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Foliar Secretory Structures in Crotoneae (Euphorbiaceae): Diversity, Anatomy, and Evolutionary Significance

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Foliar Secretory Structures in Crotoneae (Euphorbiaceae): Diversity, Anatomy, and Evolutionary Significance AMERICAN JOURNAL OF BOTANY RESEARCH ARTICLE F OLIAR SECRETORY STRUCTURES IN CROTONEAE (EUPHORBIACEAE): DIVERSITY, ANATOMY, AND 1 EVOLUTIONARY SIGNIFICANCE N ARAH C . V ITARELLI 2 , R ICARDA R IINA 3,6 , M ARIA B EATRIZ R. CARUZO 4,5 , I NÊS C ORDEIRO 5 , J AVIER F UERTES-AGUILAR 3 , AND R ENATA M. S. A. MEIRA 2 2 Universidade Federal de Viçosa, DBV, Viçosa 36570-900, Brazil; 3 Real Jardín Bot ánico, RJB-CSIC, Plaza de Murillo 2, ES-28014, Madrid, Spain; 4 Departamento de Ciências Exatas e da Terra, Universidade Federal de São Paulo, Diadema, SP, Brazil; and 5 Instituto de Botânica, Secretaria do Meio Ambiente, Cx. Postal 3005 01061-970, São Paulo, SP, Brazil • Premise of the study: Phylogenetic and morphological studies have helped clarify the systematics of large and complex groups such as the tribe Crotoneae (Euphorbiaceae). However, very little is known about the diversity, structure, and function of ana- tomical features in this tribe. Crotoneae comprises the species-rich pantropical genus Croton and six small neotropical genera. Here we characterized the anatomy of leaf secretory structures in members of this tribe and explored their function and evolu- tionary signifi cance. • Methods: Young and mature leaves of 26 species were studied using standard anatomical light microscopy techniques. Three sections of Croton and one representative of Brasiliocroton and Astraea were sampled. • Key results: We identifi ed fi ve types of secretory structures: laticifers, colleters, extrafl oral nectaries, idioblasts, and secretory trichomes. Laticifers were present in all species studied except Croton alabamensis , which instead presented secretory paren- chyma cells. Articulated laticifers are reported in Crotoneae for the fi rst time. Colleters of the standard type were observed in the majority of the sampled taxa. Extrafl oral nectaries were present in section Cleodora and in B. mamoninha , but absent in section Lamprocroton and Astraea lobata . Idioblasts were spread throughout the palisade and/or spongy parenchyma in most of the studied species. Secretory trichomes were restricted to Lamprocroton except for C. imbricatus . • Conclusions: This study revealed a high diversity of secretory structures, including novel ones, in one of the largest clades of Euphorbiaceae. Our results are promising for investigations on the anatomical and ecophysiological bases of species diversifi - cation within Euphorbiaceae. Key words: anatomy; Astraea ; Brasiliocroton ; colleters; Croton ; Euphorbiaceae; extrafl oral nectaries; laticifers; secretory idioblasts; secretory trichomes. Among the angiosperms, lineages within Euphorbiaceae show Shaanker, 1988 ; Rudall, 1989 , 1994 ; Webster et al., 1996 ; conspicuous examples of the diversifi cation of secretory ele- Freitas et al., 2001 ; de S á-Haiad et al., 2009 ; Wiedenhoeft et al., ments. In particular, the tribe Crotoneae stands out as a group for 2009 ; Narbona and Dirzo, 2010 ; Machado et al., 2015 ), al- which several types of secretory structures have been reported though detailed studies of the morphology, distribution, and ( Froembling, 1896 ; Metcalfe and Chalk, 1950 ; Ganeshaiah and nature of these features spanning the taxonomic breadth of this group have not been yet conducted. Secretory structures could 1 Manuscript received 16 January 2015; revision accepted 13 May 2015. be the sites of synthesis and/or accumulation of metabolites with This study is part of the doctoral dissertation of N.C.V. We are grateful high phytochemical and pharmacological value ( Fahn, 1979 ). to the cited herbaria for allowing us to sample their collections. We thank Such structures can also be a source of characters for systemat- Gerhard Prenner, an anonymous reviewer, the Associate Editor, Gonzalo ics, and they are likely key players in many plant–animal eco- Nieto, and Angélica Bello for thoughtful comments and suggestions that logical interactions. The ecological role of secretory structures improved an earlier version of this paper. The Real Jardín Bot ánico-CSIC in the case of Croton , the largest genus of Crotoneae, could be hosted N.C.V. for a research stage. This work was supported by CNPq related to its evolutionary success, as these structures are in- (477867/2013-8), FAPEMIG (CRA-APQ), and Centro de Ciências volved in the attraction of pollinators and seed dispersers, and Ambientais Floresta Escola (FUNARBE-6991). N.C.V. was a CAPES their secretions may also protect the plant against herbivores scholarship holder. J.F.A. was supported by grant CGL2010-16138 from and pathogens at different stages of development. Additionally, Plan Nacional de I+D+I. R.R. was a JAE-DOC holder supported by the Ministerio de Economía y Competitividad, Spain, co-funded by the mutualistic relationships appear to be common in species that European Social Fund. are rich in secretory structures ( Fahn, 1979 ). 6 Author for correspondence (e-mail: [email protected]) The tribe Crotoneae of Euphorbiaceae consists of the species- rich genus Croton L. (ca. 1300 spp.) and six small genera doi:10.3732/ajb.1500017 ( Acidocroton Griseb., Astraea Klotzsch, Brasiliocroton P.E. American Journal of Botany 102 ( 6 ): 833 – 847 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America 833 834 • VOL. 102 , NO. 6 JUNE 2015 • AMERICAN JOURNAL OF BOTANY Berry & Cordeiro, Ophellantha Standl., Sagotia Baill., and lineages or that latex is just not noticeable in species for which Sandwithia Lanj.) that together have no more than 30 species it has been reported as absent (from fi eld observations). ( Berry et al., 2005 ; Wurdack et al., 2005 ; Riina et al., 2014 ). The presence, position, and type of secretory structures have Species in this tribe range from herbs to trees and occasionally been used to support or clarify phylogenetic relationships among lianas and are found in a wide range of habitats. They are dis- several angiosperm groups as well as to understand evolutionary tributed in tropics and subtropics worldwide ( Berry et al., patterns of lineage diversifi cation ( Dickson, 2000 ; Tilney and 2005 ), but the largest concentration of species is in the neo- van Wyk, 2004 ; Marazzi et al., 2006 ; Delgado et al., 2009 ; tropics with important centers of diversity in Brazil, the Antil- Araújo et al., 2010 ; De-Paula et al., 2011 , Coutinho et al., 2012 , les, and Mexico ( Burger and Huft, 1995 ; van Ee et al., 2011 ). 2013 ; Pe čnikar et al., 2012 ; Weber and Keeler, 2013 ; Angulo Many species in this tribe, especially in the genus Croton ( Salatino and Dematteis, 2014 ). Likewise, secretory structures have been et al., 2007 ), are used in folk medicine, and some have been relevant in the taxonomy and phylogenetics of groups within the focus of phytochemistry and pharmacological studies. Crotonoideae and Crotoneae ( Caruzo et al., 2011 ; De-Paula et al., Molecular phylogenetics has been essential for clarifying the 2011 ; van Ee et al., 2011 ; Riina et al., 2014 ). For instance, the relationships among Croton and other Crotoneae lineages presence of fl oral nectaries in crotonoid genera (sensu Wurdack ( Berry et al., 2005 ; van Ee et al., 2011 ; Riina et al., 2014 ). Be- et al., 2005 ) is a diagnostic character for the CI clade. Likewise, cause Croton contains the largest number of species in the tribe, vascularized fl oral nectaries may be a diagnostic character for its systematics and taxonomy have been studied in more detail Croton , while in Astraea these structures are not vascularized (e.g., Lima and Pirani, 2008 ; Riina et al., 2010 ; van Ee and ( De-Paula et al., 2011 ). Berry, 2010 ; Caruzo et al., 2011 ; van Ee and Berry, 2011 ; Caruzo The distribution and type of secretory structures in Croto- and Cordeiro, 2013 ). However, this effort has not been paral- neae might be important characters for elucidating the evolu- leled by a thorough search of morphological and anatomical tionary history of the group, especially regarding clades whose traits that would help to interpret clade diversifi cation within species occur in contrasting environments, such as in sections this tribe. Less than 2% of the species of Crotoneae have been Cleodora (Klotzsch) Baill. and Lamprocroton (Müll. Arg.) included in anatomical surveys ( De-Paula and Sajo, 2011 ; Pax, which are sampled in this study. Secretory structures could De-Paula et al., 2011 ; de S á-Haiad et al., 2009 ; Machado et al., be also a source of new characters useful for the circumscription 2015 ). The role played by different types of secretory elements of taxa and to support phylogenetic hypotheses in Crotoneae. (e.g., laticifers, secretory ducts) in the evolution of angiosperms In this study we investigate the diversity, morphology, distri- remains an open question ( Pickard, 2008 ). bution patterns, development, and function of leaf secretory Floral and extrafl oral nectaries are probably the best-known structures of species belonging to three sections of Croton ( Ala- secretory structures in Crotoneae ( Metcalfe and Chalk, 1950 ; bamenses B.W. van Ee, Cleodora , Lamprocroton ) and two Fahn, 1979 ; Elias, 1983 ; Freitas et al., 2001 ), particularly in other Crotoneae genera (Brasiliocroton and Astraea ) ( Fig. 1 ). Croton . They were found to be related to mutualistic interac- We discuss our fi ndings under the current Crotoneae phyloge- tions, like the reward for pollinators and recruitment of plant- netic framework. This work contributes toward the goal of un- protective insects. For example, in Croton suberosus Kunth, derstanding the evolution of secretory structures and other
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