Possible hybrid speciation for two Malagasy species of Piper L. (Piperaceae)
DOI:
https://doi.org/10.13128/caryologia-1133Keywords:
Piper malgassicum, chromosomes, hybridization, DNA sequences, G3pdh, trnL, ndhF, Malagasy biodiversity, Piper tsarasotrae, PiperaceaeAbstract
Two new species of genus Piper L. from Madagascar: Piper malgassicum Papini, Palchetti, M. Gori & Rota Nodari and Piper tsarasotrae Papini, Palchetti, M. Gori & Rota Nodari, were analyzed to investigate their phylogenetic position and evolutionary history. Both plastidial and nuclear markers were used for sequencing. The plastidial markers (ndhF and trnL intron) showed a close relationship between the two species with respect to the other species of Piper. Both species appeared phylogenetically related to the African P. guineense and the Malagasyan/Mascarenhas endemic P. borbonense. The nuclear marker (G3pdh) amplification produced two separate sets of sequences: “long” sequences and “short” sequences, characterized by some long deletions. Analyzing together the nuclear sequences, we observed that the “long” sequence of P. tsarasotrae had a stricter relationship to the African accessions of P. guineense, while the accession of P. malgassicum was more strictly related to P. borbonense. On the contrary both “short” sequences of P. malgassicum and P. tsaratsotrae resulted phylogenetically related to Asian accessions and more distantly related to the formerly cited species. This unexpected result was tentatively explained with a more ancient hybridization event between an ancestor of P. malgassicum and P. tsarasotrae (and possibly P. borbonense) and an Asian species of Piper. The Asian contribution would have produced the ancestors carrying the “short” sequences. A more recent hybridization event would have led to the separation of P. malgassicum from P. tsarasotrae with an African pollen-derived genome contribution from P. guineense or, more probably, an ancestor thereof, to an ancestor of P. tsarasotrae. The chromosome numbers of P. tsarasotrae (2n = about 38) and P. malgassicum (2n = about 46), were more similar to the Asian species than to the American species. Unfortunately, no chromosome number of the African species P. guineense is currently available, to compare the chromosomal numbers.
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References
Quijano-Abril MA, Callejas-Posada R, Miranda-Esquivel DR (2006) Areas of endemism and distribution patterns for Neotropical Piper species (Piperaceae). J Biogeogr 33:1266–1278. https://doi.org/10.1111/j.1365-2699.2006.01501.x
Loconte H, Stevenson DW (1991) CLADISTICS OF THE MAGNOLIIDAE. Cladistics 7:267–296. https://doi.org/10.1111/j.1096-0031.1991.tb00038.x
Isnard S, Prosperi J, Wanke S, et al (2012) Growth Form Evolution in Piperales and Its Relevance for Understanding Angiosperm Diversification: An Integrative Approach Combining Plant Architecture, Anatomy, and Biomechanics. Int J Plant Sci 173:610–639. https://doi.org/10.1086/665821
Burger W (1972). Evolutionary trends in the Central American Species of Piper (Piperaceae). Brittonia 24: 356-362. https://doi.org/10.2307/2805498
Tebbs MC (1993). Piperaceae. In: Kubitzki K, Rohwer JG, Bittrich V, editors. Flowering Plants Dicotyledons. The Families and Genera of Vascular Plants, Vol. 2. Berlin, Germany: Springer, pp. 516-520.
Jaramillo MA, Manos PS (2001) Phylogeny and patterns of floral diversity in the genus Piper (Piperaceae). Am J Bot 88:706–716. https://doi.org/10.2307/2657072
Ulloa Ulloa C, Acevedo-Rodríguez P, Beck S, et al (2017) An integrated assessment of the vascular plant species of the Americas. Science 358:1614–1617. https://doi.org/10.1126/science.aao0398
Suwanphakdee C, Simpson DA, Hodkinson TR, Chantaranothai P (2016) Taxonomic notes on the genus Piper (Piperaceae). Nord J Bot 34:605–618. https://doi.org/10.1111/njb.01114
Smith JF, Stevens AC, Tepe EJ, Davidson C (2008) Placing the origin of two species-rich genera in the late cretaceous with later species divergence in the tertiary: a phylogenetic, biogeographic and molecular dating analysis of Piper and Peperomia (Piperaceae). Plant Syst Evol 275:9–30. https://doi.org/10.1007/s00606-008-0056-5
Weil M, Shum Cheong Sing A, Méot JM, et al (2017) Impact of blanching, sweating and drying operations on pungency, aroma and color of Piper borbonense. Food Chem 219:274–281. https://doi.org/10.1016/j.foodchem.2016.09.144
De Candolle C (1869). Piperaceae. In: De Candolle C, editor. Prodromus Systematis Naturalis Regni Vegetabilis, Vol. 16. Part 1. Paris, France: Masson, pp. 235-471 (in Latin).
De Candolle C (1923). Piperacearum clavis analytica. Candollea 1: 65-415 (in Latin).
Palchetti E, Biricolti S, Gori M., Rota Nodari G, Gandolfi N, Papini A (2018) Two new Malagasy species of genus Piper L. (Piperaceae): Piper malgassicum and Piper tsarasotrae and their phylogenetic position. Turk J of Bot 42(5): 622-610. doi:10.3906/bot-1712-2
Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot 75:1443–1458. https://doi.org/10.2307/2444695
Hurteau GJ, Spivack SD (2002) mRNA-specific reverse transcription-polymerase chain reaction from human tissue extracts. Anal Biochem 307:304-315. https://doi.org/10.1016/S0003-2697(02)00058-1
Liu Y-J, Zheng D, Balasubramanian S, et al. (2009) Comprehensive analysis of the pseudogenes of glycolytic enzymes in vertebrates: the anomalously high number of GAPDH pseudogenes highlights a recent burst of retrotrans-positional activity. BMC Genomics 10:480. https://doi.org/10.1186/1471-2164-10-480
Sun Y, Li Y, Luo D, Liao DJ (2012) Pseudogenes as weaknesses of ACTB (Actb) and GAPDH (Gapdh) used as reference genes in reverse transcription and polymerase chain reaction. PLoS ONE 7:e41659. https://doi.org/10.1371/journal.pone.0041659
Samuel R (1987) Chromosome Numbers in Piper. Kew Bull 42:465. https://doi.org/10.2307/4109710
Wühr M, Chen Y, Dumont S, et al (2008) Evidence for an Upper Limit to Mitotic Spindle Length. Curr Biol 18:1256–1261. https://doi.org/10.1016/j.cub.2008.07.092
Petry S (2016) Mechanisms of Mitotic Spindle Assembly. Annu Rev Biochem 85:659–683. https://doi.org/10.1146/annurev-biochem-060815-014528
Vanaja T, Neema VP, Mammootty KP, Rajeshkumar R (2008) Development of a promising interspecific hybrid in black pepper (Piper nigrum L.) for Phytophthora foot rot resistance. Euphytica 161:437–445. https://doi.org/10.1007/s10681-007-9602-4
.García MA, Costea M, Kuzmina M, Stefanovi? S (2014) Phylogeny, character evolution, and biogeography of Cuscuta (dodders; Convolvulaceae) inferred from coding plastid and nuclear sequences. Am J Bot 101:670–690. doi:10.3732/ajb.1300449
Stefanovi? S, Kuzmina M, and Costea M (2007) Delimitation of major lineages within Cuscuta subgenus Grammica (dodders; Convolvulaceae) using plastid and nuclear DNA sequences. Am J Bot 94: 568– 589. https://doi.org/10.3732/ajb.94.4.568
Aubriot X, Knapp S, Syfert MM, Poczai P and Buerki S (2018) Shedding new light on the origin and spread of the brinjal eggplant (Solanum melongena L.) and its wild relatives. Am J Bot 105: 1175–1187. https://doi.org/10.1002/ajb2.1133
Selvi F, Papini A, Bigazzi M (2002) Systematics of Nonea (Boraginaceae-Boragineae): new insights from phenetic and cladistic analyses. Taxon 51: 719–730. https://doi.org/10.2307/1555025
Jaramillo MA and Callejas R (2004) Current perspectives on the classification and phylogenetics of the genus Piper L. Pp. 179–198. in Piper: A model genus for studies of chemistry, ecology, and evolution, eds. L. A. Dyer and A. N. Palmer. Boston: Kluwer Academic.
Jaramillo MA, Callejas R, Davidson C, Smith JF, Stevens AC, and Tepe EJ (2008) A Phylogeny of the Tropical Genus Piper Using ITS and the Chloroplast Intron psbJ–petA. Systematic Botany 33(4): 647–60. doi:10.1600/036364408786500244.
Martines C, Carvalho MR, Marinan S, Jaramillo CA (2015) A Late Cretaceous Piper (Piperaceae) from Colombia and diversification patterns for the genus. Am J Bot 102(2): 273-289. https://doi.org/10.3732/ajb.1400427
Murray M. G., and Pitas J. W.. (1996). "Plant DNA from alcohol-preserved samples." Plant molecular biology reporter 14.3 (1996): 261-265. https://doi.org/10.1007/BF02671661
Bressan, Eduardo A., et al. "Extraction of high-quality DNA from ethanol-preserved tropical plant tissues." BMC research notes 7.1 (2014): 268. https://doi.org/10.1186/1756-0500-7-268
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109. https://doi.org/10.1007/BF00037152
Strand AE, Leebens?Mack J, Milligan BG (1997) Nuclear DNA?based markers for plant evolutionary biology. Mol Ecol 6:113–118. https://doi.org/10.1046/j.1365-294X.1997.00153.x
Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890. https://doi.org/10.1093/nar/16.22.10881
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Hall, T.A. (1999) BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98. https://doi.org/10.14601/Phytopathol_Mediterr-14998u1.29
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23:2947-2948. https://doi.org/10.1093/bioinformatics/btm404
Bandara N, Papini A, Mosti S, Brown T, Smith L (2013) A phylogeny of Onobrychis and its relationships with allied genera of Hedysareae. Turk Journ of Bot. 37(6):981-992. https://doi.org/10.3906/bot-1210-32
Simeone MC, Grimm GW, Papini A, Vessella F, Cardoni S, Tordoni E, Piredda R, Franc A, Denk T. 2016. Plastome data reveal multiple geographic origins of Quercus Group Ilex. PeerJ 4:e1897 https://doi.org/10.7717/peerj.1897
Swofford DL, 1998. PAUP* 4.1. Phylogenetic Analysis Using Parsimony. Test version. Sunderland (MA): Sinauer Associates.
Swofford DL (2001) Laboratory of Molecular Systematics Smithsonian Institution. 143
Simmons MP, Ochoterena H (2000) Gaps as Characters in Sequence-Based Phylogenetic Analyses. Syst Biol 49:369–381. https://doi.org/10.1093/sysbio/49.2.369
Young ND, Healy J (2003) GapCoder automates the use of indel characters in phylogenetic analysis. BMC Bioinformatics 4, 6 (2003). https://doi.org/10.1186/1471-2105-4-6
Papini A., Trippanera G.B., Maggini F., Filigheddu R., Biondi E. (2004) New insights in Salicornia L. and allied genera (Chenopodiaceae) inferred from nrDNA sequence data. Plant Biosystems 138(3): 215-223 https://doi.org/10.1080/11263500400006977
Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50: 913–925. https://doi.org/10.1080/106351501753462876
Nylander JAA, 2004. Mr Modeltest, version 1.0b. Department of Systematic Zoology, EBC, Uppsala University, Uppsala, Sweden.
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Ronquist F, Teslenko M, Van Der Mark P, Ayaccesseres 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: 539–42. https://doi.org/10.1093/sysbio/sys029
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Rambaut A, Drummond A. 2010. FigTree v1.3.1. http://tree.bio.ed.ac.uk/software/figtree. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.
Papini A, Banci F, Nardi E (2007) Molecular evidence of polyphyletism in the plant genus Carum L. (Apiaceae). Genet Mol Biol 30:475–482. https://doi.org/10.1590/S1415-47572007000300029
Papini A, Simeone MC, Bellarosa R, Spada F, Schirone B (2011). Quercus macranthera Fisch. & Mey. Ex Hohen. and Quercus iberica M. Bieb.: taxonomic definition and systematic relationships with European oaks inferred from nuclear Internal Transcribed Spacer (ITS) data. Plant Biosyst 145: 37-49.. https://doi.org/10.1080/11263504.2010.502684
Mosti S., Fiorini G. and Papini A. (2011) Karyological investigations on several species of genus Rebutia Sect. Digitorebutia (Cactacee). Caryologia-Firenze- 64(3):350-359 https://doi.org/10.1080/00087114.2011.10589802
Mousavi S H, Hassandokht M R, Choukan R, Sepahvand N, Khosrowchahli M, Papini A. (2013) Cytological study of chromosome and genome composition of Iranian lettuce (Lactuca sativa L.) accessions. Caryologia 66(1): 41-49. Digitorebutia (Cactaceae). Caryologia 64(3): 302-308. https://doi.org/10.1080/00087114.2013.780440
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