Flora 226:29–37

    Article  Google Scholar 

  • Babu AM, John P, Nair GM (1990) Ultrastructure of gum-resin secreting cells in the pith of Ailanthus excelsa Roxb. Acta Bot Neerl 38:389–398

    Article  Google Scholar 

  • Bachelier JB, Endress PK (2008) Floral structure of Kirkia (Kirkiaceae) and its position in Sapindales. Ann Bot 102:539–550

    Article  PubMed  PubMed Central  Google Scholar 

  • Bachelier JB, Endress PK (2009) Comparative floral morphology and anatomy of Anacardiaceae and Burseraceae (Sapindales), with a special focus on gynoecium structure and evolution. Bot J Linn Soc 159:499–571

    Article  Google Scholar 

  • Bachelier JB, Endress PK, Ronse De Craene LP (2011) Comparative floral structure and development of Nitrariaceae (Sapindales) and systematic implications. In: Wanntorp L, Ronse De Craene LP (eds) Flowers on the tree of life. Cambridge University Press, New York, pp 181–217

  • Bakker ME, Gerritsen AF (1992) The development of mucilage cells in Hibiscus schizopetalus. Acta Bot Neerl 41:31–42

    Article  Google Scholar 

  • Becerra JX (2003) Evolution of Mexican Bursera (Burseraceae) inferred from ITS, ETS, and 5S nuclear ribosomal DNA sequences. Mol Phylogenet Evol 26:300–309

    Article  CAS  PubMed  Google Scholar 

  • Behl P, Captain RM (1979) Skin-irritant and sensitizing plants found in India. S. Chand & Co, New Delhi

    Google Scholar 

  • Benedict AH (1961) The floral anatomy of Dipteronia. Am J Bot 48:918–924

    Article  Google Scholar 

  • Bennici A, Tani C (2004) Anatomical and ultrastructural study of the secretory cavity development of Citrus sinensis and Citrus limon: evaluation of schizolysigenous ontogeny. Flora 199:464–475

    Article  Google Scholar 

  • Boer E, Ella AB (2000) Plant resources of South-East Asia. No. 18. Plants producing exudates. Backhuys Publishers, Leiden

  • Bory G, Clair-Maczulajtys D (1990) Importance of foliar nectaries in the physiology of tree of heaven (Ailanthus glandulosa Desf., Simaroubaceae). Bull Soc Bot Fr Lett Bot 137:139–155

    Google Scholar 

  • Bosabalidis A, Tsekos I (1982a) Ultrastructural studies on the secretory cavities of Citrus deliciosa Ten. I Early stages of the gland cells differentiation. Protoplasma 112:55–62

    Article  Google Scholar 

  • Bosabalidis A, Tsekos I (1982b) Ultrastructural studies on the secretory cavities of Citrus deliciosa Ten. II Development of the essential oil–accumulating central space of the gland and process of active secretion. Protoplasma 112:63–70

    Article  Google Scholar 

  • Boudouris J, Queenborough SA (2013) Diversity and distribution of extra-floral nectaries in the Cerrado savanna vegetation of Brazil. PeerJ 1:e219

    Article  PubMed  PubMed Central  Google Scholar 

  • Burris TP, Montrose C, Houck KA, Osborne HE, Bocchinfuso WP, Yaden BC, Cheng CC, Zink RW, Barr RJ, Hepler CD, Krishnan V, Bullock HA, Burris LL, Galvin RJ, Bramlett K, Stayrook KR (2005) The hypolipidemic natural product guggulsterone is a promiscuous steroid receptor ligand. Mol Pharmacol 67:948–954

    Article  CAS  PubMed  Google Scholar 

  • Bussel BM, Considine JA, Spadek ZE (1995) Flower and volatile oil ontogeny in Boronia megastigma. Ann Bot 76:457–463

    Article  Google Scholar 

  • Caris P, Smets E, De Coster K, Ronse De Craene LP (2006) Floral ontogeny of Cneorum tricoccon L. (Rutaceae). Plant Syst Evol 257:223–232

    Article  Google Scholar 

  • Champagne DE, Koul O, Isman MB, Scudder GGE, Towers GHN (1992) Biological activity of limonoids from the Rutales. Phytochemistry 31:377–394

    Article  CAS  Google Scholar 

  • Chauveau O, Eggers L, Raquin C, Silvério A, Brown S, Couloux A, Cruaud C, Kaltchuk-Santos E, Yockteng R, Souza-Chies TT, Nadot S (2011) Evolution of oil-producing trichomes in Sisyrinchium (Iridaceae): insights from the first comprehensive phylogenetic analysis of the genus. Ann Bot 107:1287–1312

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Wu H (2010) Programmed cell death involved in the schizolysigenous formation of the secretory cavity in Citrus sinensis L. (Osbeck). Chin Sci Bull 55:2160–2168

    Article  CAS  Google Scholar 

  • Chen T, Wiemer D, Howard JJ (2005) A volatile leafcutter ant repellent from Astronium graveolens. Naturwissenschaften 71:97–98

    Article  Google Scholar 

  • Clark TP (1990) Studies in Trichilia—Walsura complex (Meliaceae). PhD Dissertation, Oxford University, Oxford

  • Clayton JW (2011) Simaroubaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Volume X. Flowering plants. Eudicots. Sapindales, Cucurbitales, Myrtales. Springer, Berlin, pp 408–423

  • Cojocaru M, Droby S, Glotter E, Goldman A, Gottlieb HE, Jacoby B, Prusky D (1986) 5-(12-heptadecenyl)-resorcinol, the major component of the antifungal activity in the peel of mango fruit. Phytochemistry 25:1093–1095

    Article  CAS  Google Scholar 

  • Cortez PA, Ferreira CL, Santos GNH, Pirani JR, Urbano KD, Devecchi MF, Cruz R, Gabia VS, Melo-de-Pinna GFA (2021) Strategies for the protection of shoot buds in phanerophyte and geophyte species of Homalolepis Turcz. (Simaroubaceae, Sapindales). Braz J Bot. https://doi.org/10.1007/s40415-021-00757-1

    Article  Google Scholar 

  • Corthout J, Pieters LA, Claeys M, Vanden Berghe DA, Vlietinck AJ (1991) Antiviral ellagitannins from Spondias mombin. Phytochemistry 30:1129–1130

    Article  CAS  Google Scholar 

  • Corthout J, Pieters LA, Claeys M, Vanden Berghe DA, Vlietinck AJ (1992) Antiviral caffeoyl esters from Spondias mombin. Phytochemistry 31:1979–1981

    Article  CAS  Google Scholar 

  • Corthout J, Pieters LA, Claeys M, Geerts S, Vanden Berghe D, Vlietninck AJ (1994) Antibacterial and molluscicidal phenolic acids from Spondias mombin. Planta Med 60:460–463

    Article  CAS  PubMed  Google Scholar 

  • Costa ER, Tangerina MMP, Ferreira MJP, Demarco D (2021) Two origins, two functions: the discovery of distinct secretory ducts formed during the primary and secondary growth in Kielmeyera. Plants 10:877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz R, Duarte M, Pirani JR, Melo-de-Pina GFA (2017) Phylogenetic analysis and evolution of morphological characters in Metrodorea and related species in Rutoideae (Rutaceae). Plant Syst Evol 303:927–943

    Article  Google Scholar 

  • Cunha-Neto IL, Martins FM, Sommer GV, Tamaio N (2017) Secretory structures in stems of five lianas of Paullinieae (Sapindaceae): morphology and histochemistry. Flora 235:29–40

    Article  Google Scholar 

  • Dahlgren R, Van Wyk AE (1988) Structures and relationships of families endemic to or centered in southern Africa. Monogr Syst Bot Mo Bot Gard 25:1–94

    Google Scholar 

  • Daly DC, Harley MM, Martínez-Habibe MC, Weeks A (2011) Burseraceae. In: Kubitzki K (ed) The families and genera of vascular plants. Volume X. Flowering plants. Eudicots. Sapindales, Cucurbitales, Myrtales. Springer, Berlin, pp 76–104

  • Damasceno GAB, Souto AL, da Silva IB, Roque A, Ferrari M, Giordani RB (2018) Prosopis juliflora: phytochemical, toxicological, and allelochemicals. In Merillon JM, Ramawat K (eds) Co-evolution of secondary metabolites. Reference series in phytochemistry. Springer, Cham, pp 1–21

  • Dayanandan P, Ponsamuel J (2000) Ultrastructure of terpenoid secretory cells of neem (Azadirachta indica A. Juss.). In: Gupta PD, Yamamoto H (eds) Electron Microscopy in medicine and biology. Science Pub Inc, Oxford, pp 179–195

    Google Scholar 

  • De-Paula OC, Sajo MG (2011) Morphology and development of anthers and ovules in Croton and Astraea (Euphorbiaceae). Nord J Bot 29:505–511

    Article  Google Scholar 

  • Dede RA (1962) Foliar venation patterns in the Rutaceae. Am J Bot 49:490–497

    Article  Google Scholar 

  • Dell B, McComb AJ (1979) Plant resins—their formation, secretion and possible functions. Adv Bot Res 6:277–316

    Article  Google Scholar 

  • Demarco D (2017) Floral glands in asclepiads: structure, diversity and evolution. Acta Bot Bras 31:477–502

    Article  Google Scholar 

  • Demarco D, Carmello-Guerreiro SM (2011) Pericarp ontogeny and histochemistry of the exotesta and pseudocaruncle of Euphorbia milii (Euphorbiaceae). Rodriguésia 62:477–489

    Article  Google Scholar 

  • Devecchi MF, Pirani JR (2015) A new species of Simaba sect. Grandiflorae (Simaroubaceae) from Jalapão region, Tocantins. Brazil Phytotaxa 227:167–174

    Article  Google Scholar 

  • Díaz M, Rossini C (2012) Bioactive natural products from Sapindaceae deterrent and toxic metabolites against insects. In: Perveen F (ed) Insecticides—pest engineering. IntechOpen, London, pp 287–308

    Google Scholar 

  • Drewes SE, Horn MM, Mabaso NJ (1998) Loxostylis alata and Smodingium argutum—a case of phytochemical bedfellows? S Afr J Bot 64:128–129

    Article  CAS  Google Scholar 

  • Dreyer DI (1983) Limonoids of the Rutaceae. In: Waterman PG, Grundon MF (eds) Chemistry and chemical taxonomy of the Rutales. Academic Press, London, pp 215–245

    Google Scholar 

  • Dünisch O, Bass P (2006) On the origin of intercellular canals in the secondary xylem of selected Meliaceae species. IAWA J 27:281–297

    Article  Google Scholar 

  • El Ottra JHL, Demarco D, Pirani JR (2019) Comparative floral structure and evolution in Galipeinae (Galipeeae: Rutaceae) and its implications at different systematic levels. Bot J Linn Soc 191:30–101

    Article  Google Scholar 

  • Elias TS (1983) Extrafloral nectaries: their structure and distribution. In: Bentley B, Elias TS (eds) The biology of nectaries. Columbia University Press, New York, pp 174–203

    Google Scholar 

  • Engler A (1931) Rutaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, 2nd edn. Engelmann, Leipzig, pp 187–359

    Google Scholar 

  • Faegri K, van der Pijl L (1979) The principles of pollination ecology, 3rd edn. Pergamon Press, Oxford

    Google Scholar 

  • Fahn A (1979) Secretory tissue in plants. Academic Press, London

    Google Scholar 

  • Fahn A (1990) Plant anatomy. Pergamon Press, Oxford

    Google Scholar 

  • Fang X, Zhang Y, Wang M, Li P, Zhang Q, Si J, Wei B, Miao Y, Tian L, Cai X (2019) Lysosome and proteasome pathways are distributed in laticifers of Euphorbia helioscopia L. Physiol Plant 166:1026–1038

    Article  CAS  PubMed  Google Scholar 

  • Farsam H, Amanlou M, Reza Dehpour A, Jahaniani F (2000) Anti-inflammatory and analgesic activity of Biebersteinia multifida DC. root extract. J Ethnopharmacol 71:443–447

    Article  CAS  PubMed  Google Scholar 

  • Fiala B, Linsenmair E (1995) Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia. Biodivers Conserv 4:165–182

    Article  Google Scholar 

  • Fine PVA, Daly DC, Muñoz GV, Mesones I, Cameron KM (2005) The contribution of edaphic heterogeneity to the evolution and diversity of Burseraceae trees in the western Amazon. Evolution 59:1464–1478

    PubMed  Google Scholar 

  • Fisher JB, Rutishauser R (1990) Leaves and epiphyllous shoots in Chisocheton (Meliaceae): a continuum of woody leaf and stem axes. Can J Bot 68:2316–2328

    Article  Google Scholar 

  • Franco MJCS, Albiero ALM (2018) Estruturas secretoras em folha e caule de Esenbeckia febrifuga (A.St.-Hil.) A. Juss. ex Mart. e Esenbeckia grandiflora Mart. (Rutaceae). Hoehnea 45:468–483

    Article  Google Scholar 

  • Gadek PA, Fernando ES, Quinn CJ, Hoot SB, Terrazas T, Sheahan MC, Chase MW (1996) Sapindales: Molecular delimitation and infraordinal groups. Am J Bot 83:802–811

    Article  Google Scholar 

  • Gama TSS, Rubiano VS, Demarco D (2017) Laticifer development and its growth mode in Allamanda blanchetii A. DC. (Apocynaceae). J Torrey Bot Soc 144:303–312

    Article  Google Scholar 

  • Gama TSS, Cordeiro I, Demarco D (2019) Floral structure and development in Alchornea sidifolia (Acalyphoideae) and the evolution of wind pollination in Euphorbiaceae. Braz J Bot 42:307–317

    Article  Google Scholar 

  • Gama RL, Muellner-Riehl AN, Demarco D, Pirani JR (2021a) Evolution of reproductive traits in the mahagony family (Meliaceae). J Syst Evol 59:21–43

    Article  Google Scholar 

  • Gama RL, El Ottra JHL, Pirani JR, Demarco D (2021b) Gynodioecy in Trichilia (Meliaceae) and a peculiar case of male sterility due to tapetal necrotic cell death. Braz J Bot. https://doi.org/10.1007/s40415-021-00746-4

    Article  Google Scholar 

  • Gedalovich E, Fahn A (1985) The development and ultrastructure of gum ducts in Citrus plants formed as a result of brown-rot gummosis. Protoplasma 127:73–81

    Article  Google Scholar 

  • Giuliani C, Bini LM, Lippi MM (2012) Two structures and functions in the nectary of frankincense tree (Boswellia sacra Flueck.). Flora 207:74–79

    Article  Google Scholar 

  • Gouvêa CF, Dornelas MC, Rodriguez APM (2008) Floral development in the tribe Cedreleae (Meliaceae sub–family Swietenioideae): Cedrela and Toona. Ann Bot 101:39–48

    Article  PubMed  Google Scholar 

  • Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Isr J Bot 38:125–174

    Google Scholar 

  • Gut BJ (1966) Beiträge zur Morphologie des Gynoeciums und der Blütenachse einiger Rutaceen. Bot Jahrb Syst 85:151–247

    Google Scholar 

  • Hegnauer R (1990) Chemotaxonomie der Pflanzen, Bd. 9. Birkhäuser, Basel

  • Heimsch C Jr (1942) Comparative anatomy of the secondary xylem in the “Gruinales” and “Terebinthales”, of Wettstein with reference to taxonomic grouping. Lilloa 8:83–198

    Google Scholar 

  • Heinrich G, Schultze W (1985) Composition and site of biosynthesis of the essential oil in fruits of Phellodendron amurense Rupr. (Rutaceae). Isr J Bot 34:205–217

    CAS  Google Scholar 

  • Inamdar JA, Murugan V, Subramanian RB (1988) Ultrastructure of non-articulated laticifers in Allamanda violacea. Ann Bot 62:583–588

    Article  Google Scholar 

  • Joel DM, Fahn A (1980a) Ultrastructure of the resin ducts of Mangifera indica L. (Anacardiaceae). 3. Secretion of the protein-polysaccharide mucilage in the fruit. Ann Bot 46:785–790

    Article  Google Scholar 

  • Joel DM, Fahn A (1980b) Ultrastructure of the resin ducts of Mangifera indica L. (Anacardiaceae). 1. Differentiation and senescence of the shoot ducts. Ann Bot 46:225–233

    Article  Google Scholar 

  • Kenfak D, Tindo M, Gueye M (2014) Extranuptial nectaries in Carapa Aubl. (Meliaceae-Cedreloideae). Adansonia 36:335–349

    Article  Google Scholar 

  • Koptur S, William P, Olive Z (2010) Ants and plants with extrafloral nectaries in fire successional habitats on Andros (Bahamas). Fla Entomol 93:89–99

    Article  Google Scholar 

  • Knight TG, Klieber A, Sedgley M (2001) The relationship between oil gland and fruit development in Washington navel orange (Citrus sinensis L. Osbeck). Ann Bot 88:1039–1047

    Article  Google Scholar 

  • Kubitzki K (2011) The families and genera of vascular plants. Vol. X. Flowering plants. Eudicots. Sapindales, Cucurbitales, Myrtales. Springer, Berlin

  • Lacchia APS, Carmello-Guerreiro SM (2009) Aspectos ultra-estruturais dos canais secretores em órgãos vegetativos e reprodutivos de Anacardiaceae. Acta Bot Bras 23:376–388

    Article  Google Scholar 

  • Lacchia APS, Tölke ED, Demarco D, Carmello-Guerreiro SM (2016a) Presumed domatia are actually extrafloral nectaries on leaves of Anacardium humile (Anacardiaceae). Rodriguésia 67:19–28

    Article  Google Scholar 

  • Lacchia APS, Tölke ED, Carmello-Guerreiro SM, Ascensão L, Demarco D (2016b) Foliar colleters in Anacardiaceae: first report for the family. Botany 94:337–346

    Article  CAS  Google Scholar 

  • Langenheim JH (2005) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280

    Article  Google Scholar 

  • Lersten NR (1974) Morphology and distribution of colleters and crystals in relation to the taxonomy and bacterial leaf nodule symbiosis of Psychotria (Rubiaceae). Am J Bot 61:973–981

    Article  Google Scholar 

  • Lersten NR, Pohl RW (1985) Extrafloral nectaries in Cipadessa (Meliaceae). Ann Bot 56:363–366

    Article  Google Scholar 

  • Lersten NR, Rugenstein SR (1982) Foliar nectaries in Mahogany (Swietenia Jacq.). Ann Bot 49:397–401

    Article  Google Scholar 

  • Li JX, Baskin JM, Baskin CC (1999) Pericarp ontogeny and anatomy in Rhus aromatica Ait. and R. glabra L. (Anacardiaceae). J Torrey Bot Soc 126:279–288

    Article  Google Scholar 

  • Liang S, Wu H, Lun X, Lu D (2006) Secretory cavity development and its relationship with the accumulation of essential oil in fruits of Citrus medica L. var. sarcodactylis (Noot.) Swingle. Acta Bot Sin 48:573–583

    CAS  Google Scholar 

  • Lima MP, Braga PAC, Macedo ML, Silva MFGF, Ferreira AG, Fernandes JB, Vieira PC (2004) Phytochemistry of Trattinnickia burserifolia, T. rhoifolia, and Dacryodes hopkinsii: chemosystematic implications. J Braz Chem Soc 15:385–394

    Article  CAS  Google Scholar 

  • Lima HA, Somner GV, Giulietti AM (2016) Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia. Plant Syst Evol 302:109–120

    Article  Google Scholar 

  • Lima EA, Tölke ED, Silva-Luz CL, Demarco D, Carmello-Guerreiro SM (2021) Fruit morphoanatomy of Astronium Jacq. and Myracrodruon Allemão (Anacardiaceae): taxonomic implications and development of the calycinal wings. Braz J Bot. https://doi.org/10.1007/s40415-021-00732-w

    Article  Google Scholar 

  • Liu WZ, Hu ZH (1998) Comparative anatomy of secretory cavities in leaves of the Rutaceae in China. Acta Phytotax Sin 36:119–127

    Google Scholar 

  • Liu WZ, Zhang H, Hu ZH (1998) Ultrastructural studies on the secretory cavity development and essential oil accumulation in the fruits of Evodia rutaecarpa. J Acta Bot Sin 40:401–404

    CAS  Google Scholar 

  • Liu P, Liang S, Yao N, Wu H (2012) Programmed cell death of secretory cavity cells in fruits of Citrus grandis cv. Tomentosa is associated with activation of caspase 3-like protease. Trees Struct Funct 26:1821–1835

    Article  CAS  Google Scholar 

  • Lv M, Xu P, Tian Y, Liang J, Gao Y, Xu F, Zhang Z, Sun J (2015) Medicinal uses, phytochemistry and pharmacology of the genus Dictamnus (Rutaceae). J Ethnopharmacol 171:247–263

    Article  CAS  PubMed  Google Scholar 

  • Macêdo TP, Cortez PA, Costa LCB (2016) First record of colleters in Zanthoxylum Linn. species (Rutaceae Juss., Sapindales): structural, functional and taxonomic considerations. Flora 224:66–74

    Article  Google Scholar 

  • Machado SR, Canaveze Y, Rodrigues TM (2017) Structure and functioning of oil cavities in the shoot apex of Metrodorea nigra A. St.-Hil. (Rutaceae). Protoplasma 254:1661–1674

    Article  CAS  PubMed  Google Scholar 

  • Marazzi B, Endress PK, Paganucci de Queiroz L, Conti E (2006) Phylogenetic relationships within Senna (Leguminosae, Cassiinae) based on three chloroplast DNA regions: patterns in the evolution of floral symmetry and extrafloral nectaries. Am J Bot 93:288–303

    Article  CAS  PubMed  Google Scholar 

  • Marazzi B, Bronstein JL, Koptur S (2013) The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Ann Bot 111:1243–1250

    Article  PubMed  PubMed Central  Google Scholar 

  • Marinho CR, Oliveira RB, Teixeira SP (2016) The uncommon cavitated secretory trichomes in Bauhinia s.s. (Fabaceae): the same roles in different organs. Bot J Linn Soc 180:104–122

    Article  Google Scholar 

  • Marques JP, Kitajima E, Freitas-Astúa J, Apezzato-da-Glória B (2010) Comparative morpho-anatomical studies of the lesions caused by Citrus leprosis virus on sweet orange. Ann Braz Acad Sci 82:501–511

    Article  Google Scholar 

  • Marques JPR, Amorim L, Silva-Júnior GJ, Spósito MB, Apezzato-daGlória B (2015) Structural and biochemical characteristics of citrus flowers associated with defense against a fungal pathogen. AoB Plants 7:plu090

    Article  CAS  Google Scholar 

  • Marquete O (1981) Anatomia e vascularização foliar e floral de Pilocarpus organensis Occhioni & Rizzini (Rutaceae). Arq Jard Bot RJ 25:117–159

    Google Scholar 

  • Matthews ML, Endress PK (2006) Floral structure and systematics in four orders of rosids, including a broad survey of floral mucilage cells. Pl Syst Evol 260:199–221

    Article  Google Scholar 

  • Medina MC, Sousa-Baena MS, Prado E, Acevedo-Rodríguez P, Dias P, Demarco D (2021) Laticifers in Sapindaceae: structure, evolution and phylogenetic importance. Front Plant Sci 11:612985

    Article  PubMed  PubMed Central  Google Scholar 

  • Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons: leaves, stem, and wood in relation to taxonomy with notes on economic uses. Clarendon Press, Oxford

    Google Scholar 

  • Mitchell JD (1990) The poisonous Anacardiaceae genera of the world. Adv Econ Bot 8:103–129

    Google Scholar 

  • Moore JA (1936) Floral anatomy and phylogeny in the Rutaceae. New Phytol 35:318–322

    Article  Google Scholar 

  • Morellato LPC, Oliveira PS (1991) Distribution of extrafloral nectaries in different vegetation types of Amazonian Brazil. Flora 185:33–38

    Article  Google Scholar 

  • Morellato LPC, Oliveira OS (1994) Extrafloral nectaries in the tropical tree Guarea macrophylla (Meliaceae). Can J Bot 72:157–160

    Article  Google Scholar 

  • Muellner AN (2011) Biebersteiniaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Volume X. Flowering plants. Eudicots. Sapindales, Cucurbitales, Myrtales. Springer, Berlin, pp 72–75

  • Muellner-Riehl AN, Weeks A, Clayton JW, Buerki S, Nauheimer L, Chiang YC, Cody S, Pell SK (2016) Molecular phylogenetics and molecular clock dating of Sapindales based on plastid rbcL, atpB and trnL-trnF DNA sequences. Taxon 65:1019–1036

    Article  Google Scholar 

  • Mulholland D, Cheplogoi P, Crouch N (2003) Secondary metabolites from Kirkia acuminata and Kirkia wilmsii (Kirkiaceae). Biochem Syst Ecol 31:793–797

    Article  CAS  Google Scholar 

  • Muntoreanu TG, Cruz RS, Melo-de-Pinna GF (2011) Comparative leaf anatomy and morphology of some neotropical Rutaceae: Pilocarpus Vahl and related genera. Plant Syst Evol 296:87–99

    Article  Google Scholar 

  • Muthukumran P, Begumand VH, Kalaiarasan P (2011) Antidiabetic activity of Dodonaea viscosa (L) leaf extracts. Int J Pharm Tech Res 3:136–139

    Google Scholar 

  • Nair MNB, Subrahmanyam SV (1998) Ultrastructure of the epithelial cells and oleogumresin secretion in Boswellia serrata (Burseraceae). IAWA J 19:415–427

    Article  Google Scholar 

  • Nair GM, Venkaiah K, Shah JJ (1983) Ultrastructure of gum-resin ducts in cashew (Anacardium occidentale). Ann Bot 51:297–305

    Article  Google Scholar 

  • Ning-Xi HN, Wu P (2005) The structural and developmental characteristics of floral nectaries of Litchi chinensis and their biological significance. Acta Phytotaxon Sin 44:523–537

    Article  Google Scholar 

  • Nooteboom HP (1962) Generic delimitation in Simaroubaceae tribus Simaroubeae and a conspectus of the genus Quassia L. Blumea 11:509–528

    Google Scholar 

  • Oggero A, Arana MD, Reinoso HE (2016) Comparative morphology and anatomy of the leaf and stem of species of Zanthoxylum (Rutaceae) from Central Argentina. Polibotánica 42:121–136

    Google Scholar 

  • Okoth DA, Akala HM, Johnson JD, Koorbanally NA (2016) Alkyl phenols, alkenyl cyclohexenones and other phytochemical constituents from Lannea rivae (chiov) Sacleux (Anacardiaceae) and their bioactivity. Med Chem Res 25:690–703

    Article  CAS  Google Scholar 

  • Pace MR, Gerolamo CS, Chery JG, Terrazas T, Victorio MP, Cunha-Neto IL, Angyalossy V (2021) The wood anatomy of Sapindales: diversity and evolution of wood characters. Braz J Bot 6:66

    Google Scholar 

  • Paiva EAS (2012) Anatomy, ultrastructure, and secretory activity of the floral nectaries in Swietenia macrophylla (Meliaceae). Am J Bot 99:1910–1917

    Article  PubMed  Google Scholar 

  • Paiva EAS, Buono RA, Delgado MN (2007) Distribution and structural aspects of extrafloral nectaries in Cedrela fissilis (Meliaceae). Flora 202:455–461

    Article  Google Scholar 

  • Palermo FH, Rodrigues MIA, Nicolai J, Machado SR, Rodrigues TM (2018) Resin secretory canals in Protium heptaphyllum (Aubl.) Marchand. (Burseraceae): a tridimensional branched and anastomosed system. Protoplasma 255:899–910

    Article  CAS  PubMed  Google Scholar 

  • Pell SK, Mitchell JD, Miller AJ, Lobova TA (2011) Anacardiaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Volume X. Flowering plants. Eudicots. Sapindales, Cucurbitales, Myrtales. Springer, Berlin, pp 7–50

  • Pickard WF (2008) Laticifers and secretory ducts: two other tube systems in plants. New Phytol 177:877–888

    Article  PubMed  Google Scholar 

  • Pirani JR, El Ottra JHL, Menezes NL (2010) Morfoanatomia de flores de cinco espécies de Galipea Aubl. e seu significado na evolução de flores tubulosas entre as Rutaceae neotropicais. Rev Bras Bot 33:301–318

    Article  Google Scholar 

  • Pirani JR, Majure LC, Devecchi MF (2021) An updated account of Simaroubaceae with emphasis on American taxa. Braz J Bot. https://doi.org/10.1007/s40415-021-00731-x

    Article  Google Scholar 

  • Plowden C, Uhl C, Oliveira FA (2002) Breu resin harvest by Tembé Indians and its dependence on a bark-boring beetle. In: Stepp JR, Wyndham FS, Zarger RK (eds) Ethnobiology and biocultural diversity. University of Georgia Press, Athens, pp 365–380

    Google Scholar 

  • Prado E, Demarco D (2018) Laticifers and secretory ducts: similarities and differences. In: Hufnagel L (ed) Ecosystem services and global ecology. IntechOpen, London, pp 103–123

    Google Scholar 

  • Radlkofer L (1895) Monographie der Sapindaceen – Gattung Paullinia. Verlag der K.B, Akademie, München

    Google Scholar 

  • Rafiei M, Rajaei H (2007) Structural and developmental studies on oil producing reproductive organs in Lime (Citrus aurantifolia Swingle). J Biol Sci 7:848–853

    Article  Google Scholar 

  • Rajput KS, Kothari RK (2005) Formation of gum ducts in Ailanthus excelsa in response to fungal infection. Phyton 45:33–43

    Google Scholar 

  • Rajput KS, Rao KS, Vyas H (2005) Formation of gum ducts in Azadirachta indica A. Juss J Sustain For 20:1–13

    Google Scholar 

  • Ramos MV, Demarco D, Souza ICC, Freitas CDT (2019) Laticifers, latex, and their role in plant defense. Trends Plant Sci 24:553–567

    Article  CAS  PubMed  Google Scholar 

  • Ramos MV, Freitas CDT, Morais FS, Prado E, Medina MC, Demarco D (2020) Plant latex and latex-borne defense. In: Nawrot R (ed) Latex, laticifers and their molecular components: from functions to possible applications. Advances in Botanical Research, Vol 93. Academic Press, Cambridge, pp 1–25

  • Ramp E (1988) Struktur, Funktion und Systematische Bedeutung des Gynoeciums bei dem Rutaceae und Simaroubaceae. Dissertation zur Erlangung der philosophischen Doktorwürde. Universität Zürich, Zürich

  • Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920

    Article  CAS  Google Scholar 

  • Record SJ, Hess RW (1943) Timbers of the New World. Yale University Press, New Haven

    Book  Google Scholar 

  • Ribeiro JC, Ferreira MJP, Demarco D (2017) Colleters in Asclepiadoideae (Apocynaceae): protection of meristems against desiccation and new functions assigned. Int J Plant Sci 178:465–477

    Article  Google Scholar 

  • Ribeiro JC, Tölke ED, Demarco D (2021) Secretory patterns in colleters of Apocynaceae. Plants 6:66

    Google Scholar 

  • Rickson FR, Rickson MM (1998) The cashew nut, Anacardium occidentale (Anacardiaceae), and its perennial association with ants: extrafloral nectary location and the potential for ant defense. Am J Bot 85:835–849

    Article  CAS  PubMed  Google Scholar 

  • Ronse De Craene LP, Haston E (2006) The systematic relationships of glucosinolate-producing plants and related families: a cladistic investigation based on morphological and molecular characters. Bot J Linn Soc 151:453–494

    Article  Google Scholar 

  • Rosalem PF, Picão TB, Rodrigues-Lisoni FC, Martins AR (2017) Leaf anatomy of Protium ovatum and its antiproliferative potential in cervical cells. Rev Bras Farmacog 27:673–678

    Article  Google Scholar 

  • Roy AT, De DN (1992) Studies on differentiation of laticifers through light and electron microscopy in Calotropis gigantea (Linn.) R.Br. Ann Bot 70:443–449

    Article  Google Scholar 

  • Rudall PJ (1987) Laticifers in Euphorbiaceae—a conspectus. Bot J Linn Soc 94:143–163

    Article  Google Scholar 

  • Santos-Silva J, Tozzi AMGA, Simon MF, Urquiza NG, Morales M (2013) Evolution of trichome morphology in Mimosa (Leguminosae—Mimosoideae). Phytotaxa 119:1–20

    Article  Google Scholar 

  • Saunders ER (1934) On carpel polymorphism. VI. Ann Bot 48:643–692

    Article  Google Scholar 

  • Saxena G, McCutcheon AR, Farmer S, Towers GHN, Hancock REW (1994) Antimicrobial constituents of Rhus glabra. J Ethnopharmacol 42:95–99

    Article  CAS  PubMed  Google Scholar 

  • Schmid R (1988) Reproductive versus extra-reproductive nectaries—Historical perspective and terminological recommendations. Bot Rev 54:179–232

    Article  Google Scholar 

  • Schupp EW, Feener DH (1991) Phylogeny, lifeform, and habitat dependence of ant-defended plants in a Panamanian forest. In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 175–197

    Google Scholar 

  • Setia RC, Parthasarahaty MV, Shah JJ (1977) Development, histochemistry and ultrastructure of gum-resin ducts in Commiphora mukul Engl. Ann Bot 41:999–1004

    Article  Google Scholar 

  • Shi HY, Zhou YF, Guo JS, Liu WZ (2011) Development and cytochemistry of secretory ducts in Ailanthus altissima. Acta Bot Boreal-Occid Sin 31:1291–1296

    Google Scholar 

  • Silva TFP (2009) Biologia floral e aspectos botânicos de Serjania pernambucensis Radlk (Sapindaceae). Master Thesis. Universidade Federal do Recôncavo da Bahia, Cruz das Almas

  • Simpson MG (2010) Plant systematics, 2nd edn. Elsevier, San Diego

    Google Scholar 

  • Solereder H (1908) Systematic anatomy of the dicotyledons, vol 1. Clarendon Press, Oxford

    Google Scholar 

  • Solís SM, Ferrucci MS (2006) Comparative leaf morpho-anatomical studies of two South American species of Cardiospermum (Sapindaceae) with special reference to adaxial domatia. Blumea 51:153–164

    Article  Google Scholar 

  • Solís SM, Ferrucci MS (2009) The floral nectary of Cardiospermum grandiflorum and Urvillea chacoënsis (Sapindaceae): morphoanatomy and ontogeny. Ann Bot Fenn 46:485–495

    Article  Google Scholar 

  • Solís SM, Zini LM, González VV, Ferrucci MS (2017) Floral nectaries in Sapindaceae s.s.: morphological and structural diversity, and their systematic implications. Protoplasma 254:2169–2188

    Article  PubMed  Google Scholar 

  • Souza LA (2010) Estruturas secretoras nos órgãos vegetativos aéreos de Paullinia rubiginosa Cambess. (Sapindaceae). Master Thesis. Universidade Federal de Viçosa, Viçosa

  • Souza LA, Moscheta IS, Mourão KSM, Rosa SM (2004) Morphology and anatomy of the flower and anthesis of Metrodorea nigra St. Hill. (Rutaceae). Braz Arch Biol Technol 47:107–112

    Article  Google Scholar 

  • Souza LR, Trindade FG, Oliveira RA, Costa LCB, Gomes VM, Da Cunha M (2016) Histochemical characterization of secretory ducts and essential oil analysis of Protium species (Burseraceae). J Essent Oil Res 28:166–171

    Article  CAS  Google Scholar 

  • Spiekerkoetter H (1924) Untersuchungen zur Anatomie und Systematik ostafrikanischer Meliaceen, Burseraceen und Simarubaceen. Bot Arch 7:274–320

    Google Scholar 

  • Stern WL, Brizicky GK (1960) The morphology and relationships of Diomma, gen. inc. sed. Mem NY Bot Gard 10:38–57

    Google Scholar 

  • Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 14, July 2017 [and more or less continuously updated since]. http://www.mobot.org/MOBOT/research/APweb/

  • Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Ann Bot 68:287–305

    Article  Google Scholar 

  • Thomson WW, Platt-Aloia K, Endress AG (1976) Ultrastructure of oil gland development in the leaf of Citrus sinensis L. Bot Gaz 137:330–340

    Article  Google Scholar 

  • Tilak VD, Nene PM (1976) The disc in the Rutaceae. J Univ Bombay 45:49–53

    Google Scholar 

  • Tillson AH, Bamford R (1938) The floral anatomy of the Aurantioideae. Am J Bot 25:780–793

    Article  Google Scholar 

  • Tilney PM, Nel M, van Wyk AE (2018a) Foliar secretory structures in Melia azedarach (Meliaceae), a widely cultivated and often invasive tree. N Z J Bot 56:198–215

    Article  Google Scholar 

  • Tilney PM, Nel M, van Wyk AE (2018b) Foliar secretory structures in Ekebergia capensis (Meliaceae). Heliyon 4:e00541

    Article  PubMed  PubMed Central  Google Scholar 

  • Tölke EEAD, Galetto L, Machado SR, Lacchia APS, Carmello-Guerreiro SM (2015) Stages of development of the floral secretory disk in Tapirira guianensis Aubl. (Anacardiaceae), a dioecious species. Bot J Linn Soc 179:533–544

    Article  Google Scholar 

  • Tölke ED, Lacchia APS, Demarco D, Carmello-Guerreiro SM (2017) Pericarp ontogeny of Tapirira guianensis Aubl. (Anacardiaceae) reveals a secretory endocarp in young stage. Acta Bot Bras 31:319–329

    Article  Google Scholar 

  • Tölke ED, Bachelier JB, Lima EA, Ferreira MJP, Demarco D, Carmello-Guerreiro SM (2018a) Osmophores and floral fragrance in Anacardium humile and Mangifera indica (Anacardiaceae): an overlooked secretory structure in Sapindales. AoB Plants 10:ply062

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tölke ED, Bachelier JB, Lima EA, Galetto L, Demarco D, Carmello-Guerreiro SM (2018b) Diversity of floral nectary secretions and structure, and implications for their evolution in Anacardiaceae. Bot J Linn Soc 187:209–231

    Article  Google Scholar 

  • Tölke ED, Capelli NV, Pastori T, Alencar AC, Cole TCH, Demarco D (2019) Diversity of floral glands and their secretions in pollinator attraction. In: Mérillon JM, Ramawat KG (eds) Co-evolution of secondary metabolites. Reference Series in Phytochemistry. Springer, Cham, pp 1–46

  • Tölke ED, Lacchia APS, Lima EA, Ascensão L, Demarco D, Carmello-Guerreiro SM (2021) Secretory ducts in Anacardiaceae revisited: updated concepts and new findings based on histochemical evidence. S Afr J Bot 138:394–405

    Article  CAS  Google Scholar 

  • Trachtenberg S, Fahn A (1981) The mucilage cells of Opuntia ficus-indica (L.) Mill.—development, ultrastructure, and mucilage secretion. Bot Gaz 142:206–213

    Article  CAS  Google Scholar 

  • Turner GW (1999) A brief history of the lysigenous gland hypothesis. Bot Rev 65:76–88

    Article  Google Scholar 

  • Turner GW, Berry AM, Gifford EM (1998) Schizogenous secretory cavities of Citrus limon (L.) Burm. F. and a re-evaluation of the lysigenous gland concept. Int J Plant Sci 159:75–88

    Article  Google Scholar 

  • Turner GW, Lange BM (2015) Ultrastructure of grapefruit secretory cavities and immunocytochemical localization of (1)-limonene synthase. Int J Plant Sci 176:643–661

    Article  Google Scholar 

  • van der Walt JJA, van der Schijff HP (1969) The anatomy of the petiole as an aid to the identification of South African Commiphora species. Kirkia 9:95–107

    Google Scholar 

  • Venkaiah K, Shah JJ (1984) Distribution, development and structure of gum ducts in Lannea coromandelica (Houtt.) Merrill. Ann Bot 54:175–186

    Article  Google Scholar 

  • Vitarelli NC, Riina R, Caruzo MBR, Cordeiro I, Fuertes-Aguilar J, Meira RMSA (2015) Foliar secretory structures in Crotoneae (Euphorbiaceae): diversity, anatomy, and evolutionary significance. Am J Bot 102:833–847

    Article  PubMed  Google Scholar 

  • Vogel S (1990) The role of scent glands in pollination: on the structure and function of osmophores. Amerind, New Delhi

    Google Scholar 

  • Waterman PG (1993) Phytochemical diversity in the order Rutales. In: Downum KR, Romeo JT, Stafford HA (eds) Phytochemical potential of tropical plants. Plenum Press, New York, pp 203–233

    Chapter  Google Scholar 

  • Waterman PG, Grundon MF (1983) Chemistry and chemical taxonomy of the Rutales. Academic Press, New York

    Google Scholar 

  • Weber MG, Keeler KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot 111:1251–1261

    Article  PubMed  Google Scholar 

  • Weber MG, Porturas LD, Keeler KH (2015) World list of plants with extrafloral nectaries. http://www.extrafloralnectaries.org, Accessed 3 May 2020

  • Weckerle CS, Rutishauser R (2005) Gynoecium, fruit and seed structure of Paullinieae (Sapindaceae). Bot J Linn Soc 147:159–189

    Article  Google Scholar 

  • Wilson KJ, Mahlberg PG (1978) Ultrastructure of non-articulated laticifers in mature embryos and seedlings of Asclepias syriaca L. (Asclepiadaceae). Am J Bot 65:98–109

    Article  Google Scholar 

  • Wilson KJ, Mahlberg PG (1980) Ultrastructure of developing and mature nonarticulated laticifers in the milkweed Asclepias syriaca L. (Asclepiadaceae). Am J Bot 67:1160

    Article  Google Scholar 

  • Wunnachit W, Jenner CF, Sedgley M (1992) Floral and extrafloral nectar production in Anacardium occidentale (Anacardiaceae): an andromonoecious species. Int J Plant Sci 153:413–420

    Article  Google Scholar 

  • Yamawo A (2015) Extrafloral nectaries of Melia azedarach (Meliaceae): the first record for genus Melia. J Jap Bot 90:404–406

    Google Scholar 

  • Zhang M, Wang J, Zhu L, Li T, Jiang W, Zhou J, Peng W, Wu C (2017) Zanthoxylum bungeanum Maxim. (Rutaceae): a systematic review of its traditional uses, botany, phytochemistry, pharmacology, pharmacokinetics, and toxicology. Int J Mol Sci 18:2172

    Article  CAS  PubMed Central  Google Scholar 

  • Zhou Y, Shi H, Liu W (2012) Ontogenesis of trichome-like cavities in Dictamnus dasycarpus. Flora 207:63–73

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Proc. #2014/18002-2, #2017/23882-0, #2019/10636-6) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq proc. #301206/2018-0) for financial support. We also thank Dr. Marcelo Pace for contributing with photographs of the wood of Zanthoxylum kellermanii (Rutaceae) showing traumatic ducts and Dr. Ana Paula S. Lacchia for contributing with photographs of Tapirira guianensis (Anacardiaceae) showing the secretory endocarp.

Author information

Authors and Affiliations

  1. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, 05508-090, Brazil

    Elisabeth Dantas Tölke, Maria Camila Medina, Gisele Gomes Nogueira Alves, Rebeca Laino Gama, José Rubens Pirani & Diego Demarco

  2. Departamento de Ciências Farmacêuticas, Centro de Ciências da Saúde, Universidade Federal da Paraíba, João Pessoa, PB, 58051-900, Brazil

    Augusto Lopes Souto

  3. Departamento de Ciências Básicas, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, São Paulo, Brazil

    João Paulo Rodrigues Marques

Authors
  1. Elisabeth Dantas Tölke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Camila Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Augusto Lopes Souto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. João Paulo Rodrigues Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gisele Gomes Nogueira Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rebeca Laino Gama
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José Rubens Pirani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Diego Demarco
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.D.T. and D.D. contributed to conceptualization; E.D.T., M.C.M., A.L.S., J.P.R.M., G.G.N.A., R.L.G., J.R.P., and D.D. contributed to formal analysis and investigation; E.D.T., M.C.M., A.L.S., J.P.R.M., G.G.N.A., R.L.G., J.R.P., and D.D. contributed to writing—original draft preparation; E.D.T., M.C.M., A.L.S., J.P.R.M., G.G.N.A., R.L.G., J.R.P., and D.D. contributed to writing—review and editing; E.D.T., J.R.P., and D.D. acquired funding; D.D. contributed to supervision. All authors have read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Elisabeth Dantas Tölke or Diego Demarco.

Ethics declarations

Conflict of interest

Diego Demarco is the Editor-in-chief and Elisabeth D. Tölke is an Associate Editor of the Brazilian Journal of Botany, and we assure this article was entirely handled by an Associate Editor.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tölke, E.D., Medina, M.C., Souto, A.L. et al. Diversity and evolution of secretory structures in Sapindales. Braz. J. Bot 45, 251–279 (2022). https://doi.org/10.1007/s40415-021-00778-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-021-00778-w

Keywords

Search

Navigation