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1. 1 2022-06-03T09:30:37-07:00 Tim Sisneros a58829fb647d6ce7b9c40b457c686ddadf0f976f Paullinia cupana phylogenetic placement within the Sapindaceae Tim Sisneros 4 plain 2022-06-03T09:50:05-07:00 Tim Sisneros a58829fb647d6ce7b9c40b457c686ddadf0f976f

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• 1 2022-05-11T11:21:27-07:00 From medicine to industry: the multifaceted history of Guaraná (Paullinia cupana Kunth., Sapindaceae) 42 Paullinia cupana, nature’s caffeine tablet, is a climbing shrub with a very deep history within indigenous South American tribes. Known by locals as guaraná, it has an easily recognizable fruit with an eyeball-like structure, giving it the name of “eye of the gods.” The seeds contain the highest concentrations of caffeine of any other plant – about four times the amount found in coffee beans. It was commonly used by the Sateré Maué people to make beverages and used as medicine for bodily discomfort as far back as over 2,000 years ago. Nowadays, despite its popularity, the only country that cultivates guaraná is Brazil, with over 15,000 hectares of land growing it. Its importance to Brazilians has led to the deforestation of parts of the Amazon in order to make room to grow guaraná. In 2006, the cash value of domestic production of guaraná was over $13 billion and has continued to increase due to the growing domestic and international demand. Due to the seed’s high caffeine content and unique flavor, its extract has become a widely used additive in energy drinks. The most recognizable of which is the very popular soda, Guaraná Antarctica, and is the biggest competitor of Coca Cola in Brazil. By Tim Sisneros and Edward Teng. plain 2022-06-06T19:45:52-07:00

  Nomenclatural History

  Paullinia cupana’s nomenclatural history is tenuous as it has been called guaraná by several indigenous groups throughout the Amazon. Most historians agree that the origin of guaraná’s name comes from the Tupí-Guaraní language but more particularly, the Tupí language as these people lived throughout guaraná’s range (Prance & Nesbitt, 2005). Although, as the Tupí language is extinct, the meaning of the word guaraná comes from the Guaraní word guara-ná which itself has its roots from the Sateré Maué word for the plant, warana. In Guaraní, this can mean either “fruit like the eyes of the gods” or “eyes of the gods” (Prance & Nesbitt, 2005). Other sources found the meaning to be "drink of the Lords" (Atroch et al., 2012). Guaraná was first introduced to Europeans during the late 16^th century when it was brought back to Europe from eastern Brazil by Spanish conquistadors and was formally classified by the German botanist Reinhard Gustav Paul Knuth as Paullinia cupana in 1821 from a specimen collected a decade earlier by the naturalists Humboldt and Bonpland in Venezuela (Hamerski et al., 2013). In 1823, a new species of Paullinia, P. sorbilis, was described by the botanist Karl Martius (IPNI, 2021.) and was noted to have very similar characteristics to P. cupana (Hamerski et al., 2013). Although in 1937, the Brazilian botanist, Adolpho Ducke, placed P. sorbilis as a variety of P. cupana. Then, both P. sorbilis and P. cupana var. sorbilis were circumscribed into P. cupana in 2012 by Acevedo-Rodríguez et al. (2012).
   

  Evolutionary history

  Paullinia cupana is part of the soapberry family (Sapindaceae) which contains many known species of plants such as the horse chestnut (Aesculus spp.), maples (Acer spp.), and lychee (Litchi spp.). Within the Sapindaceae, P. cupana is nestled within the monophyletic subfamily Paullinieae which contains the other genera, Thinouia, Lophostigma, Urvillea, Cardiospermum, Serjania, and Paullinia. The genus Paullinia have ca. 220 members that are mostly restricted to neotropical forests. Members of the genus Paullinia have had some controversy in terms of their relationships at the species level. Recent molecular phylogenies have failed to resolve sister taxa to Paullinia due to the lack of resolution from over 327 chloroplast markers for species-level relationships in the genus, even with other genes such as ITS and the trnL intron included (Acevedo-Rodríguez et al., 2017). The most recent phylogeny was constructed using morphological data focusing on laticifers (milky-sap secreting cell found in the leaves and stem) which was able to resolve a few other species (Medina et al., 2021), although only about half of the genus has not been sampled to date (Acevedo-Rodríguez et al., 2017; Medina et al., 2021).

   

  Ecology and life history

  Guaraná is a perennial lowland, tropical, woody, climbing shrub that is found throughout northern Amazon regions such as Guyana, Venezuela, and Brazil; in the latter, the plant occurs in the states Amazonas and Pará (Medeiros et al., 2016). The plant generally takes around 5 years to begin producing significant amounts of fruit but can have set fruit by the second year. Pollination is relatively unknown but the general pollination syndrome of guaraná tree seems to be adapted to the Hymenoptera (in particular, bees) and that the species Melipona seminigra, Xylocopa muscaria, and Apis mellifera are among the most important pollinators (Atroch et al., 2012). P. cupana has many wild relatives but the genus is utilized by local peoples where it occurs such that ancestral traits are currently being sorted (Medeiros et al., 2016). An estimated 20% of Paullinia spp. have extensive ethnobotanical uses (Beck, 1990; Brazilian Amazon Consortium for Genomic Research (REALGENE) et al., 2008; Hamerski et al., 2013).
   

  Morphology

  Guaraná is a climbing woody shrub to a semi-erect shrub up to ca. 2 meters tall that can be distinguished by the presence of 4-5 deep grooves in the main stem/different branches. The epidermis is dark green and is woody near the base. The guaraná leaves are distichously arranged, pinnately 5-foliate, and can measure up to 40 cm in length at maturity. Inflorescences are thyrses which can be solitary, racemiform, or axillary. The flowers are partially single sexed with some staminate flowers, while the others are hermaphroditic. The fruit is a bright red capsule with a black colored seed partially covered by white arils (Medeiros et al., 2016).
  

  History

  The contrasting colors of guaraná's partially dehisced fruit resemble eyeballs, which gave rise to a legend by the Sateré Maué tribe in Brazil. The myth states that a malevolent god lured a male child into the forest and killed them out of jealousy. When the people in the village found the child, a benevolent god then gifted the Sateré Maué guaraná by planting the child's left eye in the village which birth the first (Atroch et al., 2012). The seeds were traditionally toasted and ground into powder. The resulting powder was then dissolved into water alone or in combination with other herbs. Guaraná was first reported in 1669 by Bettendorf, a high-ranking Jesuit of the Company of Jesus, in Maranhao, and noted that the plant was used extensively by Sateré Maué people. In 1900s, naturalist observed the same thing, and proposed that the Sateré Maué people arrived around the Maué and Andiras River 2000 years ago, and the domestication of guaraná plant likely started after their arrival. Another theory by Ducke stated that guaraná cultivation originated on the upper Rio Negro and upper Orinoco and was brought into the region where the Sateré Maué lived (Atroch et al., 2012; Smith & Atroch, 2010).
   

  Cultivation practices

  Guaraná is grown on both small and large farms throughout Brazil (mostly in Amazonia), either as a monocrop or alongside with hedgerows. Guaraná is usually harvested by hand in the dry season when the entire fruit bunch is ripe where it is either snipped off with scissors, small pruning shears or broken off manually. If the infructescence doesn’t uniformly ripen, then they are picked individually. The guarana ́ fruits are then placed in a basket and carried back to be processed and roasted. Before roasting the seeds, the red fruits are skinned by hand, left to soak in water, or simply stored for several days until the skin softens. Currently, Brazil is the largest and only producer of guaraná in the world with 15,356 hectares of land planted with guaraná, producing 2698 metric tons of dry seeds and a productivity of 229 kg/ha. The cash value of domestic production is over 13 billion in 2006. With the domestic demand and international demand increasing, more land in Brazil has been cleared for the cultivation of guaraná (Atroch et al., 2012).
   

  Human experiences and nutritional value

  The Sateré Maué people had a wide use of the guaraná plant. They normally would crush the guaraná seed and use it as a beverage and an herb to treat diarrhea, arthritis, and deal with fatigue and hunger (Atroch et al., 2012). Currently, guaraná soda is very popular in Brazil, equally popular as Coca Cola in Brazil, and it is made from powder made from guaraná seeds. Guaraná seeds are the most consumed part of the plant due to its high tannin and caffeine content, four times as much as coffee beans. And it is often ground up into power and made into a beverage (Smith & Atroch, 2010). Modern uses for guaraná are currently being researched but there are some promissory notes on the pharmacological applications of the seed extract in increasing cognitive performance, fatigue-relief from chemotherapy, antioxidant activity, chemopreventive on carcinogenesis, and many others (Hamerski et al., 2013; Marques et al., 2019).
   

  References

  1. Acevedo-Rodríguez, P. (2012). Sapindaceae. In Oliveira SM, Flora of the Guianas, Royal Botanic Gardens, Kew. p. 196.

  2. Atroch, A. L., Filho, F. J. do N., Ângelo, P. C. da S., Vieira de Freitas, D., de Sousa, N. R., ilela de Resende, M. D., & Clement, C. R. (2012). Chapter 17: Domestication and Breeding of the guaraná’ Tree. In Domestication and Breeding: Amazonian Species (pp. 333–360). Vicosa (Brazil) Univ. Federal de Vicosa. https://www.researchgate.net/publication/303023020_Domestication_and_breeding_of_the_guaraná_tree
  3. Beck, H. T. (1990). A Survey of the Useful Species of Paullinia L. (Sapindaceae). Advances in Economic Botany, 8, 17.
  4. Brandt, W., Gürke, M. (Max), Köhler, F. E. (Franz E., Pabst, G. (Gustav), Schellenberg, G. (Gustav), & Vogtherr, M. (1883). Köhler’s Medizinal-Pflanzen in naturgetreuen Abbildungen mit kurz erläuterndem Texte: Atlas zur Pharmacopoea germanica, austriaca, belgica, danica, helvetica, hungarica, rossica, suecica, Neerlandica, British pharmacopoeia, zum Codex medicamentarius, sowie zur Pharmacopoeia of the United States of America / herausgegeben von G. Pabst. Gera-Untermhaus : Fr. Eugen Köhler, [1883-1914]. https://archive.org/details/mobot31753002839105/page/n497/mode/2up
  5. Brazilian Amazon Consortium for Genomic Research (REALGENE), Ângelo, P. C. S., Nunes-Silva, C. G., Brígido, M. M., Azevedo, J. S. N., Assunção, E. N., Sousa, A. R. B., Patrício, F. J. B., Rego, M. M., Peixoto, J. C. C., Oliveira, W. P., Freitas, D. V., Almeida, E. R. P., Viana, A. M. H. A., Souza, A. F. P. N., Andrade, E. V., Acosta, P. O. A., Batista, J. S., Walter, M. E. M. T., … Astolfi-Filho, S. (2008). Guaraná (Paullinia cupana var. sorbilis), an anciently consumed stimulant from the Amazon rain forest: The seeded-fruit transcriptome. Plant Cell Reports, 27(1), 117–124. https://doi.org/10.1007/s00299-007-0456-y
  6. Chery, J. G., Acevedo-Rodríguez, P., Rothfels, C. J., & Specht, C. D. (2019). Phylogeny of Paullinia L. (Paullinieae: Sapindaceae), a diverse genus of lianas with dynamic fruit evolution. Molecular Phylogenetics and Evolution, 140, 106577. https://doi.org/10.1016/j.ympev.2019.106577
  7. guaraná_(Paullinia_cupana)_fruits_(29055398276).jpg (3648×4504). (n.d.). Retrieved May 10, 2022, from https://upload.wikimedia.org/wikipedia/commons/2/21/guaraná%C3%A1_%28Paullinia_cupana%29_fruits_%2829055398276%29.jpg
  8. Huang, R., O’Donnell, A. J., Barboline, J. J., & Barkman, T. J. (2016). Convergent evolution of caffeine in plants by co-option of exapted ancestral enzymes. Proceedings of the National Academy of Sciences, 113(38), 10613–10618. https://doi.org/10.1073/pnas.1602575113
  9. Jud, N. A., Allen, S. E., Nelson, C. W., Bastos, C. L., & Chery, J. G. (2021). Climbing since the early Miocene: The fossil record of Paullinieae (Sapindaceae). PLOS ONE, 16(4), e0248369. https://doi.org/10.1371/journal.pone.0248369
  10. Krug, C., Garcia, M. V. B., & Gomes, F. B. (2015). A scientific note on new insights in the pollination of guaraná (Paullinia cupana var. Sorbilis). Apidologie, 46(2), 164–166. https://doi.org/10.1007/s13592-014-0304-3
  11. Lleras, E. (n.d.). Species of Paullinia with economic potential. In Neglected Crops: 1492 from a Different Perspective. Retrieved May 9, 2022, from https://hort.purdue.edu/newcrop/1492/Paullinia.html
  12. Maristela, M., Ariane, M. K., Ana, C. S. dos S., Ormezinda, C. C. F., & Vildes, M. S. (2014). Evaluation of ochratoxin A and fungi in powdered guaraná (Paullinia cupana Kunth), a caffeine rich product from Amazon forest. African Journal of Microbiology Research, 8(6), 545–550. https://doi.org/10.5897/AJMR2013.6579
  13. Marques, L. L. M., Ferreira, E. D. F., Paula, M. N. de, Klein, T., & Mello, J. C. P. de. (2019). Paullinia cupana: A multipurpose plant – a review. Revista Brasileira de Farmacognosia, 29(1), 77–110. https://doi.org/10.1016/j.bjp.2018.08.007
  14. Medeiros, H., Forzza, R. C., & Acevedo-Rodríguez, P. (2016). Wild Relatives of guaraná ( Paullinia cupana , Sapindaceae) in Southwestern Brazilian Amazon. Systematic Botany, 41(1), 202–228. https://doi.org/10.1600/036364416X690606
  15. 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, 612985. https://doi.org/10.3389/fpls.2020.612985
  16. Natural And Organic Energy Shot—Organic Energy Shots | SuddenRush guaraná. (n.d.). SuddenRush guaraná USA. Retrieved May 10, 2022, from https://suddenrushGuaraná.com/pages/our-mission
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  18. Smith, N., & Atroch, A. L. (2010). Guaraná’s Journey from Regional Tonic to Aphrodisiac and Global Energy Drink. Evidence-Based Complementary and Alternative Medicine, 7(3), 279–282. https://doi.org/10.1093/ecam/nem162