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CIAT Research Online - Accepted Manuscript CIAT Research Online - Accepted Manuscript Morphological characterization in the genus Passiflora L.: an approach to understanding its complex variability The International Center for Tropical Agriculture (CIAT) believes that open access contributes to its mission of reducing hunger and poverty, and improving human nutrition in the tropics through research aimed at increasing the eco-efficiency of agriculture. CIAT is committed to creating and sharing knowledge and information openly and globally. We do this through collaborative research as well as through the open sharing of our data, tools, and publications. Citation: Ocampo Pérez, John Albeiro; d’Eeckenbrugge, Geo Coppens. 2017. Morphological characterization in the genus Passiflora L.: an approach to understanding its complex variability. Plant Systematics and Evolution 303(4): 531-558. Publisher’s DOI: http://dx.doi.org/10.1007/s00606-017-1390-2 Access through CIAT Research Online: http://hdl.handle.net/10568/80128 Terms: © 2017. CIAT has provided you with this accepted manuscript in line with CIAT’s open access policy and in accordance with the Publisher’s policy on self-archiving. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. You may re-use or share this manuscript as long as you acknowledge the authors by citing the version of the record listed above. You may not use this manuscript for commercial purposes. For more information, please contact CIAT Library at [email protected]. Manuscript Click here to download Manuscript Morphological descriptor_Passiflora_07_07_2016_JO.doc Click here to view linked References Morphological characterization in the genus Passiflora L.: an approach to understanding its 1 complex variability 2 3 4 Morphological characterization in the genus Passiflora 5 6 7 John Ocampo Pérez1* and Geo Coppens d’Eeckenbrugge2 8 1 9 Universidad Nacional de Colombia, sede Palmira. Departamento de Ciencias Biológicas / International 10 Center for Tropical Agriculture – CIAT. Carrera 32 No 12 - 00 Chapinero, vía Candelaria Palmira - Valle 11 12 del Cauca – Colombia. 13 2CIRAD, UMR AGAP, Avenue Agropolis, 34398 Montpellier, France. 14 15 16 *Corresponding author: [email protected] 17 18 19 Abstract 20 21 22 Morphological variation was studied in 124 accessions from 61 species of genus Passiflora, using 23 variance component and principal component analyses (PCA) on 43 quantitative traits, and neighbor 24 25 joining cluster analysis on 85 qualitative traits. Coefficients of variation were generally higher for 26 subgenus Decaloba, indicating stronger differentiation when compared with subgenera Passiflora. 27 28 Twenty-four quantitative descriptors showing high variation at the subgenus level were selected for the 29 30 PCA. The five principal components retained 84% of the total variation, being the first (32%) closely 31 associated with flower length (hypanthium, nectary-chamber, androgynophore) and secondarily with 32 33 floral cup constriction above the nectary chamber. The second (27%) is associated with flower width 34 (length of bracts and length of corolla and corona-elements) and bract shape, and the third (14%) with 35 36 peduncle branching, stem width and leaf length, which relates it clearly with variation between subgenera 37 Astrophea and Deidamioides. The projection of accessions in the resulting tridimensional space 38 39 consistently separates subgenera. A selection of 32 qualitative traits and four categorized quantitative 40 variables, whose segregation follows divisions among Killip’s subgenera, allowed classifying consistently 41 42 our species sample using a strictly phenetic approach. Eight of the nine subgenera established by Killip 43 represented in our sample were supported by the morphological analysis, although subgenus 44 45 Deidamioides is only supported in the quantitative analysis. Our results support seven of the eight Killip’s 46 subgenera of our sample, but no infrasubgeneric classifications. However, Feuillet & MacDougal´s 47 48 classification of subgenus Decaloba was partly supported and converged on many points with previous 49 phylogenetic results obtained with DNA sequences. 50 51 52 53 54 Key words Passiflora, systematics, morphological descriptors, principal component analysis, plant 55 genetic resources. 56 57 58 59 60 Introduction 61 62 1 63 64 65 With more than 576 species, Passiflora L. is by far the most important genus in the family Passifloraceae, 1 both numerically and economically. It is mostly distributed in the Neotropics, from coastal zones up to 2 3 4,300 m.a.s.l. in Andean páramos; only 23 species are native to the Old World in Southeast Asia, 4 Australia and Oceania (Killip 1938; Ulmer and MacDougal 2004). The origin of Passifloraceae is very 5 6 ancient from 65.5 million years ago (Paleocene) and seems to follow a biogeographic scenario proposed 7 for several plant groups, originating in Africa, crossing to Europe/Asia and arriving in the New World by 8 9 way of land bridges (Muschner et al., 2012). The chromosome base number varies among x = 6 and x = 9 10 (De Melo et al. 2001), and the average genome size is 1.03 pg (Yotoko et al. 2011). 11 12 Passionflowers are herbaceous or woody vines usually climbing with tendrils, but a few are trees or 13 shrubs. Other typical vegetative traits include alternate leaves, axillary stipules, and petiolar and/or 14 15 laminar nectary glands. In addition, the genus exhibits several unique floral features such as an 16 androgynophore, a complex corona constituted by one or several concentric rows of filaments, and a 17 18 limen-operculum system limiting access to the nectary chamber, with impressive interspecific variation in 19 size, shape and colors (Killip 1938). Their wide morphological variation seems to be the result of their 20 21 habitat diversity as well as their co-evolutionary relationships with many organisms, including a wide 22 range of pollinators as small and large insects, birds and bats (Ulmer and MacDougal 2004). 23 24 Many species exhibit interesting fruits, pharmacological properties (e.g. sedative effect) and/or 25 ornamental potential. More than 80 Passiflora species produce edible fruits, all of them belonging to 26 27 subgenus Passiflora (Yockteng et al. 2011). The two botanicals forms of P. edulis Sims, flavicarpa 28 Degener (yellow passion fruit) and edulis (purple passion fruit) are by far the most important crops in the 29 30 family, with a world production estimated at ca. 640.000 tons. Other cultivated passion fruits are P. 31 32 tripartita var. mollissima (Kunth) Holm-Nielsen & Jørgensen (curuba de Castilla), P. tarminiana Coppens 33 & Barney (curuba India), P. ligularis Juss. (sweet granadilla), P. maliformis L. (granadilla de piedra or 34 35 stone granadilla), P. quadrangularis L. (giant granadilla), P. popenovii Killip (granadilla de Quijos), 36 P. alata Curtis (fragrant granadilla) and P. setacea DC (sururuca). The high potential of Passiflora for 37 38 crop diversification and economic development induced research institutions of different countries to 39 prioritize the characterization and evaluation of wild and cultivated populations (Cerqueira-Silva et al. 40 41 2016), and develop strategies for conservation and improvement of these genetic resources. 42 The high diversity of character combinations related to nectary glands, stipules, corona, operculum 43 44 and limen have been heavily used to delimit infrageneric divisions in Passiflora taxonomy, separating 45 subgenera, sections, and series. Although most species appear well delimited, there are many cases in low 46 47 level taxa as sections and series, where two or more species are very difficult to distinguish. The largest 48 monograph and most important reference work was that of Killip (1938) who described 355 American 49 50 species plus 20 species in 1960, placing them in 22 subgenera. Escobar (1988a,b, 1989, 1990, 1994) 51 reviewed subgenera Astrophea, Distephana, Manicata, Rathea and Tacsonia, merging subgenera 52 53 Tacsoniopsis and Tacsonia, subdivided into sections and series, and proposing one additional subgenus, 54 Porphyropathanthus. MacDougal and Feuillet (2004) have proposed a new infrageneric classification of 55 56 Passiflora, taking into account the Old World species and recognizing only four subgenera, Astrophea 57 (unchanged; trees and shrubs, rarely lianas), Decaloba (vines with small flowers and fruits, the latter 58 59 usually black), Deidamioides (vines, with two-flowered peduncles, not clearly defined as a morphological 60 61 62 2 63 64 65 group) and Passiflora (vines to lianas, with large flowers and fruits). This classification needs to be 1 revised, and completed with the explicit inclusion of many more species. Thus, Krosnick et al. (2009) 2 3 with DNA molecular data recognized a fifth subgenus, Tetrapathea (vines, inflorescences, small flowers 4 and fruits, yellow-green to red at maturity) from Oceania. 5 6 Both classifications of Killip (1938) and Feuillet and MacDougal (2003) are based on the extreme 7 morphological richness and complexity of Passiflora, whose species present numerous particular traits, 8 9 including a wide variation in leaf shape, even within species and within individuals (heterophylly and 10 heteroblasty are very common), the presence of extrafloral nectaries in different parts (on leaf petiole, 11 12 lamina or margins, on bracts, on sepals), floral traits showing a high level of coevolution with particular 13 pollinators particularly in corolla color,
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