Abstract
Mucuna comprises 105 species with an overall pantropical distribution and is divided into three subgenera: M. subg. Mucuna, M. subg. Stizolobium and M. subg. Macrocarpa. Although phylogenetic studies have supported the occurrence of three main clades, evolutionary relationships among them are not fully resolved. The objective of this study was to examine pollen grain morphology from representatives of all three subgenera and map these onto the phylogenetic trees generated by analysis of other characters. Pollen grain surface, form, size, and aperture number were compared. A Bayesian inference tree using matK sequences was constructed. The results indicate that the representatives of M. subg. Macrocarpa have the smallest pollen grains in the genus (a synapomorphic character here identified for this subgenus) and that species of subgenus Mucuna (those with umbelliform inflorescences) have the largest pollen grains. Additional morphological diversity of the pollen grain surface was noted: reticulate and/or micro-reticulate (in all three subgenera), perforate, gemmate or verrucose (only in M. subg. Mucuna). For all studied taxa, the pollen grains are triaperturate, except for two species of M. subg. Mucuna, which have tetraperturate pollen. The phylogenetic tree obtained using the matK marker resolved M. subg. Stizolobium as the earliest diverging lineage in Mucuna. Based on this phylogeny, a reticulate ornamentation pattern of the pollen surface may represent the ancestral state for the genus, while the larger pollen size and the foraminate, gemmate, and verrucose ornamentations are derived characteristics within the genus. These putative derived ornamentations have been observed only in neotropical species.
Similar content being viewed by others
References
Agostini K (2008) Ecologia da reprodução de duas espécies de Mucuna (Leguminosae, Faboideae, Phaseoleae)—embriologia, citogenética e variabilidade genética—do litoral norte de São Paulo. PhD Thesis, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Control 19:716–723
Armstrong RA (2014) When to use Bonferroni correction. Ophthalmic Physiol Opt 34:502–508. https://doi.org/10.1111/opo.12131
Banks H, Rudall PJ (2016) Pollen structure and function in caesalpinioid legumes. Amer J Bot 103:1–14. https://doi.org/10.3732/ajb.1500248
Cardoso D, Queiroz LP, Pennington T, Lima HC, Fonty E, Wojciechowski MF, Lavin M (2012) Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages. Amer J Bot 99:1991–2013. https://doi.org/10.3732/ajb.1200380
Duke JA (1981) Handbook of legumes of world economic importance. Plenum, New York
Ferguson IK (1981) The pollen morphology of Macrotyloma (Leguminosae: Phaseoleae). Kew Bull 36:455–461. https://doi.org/10.2307/4117580
Ferguson IK (1990) The significance of some pollen morphological characters of the tribe Amorpheae and the genus Mucuna (tribe Phaseoleae) in the biology and systematics of subfamily Papilionoideae (Leguminosae). Rev Palaeobot Palynol 64:129–136. https://doi.org/10.1016/0034-6667(90),90125-3
Fernandéz VA, Gatello L, Astegiano J (2009) Influence of flower functionality and pollinator system on the pollen size-pistil length relationship. Organisms Diversity Evol 9:75–82. https://doi.org/10.1016/j.ode.2009.02.001
Garcia JA, Fragoso C (2003) Influence of different food substrate on growth and reproduction of two tropical earthworm species (Pontoscolex corethrurus and Amynthas corticis). Pedobiologia 47:754–763. https://doi.org/10.1078/0031-4056-00255
Graham A, Tomb AS (1977) Palynology of Erythrina (Leguminosae: Papilionoideae): The subgenera, sections, and generic relationships. Lloydia 40:413–435
Halbritter H (1998) Preparing living pollen material for scanning electron microscopy using 2,2-dimethoxypropane (DMP) and critical-point drying. Biotech Histochem 73:137–143
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Paleontol Electronica 4:1–9
Hesse M, Halbritter H, Zetter R, Weber M, Buchne R, Frosch-Radivo A, Ulrich S (2009) Pollen terminology, an illustrated handbook. Springer, Wien
Hu JM, Lavin M, Wojciechowski MF, Sanderson MJ (2000) Phylogenetic systematics of the tribe Millettieae (Leguminosae) based on chloroplast marker trnK/matK sequences and its implication for evolutionary patterns in Papilionoideae. Amer J Bot 87:418–430
Klitgaard BB, Ferguson IK (1992) Pollen morphology of Browneopsis (Leguminosae: Caesalpinioideae), and its evolutionary significance. Grana 31:285–290. https://doi.org/10.1080/00173139209429451
Kloeppe JW, Rodríguez-Kábana R, Zehnder AW, Murphy JF, Sikora E, Fernandéz C (1999) Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Austral Pl Pathol 28:21–26. https://doi.org/10.1071/AP99003
Lackey JA (1981) Tribe 10. Phaseoleae DC. In: Polhill RM, Raven PH (eds) Advances in legume systematics, part 1. Royal Botanic Gardens, Kew, pp 301–327
Lavin M, Schrire BD, Lewis GP, Pennington RT, Delgado-Salinas A, Thulin M, Hughes CE, Matos AB, Wojciechowski MF (2004) Metacommunity process rather than continental tectonic history better explains geographically structured phylogenies in legumes. Philos Trans Roy Soc London B Biol Sci 359:1509–1522. https://doi.org/10.1098/rstb.2004.1536
Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54:575–594. https://doi.org/10.1080/10635150590947131
Lee S (1978) A factor analysis study of the functional significance of angiosperm pollen. Syst Bot 3:1–19. https://doi.org/10.2307/2418528
LPWG—The Legume Phylogeny Working Group (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66:44–77. https://doi.org/10.12705/661.3
Moura TM, Vatanparast M, Tozzi AMGA, Forest F, Wilmot-Dear M, Simon MF, Mansano VF, Kajita T, Lewis GP (2016a) A molecular phylogeny and new infrageneric classification of Mucuna Adans. (Leguminosae-Papilionoideae) including insights from morphology and hypotheses about biogeography. Int J Pl Sci 177:76–89. https://doi.org/10.1086/684131
Moura TM, Wilmot-Dear M, Vatanparast M, Fortuna-Perez AP, Tozzi AMGA, Lewis GP (2016b) A new infrageneric classification of Mucuna (Leguminosae–Papilionoideae): supported by morphology, molecular phylogeny and biogeography. Syst Bot 41:606–616. https://doi.org/10.1600/036364416X692532
Moura TM, Lewis GP, Mansano VF, Tozzi AMGA (2018) A revision of the neotropical Mucuna species (Leguminosae–Papilionoideae). Phytotaxa 337:1–65. https://doi.org/10.11646/phytotaxa.337.1.1
Nylander JAA (2004) MrModeltest. v2 ed. Program distributed by the author, Uppsala University, Uppsala
Ortiz-Ceballos AI, Fragoso C (2004) Earthworm populations under tropical maize cultivation: the effect of mulching with velvet bean. Biol Fertil Soils 39:438–445. https://doi.org/10.1007/s00374-004-0732-8
Ortiz-Ceballos AI, Peña-Cabriales JJ, Fragoso C, Brown GG (2007a) Mycorrhizal colonization and nitrogen uptake by maize: combined effect of tropical earthworms and velvet bean mulch. Biol Fertil Soils 44:181–186. https://doi.org/10.1007/s00374-007-0193-y
Ortiz-Ceballos AI, Fragoso C, Brown GG (2007b) Synergistic effect of a tropical earthworm Balanteodrilus pearsei and velvet bean Mucuna pruriens var. utilis on maize growth and crop production. Appl Soil Ecol 35:356–362. https://doi.org/10.1016/j.apsoil.2006.07.009
Osborn JM, Philbrick CT (1994) Comparative pollen structure and pollination biology in the Callitrichaeceae. Acta Bot Gallica 141:257–266
Osborn JM, Taylor TN, Schneider EL (1991) Pollen morphology and ultrastructure of the Cabombaceae: correlation with pollination biology. Amer J Bot 78:1367–1378. https://doi.org/10.2307/2445275
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v. 1.6. Available at: http://beast.bio.ed.ac.uk/Tracer
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Ruiz LK (2009) Sinopsis de las especies Colombianas de Mucuna (Leguminosae: Papilionoideae: Phaseoleae). In: Forero E (ed) Estúdios en leguminosas colombianas II. Universidad Nacional Colombiana, Bogotá, pp 387–417
Salsis-Ladoudakis C, Chase MW, Robinson DN, Russell J, Klitgaard B (2008) Phylogenetics of neotropical Platymiscium (Leguminosae: Dalbergieae): systematics, divergence times, and biogeography inferred from nuclear ribosomal and plastid DNA sequence data. Amer J Bot 95:1270–1286. https://doi.org/10.3732/ajb.0800101
Santos FAR, Novaes DM, Queiroz LP (2012) Pollen of Bauhinia L. and Phanera Lour. (Leguminosae: Caesalpinioideae) from the Brazilian Caatinga. Amer J Pl Sci 3:909–920. https://doi.org/10.4236/ajps.2012.37108
Schrire BD, Lavin M, Lewis GP (2005) Global distribution patterns of the Leguminosae: insights from recent phylogenies. Biol Skr 55:375–422
Sousa M, Moura TM (2016) Mucuna chiapaneca (Leguminosae–Papilionoideae) a new species from Mexico. Phytotaxa 246:198–202. https://doi.org/10.11646/phytotaxa.246.3.4
Stefanovíc S, Pfeil BE, Palmer JD, Doyle JJ (2009) Relationships among phaseoloid legumes based on sequences from eight chloroplast regions. Syst Bot 34:115–128. https://doi.org/10.1600/036364409787602221
Stroo A (2000) Pollen morphological evolution in bat pollinated plants. Pl Syst Evol 222:225–242. https://doi.org/10.1007/BF00984104
Verdcourt B (1970) Studies in the Leguminosae-Papilionoideae for the ‘Flora of Tropical East Africa’: II. Kew Bull 24:235–307. https://doi.org/10.2307/4103051
Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Amer J Bot 91:1846–1862. https://doi.org/10.3732/ajb.91.11.1846
Xu B, Gao XF, Wu N, Zhang LB (2011) Pollen diversity and its systematics implication in Lespedeza (Fabaceae). Syst Bot 36:352–361. https://doi.org/10.1600/036364411X569534
Acknowledgements
The authors thank the Missouri Botanical Garden for access to herbarium specimens, literature, and the SEM laboratory. TMM also thanks the REFLORA project (granted for the years 2015–2016) for an overseas scholarship and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, and the Science without Borders Program for the post-doctoral scholarship (process 245590/2012-9) at the Royal Botanic Garden, Kew (2013–2015). We thank the two anonymous reviewers for their important suggestions and the journal editor for constructive feedback.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling editor: Mike Thiv.
Appendices
Appendix I
Genbank accessions for the phylogenetic matK analysis.
Mucuna holtonii (JQ587790.1); Mucuna mutisiana (KJ593957.1); Mucuna pruriens (JQ587787.1); Mucuna interrupta (AB627862.1); Mucuna warburgii (AB627861.1); Mucuna gigantea (AB627860.1); Mucuna monosperma (AB627859.1); Mucuna macrocarpa (AB627858.1); Mucuna hainanensis (HM049512.1); Mucuna poggei (KX146301.1).
External group: Desmodium incanum (JQ587594.1); Desmodium barbatum (JQ587587.1); Apios americana (AY386926.1).
Appendix II
Specimen vouchers at MO used to prepare the images in Fig. 1
Species | Country of origin | Voucher |
---|---|---|
M. argyrophylla Standl. | Mexico | H. Hernández 474 |
M. birdwoodiana Tutcher | China | A.J.M. Leeuwenerg 14071 |
M. bracteata DC. ex Kurz | Thailand | C.F. van Beusekom et al. 4297 |
M. coriacea Baker | Zimbabwe | N.C. Chase 4955 |
M. gigantea (Willd.) DC. | Madagascar | S.N. Andrianarivelo et al. 43 |
M. holtonii (Kuntze) Moldenke | Nicaragua | M. Jacinto Prado 145 |
M. klitgaardiae T.M.Moura et al. | Ecuador | B.B. Klitgaard 99502 |
M. macrocarpa Wall. | Taiwan | Y. Endo 1913 |
M. membranacea Hayata | Ryukyus Ils., Japan | Hirano 4103 |
M. mollis (Kunth) DC. | Colombia | R. Romero 6129 |
M. monticola Zamora et al. | Costa Rica | A.F. Skutch 3723 |
M. neocaledonica Baker f. | New Caledonia | McPherson 5261 |
M. poggei Taub. | Zambia | Davidse and Handlos 7200 |
M. pruriens (L.) DC. | Burundi | Lewalle 4556 |
M. sloanei Fawc. & Rendle | Ghana | M. Merello et al. 1591 |
M. stans Welw. ex Baker | Rwanda | G. Troupin 5979 |
Rights and permissions
About this article
Cite this article
de Moura, T.M., Bogler, D., Miranda, J.M.D. et al. Morphological variation in pollen grains of Mucuna (Leguminosae): new biogeographic and evolutionary patterns. Plant Syst Evol 304, 861–869 (2018). https://doi.org/10.1007/s00606-018-1516-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-018-1516-1