Abstract
Understanding the extent and partitioning of diversity within and among crop landraces and their wild/weedy relatives constitutes the first step in conserving and unlocking their genetic potential. This study aimed to characterize the genetic structure and relationships within and between cultivated and wild sorghum at country scale in Kenya, and to elucidate some of the underlying evolutionary mechanisms. We analyzed at total of 439 individuals comprising 329 cultivated and 110 wild sorghums using 24 microsatellite markers. We observed a total of 295 alleles across all loci and individuals, with 257 different alleles being detected in the cultivated sorghum gene pool and 238 alleles in the wild sorghum gene pool. We found that the wild sorghum gene pool harbored significantly more genetic diversity than its domesticated counterpart, a reflection that domestication of sorghum was accompanied by a genetic bottleneck. Overall, our study found close genetic proximity between cultivated sorghum and its wild progenitor, with the extent of crop-wild divergence varying among cultivation regions. The observed genetic proximity may have arisen primarily due to historical and/or contemporary gene flow between the two congeners, with differences in farmers’ practices explaining inter-regional gene flow differences. This suggests that deployment of transgenic sorghum in Kenya may lead to escape of transgenes into wild-weedy sorghum relatives. In both cultivated and wild sorghum, genetic diversity was found to be structured more along geographical level than agro-climatic level. This indicated that gene flow and genetic drift contributed to shaping the contemporary genetic structure in the two congeners. Spatial autocorrelation analysis revealed a strong spatial genetic structure in both cultivated and wild sorghums at the country scale, which could be explained by medium- to long-distance seed movement.
Similar content being viewed by others
References
Aldrich PR, Doebley J (1992) Restriction fragment variation in the nuclear and chloroplast genomes of cultivated and wild Sorghum bicolor. Theor Appl Genet 85:293–302
Aldrich PR, Doebley J, Schertz KF, Stec A (1992) Patterns of allozyme variation in cultivated and wild Sorghum bicolor. Theor Appl Genet 85:451–460
Auer C (2008) Ecological risk assessment and regulation for genetically-modified ornamental plants. Crit Rev Plant Sci 27:255–271
Ayana A, Bekele E, Bryngelsson T (2000a) Genetic variation in wild sorghum (Sorghum bicolor ssp verticilliflorum (L.) Moench) germplasm from Ethiopia assessed by random amplified polymorphic DNA (RAPD). Hereditas 132:249–254
Ayana A, Bryngelsson T, Bekele E (2000b) Genetic variation of Ethiopian and Eritrean sorghum (Sorghum bicolor (L.) Moench) germplasm assessed by random amplified polymorphic DNA (RAPD). Genet Resour Crop Evol 47:471–482
Ayana A, Byngelsson T, Bekele E (2001) Geographic and altitudinal allozyme variation in sorghum (Sorghum bicolor (L.) Moench) landraces from Ethiopia and Eritrea. Hereditas 135:1–12
Barnaud A, Deu M, Garine E, Mckey D, Joly HI (2007) Local genetic diversity of sorghum in a village in northern Cameroon: structure and dynamics of landraces. Theor Appl Genet 114:237–248
Barrett BA, Kidwell KK (1998) AFLP-based genetic diversity assessment among wheat cultivars from the Pacific Northwest. Crop Sci 38:1261–1271
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
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 405, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier
Bhatia CR, Mitra R (2003) Consequences of gene flow from genetically engineered crops. Curr Sci India 84:138–141
Casa AM, Mitchell SE, Hamblin MT, Sun H, Bowers JE, Paterson AH, Aquadro CF, Kresovich S (2005) Diversity and selection in Sorghum: simultaneous analyses using simple sequence repeats. Theor Appl Genet 111:23–30
Chandler S, Dunwell JM (2008) Gene flow, risk assessment and the environmental release of transgenic plants. Crit Rev Plant Sci 27:25–49
Clayton WD, Renvoize RD (1982) Poaceae. Flora of Tropical East Africa, Part 3 AA Balkema, Rotterdam
Cleveland DA, Soleri D (2005) Rethinking the risk management process for genetically engineered crop varieties in small-scale, traditionally based agriculture. Ecol Soc 10:1–33
Conner AJ, Glare TR, Nap JP (2003) The release of genetically modified crops into the environment. Part II. Overview of ecological risk assessment. Plant J 33:19–46
Cui YX, Xu GW, Magill CW, Schertz KF, Hart GE (1995) RFLP-based assay of Sorghum bicolor (L) Moench. genetic diversity. Theor Appl Genet 90:787–796
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
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 116:903–913
Djè Y, Ater M, Lefèbvre C, Vekemans X (1998) Patterns of morphological and allozyme variation in sorghum landraces of northwestern Morocco. Genet Resour Crop Evol 45:541–548
Djè Y, Forcioli D, Ater M, Lefèbvre C, Vekemans X (1999) Assessing population genetic structure of sorghum landraces from North-western Morocco using allozyme and microsatellite markers. Theor Appl Genet 99:157–163
Dogget H (1988) Sorghum. Longman Scientific and Technical, Essex
Dogget H, Majisu BN (1968) Disruptive selection in crop development. Heredity 23:1–23
Dogget H, Prasada Rao KE (1995) Sorghum. In: Smartt J, Simmonds NW (eds) Evolution of crop plants, 2nd edn. Longman Group, Essex, pp 140–159
Duncan RR, Bramel-Cox PJ, Miller FR (1991) Contributions of introduced sorghum germplasm to hybrids development in the USA. In: Shands HL, Wiesner LE (eds) Use of plant introductions in the cultivar development. Crop Science Society of America, Madison, pp 69–101
Ellstrand NC (1992) Gene flow by pollen: Implications for plant conservation genetics. Oikos 63:77–86
Ellstrand NC, Prentice HC, Hancock JF (1999) Geneflow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30:539–563
Epperson BK (1993) Recent advances in correlation analysis of spatial patterns of genetic variation. Evol Biol 27:95–155
Epperson BK (2004) Multilocus estimation of genetic structure within populations. Theor Popul Biol 65:227–237
Evanno S, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval LG, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
FAO (2008) FAOSTAT. http://faostat.fao.org
Folkertsma RF, Rattunde HFW, Chandra S, Raju GS, 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
Frankel OH, Hawkes JG (1975) Crop genetic resources for today and tomorrow. Cambridge University Press, Cambridge
Frankel OH, Brown AHD, Burdon JJ (1995) The conservation of plant diversity. Cambridge University Press, New York
Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sanchez G, Liu K, Buckler ES, Doebley J (2005) Genetic diversity and population structure of teosinte. Genetics 169:2241–2254
Gepts P (2004) Crop domestication as a long-term selection experiment. In: Jannick J (ed) Plant breeding reviews, Volume 24, Part 2: long-term selection: crops, animals, bacteria. Wiley, New York
Ghebru B, Schmidt RJ, Bennetzen JL (2002) Genetic diversity of Eritrean sorghum landraces assessed with simple sequence repeat (SSR) markers. Theor Appl Genet 105:229–236
Goudet J (2002) FSTAT, a program to estimate and test gene diversity and fixation indices. (version 2932)
Gurney AL, Press MC, Scholes JD (2002) Can wild relatives of sorghum provide new sources of resistance or tolerance against Striga species? Weed Sci 42:317–324
Halfhill MD, Zhu B, Warwick SI, Raymer PI, Millwood RJ, Weissinger AK, Stewart NC Jr (2004) Hybridization and backcrossing between transgenic oilseed rape and two related weed species under field conditions. Environ Biosafety Res 3:73–81
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol 2:618–620
Harlan JR, De Wet JMJ (1972) A simplified classification of cultivated sorghum. Crop Sci 12:172–177
Hartl DL, Clark G (1997) Principles of population genetics. Sinauer Associates Inc, Sunderland
Haygood R, Ives AR, Andow DA (2003) Consequences of recurrent gene flow from crops to wild relatives. Proc R Soc Lond B 270:1879–1886
Hulbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586
Idury RM, Cardon LR (1997) A simple method for automated allele binning in microsatellite markers. Genome Res 11:1104–1109
International Ltd VSN (2007) GenStat Discovery Edition 3 VSN International Ltd. Hernel Hempstead, UK
Kalinowski S (2005) HP-RARE 10: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol 5:187–189
Kamala V, Singh SD, Bramel PJ, Rao DM (2002) Sources of resistance to downy mildew in wild and weedy sorghums. Crop Sci 42:1357–1360
Kamala V, Sharma HC, Manohar Rao D, Varaprasad KS, Bramel PJ (2009) Wild relatives of sorghum as sources of resistance to sorghum shoot fly, Atherigona soccata. Plant Breed 128:137–142
Ladizinsky G (1999) Plant evolution under domestication. Kluwer Academic Publishers, London
Levin DA, Kerster HW (1974) Gene flow in seeds plants. Evol Biol 7:139–220
Mace EM, Buhariwalla HK, Crouch JH (2003) A high-throughput DNA extraction protocol for tropical molecular breeding programs. Plant Mol Biol Rep 21:459a–500h
Mariac C, Luong V, Kapran I, Mamadou A, Sagnard F, Deu M, Chantereau J, Gérard B, Ndjeunga J, Bezançon G, Pham JL, Vigouroux Y (2006) 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
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
Mohammadi SA, Prasanna BM (2003) Analysis of genetic diversity in crop plants—salient statistical tools and considerations. Crop Sci 43:1235–1248
Morden CW, Doebley JF, Schertz KF (1990) Allozyme variation among the spontaneous species of Sorghum section Sorghum (Poaceae). Theor Appl Genet 80:296–304
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
Neal D (2004) Introduction to population biology. Cambridge University Press, Cambridge
Nkongolo KK, Nsapato L (2003) Genetic diversity in Sorghum bicolor (L.) Moench accessions from different ecogeographical regions in Malawi assessed with RAPDs. Genet Resour Crop Evol 50:149–156
Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/darwin
Prasanth V, Chandra S, Jayashree B, Hoisington D (2006) AlleloBin—a program for allele binning of microsatellite markers based on the algorithm of Idury and Cardon (1997). ICRISAT International Crops Research Institute for the Semi, Arid Tropics
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rao Kameswara N, Reddy LJ, Bramel PJ (2003) Potential of wild species for genetic enhancement of some semi-arid food crops. Genet Resour Crop Evol 50:707–721
Reed JD, Ramundo BA, Claflin LF, Tuinstra MR (2002) Analysis of resistance to ergot in sorghum and potential alternate hosts. Crop Sci 42:1135–1138
Rich PJ, Grenier U, Ejeta G (2004) Striga resistance in the wild relatives of sorghum. Crop Sci 44:2221–2229
Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
Sagnard F, Barnaud A, Deu M, Barro C, Luce C, Billot C, Rami JF, Bouchet S, Dembelé D, Pomies V, Calatayud C, Rivallan R, Joly H, vom Brocke K, Touré A, Chantereau J, Bezançon G, Vaksmann M (2008) Multi-scale analysis of sorghum genetic diversity: understanding the evolutionary processes for in situ conservation. Cah Agric 17:114–121
Schuelke M (2000) An economic method for the fluorescent labelling of PCR fragments. A poor man’s approach to genotyping for research and high throughput diagnostics. Nat Biotechnol 18:233–234
Sharma HC, Franzmann BA (2001) Host plant preference and oviposition responses of the sorghum midge Stenodiplosis sorghicola (Coquillett) (Dipt., Cecidomyiidae) towards wild relatives of Sorghum. J Appl Ent 125:109–114
Snow AA, Moran-Palma P (1997) Commercialization of transgenic plants: potential ecological risks. Bioscience 47:86–96
Sokal RR, Oden NL (1978) Spatial autocorrelation in biology 2. Some biological implications and four applications of evolutionary and ecological interest. Biol J Linn Soc 10:249
Sombroek WC, Braun HMH, van der Pour BJA (1982) Explanatory soil map and agro-climatic zone map of Kenya. Report E1:1–56
R Development Core Team (2007) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org
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
Thies JE, Devare MH (2007) An ecological assessment of transgenic crops. J Dev Stud 43:97–129
Uptmoor R, Wenzel W, Friedt W, Donaldson G, Ayisi K, Ordon F (2003) Comparative analysis on the genetic relatedness of Sorghum bicolor accessions from Southern Africa by RAPDs, AFLPs and SSRs. Theor Appl Genet 106:1316–1325
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Acknowledgments
This study formed part of the project, “Environmental risk assessment for the introduction of genetically modified sorghum in Mali and Kenya” funded by the United States Agency for International Development (USAID) Biotechnology and Biodiversity Interface (BBI) Program. We are deeply indebted to the late Dr. Fabrice Sagnard (Principle Investigator), who offered exemplary leadership and immense scientific contribution to the entire project. We acknowledge Caroline Mwongera, Charles Marangu and Bernard Rono who participated in collections as well as farmers from various sorghum growing areas of Kenya and the National Genebank of Kenya for providing the seed samples used in this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. Luebberstedt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mutegi, E., Sagnard, F., Semagn, K. et al. 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 (2011). https://doi.org/10.1007/s00122-010-1504-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-010-1504-5