Evolutionary history and leaf succulence as explanations for medicinal use in aloes and the global popularity of Aloe vera

BMC Evolutionary Biology

Nina Rønsted⁹  Monique SJ Simmonds⁵  Sebsebe Demissew¹  Sophie Neale⁶  Charlotte S Bjorå⁷  Ronell R Klopper^1,10  Gideon F Smith²  Abraham E van Wyk⁴  Félix Forest⁵  Matthew RE Symonds⁸  Sven Buerki³  Olwen M Grace⁹ 

[1] Department of Plant Biology and Biodiversity Management, National Herbarium, College of Natural Sciences, Addis Ababa University, Addis Ababa, Ethiopia;Departamento de Ciências da Vida, Centre for Functional Ecology, Universidade de Coimbra, Coimbra, 3001-455, Portugal;Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK;Department of Plant Science, H.G.W.J. Schweickerdt Herbarium, University of Pretoria, Pretoria 0002, South Africa;Jodrell Laboratory, Royal Botanic Gardens, Kew, Surrey, London TW9 3DS, UK;Centre for Middle Eastern Plants, Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK;Natural History Museum, University of Oslo, Blindern NO-0318, Oslo, Norway;Centre for Integrative Ecology, School of Life & Environmental Sciences, Deakin University, 221 Burwood Highway, Burwood 3125, Victoria, Australia;Natural History Museum of Denmark, University of Copenhagen, Sølvgade 83 Entrance S, Copenhagen K, DK1307, Denmark;Biosystematics Research & Biodiversity Collections Division, South African National Biodiversity Institute, Private Bag X101, 0001, Pretoria, South Africa

关键词: Succulent plants;    Medicinal use;    Phylogeny;    Biogeography;    Evolution;    Aloe vera;   

Others  :  1158304
DOI  :  10.1186/s12862-015-0291-7

 received in 2014-10-07, accepted in 2015-01-15,  发布年份 2015

【 摘 要 】

Background

Aloe vera supports a substantial global trade yet its wild origins, and explanations for its popularity over 500 related Aloe species in one of the world’s largest succulent groups, have remained uncertain. We developed an explicit phylogenetic framework to explore links between the rich traditions of medicinal use and leaf succulence in aloes.

Results

The phylogenetic hypothesis clarifies the origins of Aloe vera to the Arabian Peninsula at the northernmost limits of the range for aloes. The genus Aloe originated in southern Africa ~16 million years ago and underwent two major radiations driven by different speciation processes, giving rise to the extraordinary diversity known today. Large, succulent leaves typical of medicinal aloes arose during the most recent diversification ~10 million years ago and are strongly correlated to the phylogeny and to the likelihood of a species being used for medicine. A significant, albeit weak, phylogenetic signal is evident in the medicinal uses of aloes, suggesting that the properties for which they are valued do not occur randomly across the branches of the phylogenetic tree.

Conclusions

Phylogenetic investigation of plant use and leaf succulence among aloes has yielded new explanations for the extraordinary market dominance of Aloe vera. The industry preference for Aloe vera appears to be due to its proximity to important historic trade routes, and early introduction to trade and cultivation. Well-developed succulent leaf mesophyll tissue, an adaptive feature that likely contributed to the ecological success of the genus Aloe, is the main predictor for medicinal use among Aloe species, whereas evolutionary loss of succulence tends to be associated with losses of medicinal use. Phylogenetic analyses of plant use offer potential to understand patterns in the value of global plant diversity.

【 授权许可】

   
2015 Grace et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Schulz H. Global aloe market estimated at $13 billion. Available at http://www.nutraingredients-usa.com/Markets/Global-aloe-market-estimated-at-13-billion.
• [2]Reynolds T, Dweck AC: Aloe vera leaf gel, a review updated. J Ethnopharmacol 1999, 68:3-37.
• [3]Hodge WH: The drug aloes of commerce, with special reference to the Cape species. Econ Bot 1953, 7:99-129.
• [4]Grace OM: Current perspectives on the economic botany of the genus Aloe Xanthorrhoeaceae. S Afr J Bot 2011, 98:980-987.
• [5]Grindlay D, Reynolds T: The Aloe vera phenomenon – a review of the properties and modern uses of the leaf parenchyma gel. J Ethnopharmacol 1986, 16:117-151.
• [6]Grace OM, Dzajic A, Jager AK, Nyberg NT, Onder A, Rønsted N: Monosaccharide analysis of succulent leaf tissue in Aloe. Phytochem 2013, 93:79-87.
• [7]Ogburn RM, Edwards EJ: The ecological water-use strategies of succulent plants. In Advances in Botanical Research Vol. 55. Edited by Kader J-C, Delseny M. Academic Press, Burlington; 2010:179-225.
• [8]Grace OM. Systematics and biocultural value of Aloe L. (Asphodelaceae). PhD Thesis. University of Pretoria; 2009.
• [9]Mittermeier RA, Gill PR, Hoffman M, Pilgrim J: Hotspots Revisited, Earth’s biologically richest and most threatened terrestrial ecoregions. Cemex & Conservation International, Washington; 2004.
• [10]Arakaki M, Christian P-A, Nyffeler R, Lendel A, Eggli U, Ogurn RM, Spriggs E, Moore MJ, Edwards EJ, et al.: Contemporaneous and recent radiations of the world’s major succulent plant lineages. Proc Natl Acad Sci U S A 2011, 108:8379-8384.
• [11]Daru BH, Manning JC, Boatwright JS, Maurin O, Maclean N, Schaefer H, Kuzmina M, Van der Bank M, et al.: Molecular and morphological analysis of subfamily Alooideae (Asphodelaceae) and the inclusion of Chortolirion in Aloe. Taxon 2013, 62:62-76.
• [12]Manning JC, Boatwrights JS, Daru BH, Maurin O, Van der Bank M: A molecular phylogeny and generic classification of Asphodelaceae subfamily Alooideae: a final resolution of the prickly issue of polyphyly in the alooids? Syst Bot 2014, 39:55-74.
• [13]Treutlein J, Smith GF, Van Wyk B-E, Wink M: Phylogenetic relationships in Asphodelaceae subfamily Alooideae inferred from chloroplast DNA sequences (rbcL, matK) and from genomic fingerprinting (ISSR). Taxon 2003, 52:193-207.
• [14]Zhu F, Qin C, Tao L, Liu X, Ma X, Jia J, Tan Y, Cui C, Link J, Tan C, Jiang Y, Chen Y, et al.: Clustered patterns of species origins of nature-derived drugs and clues for future prospecting. Proc Natl Acad Sci U S A 2011, 108:12943-12948.
• [15]Rønsted N, Symonds MRE, Birkholm T, Christensen SB, Meerow AW, Molander M, Mølgaard P, Petersen G, Rasmussen N, Van Staden J, Stafford GI, Jäger AK: Can phylogeny predict chemical diversity and potential medicinal activity of plants? A case study of Amaryllidaceae. BMC Evol Biol 2012, 12:182. BioMed Central Full Text
• [16]Saslis-Lagoudakis CH, Savolainen V, Williamson EM, Forest F, Wagstaff SJ, Baral SR, Watson MR, Pendry CA, Hawkins JA, et al.: Phylogenies reveal predictive power of traditional medicine in bioprospecting. Proc Natl Acad Sci U S A 2012, 109:15835-15840.
• [17]Guénard G, Von der Ohe PC, Walker SC, Lek S, Legendre P: Using phylogenetic information and chemical properties to predict species tolerances to pesticides. Proc R Soc B 2014, 281:20133239.
• [18]Grace OM, Simmonds MSJ, Smith GF, Van Wyk AE: Documented utility and biocultural value of Aloe L. Ec Bot 2009, 63:167-178.
• [19]Doyle JJ, Doyle JL: A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 1987, 19:11-15.
• [20]Shaw J, Lickey EB, Schilling WEE, Small RL: Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in Angiosperms, the tortoise and the hare III. Am J Bot 1994, 94:275-288.
• [21]Edgar RC: MUSCLE, multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 2004, 32:1792-1797.
• [22]Gouy M, Guindon S, Gascuel O: SeaView version 4, a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224.
• [23]Hall TA: BioEdit, a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1991, 41:95-98.
• [24]R Core Team. R: A Language and Environment for Statistical Computing. Available at http://www.r-project.org.
• [25]Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop GCE. 14 November 2010, New Orleans, LA.; 2010.
• [26]Nixon KC: The Parsimony Ratchet, a new method for rapid parsimony analysis. Cladistics 1999, 15:407-414.
• [27]Stamatakis A. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics; 2014. doi.10.1093/bioinformatics/btu033
• [28]Simmons MP, Ochoterena H: Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 2000, 49:369-381.
• [29]Borchsenius F. FastGap 1.2. Department of Biosciences, Aarhus University, Denmark. Available at http://www.aubot.dk/FastGap_home.htm.
• [30]Ronquist F, Hulsenbeck JP: MRBAYES 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1752-1754.
• [31]Posada D, Crandall KA: Modeltest, testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
• [32]Rambaut A, Drummond AJ. Tracer v1.5. Available at http://beast.bio.ed.ac.uk/Tracer.
• [33]Buerki S, Jose S, Yadav SR, Goldblatt P, Manning JC, Forest F: Contrasting biogeographic and diversification patterns in two Mediterranean-type ecosystems. PLoS One 2012, 7:e39377.
• [34]Chen S, Kim D-K, Chase MW, Kim J-H: Networks in a large-scale phylogenetic analysis, reconstructing evolutionary history of Asparagales (Lilianeae). based on four plastid genes. PLoS One 2013, 8:e59472.
• [35]Sanderson MJ: Estimating absolute rates of molecular evolution and divergence times. A penalized likelihood approach. Mol Biol Evol 2002, 19:101-109.
• [36]Sanderson MJ. r8s version 1.8. Available at http://loco.biosci.arizona.edu/r8s/.
• [37]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
• [38]Ree RH, Smith SA: Maximum-likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 2008, 57:4-14.
• [39]Newton LE: Aloe. In CITES Aloe and Pachypodium Checklist . Edited by Eggli U. Royal Botanic Gardens, Kew; 2001:121-160.
• [40]Newton LE, Govaerts R. World Checklist of Xanthorrhoeaceae. Facilitated by the Royal Botanic Gardens, Kew. Available at http://apps.kew.org/wcsp/.
• [41]Brummitt RK: World Geographical Scheme for Recording Plant Distributions, 2nd ed. Carnegie Mellon University, Pittsburg; 2001.
• [42]Linder HP, De Klerk HM, Born J, Burgess NF, Fjelsda J, Rahbek C: The partitioning of Africa, statistically defined biogeographical regions in sub-Saharan Africa. J Biogeog 2012, 39:1189-1205.
• [43]Cook FEM: Economic Botany Data Collection Standard. Royal Botanic Gardens, Key; 1995.
• [44]Fritz SA, Purvis A: Selectivity in mammalian extinction risk and threat types, a new measure of phylogenetic signal in binary traits. Conserv Biol 2010, 24:1042-1051.
• [45]Orme D. Caper, Comparative Analysis of Phylogenetics and Evolution in R. Available at http://cran.r-project.org/package=caper.
• [46]Reynolds GW: The Aloes of South Africa. Aloes of South Africa Book Fund, Johannesburg; 1950.
• [47]Reynolds GW: The Aloes of Tropical Africa and Madagascar. Mbabane, Aloes Book Fund; 1966.
• [48]Carter S, Lavranos JJ, Newton LE, Walker CC: Aloes, The Definitive Guide. Royal Botanic Gardens, Kew; 2011.
• [49]Maddison WP, Maddison DR. Mesquite, a modular system for evolutionary analysis, v2.73. Available at http://mesquiteproject.wikispaces.com/.
• [50]Maddison WP: Testing character correlation using pairwise comparisons on a phylogeny. J Theor Biol 2000, 202:195-204.
• [51]Grace OM, Klopper RR, Smith GF, Crouch NR, Figueiredo E, Rønsted N, Van Wyk AE: A revised generic classification of Aloe (Xanthorrhoeaceae subfam. Asphodeloideae). Phytotaxa 2013, 76:7-14.
• [52]Buerki S, Forest F, Acevedo-Rodriguez P, Callmander MW, Nylander JAA, Harrington M, Sanmartin I, Kupfer P, Alvarez N, et al.: Plastid and nuclear DNA markers reveal intricate relationships at subfamiliar and tribal levels in the soapberry family (Sapindaceae). Mol Phy Evol 2009, 51:238-258.
• [53]Wiens JJ: Can incomplete taxa rescue phylogenetic analyses from long-branch attractions? Syst Bio 2005, 54:731-742.
• [54]Wiens JJ: Missing data and the design of phylogenetic analyses. J Biomed Inform 2006, 39:34-42.
• [55]Lavranos JJ: Notes on the aloes of Arabia with descriptions of six new species. J S Afr Bot 1965, 31:55-81.
• [56]Holland PG: An evolutionary biogeography of the genus Aloe. J Biogeog 1978, 5:213-226.
• [57]Linder HP: The radiation of the Cape Flora, southern Africa. Biol Rev 2003, 78:597-638.
• [58]Cowling RM, Rundel PW, Desmet PG, Esler KJ: Extraordinary high regional-scale plant diversity in southern African arid lands, subcontinental and global comparisons. Diversity Distrib 1998, 4:27-36.
• [59]Valente LM, Britton AW, Powell MP, Papadopulos AST, Burgoyne PM, Savolainen V: Correlates of hyperdiversity in southern African ice plants Aizoaceae. Bot J Linn Soc 2013, 174:110-129.
• [60]Eggli U: Illustrated Handbook of Succulent Plants, Crassulaceae. Springer-Verlag, Berlin; 2003.
• [61]Good-Avila SV, Souza V, Gaut BS, Eguiarte LE: Timing and rate of speciation in Agave (Agavaceae). Proc Natl Acad Sci U S A 2006, 103:9124-9129.
• [62]Edwards EJ, Donoghue MJ: Pereskia and the origin of the cactus life-form. Am Nat 2006, 167:777-793.
• [63]Nyffeler R, Eggli U, Ogburn M, Edwards E: Variation on a theme, repeated evolution of succulent life forms in the Portulacineae (Caryophyllales). Haseltonia 2008, 14:26-36.
• [64]O’Brien C, Van Wyk B-E, Van Heerden FR: Physical and chemical characteristics of Aloe ferox leaf gel. S Afr J Bot 2008, 77:988-995.
• [65]Morton JF: Folk uses and commercial exploitation of Aloe leaf pulp. Econ Bot 1961, 15:311-319.
• [66]Grace OM, Buerki S, Symonds MRE, Forest F, van Wyk AE, Smith GF, et al. Xanthorrhoeaceae Bayesian tree. 2015. http://purl.org/phylo/treebase/phylows/study/TB2:S16954?format=html.