Abstract
This study presents the first comparative analysis of the leaf secretory structures across Asteraceae. In this work, the leaf secretory structures of more than 500 species of 35 of the 40 tribes and 11 of the 13 subfamilies of Asteraceae are described and compared to evaluate their diversity at the tribe level and to identify evolutionary patterns. Leaf secretory structures are present in 28 of the 35 analyzed tribes and correspond to canals (recorded in 17 tribes), secretory cavities (1 tribe), hydathodes (19 tribes), laticifers (4 tribes) and glandular trichomes (24 tribes). Canals are mostly associated with vascular bundles and predominate in Asteroideae, while cavities were only present within Tageteae. Hydathodes occur in leaves without divisions and with well-developed teeth. Laticifers were observed only in the tribes of Cichorioideae. Seven glandular trichome morphotypes were differentiated by their cellular composition and shape. These observations together with the available information showed that secretory structures are found in 80% of the Asteraceae tribes. Four of the 40 tribes did not present any type of secretory structure. Our study reveals that almost all of the tribes possess one to three types of secretory structures, and are absent in some early-diverging clades. Character evolution analyses show that glandular trichomes are plesiomorphic in Asteraceae. This study found that secretory structures prevail in late-diverging lineages and were taxonomically informative at different levels. Our comparative study of the secretory structures in Asteraceae is essential for the standardization of its terminology and will provide a frame of reference for future studies.
Similar content being viewed by others
References
Aguilera, D. B., Meira, R. M. S. A., & Ferreira, F. A. (2004). Anatomia e histoquímica dos órgãos vegetativos de Siegesbeckia orientalis (Asteraceae). Planta Daninha 22: 483–489. https://doi.org/10.1590/S0100-83582004000400001
Arciniegas, A., Pérez-Castorena, A. L., Meléndez-Aguirre, M., Guillermo Ávila, J., García-Bores, A. M., Villaseñor, J. L., Romo de Vivar, A. (2018). Chemical composition and antimicrobial activity of Ageratina deltoidea. Chemistry and Biodiversity 15(3): e1700529. DOI: https://doi.org/10.1002/cbdv.201700529
Arciniegas, A., Polindara, L. A., Pérez-Castorena, A. L., García, A. M., Ávila, G., Villaseñor, J. L., & Romo de Vivar, A. (2011). Chemical composition and biological activity of Laennecia schiedeana. Zeitschrift fur Naturforschung. C, Journal of biosciences 66(3–4): 115–22. https://doi.org/10.1515/znc-2011-3-404.
Aschenbrenner, A. K., Horakh, S., & Spring, O. (2013). Linear glandular trichomes of Helianthus (Asteraceae): morphology, localization, metabolite activity and occurrence. AoB PLANTS 5: 1–9. https://doi.org/10.1093/aobpla/plt028
Bauer, G., Gorb, S. N., Klein, M. C., Nellesen, A., von Tapavicza, M., & Speck, T. (2014). Comparative study on plant latex particles and latex coagulation in Ficus benjamina, Campanula glomerata and three Euphorbia species. PLoS ONE 9(11): e113336. https://doi.org/10.1371/journal.pone.0113336
Beck, C. B. 2010. An introduction to plant structure and development. Plant anatomy for the twenty-first century. Cambridge University Press.
Bezerra, L. D. A., Mangabeira, P. A. O., de Oliveira, R. A., Costa, L. C. D. B., & Da Cunha, M. (2018). Leaf blade structure of Verbesina macrophylla (Cass.) F. S. Blake (Asteraceae): ontogeny, duct secretion mechanism and essential oil composition. Plant Biology (Stuttg) 20: 433–443. https://doi.org/10.1111/plb.12700
Bohm, B. A., & Stuessy, T. F. (1995). Flavonoid chemistry of Barnadesioideae (Asteraceae). Systematic Botany 20(1): 22–27. https://doi.org/10.2307/2419629
Bombo, A. B., Santos De Oliveira, T., Da Silva Santos De Oliveira, A., Garcia Rehder, V. L., Galvão Magenta, M. A., & Appezzato-Da-Glória, B. (2012). Anatomy and essential oils from aerial organs in three species of Aldama (Asteraceae-Heliantheae) that have a difficult delimitation. Australian Journal of Botany 60: 632–642. https://doi.org/10.1071/BT12160
Budel, J. M., Duarte, M. R., Santos, C. A. M., & Farago, P. V. (2004). Morfoanatomia foliar e caulinar de Baccharis dracunculifolia DC., Asteraceae. Acta Farmacéutica Bonaerense 23: 477–483.
Budel, J. M., Raman, V., Monteiro, L. M., Almeida, V. P., Bobek, V. B., Heiden, G., Takeda, I. J. M., & Khan, I. A. (2018). Foliar anatomy and microscopy of six Brazilian species of Baccharis (Asteraceae). Microscopy Research and Technique 81(8): 832–842. https://doi.org/10.1002/jemt.23045
Carlquist, S. (1958). Structure and ontogeny of glandular trichomes of Madinae (Compositae). American Journal of Botany 45(2): 675–682. https://doi.org/10.1002/j.1537-2197.1958.tb12221.x
Carlquist, S. (1959a). The leaf of Calycadenia and its glandular appendages. American Journal of Botany 46(2): 70–80. https://doi.org/10.1002/j.1537-2197.1959.tb06985.x
Carlquist, S. (1959b). Glandular structures of Holocarpha and their ontogeny. American Journal of Botany 46(4): 300–308. https://doi.org/10.1002/j.1537-2197.1959.tb07016.x
Carlquist, S. (1959c). Studies on Madinae: anatomy, cytology and evolutionary relationships. Aliso 4: 171–236.
Castelblanque, L., Balaguer, B., Martí, C., Rodríguez, J. J., Orozco, M., & Vera, P. (2016). Novel insights into the organization of laticifer cells: A cell comprising a unified whole system. Plant Physiology 172: 1032–1044. https://doi.org/10.1104/pp.16.00954
Castro, M. M., Leitão-Filho, H. F., & Rossi Monteiro, W. (1997). Utilização de estruturas secretoras na identificação dos gêneros de Asteraceae de uma vegetação de cerrado. Revista Brasileira de Botânica 20: 163–174. https://doi.org/10.1590/S0100-84041997000200007
Cilia-López, V. G., Cariño-Cortés, R., & Zurita-Salinas, L. R. (2021). Ethnopharmacology of the Asteraceae family in Mexico. Botanical Sciences 99(3): 455–486. https://doi.org/10.17129/botsci.2715
Crang, R., Lyons-Sobaski, S., & Wise, R. (2018). Plant anatomy: A concept-based approach to the structure of seed plants. Springer International Publishing AG.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, David. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8): 772. https://doi.org/10.1038/nmeth.2109
De Pinna, M. C. C. (1991). Concepts and tests of homology in the cladistic paradigm. Cladistics 7(4): 367–394. https://doi.org/10.1111/j.1096-0031.1991.tb00045.x
Delbón, N., Cosa, M., & Dottori, N. (2007). Anatomía de órganos vegetativos en Flourensia campestris y F. oolepis (Asteraceae), con especial referencia a las estructuras secretoras. Arnaldoa 14: 61–70. https://doi.org/10.1590/S0102-33062012000100002
Delbón, N., Cosa, M., & Bernardello, G. (2012). Exomorfología y anatomía de órganos vegetativos aéreos en especies de Flourensia DC. (Asteraceae) con importancia fitoquímica. Acta Botanica Brasilica 26: 2–10. https://doi.org/10.1590/S0102-33062012000100002
Dere, S. & Aytas Akcin, T. (2017). Anatomical and micromorphological properties of some Tanacetum L. (Asteraceae) taxa from Turkey and their systematic implications. Acta Botanica Croatica 76: 1–15. https://doi.org/10.1515/botcro-2017-0005
Dickison, W. C. (2000). Integrative plant anatomy. Academic Press.
Esau, K. (1977). Anatomy of seed plants. John Wiley & Sons.
Evans, W. C. (2009). Trease and Evans pharmacognosy. Saunders/Elsevier.
Evert, R. F. (2006). Esau’s plant anatomy: meristems, cells, and tissues of the plant body. Their structure, function and development. John Wiley & Sons.
Fahn, A. (1979). Secretory tissues in plants. Academic Press Inc.
Fahn, A. (1982). Plant anatomy. Pergamon Press.
Fahn, A. (1988). Secretory tissues in vascular plants. New Phytologist 108: 229–257. https://doi.org/10.1111/j.1469-8137.1988.tb04159.x
Fahn, A. (2000). Structure and function of secretory cells. Advances in Botanical Research 31: 37–75. https://doi.org/10.1016/S0065-2296(00)31006-0
Favi, F., Cantrell, C. L., Mebrahtu, T., & Kraemer, M. E. (2008). Leaf peltate glandular trichomes of Vernonia galamensis ssp. galamensis var. aethiopica Gilbert: development, ultrastructure, and chemical composition. International Journal of Plant Sciences 169: 605–614. https://doi.org/10.1086/533598
Ferraro, A., & Scremin-Dias, E. (2017). Structural features of species of Asteraceae that arouse discussions about adaptation to seasonally dry environments of the Neotropics. Acta Botanica Brasilica 32(1): 113–127. https://doi.org/10.1590/0102-33062017abb0246
Filartiga, A. L., Bombo, A. B., Garcia, V. L., & Appezzato-da-Glória, B. (2016). Leaf and stem anatomy and essential oil composition of four Brazilian Aldama species (Asteraceae) and their taxonomic significance. Brazilian Journal of Botany 40: 503–516. https://doi.org/10.1007/s40415-016-0350-3
Fonseca, M. C. M., Meira, R. M. S. A., & Casali, V. W. D. (2006). Anatomia dos órgãos vegetativos e histolocalização de compostos fenólicos e lipídicos em Porophyllum ruderale (Asteraceae). Planta Daninha 24(4): 707–713. https://doi.org/10.1590/S0100-83582006000400011
Funk, V. A., Susanna, A., Stuessy, T. F., & Bayer, Y. R. J. (2009). Systematics, evolution and biogeography of the Compositae. International Association for Plant Taxonomy (IAPT).
Funk, V. A., Kelloff, C., & Chan, R. (2012). Phylogeny and biogeography of the tribe Liabeae (Compositae subfamily Cichorioideae). Taxon 61(2): 437–455. https://doi.org/10.1002/tax.612013
García-Sánchez, F., López-Villafranco, M. E., Aguilar-Rodríguez, S., & Aguilar-Contreras, A. (2012). Etnobotánica y morfo-anatomía comparada de tres especies de Tagetes que se utilizan en Nicolás Romero, Estado de México. Botanical Sciences 90: 221–232. https://doi.org/10.17129/botsci.388
Gras, A., Hidalgo, O., D’Ambrosio, U., Parada, M., Garnatje, T., & Vallès, J. (2021). The role of botanical families in medicinal ethnobotany: a phylogenetic perspective. Plants 10(1): 1–17. https://doi.org/10.3390/plants10010163
Gutiérrez, D. G., & Luján Luna, M. (2013). A comparative study of latex-producing tissues in genera of Liabeae (Asteraceae). Flora 208: 33–44. https://doi.org/10.1016/j.flora.2012.11.001
Gutiérrez, D. G., Muñoz-Schick, M., Grossi, M. A., Rodríguez Cravero, J. F., Morales, V., & Moreira-Muñoz, A. (2016). The genus Stevia (Eupatorieae, Asteraceae) in Chile: a taxonomical and morphological analysis. Phytotaxa 282(1): 1–18. https://doi.org/10.11646/phytotaxa.282.1.1
Hadad, M., Gattuso, S., Gattuso, M., Feresin, G., & Tapia, A. (2013). Anatomical studies of Baccharis grisebachii Hieron. (Asteraceae). Used in folk medicine of San Juan province, Argentina. Dominguezia 29: 41–47.
Hagel, J. M., Yeung, E. C., & Facchini, P. J. (2008). Got milk? The secret life of laticifers. Trends in Plant Science 13: 631–639. https://doi.org/10.1016/j.tplants.2008.09.005
Hayat, M. Q., Ashraf, M., Khan, M. A., Yasmin, G., Shaheen, N., & Jabeen, S. (2009). Diversity of foliar trichomes and their systematic implications in the genus Artemisia (Asteraceae). International Journal of Agriculture and Biology 11(5): 542–546.
Heinrich, M., Barnes, J., Gibbons, S., & Williamson, E. M. (2012). Fundamentals of pharmacognosy and phytotherapy. Elsevier.
Johansen, D. A. (1940). Plant microtechnique. McGraw-Hill.
Karis, P. O. (2006). Morphological data indicates two major clades of the subtribe Gorteriinae (Asteraceae-Arctotideae). Cladistics 22: 199–221. https://doi.org/10.1111/j.1096-0031.2006.00109.x
Katoh, K., Misawa K., Kuma K., & Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30(14): 3059–3066. https://doi.org/10.1093/nar/gkf436
Krak, K., & Mráz, P. (2008). Trichomes in the tribe Lactuceae (Asteraceae) - taxonomic implications. Biologia 63: 616–630. https://doi.org/10.2478/s11756-008-0106-z
Lersten, N. R., & Curtis, J. D. (1985). Distribution and anatomy of hydathodes in Asteraceae. Botanical Gazette 146(1): 106–114. https://doi.org/10.1086/337504
Lersten, N. R., & Curtis, J. D. (1989). Foliar oil reservoir anatomy and distribution in Solidago canadensis (Asteraceae, tribe Astereae). Nordic Journal of Botany 9(3): 281–287. https://doi.org/10.1111/j.1756-1051.1989.tb01003.x
Lewinsohn, T. M. (1991). The geographical distribution of plant latex. Chemoecology 2: 64–68. https://doi.org/10.1007/BF01240668
Liesenfeld, V., Gentz, P., de Freitas, E. M., & Martins, S. (2019). Morphological diversity of foliar trichomes in Asteraceae from Sandfields of the Pampa biome, Rio Grande do Sul State, Brazil. Hoehnea 46(3): e752018. https://doi.org/10.1590/2236-8906-75/2018
Lizárraga, E., Mercado, M. I., Gálvez, C., Ruiz, A. I., Ponessa, G. I., & Catalán, C. A. N. (2017). Morpho anatomical characterization and essential oils of Tagetes terniflora and Tagetes minuta (Asteraceae) growing in Tucumán (Argentina). Boletín de la Sociedad Argentina de Botánica 52(1): 55–68.
Loockerman, D. J., Turner, B. L., & Jansen, R. K. (2003). Phylogenetic relationships within the Tageteae (Asteraceae) based on nuclear ribosomal ITS and chloroplast ndhF gene sequences. Systematic Botany 28(1): 191–207. https://doi.org/10.1043/0363-6445-28.1.191
Lusa, M. G., Da Costa, F. B., & Appezzato-da-Glória, B. (2016). Histolocalization of chemotaxonomic markers in Brazilian Vernonieae (Asteraceae). Botanical Journal of the Linnean Society 182(3): 581–593. https://doi.org/10.1111/boj.12481
Lusa, M. G., Loeuille, B. F. P., Ciccarelli, D., & Appezzato-da-Glória, B. (2017). Evolution of stem and leaf structural diversity: a case study in Lychnophorinae (Asteraceae). The Botanical Review 84: 203–241. https://doi.org/10.1007/s12229-017-9191-4
Machado, R. R. P., Marques, A. M., Valente Júnior, W., Coimbra, E. S., Duarte, R. S., Soares, G. L. G., & Kaplan, M. A. C. (2012). Evaluation of in vitro antileishmanial and antimycobacterial activities of Stifftia chrysantha J.C. Mikan extracts. Revista Fitos 7(4): 252–258.
Makbul, S., Coskuncelebi, K., Türkmen, Z., & Beyazoglu, O. (2011). Comparison of foliar anatomy of Scorzonera L. (Asteraceae) taxa from North East Anatolia. Pakistan Journal of Botany 43(1): 135–155.
Makbul, S., Coskuncelebi, K., Okur, S., & Gültepe, M. (2016). Contribution to the taxonomy of Turkish Scorzonera (Asteraceae) taxa based on vegetative anatomy. Nordic Journal of Botany 34(6): 670–684. https://doi.org/10.1111/njb.01159
Marques, A. M., Lima, M. C., Araújo Filho, H. C., Esteves, R. L., & Kaplan, M. A. C. (2012). Evaluation of the volatile components and the seasonal variation of the methyl salicylate from Stifftia chrysantha Mikan by HS-SPME/GC-MS. Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas 11(5): 413–419.
Martínez-Cabrera, D., Terrazas, T., & Ochoterena, H. (2007). Leaf architecture of Hamelieae (Rubiaceae). Feddes Repertorium 118(7): 286–310. https://doi.org/10.1002/fedr.200711140
Mauseth, J. D. (1988). Plant anatomy. Benjamin/Cummings Publishing Company.
Meade, A., & Pagel, M. (2017). BayesTraits v.3.0 (Reading Evolutionary Biology Group).
Medina, M. C., Sousa-Baena, M. S., Prado, E., Acevedo-Rodríguez, P., Dias, P., & Demarco, D. (2021). Laticifers in Sapindaceae: structure, evolution and phylogenetic importance. Frontiers in Plant Science 11: e612985. https://doi.org/10.3389/fpls.2020.612985
Melo-de-Pinna, G. F. A. (2004). Anatomia foliar de Richterago Kuntze (Mutisieae, Asteraceae). Acta Botanica Brasilica 18(3): 591–600. https://doi.org/10.1590/S0102-33062004000300017
Melo-de-Pinna, G. F. A. & Menezes, N. L. (2003). Meristematic endodermis and secretory structures in adventitious roots of Richterago Kuntze (Mutisieae-Asteraceae). Brazilian Journal of Botany 26(1): 1–10. https://doi.org/10.1590/S0100-84042003000100002
Metcalfe, C. R. (1967). Distribution of latex in the plant kingdom. Economic Botany 21: 115–127. https://doi.org/10.1007/BF02897859
Milan, P., Hissae Hayashi, A., & Appezzato-da-Glória, B. (2006). Comparative leaf Morphology and anatomy of three Asteraceae species. Brazilian Archives of Biology and Technology 49(1): 135–144. https://doi.org/10.1590/S1516-89132006000100016
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE). 1–8.
Moerman, D. E., Pemberton, R. W., Kiefer, D., & Berlin, B. (1999). A comparative analysis of five medicinal floras. Journal of Ethnobiology 19(1): 49–67.
Muravnik, L. E., Kostina, O. V., & Shavarda, A. L. (2016). Glandular trichomes of Tussilago farfara (Senecioneae, Asteraceae). Planta 244: 737–752. https://doi.org/10.1007/s00425-016-2539-x
Narayana, B. M. (1979). Taxonomic value of trichomes in Vernonia Schreb. (Asteraceae). Proceedings of the Indian Academy of Sciences 88: 347–357. https://doi.org/10.1007/BF03046107
O’Dowd, D. J., & Catchpole, E.A. (1983). Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp. - ant interactions. Oecologia 59(2): 191–200. https://doi.org/10.1007/BF00378837
Oliveira, T., Bombo, A. B., & Appezzato-da-Glória, B. (2013). Anatomy of vegetative organs with an emphasis on the secretory structures of two species of Aldama (Asteraceae–Heliantheae). Botany 91(6): 335–342. https://doi.org/10.1139/cjb-2012-0271
Oliveira, T., Vasconcelos Filho, S. C., Bastos, A. V. S., Vasconcelos, J. M., & Rodrigues, A. A. (2015). Anatomical and histochemical analysis of vegetative organs of Vernonia ferruginea Less. (Asteraceae). African Journal of Biotechnology 14(38): 2734–2739. https://doi.org/10.5897/AJB2015.14934
Ozcan, M., Demirala, M., & Kahriman, A. (2015). Leaf anatomical notes on Cirsium Miller (Asteraceae, Carduoideae) from Turkey. Plant Systematics and Evolution 301: 1995–2012. https://doi.org/10.1007/s00606-015-1209-y
Páez, V. A., Albornoz, P. L., Lizárraga, E., Sobrero, M. T., & Chaila, S. (2019). Anatomía foliar y caulinar, y caracterización fitoquímica foliar de Flaveria bidentis y F. haumanii (Asteraceae) de Santiago del Estero, Argentina. Acta Botanica Mexicana 126: 1–12. https://doi.org/10.21829/abm126.2019.1409
Panero, J. L., & Crozier, B. S. (2016). Macroevolutionary dynamics in the early diversification of Asteraceae. Molecular Phylogenetics and Evolution 99: 116–132. https://doi.org/10.1016/j.ympev.2016.03.007
Panero, J. L. & Funk, V. A. (2008). The value of sampling anomalous taxa in phylogenetic studies: major clades of the Asteraceae revealed. Molecular Phylogenetics and Evolution 47: 757–782. https://doi.org/10.1016/j.ympev.2008.02.011
Pérez-Castorena, A. L., Arciniegas, A., Martínez, F., Villaseñor, J. L., & Romo de Vivar, A. (2000). Pyrrolizidine alkaloids from four Senecio species. Biochemical Systematics and Ecology 28(3): 279–282. https://doi.org/10.1016/S0305-1978(99)00057-5
Pérez-Castorena, A. L., Arciniegas, A., Martínez, F., Marquez, C., Villaseñor, J. L., & Romo de Vivar, A. (2001). Chemical constituents of Packera coahuilensis and Packera bellidifolia. Biochemical Systematics and Ecology 29(2): 203–206. https://doi.org/10.1016/S0305-1978(00)00043-0
Pickard, W. F. (2007). Laticifers and secretory ducts: two other tube systems in plants. New Phytologist 177(4): 877–888. https://doi.org/10.1111/j.1469-8137.2007.02323.x
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Redonda-Martínez, R., Villaseñor, J. L., & Terrazas, T. (2012). Trichome diversity in the Vernonieae (Asteraceae) of Mexico I: Vernonanthura and Vernonia (Vernoniinae). Journal of the Torrey Botanical Society 139(3): 235–247. https://doi.org/10.3159/TORREY-D-11-00069.1
Redonda-Martínez, R., Villaseñor, J. L., & Terrazas, T. (2016). Trichome diversity in the subtribe Leiboldiinae (Vernonieae, Asteraceae). Journal of the Torrey Botanical Society 143(3): 298–310. https://doi.org/10.3159/TORREY-D-14-00062.1
Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3(2): 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rios, A. B. M., Oliveira Menino, G. C., & Casagrande Dalvi, V. (2020). Leaf teeth in eudicots: what can anatomy elucidate? Botanical Journal of the Linnean Society 193: 504–522. https://doi.org/10.1093/botlinnean/boaa028
Rivera, P., Villaseñor, J. L., Terrazas, T., & Panero, J. L. (2020). The importance of the Mexican taxa of Asteraceae in the family phylogeny. Journal of Systematics and Evolution 0(0): 1–16. https://doi.org/10.1111/jse.12681
Robinson, H. (2009). An introduction to micro-characters of Compositae. In V. A. Funk, A. Susanna, T. F. Stuessy, & Y. R. J. Bayer (Eds.), Systematics, evolution and biogeography of the Compositae (pp. 89–99). International Association for Plant Taxonomy (IAPT).
Rojas-Leal, A., Villaseñor, J. L., & Terrazas, T. (2017). Tricomas foliares en Senecio sección Mulgediifolii (Senecioneae, Asteraceae). Acta Botanica Mexicana 119: 69–78. https://doi.org/10.21829/abm119.2017.1232
Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12): 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
RStudio Team. (2020). RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. http://www.rstudio.com/
Ruzin, S. E. (1999). Plant microtechnique and microscopy. Oxford University Press.
Sayers, E. W., Cavanaugh, M., Clark, K., Ostell, J., Pruitt, K. D., & Karsch-Mizrachi, I. (2020). GenBank. Nucleic Acids Research 48(D1): D84–D86. https://doi.org/10.1093/nar/gkz956
Silva, T. M., Vilhalva, D. A. A., Moraes, M. G., & Figueiredo-Ribeiro, R. C. L. (2015). Anatomy and fructan distribution in vegetative organs of Dimerostemma vestitum (Asteraceae) from the campos rupestres. Anais da Academia Brasileira de Ciências 87(2): 797–812. https://doi.org/10.1590/0001-3765201520140214
Simon, P.M., Katinas, L., & Arambarri, A. M. (2002). Secretory structures in Tagetes minuta (Asteraceae, Helenieae). Boletín de la Sociedad Argentina de Botánica 37(3–4): 181–191.
Solovchenko, A. (2010). Photoprotection in plants: optical screening-based mechanisms. Springer-Verlag.
Souza da Silva, E. M., Hissae Hayashi, A., & Appezzato-da-Glória, B. (2014). Anatomy of vegetative organs in Aldama tenuifolia and A. kunthiana (Asteraceae: Heliantheae). Brazilian Journal of Botany 37: 505–517. https://doi.org/10.1007/s40415-014-0101-2
Steyn, W. J., Wand, S. J. E., Holcroft, D. M., & Jacobs, G. (2002). Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytologist 155: 349–361. https://doi.org/10.1046/j.1469-8137.2002.00482.x
Villaseñor, J. L. (2018). Diversidad y distribución de la familia Asteraceae en México. Botanical Sciences 96: 332–358. https://doi.org/10.17129/botsci.1872
Vitali, M. (2017). Anatomia foliar del género Smallanthus (Asteraceae, Millerieae). Boletín de la Sociedad Argentina de Botánica 52(3): 463–472. https://doi.org/10.31055/1851.2372.v52.n3.18027
Ybarra, M. I., Borkosky, S. A., Catalán, C. A. N., Cerda-García-Rojas, C. M., & Nathan, P. J. (1997). Diterpenes from Hyalis argentea. Phytochemistry 44(3): 479–483. https://doi.org/10.1016/S0031-9422(96)00517-1
Younis, S., Shaheen, S., Zaib, M., Harun, N., Khalid, S., Hussain, K., Hanif. U., & Khan. F. (2020). Scanning electron microscopic screening of 20 medicinally important Asteroideae taxa. Microscopy Research and Technique 83(8): 988–1006. https://doi.org/10.1002/jemt.23492
Acknowledgements
This paper is part of Daniel M. Martínez-Quezada’s (DMMQ) dissertation and is presented as a partial requirement for the Ph.D. degree from the Postgraduate Program in Biological Sciences at the National Autonomous University of Mexico. This work was supported by the National Autonomous University of Mexico - Support Program for Research and Technological Innovation Projects (PAPIIT IN213916, IN209519) to JLV, as well as by the National Council of Science and Technology (CONACyT) for the scholarship granted to DMMQ for his graduate studies (736,800). Comments on the manuscript by Dr. Rosario Redonda-Martínez are appreciated. To Dr. José Luis Panero for facilitating the consultation and allowing us to remove samples of material deposited at the herbarium of the University of Texas at Austin. To George Yatskievych and Amalia Díaz for their assistance during sampling of herbarium specimens at TEX, as well as Julio César Montero-Rojas for artwork. We appreciate the comments of two anonymous reviewers that allowed us to improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Martínez-Quezada, D.M., Rivera, P., Rojas-Leal, A. et al. Leaf Secretory Structures in Asteraceae: A Synthesis of Their Diversity and Evolution. Bot. Rev. 89, 59–90 (2023). https://doi.org/10.1007/s12229-022-09276-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12229-022-09276-4