Abstract
Bottle gourd (Lagenaria siceraria), a multipurpose crop, is among the first domesticates of humans. This study analyses nuclear ribosomal DNA (nrDNA) of the two cultivated subspecies to improve our understanding on the African origin and the dispersal to Asia. A total of 146 nrDNA sequences representing 79 individuals from African cultivars and 67 individuals from Asian cultivars were compared; the resulting nrDNA sequences were composed of 35 and 16 haplotypes specific to Africa and Asia, respectively, and two additional haplotypes shared by both continents. When all the rDNA haplotypes were bulked, the genetic differentiation (F ST ) was significant between the subspecies (P < 0.001), within Africa (P < 0.001) and within Asia (P < 0.05), and the nucleotide diversity was 2.5-fold higher in Africa. Sorting the haplotypes by classes of paralogs revealed more classes in Africa, and in classes where African and Asian cultivars were represented, the diversity was higher in Africa, in general. The 5.8S-coding regions showed two to four amino acid differences resulting to nine protein sequence variants, one of which encompassed all the Asian cultivars. The nucleotide diversity at that shared variant was 1.43-fold higher in Africa than in Asia. Analyses of phylogenetic networks revealed major shared haplotypes containing 23.91 % of the cultivars and having founder locations. We suggest that African cultivars reached Asia. The study tags for the first time nrDNA haplotypes capable of discriminating between and within the subspecies. Thirty single nucleotide polymorphisms (SNPs) and five insertion-deletions (Indels) derived from the haplotypes and registered in GenBank are provided.
Similar content being viewed by others
References
Adhikari A, Rana G, Mandal T (2014) An in silico assessment of molecular evolution at 16S rRNA of Pseudomonas sp. Int J Curr Microbiol Appl Sci 3:518–527
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434
Badifu GI (1993) Food potentials of some unconventional oilseeds grown in Nigeria: a brief review. Plant Foods Hum Nutr 43:211–224
Bandelt H-J, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Baroni M, Semple C, Steel MA (2004) A framework for representing reticulate evolution. Ann Comb 8:391–408
Bayly MJ, Ladiges PY (2007) Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae). Mol Phylogenet Evol 44:346–356
Buckler ES IV, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA divergent paralogues and phylogenetic implications. Genetics 145:821–832
Carranza S, Bagun J, Riutort M (1999) Origin and evolution of paralogous rRNA gene clusters within the flatworm family Dugesiidae (Platyhelminthes, Tricladida). J Mol Evol 49:250–259
Clarke AC, Burtenshaw MK, McLenachan PA, Erickson DL, Penny D (2006) Reconstructing the origins and dispersal of the Polynesian bottle gourd (Lagenaria siceraria). Mol Biol Evol 23:893–900
Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of phytophthora and related oomycetes. Fungal Genet Biol 30:17–32
Crawford GW (1992) in origins of agriculture: an international perspective. In: Cowan CW, Watson PJ (eds) Smithsonian Institution Press. Washington, DC, pp 7–38
Decker-Walters DS, Staub J, Lopez-Sese A, Nakata E (2001) Diversity in landraces and cultivars of bottle gourd (Lagenaria siceraria, Cucurbitaceae) as assessed by random amplified polymorphic DNA. Genet Resour Crop Evol 48:369–380
Decker-Walters DS, Wilkins-Ellert M, Chung SS, Staub J (2004) Discovery and genetic assessment of wild bottle gourd [Lagenaria siceraria (Mol.) Standley; Cucurbitaceae] from Zimbabwe. Econ Bot 58:501–508
Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Report 1:19–21
Erickson DL, Smith BD, Clarke AC, Sandweiss DH, Tuross N (2005) An Asian origin for a 10,000-year-old domesticated plant in the Americas. Proc Natl Acad Sci 51:18315–18320
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinforma 1:47–50
Hartmann S, Nason JD, Bhattacharya D (2001) Extensive ribosomal DNA genic variation in the columnar cactus Lophocereus. J Mol Evol 53:124–134
Heiser CB (1973) Variation in the bottle gourd. In: Meggers BJ, Ayensu ES, Duckworth WD (eds) Tropical forest ecosystems in Africa and South America: a comparative review. Smithsonian Institution Press, Washington, DC, pp 121–128
Heiser CB (1979) The gourd book. University of Oklahoma Press, Norman United States
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267
Ironside JE (2013) Diversity and recombination of dispersed ribosomal DNA and protein coding genes in Microsporidia. PLoS One 8, e55878
Jaiswal R, Kuhnert N (2014) Identification and characterization of the phenolic glycosides of Lagenaria siceraria Stand. (Bottle gourd) fruit by liquid chromatography-tandem mass spectrometry. J Agric Food Chem 62:1261–71
Jobes DV, Thien LB (1997) A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Plant Mol Biol Report 15:326–334
Jobst J, King K, Hemleben V (1998) Molecular evolution of the internal transcribed spacers (ITS1 and ITS2) and phylogenetic relationships among species of the family cucurbitaceae. Mol Phylogenet Evol 9:204–219
Kavanagh TA, Timmis JN (1988) Structure of melon rDNA and nucleotide sequence of the 17-25S spacer region. Theor Appl Genet 76:673–680
Kistler L, Montenegro A, Smith BD, Giffordd JA, Greene RE, Newsoma LA, Shapiro B (2014) Transoceanic drift and the domestication of African bottle gourds in the Americas. Proc Natl Acad Sci 111:2937–2941
Liston A, Robinson WA, Oliphant JM, Alvarez-Buylla ER (1996) Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-Xowering seed plants. Syst Bot 21:109–120
Loukou AL, Gnakri D, Djè Y, Kippré AV, Malice M, Baudoin JP, Zoro BIA (2007) Macronutrient composition of three cucurbit species cultivated for seed consumption in Côte d’Ivoire. Afr J Biotechnol 6:529–533
Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563
Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics Appl Note 26:2462–2463
Mentewab AB, Jacobsen MJ, Flowers RA (2011) Incomplete homogenization of 18 S ribosomal DNA coding regions in Arabidopsis thaliana. BMC Res Notes 4:93
Morrison D (2005) Networks in phylogenetic analysis: new tools for population biology. Int J Parasitol 35:567–582
N’dri ANA, Vroh-Bi I, Zoro BIA, Kouamé LP (2010) Association mapping in Lagenaria siceraria for seed germination traits: sequence analysis of genes involved in the production of 9-cis epoxycarotenoid dioxygenase, a key enzyme of abscissic acid biosynthesis. In: NCBI GenBank (http://www.ncbi.nlm.nih.gov), accession numbers HQ586013-HQ586040
Nei M (1987) Molecular evolutionary genetics. Columbia University press, New York, NY, USA
Poczai P, Hyvönen J (2010) Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects. Mol Biol Rep 37:1897–1912
Renner SS, Schaefer H, Kocyan A (2007) Phylogenetics of Cucumis (Cucurbitaceae): cucumber (C. sativus) belongs in an Asian/Australian clade far from melon (C. melo). BMC Evol Biol 7:58
Richardson JB (1972) The pre-Columbian distribution of the bottle gourd (Lagenaria siceraria): a re-evaluation. Econ Bot 26:265–273
Saha P, Sen SK, Bala A, Mazumder UK, Haldar PK (2011) Evaluation of anticancer activity of Lagenaria siceraria aerial parts. Int J Canc Res 7:244–253
Sanchez-Villedas H, Schroeder S, Polacco M, McMullen M, Havermann S, Davis G, Vroh-Bi I, Cone K, Sharopova N, Yim Y, Chultz L, Duru N, Musket T, Houchins K, Fang Z, Gardiner J, Coe E (2003) Development of an integrated laboratory information management system for the maize mapping project. Bioinformatics 16:2022–2030
Schlumbaum A, Vandorpe P (2012) A short history of Lagenaria siceraria (bottle gourd) in the Roman provinces: morphotypes and archaeogenetics. Veg Hist Archaeobot 21:499–509
Schweinfurth G (1884) Further discoveries in the flora of ancient Egypt. Nature 29:312–315
Sebastian P, Schaefer H, Telford IRH, Renner SS (2010) Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc Natl Acad Sci 107:14269–14273
Szabo Z, Gyulai G, Humphreys M, Horvάth L, Bittsάnszky A, Lάgler R, Heszky L (2005) Genetic variation of melon (C. melo) compared to an extinct landrace from the Middle Ages (Hungary) I. rDNA, SSR and SNP analysis of 47 cultivars. Euphytica 146:87–94
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tyagi N, Sharma GN, Hooda V (2012) Phytochemical and pharmacological profile of Lagenaria siceraria: an overview. Int Res J Pharm 3:1–4
Vroh-Bi I, McMullen MD, Sanchez-Villeda H, Schroeder S, Gardiner J, Polacco M, Soderlund C, Wing R, Fang Z, Coe EH (2006) Single nucleotide polymorphisms and insertion-deletions for genetic markers and anchoring the maize fingerprint contig physical map. Crop Sci 46:12–21
Vroh-Bi I, Anagbogu C, Nnadi S, Tenkouano A (2011) Genomic characterization of natural and somaclonal variations in bananas (Musa spp.). Plant Mol Biol Report 29:440–448
Whitaker TW, Carter GF (1954) Oceanic drift of gourds - Experimental observations. Am J Bot 41:697–700
Whitaker TW, Carter GF (1961) A note on the longevity of seed of Lagenaria siceraria (Mol.) after floating in sea water. Bull Torrey Bot Club 88:104–106
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to methods and applications. Academic Press, Inc. pp 315–322
Xu P, Wu X, Luo J, Wang B, Liu Y, Ehlers JD, Wang S, Lu Z, Li G (2011) Partial sequencing of the bottle gourd genome reveals markers useful for phylogenetic analysis and breeding. BMC Genomics 12:467–476
Zandjanakou-Tachin M, Vroh-Bi I, Ojiambo PS, Tenkouano A, Gumedzoe YM, Bandyopadhyay R (2009) Identification and genetic diversity of Mycosphaerella species on banana and plantain in Nigeria. Plant Pathol 58:536–546
Zhou XZ, Chen Y, Chen S, Wu YF, Zhao YJ (2011) Studies on geographic divergence of Lagenaria siceraria ssp. asiatica based on 5.8S rDNA and ITS sequence data. China Vegetables 1:49–53
Zoro BIA, Koffi KK, Djè Y (2003) Caractérisation botanique et agronomique de trois espèces de cucurbites consommées en sauce en Afrique de l’Ouest: Citrullus sp., Cucumeropsis mannii Naudin et Lagenaria siceraria (Molina) Standl. Biotechnol Agron Soc Environ 7:189–199
Zoro BIA, Koffi KK, Djè Y, Malice M, Baudoin JP (2006) Indigenous cucurbits of Côte d’Ivoire: a review of their genetic resources. Sci Nat 3:1–9
Acknowledgments
The first author is grateful to the Food Security Center (FSC) of the University of Hohenheim (Stuttgart, Germany) for the visiting PhD sandwich scholarship that made this research work possible. We thank the anonymous reviewers whose contributions improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 104 kb)
Rights and permissions
About this article
Cite this article
N’dri, A.N.A., Zoro, B.I.A., Kouamé, L.P. et al. On the Dispersal of Bottle Gourd [Lagenaria siceraria (Mol.) Standl.] Out of Africa: a Contribution from the Analysis of Nuclear Ribosomal DNA Haplotypes, Divergent Paralogs and Variants of 5.8S Protein Sequences. Plant Mol Biol Rep 34, 454–466 (2016). https://doi.org/10.1007/s11105-015-0936-0
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-015-0936-0