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Genetic diversity, structure, gene flow and evolutionary relationships within the Sorghum bicolor wild–weedy–crop complex in a western African region

Theoretical and Applied Genetics volume 123, pages 1231–1246 (2011)Cite this article

Abstract

Gene flow between domesticated plants and their wild relatives is one of the major evolutionary processes acting to shape their structure of genetic diversity. Earlier literature, in the 1970s, reported on the interfertility and the sympatry of wild, weedy and cultivated sorghum belonging to the species Sorghum bicolor in most regions of sub-Saharan Africa. However, only a few recent surveys have addressed the geographical and ecological distribution of sorghum wild relatives and their genetic structure. These features are poorly documented, especially in western Africa, a centre of diversity for this crop. We report here on an exhaustive in situ collection of wild, weedy and cultivated sorghum assembled in Mali and in Guinea. The extent and pattern of genetic diversity were assessed with 15 SSRs within the cultivated pool (455 accessions), the wild pool (91 wild and weedy forms) and between them. F ST and R ST statistics, distance-based trees, Bayesian clustering methods, as well as isolation by distance models, were used to infer evolutionary relationships within the wild–weedy–crop complex. Firstly, our analyses highlighted a strong racial structure of genetic diversity within cultivated sorghum (F ST = 0.40). Secondly, clustering analyses highlighted the introgressed nature of most of the wild and weedy sorghum and grouped them into two eco-geographical groups. Such closeness between wild and crop sorghum could be the result of both sorghum’s domestication history and preferential post-domestication crop-to-wild gene flow enhanced by farmers’ practices. Finally, isolation by distance analyses showed strong spatial genetic structure within each pool, due to spatially limited dispersal, and suggested consequent gene flow between the wild and the crop pools, also supported by R ST analyses. Our findings thus revealed important features for the collection, conservation and biosafety of domesticated and wild sorghum in their centre of diversity.

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References

  • Arnold MJ (2004) Natural hybridization and the evolution of domesticated, pest and disease organisms. Mol Ecol 13:997–1007

    Article  PubMed  CAS  Google Scholar 

  • Barnaud A, Deu M, Garine E, McKey D, Joly H (2007) Local genetic diversity of sorghum in a village in northern Cameroon: structure and dynamics of landraces. Theor Appl Genet 114:237–248

    Article  PubMed  Google Scholar 

  • Barnaud A, Deu M, Garine E, Chantereau J, Bolteu J, Koïda EO, Mc Key D, Joly HI (2009) A weed–crop complex in sorghum: the dynamics of genetic diversity in a traditional farming system. Amer J Bot 96(10):1869–1879

    Article  CAS  Google Scholar 

  • Barro-Kondombo C, Sagnard F, Chantereau J, Deu M, vom Brocke K, Durand P, Gozé E, Zongo JD (2010) Genetic structure among sorghum landraces as revealed by morphological variation and microsatellite markers in three agroclimatic regions of Burkina Faso. Theor Appl Genet 120:1511–1523

    Article  PubMed  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2002) Genetix 4.04, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France. (Available from http://www.univ-montp2.fr/~genetix/genetix/genetix.htm)

  • Bezançon G, Pham JL, Deu M, Vigouroux Y, Sagnard F, Mariac C, Kapran I, Mamadou A, Gérard B, Ndjeunga J, Chantereau J (2009) Changes in the diversity and geographic distribution of cultivated millet (Pennisetum glaucum [L.] R. Br.) and sorghum (Sorghum bicolor (L.) Moench) varieties in Niger between 1976 and 2003. Genet Resour Crop Evol 56:223–236

    Article  Google Scholar 

  • Brown PJ, Myles S, Kresovich S (2011) Genetic support for phenotype-based racial classification in Sorghum. Crop Sci 51:224–230

    Article  Google Scholar 

  • de Wet JMJ (1978) Systematics and evolution of Sorghum sect. Sorghum (Gramineae). Am J Bot 65(4):477–484

    Article  Google Scholar 

  • de Wet JMJ, Harlan JR (1971) The origin and domestication of Sorghum bicolor. Econ Bot 25:129–134

    Article  Google Scholar 

  • de Wet JMJ, Harlan JR, Price EG (1970) Origin of variability in the spontanea complex of Sorghum bicolor. Am J Bot 57(6):704–707

    Article  Google Scholar 

  • de Wet JMJ, Harlan JR, Price EG (1976) Variability in Sorghum bicolor. In: Harlan JR, de Wet JMJ, Stemler ABL (eds) Origins of African plant domestication. Mouton, The Hague, pp 453–463

    Google Scholar 

  • Deu M, Hamon P, Chantereau J, Dufour P, D’Hont A, Lanaud C (1995) Mitochondrial DNA diversity in wild and cultivated sorghum. Genome 38:635–645

    Article  PubMed  CAS  Google Scholar 

  • Deu M, Rattunde F, Chantereau J (2006) A global view of genetic diversity in cultivated sorghums using a core collection. Genome 49:168–180

    PubMed  CAS  Google Scholar 

  • Deu M, Sagnard F, Chantereau J, Calatayud C, Hérault D, Mariac C, Pham JL, Vigouroux Y, Kapran I, Traoré PS, Mamadou A, Gérard B, Ndjeunga J, Bezançon G (2008) Niger-wide assessment of in situ sorghum genetic diversity with microsatellite markers. Theor Appl Genet 116:903–916

    Article  PubMed  CAS  Google Scholar 

  • Deu M, Sagnard F, Chantereau J, Calatayud C, Vigouroux Y, Pham JL, Mariac C, Kapran I, Mamadou A, Gérard B, Ndjeunga J, Bezançon G (2010) Spatio-temporal dynamics of genetic diversity in Sorghum bicolor in Niger. Theor Appl Genet 120:1301–1313

    Google Scholar 

  • Doggett H (1988) Sorghum, 2nd edn. Longman Scientific and Technical, London

    Google Scholar 

  • Ejeta G, Grenier C (2005) Sorghum and its weedy hybrids. In: Gressel J (ed) Crop ferality and volunteerism. Taylor & Francis, Boca Raton, pp 123–135

    Google Scholar 

  • Ellstrand NC (2003) Current knowledge on gene flow in plants: implications for transgene flow. Phil Trans R Soc Lond B 358:1163–1170

    Article  Google Scholar 

  • Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30:539–563

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Folkertsma RT, Rattunde HFW, Chandra S, Soma Raju W, Hash CT (2005) The pattern of genetic diversity of Guinea-race Sorghum bicolor (L.) Moench landraces as revealed with SSR markers. Theor Appl Genet 111:399–409

    Article  PubMed  CAS  Google Scholar 

  • Gepts P, Papa R (2003) Possible effects of (trans)gene flow from crops on the genetic diversity from landraces and wild relatives. Environ Biosafety Res 2:89–103

    Article  PubMed  Google Scholar 

  • Goudet J (2002) FSTAT, a program to estimate and test gene diversity and fixation indices (version 2.9.3.2. Available from http://www.unil.ch/izea/softwares/fstat.html)

  • Gressel J (2005) Introduction—the challenges of ferality. In: Gressel J (ed) Crop ferality and volunteerism. Taylor & Francis, Boca Raton, pp 1–7

    Chapter  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    PubMed  CAS  Google Scholar 

  • Harlan JR, de Wet JMJ (1971) Toward a rational classification of cultivated plants. Taxon 20(4):509–517

    Article  Google Scholar 

  • Harlan JR, de Wet JMJ (1972) A simplified classification of cultivated sorghum. Crop Sci 12:172–176

    Article  Google Scholar 

  • Jarvis DI, Hodgkin T (1999) Wild relatives and crop cultivars: detecting natural introgression and famer selection of new genetic combinations in agroecosystems. Mol Ecol 8:159–173

    Article  Google Scholar 

  • Jarvis A, Lane A, Hijmans RJ (2008) The effect of climate change on crop wild relatives. Agric Ecosyst Environ 126:13–23

    Article  Google Scholar 

  • Kalinowski ST (2005) HP-RARE1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kameswara Rao N, Reddy LJ, Bramel PJ (2003) Potential of wild species for genetic enhancement of some semi-arid food crops. Genet Resour Crop Evol l50:707–721

    Article  Google Scholar 

  • Kouressy M, Traoré S, Vaksmann M, Grum M, Maikano I, Soumaré M, Traoré PS, Bazile D, Dingkuhn M, Sidibé A (2008) Adaptation des sorghos du Mali à la variabilité climatique. Cah Agric 17(2):95–100

    Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data. Available from http://hydrodictyon.eeb.uconn.edu/people/plewis/software.php

  • Mariac C, Robert T, Allinne C, Remigereau MS, Luxereau A, Tidjani M, Seyni O, Bezançon G, Pham JL, Sarr A (2006a) Genetic diversity and gene flow among pearl millet crop/weed complex: a case study. Theor Appl Genet 113:1003–1004

    Article  PubMed  CAS  Google Scholar 

  • Mariac C, Luong V, Kapran I, Mamadou A, Sagnard F, Deu M, Chantereau J, Gérard B, Ndjeunga J, Bezancon G, Pham JL, Vigouroux Y (2006b) Diversity of wild and cultivated pearl millet accessions (Pennisetum glaucum [L.] R. Br.) in Niger assessed by microsatellite markers. Theor Appl Genet 114:49–58

    Article  PubMed  CAS  Google Scholar 

  • Martel C, Réjasse A, Rousset F, Bethenod M-T, Bourguet D (2003) Host-plant-associated genetic differentiation in Northern French populations of the European corn borer. Heredity 90:141–149

    Article  PubMed  CAS  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084

    Article  PubMed  CAS  Google Scholar 

  • Maxted N, Ford-Lloyd BV, Jury S, Kell S, Scholten M (2006) Towards a definition of a crop wild relative. Biodivers Conserv 15:2673–2685

    Article  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A genetic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    PubMed  CAS  Google Scholar 

  • Muraya MM, Sagnard F, Parzies HK (2010) Investigation of recent populations bottlenecks in Kenyan wild sorghum populations (Sorghum bicolor (L.) Moench ssp. verticilliflorum (Steud.) De Wet) based on microsatellite diversity and genetic disequilibria. Genet Resour Crop Evol 57:995–1005

    Article  CAS  Google Scholar 

  • Mutegi E, Sagnard F, Muraya M, Kanyenji B, Rono B, Mwongera C, Marangu C, Kamau J, Parzies H, de Villiers S, Semagn K, Traoré PS, Labuschagne M (2010) Ecogeographical distribution of wild, weedy and cultivated Sorghum bicolor (L.) Moench in Kenya: implications for conservation and crop-to-wild gene flow. Genet Resour Crop Evol 57:243–253

    Article  Google Scholar 

  • Mutegi E, Sagnard F, Semagn K, Deu M, Muraya M, Kanyenji S, de Villiers S, Kiambi D, Herselman L, Labuschagne M (2011) Genetic structure and relationships within and between cultivated and wild sorghum (Sorghum bicolor (L.) Moench) in Kenya as revealed by microsatellite markers. Theor Appl Genet 122:989–1004

    Article  PubMed  CAS  Google Scholar 

  • Papa R, Gepts P (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica. Theor Appl Genet 106:239–250

    PubMed  CAS  Google Scholar 

  • Papa R, Acosta J, Delgado-Salinas A, Gepts P (2005) A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica. Theor Appl Genet 111:1147–1158

    Article  PubMed  CAS  Google Scholar 

  • Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/darwin

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Risterucci AM, Grivet L, N’Goran JAK, Pieretti I, Flament MH, Lanaud C (2000) A high-density linkage map of Theobroma cacao L. Theor Appl Genet 101:948–955

    Article  CAS  Google Scholar 

  • Rousset F (1999) Genetic differentiation within and between two habitats. Genetics 151:397–407

    PubMed  CAS  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP’ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sagnard F, Barnaud A, Deu M, Barro C, Luce C, Billot C, Rami JF, Bouchet S, Dembélé D, Pomiès V, Calatayud C, Rivallan R, Joly H, vom Brocke K, Touré A, Chantereau J, Bezançon G, Vaksmann M (2008) Analyse multiéchelle de la diversité génétique des sorghos: compréhension des processus évolutifs pour la conservation in situ. Cah Agric 17(2):114–121

    Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allelic frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Snowden JD (1936) The cultivated races of sorghum. Adlard, London, pp 1–274

    Google Scholar 

  • Teshome A, Fahrig L, Torrance JK, Lambert JD, Arnason TJ, Baum BR (1999) Maintenance of sorghum (Sorghum bicolor, Poaceae) landrace diversity by farmers’ selection in Ethiopia. Econ Bot 53:79–88

    Article  Google Scholar 

  • Tesso T, Kapran I, Grenier C, Snow A, Sweeney P, Pedersen J, Marx D, Bothma G, Ejeta G (2008) The potential for crop-to-wild gene flow in sorghum in Ethiopia and Niger: a geographic survey. Crop Sci 48:1425–1431

    Article  Google Scholar 

  • Vigouroux Y, Mitchell S, Matsuoka Y, Hamblin M, Kresovich S, Smith JSC, Jaqueth J, Smith OS, Doebley J (2005) An analysis of genetic diversity across the maize genome using microsatellites. Genetics 169:1617–1630

    Article  PubMed  CAS  Google Scholar 

  • Zizumbo-Villarreal D, Colunga-Garcia Marin P, Payro de la Cruz E, Delgado-Valerio P, Gepts P (2005) Population structure and evolutionary dynamics of wild–weedy–domesticated complexes of common bean in a Mesoamerican region. Crop Sci 45:1073–1083

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This paper is dedicated by the co-authors to Dr. Fabrice Sagnard, the principal investigator of the project “Environmental Risk Assessment of Genetically Engineered Sorghum in Mali and Kenya”, who passed away in November 2008. We are grateful to the Biotechnology and Biodiversity Interface and Plant Biosafety Systems program funded by USAID for supporting the research activities reported here. We also acknowledge the Fonds Français pour l’Environnement Mondial (FFEM), which supported part of this project. We thank all the farmers from Mali and Guinea who shared their varieties and knowledge. The collection was performed in full compliance with the Convention on Biological Diversity. The authors thank the IER (Institut d’Economie Rurale, Mali) for the storage of all collected samples in view of future utilisation. We are also grateful to Dr. Ousmane Köita (professor at the University of Bamako) for hosting the master’s student in charge of DNA extractions in his laboratory. The authors thank J. Chantereau for interesting discussions and comments on the manuscript and the two anonymous reviewers for valuable suggestions. A part of this work was carried out using the resources of the Computational Biology Service Unit from Cornell University.

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Authors and Affiliations

  1. CIRAD, UMR AGAP, Avenue d’Agropolis, 34398, Montpellier, France

    Fabrice Sagnard, Monique Deu, Caroline Calatayud, Michel Vaksmann & Sophie Bouchet

  2. ICRISAT, co/ILRI, PO Box 39063, Nairobi, Kenya

    Fabrice Sagnard

  3. ICRISAT, Station de Samanko, PB 320, Bamako, Mali

    Dékoro Dembélé, Yaya Mallé, Sabine Togola & Pierre C. Sibiry Traoré

  4. INRA, UMR CBGP (INRA-IRD-CIRAD-Montpellier SupAgro), Campus International de Baillarguet, 34988, Montferrier-sur-Lez Cedex, France

    Raphaël Leblois

  5. IER-Sotuba, P.O. Box 1704, Bamako, Mali

    Lassana Touré & Michel Vaksmann

  6. IRAG, CRA Bordo- Programme Céréales, Kankan, Guinea

    Mohamed Diakité

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  1. Fabrice Sagnard
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  2. Monique Deu
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  3. Dékoro Dembélé
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Correspondence to Monique Deu.

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Communicated by H. H. Geiger.

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Sagnard, F., Deu, M., Dembélé, D. et al. Genetic diversity, structure, gene flow and evolutionary relationships within the Sorghum bicolor wild–weedy–crop complex in a western African region. Theor Appl Genet 123, 1231–1246 (2011). https://doi.org/10.1007/s00122-011-1662-0

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Keywords

  • Gene Flow
  • Sorghum
  • Sweet Sorghum
  • Wild Accession
  • Wild Sorghum

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