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The short but useful life of Prepusa montana Mart. (Gentianaceae Juss.) leaf colleters—anatomical, micromorphological, and ultrastructural aspects

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Abstract

Colleters are secretory structures involved in the protection of young and developing plant organs. Although the presence of colleters in Gentianales is described as a synapomorphy, studies on the morphofunctionality of colleters and the mechanisms underlying the synthesis and release of colleter secretion in Gentianaceae are scarce. Here, we described the ontogeny and the morphological and functional aspects of colleters of Prepusa montana, revealed the nature of the key compounds present in the secretion, and explored the cellular aspects of the synthesis and release of secretion and senescence of colleters. Samples of the stem apical meristem with leaf primordium and young leaves; adult and senescent leaves were observed using light and electron microscopy. The colleters, located in the axil of the leaf, have a protodermal origin and develop asynchronously. They are digitiform, possessing a short peduncle and a secretory head containing homogeneous cells with dense cytoplasm and abundant endoplasmic reticulum and Golgi bodies. The secretion, composed of polysaccharides and proteins, is accumulated in schizogenous spaces and released through the separation of peripheral secretory cells and loosening of the external periclinal wall. Presumably, senescence is caused by programmed cell death. The morphoanatomical characterization of P. montana leaf colleters described here is the first record for the genus and the peculiar accumulation of colleter secretion in schizogenous spaces expanding our knowledge on the diversity of these secretory structures. Our results also provide insights into programmed cell death as an eminent topic related to secretory structures.

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References

  • Almeida AL, Paiva EAS (2019) Colleters in Mabea fistulifera Mart. (Euphorbiaceae): anatomy and biology of the secretory process. Flora 258:1–9. https://doi.org/10.1016/j.flora.2019.151439

    Article  Google Scholar 

  • Appezzato-da-Glória B, Estelita MEM (2000) Development, structure and distribution of colleters in Mandevilla illustris and M. velutina (Apocynaceae). Brazil J Bot 23(2):113–120

  • Ballego-Campos I, Paiva EAS (2018) Colleters in the vegetative axis of Aechmea blanchetiana (Bromeliaceae): anatomical, ultrastructural and functional aspects. Austral J Bot 66(5):379–387. https://doi.org/10.1071/BT18095

    Article  Google Scholar 

  • Calió MF, Lepis KB, Pirani JR, Struwe L (2017) Phylogeny of Helieae (Gentianaceae): resolving taxonomic chaos in a Neotropical clade. Molec Phylogen Evol 106:192–208. https://doi.org/10.1016/j.ympev.2016.09.013

    Article  Google Scholar 

  • Calió MF, Pirani JR, Struwe L (2008) Morphology-based phylogeny and revision of Prepusa and Senaea (Gentianaceae: Helieae) - rare endemics from eastern Brazil. Kew Bull 63(2):169–191

    Article  Google Scholar 

  • Calió MFA (2009) Sistemática de Helieae Gilg (Gentianaceae). Dissertation, University of the São Paulo, São Paulo, Brazil.

  • Canaveze Y, Machado SR (2015) Leaf colleters in Tabernaemontana catharinensis (Apocynaceae, Rauvolfioideae): structure, ontogenesis, and cellular secretion. Botany 93(5):287–296

  • Cardoso-Gustavson P, Campbell LM, Viveiros-Mazzoni SC, de Barros F (2014) Floral colleters in Pleurothallidinae (Epidendroideae: Orchidaceae). Amer J Bot 101(4):587–597. https://doi.org/10.3732/ajb.1400012

    Article  Google Scholar 

  • Cassola F, Nunes CEP, Lusa MG, Garcia VL, Mayer JLS (2019) Deep in the jelly: histochemical and functional aspects of mucilage-secreting floral colleters in the orchids Elleanthus brasiliensis and E. crinipes Front Pl Sci 10(518):1–11. https://doi.org/10.3389/fpls.2019.00518

  • Célino A, Fréour S, Jacquemin F, Casari P (2014) The hygroscopic behavior of plant fibers: a review. Front Chem 43:1–12

    Google Scholar 

  • Coelho VPM, Leite JPV, Fietto LG, Ventrella MC (2013) Colleters in Bathysa cuspidata (Rubiaceae): development, ultrastructure and chemical composition of the secretion. Flora, Morphol Distrib Funct Ecol Pl 208(10–12):579–590. https://doi.org/10.1016/j.flora.2012.08.005

    Article  Google Scholar 

  • Costa ISC, Lucena EMP, Bonilla OH, IR Guesdon Coutinho ÍAC (2020) Seasonal variation in colleter exudates in Myrcia splendens (Myrtaceae). Austral J  Bot 68:403–412. https://doi.org/10.1071/BT20020

  • Coutinho ÍAC, Francino DMT, Meira RMSA (2015) New records of colleters in Chamaecrista (Leguminosae, Caesalpinioideae s.l.): structural diversity, secretion, functional role, and taxonomic importance. Int J Pl Sci 176(1):72–85. https://doi.org/10.1086/679016

  • da Silva CJ, Barbosa LCA, Marques AE, Baracat-Pereira MC, Pinheiro AL, Meira RMSA (2012) Anatomical characterisation of the foliar colleters in Myrtoideae (Myrtaceae). Austral J Bot 60:707–717. https://doi.org/10.1071/bt12149

    Article  Google Scholar 

  • da Silva CJ, Ribeiro JPO, Meira RMSA (2019) New registers of colleters in species of Myrtaceae from Brazilian Cerrado. Rodriguésia 70:1–9. https://doi.org/10.1590/2175-7860201970055

    Article  Google Scholar 

  • Dalvi VC, Cardinelli LS, Meira RMSA, Azevedo AA (2014) Foliar colleters in Macrocarpaea obtusifolia (Gentianaceae): anatomy, ontogeny, and secretion. Botany 92(1):59–67. https://doi.org/10.1139/cjb-2013-0203

  • Dalvi VC, de Faria GS, Azevedo AA (2020) Calycinal secretory structures in Calolisianthus pedunculatus (Cham. & Schltdl) Gilg (Gentianaceae): anatomy, histochemistry, and functional aspects. Protoplasma 257:275–284. https://doi.org/10.1007/s00709-019-01436-5

  • Dalvi VC, Meira RMSA, Francino DMT, Silva LC, Azevedo AA (2013) Anatomical characteristics as taxonomic tools for the species of Curtia and Hockinia (Saccifolieae-GentianaceaeJuss.). Pl Sys Evol 300(1):99–112. https://doi.org/10.1007/s00606-013-0863-1

  • Delgado MN, Azevedo AA, Silva LC, Valente GE, Kasuya MCM (2011) Comparative anatomy of Calolisianthus species (Gentianaceae – Helieae) from brazil: taxonomic aspects. Edinburgh J Bot 68(1):139–155. https://doi.org/10.1017/s0960428610000284

    Article  Google Scholar 

  • Demarco D (2008) Glândulas de órgãos vegetativos aéreos e florais de espécies de Asclepiadeae (R. Br) Duby (Asclepiadoideae, Apocynaceae) de Mata Atlântica do estado de São Paulo. Ph.D. Thesis, University of Campinas, Campinas, Brazil.

  • Dexheimer J, Guenin F (1981) Étude de la sécrétion de mucilage par le trichomes stipulaires de Psychotria bacteriophyla (Rubiaceae). Cytologia 46:731–747

  • Dupree P, Sherrier DJ (1998) The plant Golgi apparatus. Biochim Biophys Acta 1404:259–270

    Article  CAS  Google Scholar 

  • Evert RF (2006) Esau’s Plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. John Wiley & Sons Inc, Hoboken

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

    Google Scholar 

  • Fahn A (2000) Structure and function of secretory cells. Advances Bot Res 31:37–75. https://doi.org/10.1016/s0065-2296(00)31006-0

    Article  CAS  Google Scholar 

  • Fernandes VF, Thadeo M, Dalvi VC, Marquete R, Meira RMSA (2016) Colleters in Casearia (Salicaceae): a new interpretation for the theoid teeth. Bot J Linn Soc 181(4):682–691. https://doi.org/10.1111/boj.12432

  • Gabe M (1968) Techniques histologiques. Masson and Cie, Paris

    Google Scholar 

  • Guimarães EF, Dalvi VC, Azevedo AA (2013) Morphoanatomy of Schultesia pachyphylla (Gentianaceae): a discordant pattern in the genus. Botany 91(12):830–839. https://doi.org/10.1139/cjb-2013-0077

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York

    Google Scholar 

  • Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2009) Sistemática Vegetal um enfoque filogenético, 3rd edn. Porto Alegre, Artmed

    Google Scholar 

  • Kamdee C, Kirasak K, Ketsa S, van Doorn WG (2015) Vesicles between plasma membrane and cell wall prior to visible senescence of Iris and Dendrobium flowers. J Pl Physiol 188:37–43. https://doi.org/10.1016/j.jplph.2015.02.013

  • Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Khan MS, Hemalatha S (2015) Autophagy: molecular insight and role in plant programmed cell death and defense mechanism. Int Res J Biological Sci 4(2):78–83

    Google Scholar 

  • Klein DE, Gomes VM, Silva-Neto SJ, Cunha M (2004) The structure of colleters in several species of Simira (Rubiaceae). Ann Bot 94(5):733–740

  • Leitão CAE, Cortelazzo AL (2008) Structural and histochemical characterisation of the colleters of Rodriguezia venusta (Orchidaceae). Austral J Bot 56:161–165

    Article  Google Scholar 

  • Lersten NR (1974a) Colleter morphology in Pavetta, Neorosea and Tricalysia (Rubiaceae) and its relationship to the bacterial leaf nodule symbiosis. Bot J Linn Soc 69(2):125–136. https://doi.org/10.1111/j.1095-8339.1974.tb01620.x

    Article  Google Scholar 

  • Lersten NR (1974b) Morphology and distribution of colleters and crystals in relation to the taxonomy and bacterial leaf nodule symbiosis of Psychotria (Rubiaceae). Amer J Bot 61(9):973–981. https://doi.org/10.1002/j.1537-2197.1974.tb14037.x

  • Lersten NR (1975) Colleter types in Rubiaceae, especially in relation to the bacterial leaf nodule symbiosis. Bot J Linn Soc 71(4):311–319. https://doi.org/10.1111/j.1095-8339.1975.tb01207.x

    Article  Google Scholar 

  • Lillie RD (1965) Histopathologic technic and practical histochemistry. McGraw Hill, New York

    Google Scholar 

  • Machado SR, Barreiro DP, Rocha JF, Rodrigues TM (2012) Dendroid colleters on vegetative and reproductive apices in Alibertia sessilis (Rubiaceae) differ in ultrastructure and secretion. Flora, Morphol Distrib Funct Ecol Pl 207(12):868–877. https://doi.org/10.1016/j.flora.2012.09.013

    Article  Google Scholar 

  • Machado SR, Paleari LM, Paiva ÉAS, Rodrigues TM (2015) Colleters on the inflorescence axis of Croton glandulosus (Euphorbiaceae): structural and functional characterization. Int J Pl Sci 176(1):86–93. https://doi.org/10.1086/678469

    Article  Google Scholar 

  • Martius CFP von. (1826) 1827. Nova genera et species plantarum quas in itinere per Brasiliam annis 1817–1820. Vol. 2. Wolf, München 148 pp.

  • Marty F (1978) Cytochemical studies on GERL, provacuoles, and vacuoles in root meristematic cells of Euphorbia. Proc Natl Acad Sci 75(2):852–856. https://doi.org/10.1073/pnas.75.2.852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marty F (1999) Plant vacuoles. Pl. Cell 11(4):587–599. https://doi.org/10.1105/tpc.11.4.587

    Article  CAS  Google Scholar 

  • Matile P, Moor H (1968) Vacuolation: origin and development of the lysosomal apparatus in root-tip cells. Planta (Berl. 80: 159–175. https://doi.org/https://doi.org/10.1007/bf00385592.

  • Mayer JLS, Cardoso-Gustavson P, Appezzato-da-Glória B (2011) Colleters in monocots: new record for Orchidaceae. Flora, Morphol Distrib Funct Ecol Pl 206:185–190. https://doi.org/10.1016/j.flora.2010.09.003

    Article  Google Scholar 

  • Mayer JLS, Carmello-Guerreiro SM, Mazzarefa P (2013) A functional role for the colleters of coffee flowers. AoB Plants 5:1–13. https://doi.org/10.1093/aobpla/plt029

    Article  Google Scholar 

  • McManus JFA (1948) Histological and histochemical uses of periodic acid. Stain Technol 23:99–108

    Article  CAS  Google Scholar 

  • Mercadante-Simões MO, Paiva EAS (2013) Leaf colleters in Tontelea micrantha (Celastraceae, Salacioideae): Ecological, morphological and structural aspects. C R Biol 336:400–406. https://doi.org/10.1016/j.crvi.2013.06.007

  • Miguel EC, da Cunha M, Miguel TBAR, Barros CF (2016) Ontogenesis secretion and senescence of Tocoyena bullata (Vell.) Mart. (Rubiacaeae) colleters. Pl Biol 18(5):851–858. https://doi.org/10.1111/plb.12473

  • Miguel EC, Gomes VM, de Oliveira MA, da Cunha M (2006) Colleters in Bathysa nicholsonii K. Schum. (Rubiaceae): ultrastructure, secretion protein composition, and antifungal activity. Pl Biol 8:15–722

  • Miguel EC, Klein DE, de Oliveira MA, da Cunha M (2010) Ultrastructure of secretory and senescence phase in colleters of Bathysa gymnocarpa and B. stipulata (Rubiaceae). Brazil J Bot 33(3):425–436. https://doi.org/10.1590/s0100-84042010000300006

  • Miguel EC, Pireda S, Barros CF, Zottich U, Gomes VM, Miguens FC, da Cunha M (2017) Outer cell wall structure and the secretion mechanism of colleters of Bathysa nicholsonii K. Schum. (Rubiaceae). Acta Bot Brasil 31(3):411–419

  • Miller IM, Scott A, Gardner IC (1983) The development, structure and function of dendroid colleters in Psychotria kirkii Hiern (Rubiaceae). Annals Bot 51(5):621–630. https://doi.org/10.1093/oxfordjournals.aob.a086509

  • Molina J, Struwe L (2009) Utility of secondary structure in phylogenetic reconstructions using nrDNA ITS sequences—an example from Potalieae (Gentianaceae: Asteridae). Syst Bot 34:414–428

    Article  Google Scholar 

  • Mollenhauer HH, Morre DJ (1966) Golgi apparatus and plant secretion. Annual RPl Physiol 17(1):27–46. https://doi.org/10.1146/annurev.pp.17.060166.000331

    Article  Google Scholar 

  • Nebenführ A, Staehelin LA (2001) Mobile factories: Golgi dynamics in plant cells. Trends Plant Sci 6(4):160–167. https://doi.org/10.1016/s1360-1385(01)01891-x

    Article  PubMed  Google Scholar 

  • Nemomissa S (1997) Floral character states of the Northeast and Tropical East African Swertia species (Gentianaceae). Nordic J Bot 17(2):145–156. https://doi.org/10.1111/j.1756-1051.1997.tb00301.x

  • O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373

  • O’Brien TP, Mccully ME (1981) The study of plant structure principles and selected methods. Termarcarphi Ptey. Ltd., Melbourne

  • Oliveira CS, Salino A, Paiva EAS (2017) Colleters in Thelypteridaceae: unveiling mucilage secretion and its probable role in ferns. Flora 228:65–70. https://doi.org/10.1016/j.flora.2017.01.009

    Article  Google Scholar 

  • Paiva EAS (2009) Occurrence, structure and functional aspects of the colleters of Copaifera langsdorffii Desf. (Fabaceae, Caesalpinioideae). C R Bio 332(12):1078–1084. https://doi.org/10.1016/j.crvi.2009.08.003

  • Paiva EAS (2016) How do secretory products cross the plant cell wall to be released? A new hypothesis involving cyclic mechanical actions of the protoplast. Annals Bot 117(4):533–540. https://doi.org/10.1093/aob/mcw012

    Article  CAS  Google Scholar 

  • Paiva EAS, Machado SR (2006) Ontogenesis, structure and ultrastructure of Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) colleters. Revista Biol Trop 54(3):943–950

    Article  Google Scholar 

  • Pearse AGE (1985) Histochemistry theoretical and applied: preparative and optical technology. Churchill Livingston, Edinburgh

    Google Scholar 

  • Pinheiro SKP, Teófilo FBS, Lima AKM, Cordoba BV, Migeul TBAR, Miguel EC (2019) Ontogegenesis and secretion mecanismo of Morinda citrifolia L. (Rubiaceae) colleters. S African J Bot 21:26–33

  • Renobales G, Diego E, Urcelay B, López-Quintana A (2001) Secretory hairs in Gentiana and allied genera (Gentianaceae, subtribe Gentianinae) from the Iberian Peninsula. Bot J Linn Soci 136(1):119–129. https://doi.org/10.1111/j.1095-8339.2001.tb00560.x

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17(1):208–212

    Article  CAS  Google Scholar 

  • Ribeiro JC, Ferreira MJP, Demarco D (2017) Colleters in Asclepiadoideae (Apocynaceae): protection of meristems against desiccation and new functions assigned. Int J Pl Scis 178(6):465–477. https://doi.org/10.1086/692295

    Article  Google Scholar 

  • Rios ABM, Menino GCdeO, Dalvi VC, (2020) Leaf teeth in eudicots: what can anatomy elucidate? Bot J Lin Soc 193(4):504–522. https://doi.org/10.1093/botlinnean/boaa028

    Article  Google Scholar 

  • Robbrecht E (1983) The African genus Tricalysia A. Rich. (Rubiaceae) 3. Probletostemon revived as a section of subgenus Tricalysia. Bulletin van Natomale Plantentuin van Belgie 53:299–320

  • Robbrecht E (1987) The African genus Tricalysia A. Rich. (Rubiaceae) 4. A revision of the species of section Tricalysia. Bulletin van Natomale Plantentuin van Belgie 57:39–208

  • Roshchina VV, Roshchina VD (1993) The excretory function of higher plants. Springer-Verlang, Berlin

    Book  Google Scholar 

  • Sacher JA (1954) Structure and seasonal activity of the shoot apices of Pinus lambertiana and Pinus ponderosa. Amer J Bot 41(9):749–759. https://doi.org/10.2307/2438961

  • Sacher JA (1955) Cataphyll ontogeny in Pinus lambertiana. Amer J Bot 42(1):82–91. https://doi.org/10.2307/2438596

  • Santos de Faria DN, Fernandes VF, Marquete R, Meira RMSA (2019) Morphology, anatomy, and exudates of stipularcolleters in Casearia Jacq (Salicaceae) across two tropical plant communities. Int J Pl Sci 180:141–152. https://doi.org/10.1086/700637

  • Sheue C-R, Chesson P, Chen Y-J, Wu S-Y, Wu Y-H, Yong JWH, Guu T-Y et al (2013) Comparative systematic study of colleters and stipules of Rhizophoraceae with implications for adaptation to challenging environments. Bot J Linn Soc 172(4):449–464. https://doi.org/10.1111/boj.12058

    Article  Google Scholar 

  • Simões AO, Castro MM, Kinoshita LS (2006) Calycine colleters of seven species of Apocynaceae (Apocynoideae) from Brazil. Bot J Linn Soc 152:387–398

    Article  Google Scholar 

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

    Google Scholar 

  • Struwe L, Albert VA (2002) Gentianaceae: systematic and natural history. University Press, Cambridge

    Google Scholar 

  • Struwe L, Albert VA, Calió FM, Frasier C, Lepis KB, Mathews KG, Grant JR (2009) Evolutionary patterns in neotropical Helieae (Gentianaceae): evidence from morphology, chloroplast and nuclear DNA sequences. Taxon 58(2):479–499. https://doi.org/10.1002/tax.582013

    Article  Google Scholar 

  • Thomas V (1991) Review article. Structural, functional and phylogenetic aspects of the colleter. Annals Bot 68(4): 287–305. https://doi.org/https://doi.org/10.2307/42758461.

  • Thomas V, Dave Y (1989) Histochemistry and senescence of colleters of Allamanda cathartica (Apocynaceae). Annals Bot 64(2):201–203

    Article  Google Scholar 

  • Tresmondi F, Nogueira A, Guimarães E, Machado SR (2015) Morphology, secretion composition, and ecological aspects of stipular colleters in Rubiaceae species from tropical forest and savanna. Sci Nat 102(11–12):1–15. https://doi.org/10.1007/s00114-015-1320-5

    Article  CAS  Google Scholar 

  • Tresmondi F, Canaveze Y, Guimarães E, Machado SR (2017) Colleters in Rubiaceae from forest and savanna: the link between secretion and environment. Sci Nat 104(3–4):1–12. https://doi.org/10.1007/s00114-017-1444-x

    Article  CAS  Google Scholar 

  • Tullii CF, Miguel EC, Lima NB, Fernandes KVS, Gomes VM, da Cunha M (2013) Characterization of stipular colleters of Alseis pickelii. Botany 91(6):403–413. https://doi.org/10.1139/cjb-2012-0249

    Article  CAS  Google Scholar 

  • van Doorn WG, Papini A (2013) Ultrastructure of autophagy in plant cells - a review. Autophagy 9(12):1922–1936. https://doi.org/10.4161/auto.26275

    Article  CAS  PubMed  Google Scholar 

  • van Doorn WG, Woltering EJ (2005) Many ways to exit? Cell death categories in plants. Trends Pl Sci 10(3):117–122. https://doi.org/10.1016/j.tplants.2005.01.006

    Article  CAS  Google Scholar 

  • Viotti C (2014) ER and vacuoles: never been closer Front. Plant Sci 5(1):7. https://doi.org/10.3389/fpls.2014.00020

    Article  Google Scholar 

  • Viotti C, Kruger F, Krebs M, Neubert C, Fink F, Lupanga U, Scheuring D et al (2013) The endoplasmic reticulum is the main membrane source for biogenesis of the lytic vacuole in Arabidopsis. Pl Cell 25(9):3434–3449. https://doi.org/10.1105/tpc.113.114827

    Article  CAS  Google Scholar 

  • Zanotti A (2018) Estruturas secretoras em Calolisianthus speciosus (Cham. & Schltdl.) Gilg. (Gentianaceae): ontogenia e biologia da secreção. Dissertation, Federal University of Viçosa, Viçosa, Brazil.

  • Zer H, Fahn A (1992) Floral nectaries of Rosmarinus officinalis L. structure, ultrastructure and nectar secretion. Ann Bot 70:391–397

    Article  Google Scholar 

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Acknowledgements

We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting a Scientific Initiation scholarship to Jailma Rodrigues Gonçalves. We thank the Ministério da Ciência e Tecnologia/Conselho Nacional de Desenvolvimento Científico e Tecnológico (MCT/CNPq; Brasília, Brazil; Grant 406824/2016-9) and the Instituto Federal de Educação, Ciência e Tecnologia Goiano (IF Goiano, campus Rio Verde) for the financial support, the Laboratório Multiusuário de Microscopia de Alta Resolução (LabMic) of the Universidade Federal de Goiás (UFG) and Núcleo de Microscopia e Microanálise of the Universidade Federal de Viçosa (UFV) for the preparation and analysis of electron microscopy samples, and the Instituto Chico Mendes de Conservação da Biodiversidade/Sistema de Autorização e Informação em Biodiversidade (ICMBio/SISBIO) for collection license.

Funding

This study was supported by the Ministério da Ciência e Tecnologia/Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brasília, Brazil; Grant 406824/2016–9 to Valdnéa Casagrande Dalvi).

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  1. Instituto Federal de Educação, Ciência e Tecnologia Goiano (IF Goiano, Campus Rio Verde), Rodovia Sul Goiana, Km 01, Zona Rural, Rio Verde, Goiás, CEP 75901-970, Brazil

    Jailma Rodrigues Gonçalves, Luana Silva dos Santos & Valdnéa Casagrande Dalvi

  2. Departamento de Agronomia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, CEP 36570-900, Brazil

    Diego Ismael Rocha

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  4. Valdnéa Casagrande Dalvi
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The research project was designed by Valdnéa Casagrande Dalvi. The samples were collected by Valdnéa Casagrande Dalvi; light microscopy and histochemical analyses were performed by Jailma Rodrigues Gonçalves and Luana Silva dos Santos; scanning and transmission microscopy were performed by Valdnéa Casagrande Dalvi, Jailma Rodrigues Gonçalves, and Diego Ismael Rocha. The manuscript was written by Valdnéa Casagrande Dalvi, Jailma Rodrigues Gonçalves, and Diego Ismael Rocha.

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Gonçalves, J.R., Rocha, D.I., dos Santos, L.S. et al. The short but useful life of Prepusa montana Mart. (Gentianaceae Juss.) leaf colleters—anatomical, micromorphological, and ultrastructural aspects. Protoplasma 259, 187–201 (2022). https://doi.org/10.1007/s00709-021-01651-z

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