Abstract
Pearl millet [Pennisetum glaucum (L.) R. Br.] is a food security crop in the harshest agricultural regions of the world. While low soil phosphorus (P) availability is a big constraint on its production, especially in West Africa (WA), information on genomic regions responsible for low-P tolerance in pearl millet is generally lacking. We present the first report on genetic polymorphisms underlying several plant P-related parameters, flowering time (FLO) and grain yield (GY) under P-limiting conditions based on 285 diversity array technology markers and 151 West African pearl millet inbred lines phenotyped in six environments in WA under both high-P and low-P conditions. Nine markers were significantly associated with P-related traits, nine markers were associated with FLO, whereas 13 markers were associated with GY each explaining between 5.5 and 15.9 % of the observed variation. Both constitutive and adaptive associations were observed for FLO and GY, with markers PgPb11603 and PgPb12954 being associated with the most stable effects on FLO and GY, respectively, across locations. There were a few shared polymorphisms between traits, especially P-efficiency-related traits and GY, implying possible colocation of genomic regions responsible for these traits. Our findings help bridge the gap between quantitative and molecular methods of studying complex traits like low-P tolerance in WA. However, validation of these markers is necessary to determine their potential applicability in marker-assisted selection programs targeting low-P environments, which are especially important in WA where resource-poor farmers are expected to be the hardest hit by the approaching global P crisis.
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References
Anand Kumar K, Andrews DJ (1993) Genetics of quantitative traits in pearl millet: an overview. Crop Sci 33:1–20
Andrews DJ, Kumar KA (1992) Pearl millet for food, feed and forage. Adv Agron 48:89–139
Andrews DJ, Kumar KA (1996) Use of the West African pearl millet landrace Iniadi in cultivar development. Plant Genet Resour Newsl 105:15–22
Bashir EMA, Abdelbagi MA, Adam MA, Melchinger AE, Parzies HK, Haussmann BIG (2014a) Characterization of Sudanese pearl millet germplasm for agro-morphological traits and grain nutritional values. Plant Genet Res 12:35–47
Bashir EMA, Ali AM, Ali AM, Ismail MI, Parzies HK, Haussmann BIG (2014b) Patterns of pearl millet genotype-by-environment interaction for yield performance and grain quality traits in Sudan. Field Crops Res 166:82–91
Bashir EMA, Abdelbagi MA, Adam MA, Mohamed ETI, Melchinger AE, Parzies HK, Haussmann BIG (2015) Genetic diversity of Sudanese pearl millet (Pennisetum glaucum (L.) R. Br.) landraces as revealed by SSR markers, and relationship between genetic and agro-morphological diversity. Genet Resour Crop Evol 62:579–591. doi:10.1007/s10722-014-0183-5
Baskaran K, Hash CT, Senthilvel S, Bhasker Raj AG, Muthiah AR (2009) SSR allele frequency changes in response to recurrent selection for pearl millet grain yield and other agronomic traits. J SAT Agric Res 7:8. http://oar.icrisat.org/577/
Baskaran K, Senthilvel S, Bhasker Raj AG, Chandra S, Muthiah A, Dhanapal AP, Hash CT (2014) Association analysis of SSR markers with phenology, grain and stover-yield related traits in pearl millet (Pennisetum glaucum (L.) R. Br.). Sci World J. doi:10.1155/2014/562327
Bationo A, Mokwunye AU (1991) Role of manures and crop residues in alleviating soil fertility constraints to crop production: with special reference to the Sahelian and Sudanian zones of West Africa. Fert Res 29:117–125
Bationo A, Mughogho SK, Mokwunye AU (1986) Agronomic evaluation of phosphate fertilizers in tropical Africa. In: Mokwunye AU, Vlek PLG (eds) Management of nitrogen and phosphorus fertilizers of sub-Saharan Africa. Developments in plant and soil sciences 24. Martinus Nijhoff, Dordrecht, pp 283–318
Bationo A, Chien SH, Henao J, Christianson BC, Mokwunye AU (1990) Agronomic evaluation of two unacidulated and partially acidulated phosphate rocks indigenous to Niger. Soil Sci Soc Am J 54:1772–1777
Beebe SE, Rojas-Pierce M, Yan X, Blair MW, Pedraza F, Munoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46:413–423
Beebe SE, Rao IM, Cajiao C, Grajales M (2007) Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Sci 48:582–592
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and multiple approach to multiple testing. J R Stat Soc 57(1):289–300
Bhattacharjee R, Khairwal IS, Bramel PJ, Reddy KN (2007) Establishment of a pearl millet [Pennisetum glaucum (L.) R. Br.] core collection based on geographical distribution and quantitative traits. Euphytica 155:35–45
Bidinger FR, Serraj R, Rizvi SMH, Howarth C, Yadav RS, Hash CT (2005) Field evaluation of drought tolerance QTL effects on phenotype and adaptation in pearl millet [Pennisetum glaucum (L.) R. Br.] topcross hybrids. Field Crops Res 94:14–32
Bidinger FR, Nepolean T, Hash CT, Yadav RS, Howarth CJ (2007) Identification of QTLs for grain yield of pearl millet [Pennisetum glaucum (L.) R Br] in environments with variable moisture during grain filling. Crop Sci 47:969–980
Bolibok-Bragoszewska H, Heller-Uszynska K, Wenzl P, Uszynski G, Kilian A, Rakoczy-Trojanowska M (2009) DArT markers for the rye genome-genetic diversity and mapping. BMC Genomics 10:578
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635
Breese WA, Hash CT, Devos KM, Howarth CJ (2002) Pearl millet genomics—an overview with respect to breeding for resistance to downy mildew. In: Leslie JF (ed) Sorghum and millets pathology 2000. Iowa State Press, Ames, pp 243–246
Brück H, Payne WA, Sattelmacher B (2000) Effects of phosphorus and water supply on yield, transpirational water-use efficiency, and carbon isotope discrimination in pearl millet. Crop Sci 40:120–125
Brück H, Sattelmacher B, Payne WA (2003) Varietal differences in shoot and rooting parameters of pearl millet on sandy soils in Niger. Plant Soil 251:175–185
Camus-Kulandaivelu L, Veyrieras JB, Madur D, Combes V, Fourmann M, Barraud S, Dubreuil P, Gouesnard B, Manicacci D, Charcosset A (2006) Maize adaptation to temperate climate: relationship between population structure and polymorphism in the Dwarf8 gene. Genetics 172:2449–2463
Chan EK, Rowe HC, Kliebenstein DJ (2010) Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics 185(3):991–1007
Chen J, Xu L, Cai Y, Xu J (2009) Identification of QTLs for phosphorus utilization efficiency in maize (Zea mays L.) across P levels. Euphytica 167:245–252. doi:10.1007/s10681-009-9883-x
Chen J, Cai Y, Xu L, Wang J, Zhang W, Wang G, Xu D, Chen T, Lu X, Sun H, Huang A, Liang Y, Dai G, Qin H, Huang Z, Zhu Z, Yang Z, Xu J, Kuang S (2011) Identification of QTLs for biomass production in maize (Zea mays L.) under different phosphorus levels at two sites. Front Agric China 5:152–161. doi:10.1007/s11703-011-1077-3
Clotault J, Thuillet A-C, Buiron M, De Mita S, Couderc M et al (2012) Evolutionary history of pearl millet (Pennisetum glaucum [L.] R. Br.) and selection on flowering genes since its domestication. Mol Biol Evol 29:1199–1212
Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147:469–486. doi:10.1104/pp.108.118117
Cooper M, Delacy IH, Basford KE (1996) Relationships among analytical methods used to analyze genotypic adaptation in multi-environment trials. In: Cooper M, Hammer GL (eds) Plant adaptation and crop improvement. CAB International, Wallingford, pp 193–224
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374
Flint-Garcia SA, Thuillet A, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064
Gahoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260:47–57
Gemenet DC, Wachira FN, Pathak RS, Munyiri SW (2010) Identification of molecular markers linked to drought tolerance using bulked segregant analysis in Kenyan maize landraces (Zea mays L.). JAPS 9(1):1122–1134
Gemenet DC, Hash CT, Sy O, Zangre RG, Sanogo MD, Leiser WL, Parzies HK, Haussmann BIG (2014) Pearl millet inbred and testcross performance under low phosphorus in West Africa. Crop Sci 54:2574–2585
Gemenet DC, Hash CT, Sanogo MD, Sy O, Zangre RG, Leiser WL, Haussmann BIG (2015a) Phosphorus uptake and utilization efficiency in West African pearl millet inbred lines. Field Crops Res 171:54–66
Gemenet DC, Beggi F, Hash CT, Sy O, Sanogo MD, Zangre RG, Falalou H, Buerkert A, Haussmann BIG (2015b) Towards understanding the traits contributing to performance of pearl millet open-pollinated varieties in phosphorus-limited environments of West Africa. Plant Soil (in press)
Goswami AK, Sharma KP, Sehgal KI (1969) Nutritive value of proteins of pearl millet of high-yielding varieties and hybrids. Br J Nutr 23:913–916
Gulia SK, Hash CT, Thakur RP, Breese WA, Sangwan RS (2007) Mapping new QTLs for downy mildew [Sclerospora graminicola (Sacc.) J. Schroet.] resistance in pearl millet (Pennisetum glaucum (L.) R. Br.). In: Singh DP, Tomar VS, Behl RK, Upadhyaya SD, Bhale MS, Khare K (eds) Crop production in stress environments—genetic and management options. Agrobios Publishers, Jodhpur, pp 373–386
Gupta SK, Nepolean T, Rai KN, Hash CT, Bhattacharjee R, Rathore A (2012) Within-line genetic variation for quantitative characters and SSRs in long-time maintained inbreds in pearl millet [Pennisetum glaucum (L). R. Br.]. Eur J Plant Sci Biotech 6(SI 2):109–113
Haesler S (2012) Drought with subsequent floods in the area of Sahel West Africa 2011/2012. http://www.dwd.de/bvbw/generator/DWDWWW/Content/Oeffentlichkeit/KU/KU2/KU24/besondere__ereignisse__global/niederschlaege/englischeberichte/2012__drought__Sahel,templateId=raw,property=publicationFile.pdf/2012_drought_Sahel.pdf. Accessed Dec 2014
Hao D, Cheng H, Yin Z, Cui S, Zhang D, Wang H, Yu D (2012) Identification of single nucleotide polymorphisms and haplotypes associated with yield and yield components in soybean (Glycine max) landraces across multiple environments. Theor Appl Genet 124:447–458
Harlan J, De Wet J, Stemler A (1976) Origins of African plant domestication. Mouton Publishers, La Hague
Hash CT, Witcombe JR (2001) Pearl millet molecular marker research. Int Sorghum Millets Newsl 42:8–15 (published 2005)
Hash CT, Cavan GP, Bidinger FR, Howarth CJ, Singh SD (1995) Downy mildew resistance QTLs from a seedling heat tolerance mapping population. Int Sorghum Millets Newsl 36:66–67
Hash CT, Schaffert RE, Peacock JM (2002) Prospects for using conventional techniques and molecular biological tools to enhance performance of ‘orphan’ crop plants on soils low in available phosphorus. Plant Soil 245:135–146
Hash CT, Bhasker Raj AG, Lindup S, Sharma A, Beniwal CR, Folkertsma RT, Mahalakshmi V, Zerbini E, Blümmel M (2003) Opportunities for marker-assisted selection (MAS) to improve the feed quality of crop residues in pearl millet and sorghum. Field Crop Res 84:79–88
Hash CT, Thakur RP, Rao VP, Bhasker Raj AG (2006a) Evidence for enhanced resistance to diverse isolates of pearl millet downy mildew through gene pyramiding. Int Sorghum Millets Newsl 47:134–138
Hash CT, Sharma A, Kolesnikova-Allen MA, Singh SD, Thakur RP, Bhasker Raj AG, Ratnaji Rao MNV, Nijhawan DC, Beniwal CR, Sagar P, Yadav HP, Yadav YP, Srikant S, Bhatnagar SK, Khairwal IS, Howarth CJ, Cavan GP, Gale MD, Liu C, Devos KM, Breese WA, Witcombe JR (2006) Teamwork delivers biotechnology products to Indian small-holder crop-livestock producers: Pearl millet hybrid “HHB 67 Improved” enters seed delivery pipeline. SAT eJ 2(1). http://www.icrisat.org/Journal/bioinformatics/v2i1/v2i1teamwork.pdf
Haussmann BIG, Rattunde HF, Weltzien-Rattunde E, Traore PSC, vom Brocke K, Parzies HK (2012) Breeding strategies for adaptation of pearl millet and sorghum to climate variability and change in West Africa. J Agron Crop Sci 198:327–339. doi:10.1111/j.1439-037X.2012.00526.x
Hedrick PW (2005) Genetics of populations. Jones and Bartlett Publishers, Massachusetts, p 737
Hufnagel B, de Sousa SM, Assis L et al (2014) Duplicate and conquer: multiple homologs of phosphorus-starvation tolerance 1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiol 166:659–677
Hurtado P, Olsen KM, Buitrago C, Ospina C, Marin J, Duque M, de Vicente C, Wongtiem P, Wenzel P, Kilian A, Adeleke M, Fregene M (2008) Comparison of simple sequence repeat (SSR) and diversity array technology (DArT) markers for assessing genetic diversity in cassava (Manihot esculenta Crantz). Plant Genet Resour Charact Util 6(3):208–214
Jaccoud D, Peng K, Feinstein D, Kilian A (2001) Diversity arrays: a solid state technology for sequence information independent genotyping. Nucleic Acids Res 29(4):e25
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Jing H-C, Bayon C, Kanyuka K, Berry S, Wenzl P, Huttner E, Kilian A, Hammond-Kosack KE (2009) DArT markers: diversity analyses, genomes comparison, mapping and integration with SSR markers in Triticum monococcum. BMC Genomics 10:458. doi:10.1186/1471-2164-10-458
Jones ES, Liu CJ, Gale MD, Hash CT, Witcombe JR (1995) Mapping quantitative trait loci for downy mildew resistance in pearl millet. Theor Appl Genet 91:448–456
Jones ES, Breese WA, Liu CJ, Singh SD, Shaw DS, Witcombe JR (2002) Mapping quantitative trait loci for resistance to downy mildew in pearl millet. Crop Sci 42:1316–1323. doi:10.2135/cropsci2002.1316
Kapila RK, Yadav RS, Plaha P, Rai KN, Yadav OP, Hash CT, Howarth CJ (2008) Analysis of genetic diversity in pearl millet inbreds using microsatellite markers. Plant Breed 127(1):33–37. doi:10.1111/j.1439-0523.2007.01433.x
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53(3):983–997
Khairwal IS, Hash CT (2007) “HHB 67-Improved”—the first product of marker-assisted crop breeding in India. Asia-Pacific Consortium on Agricultural Biotechnology (APCoAB) e-News. http://www.apcoab.org/special_news.html
Kholová J, Hash CT, Kakkera A, Kočová M, Vadez V (2010a) Constitutive water-conserving mechanisms are correlated with the terminal drought tolerance of pearl millet [Pennisetum glaucum (L.) R. Br.]. J Exp Bot 61:369–377. doi:10.1093/jxb/erp314
Kholová J, Hash CT, Lava Kumar P, Yadav RS, Kočová M, Vadez V (2010b) Terminal drought tolerant pearl millets [Pennisetum glaucum (L.) R. Br.] have high leaf ABA and limit transpiration at high vapor pressure deficit. J Exp Bot 61:1431–1440
Kholová J, Nepolean T, Hash CT, Supriya A, Rajaram V, Senthilvel S, Kakkera A, Yadav RS, Vadez V (2012) Water saving traits co-map with a major terminal drought tolerance quantitative trait locus in pearl millet (Pennisetum glaucum (L.) R. Br.). Mol Breed 30:1337–1353. doi:10.1007/s11032-012-9720-0
King KE, Lauter N, Lin SF, Scott MP, Shoemaker RC (2013) Evaluation and QTL mapping of phosphorus concentration in soybean seed. Euphytica 189:261–269
Kraakman ATW, Niks RE, Van den Berg PMMM, Piet Stam P, van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446. doi:10.1534/genetics.104.026831
Lakis G, Navascués M, Rekima S, Simon M, Remigereau M-S, Leveugle M, Takvorian N, Lamy F, Depaulis F, Robert T (2012) Evolution of neutral and flowering genes along pearl millet (Pennisetum glaucum) domestication. PLoS ONE 7:e36642. doi:10.1371/journal.pone.0036642
Lebreton C, LazicJancic V, Steed A, Pekic SQS (1995) Identification of QTL for drought responses in maize and their use in testing causal relationships between traits. J Exp Bot 46:853–865
Leiser WL, Rattunde HFW, Piepho HP, Weltzien E, Diallo A, Melchinger AE, Parzies HK, Haussmann BIG (2012) Selection strategy for sorghum targeting phosphorus limited environments in West Africa: analysis of multi-environment experiments. Crop Sci 52:2517–2527
Leiser WL, Rattunde HFW, Weltzien E, Cisse N, Abdou M, Diallo A, Tourè AO, Magalhaes JV, Haussmann BIG (2014) Two in one sweep: aluminum tolerance and grain yield in P-limited soils are associated to the same genomic region in West African sorghum. BMC Plant Biol 14:206. http://www.biomedcentral.com/1471-2229/14/206
Lewis LR (2010) Biogeography and genetic diversity of pearl Millet (Pennisetum glaucum) from Sahelian Africa. Prof Geogr 62:377–394
Li YD, Wang YJ, Tong YP, Gao JG, Zhang JS, Chen SY (2005) QTL mapping of phosphorus deficiency tolerance in soybean (Glycine max L. Merr.). Euphytica 142:137–142. doi:10.1007/s10681-005-1192-4
Li M, Guo X, Zhang M, Wang X, Zhang G, Tian Y, Wang Z (2010) Mapping QTLs for grain yield and yield components under high and low phosphorus treatments in maize (Zea mays L.). Plant Sci 178:454–462. doi:10.1016/j.plantsci.2010.02.019
Mace ES, Xia L, Jordan DR, Halloran K, Parh DK, Huttner E, Wenzl P, Kilian A (2008) DArT markers: diversity analyses and mapping in Sorghum bicolor. BMC Genom 9:26
Manning K (2011) 4500-Year old domesticated pearl millet (Pennisetum glaucum) from the Tilemsi Valley, Mali: new insights into an alternative cereal domestication pathway. J Archaeol Sci. doi:10.1016/j.jas.2010.09.007
Mariac C, Luong V, Kapran I, Mamadou A, Sagnard F, Deu M, Chantereau J, Gerard B, Ndjeunga J, Bezancon G, Pham J-L, 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. doi:10.1007/s00122-006-0409-9
Mendes FF, Guimarães LJM, Souza JC, Guimarães PEO, Magalhaes JV, Garcia AAF, Parentoni SN, Guimaraes C (2014) Genetic architecture of phosphorus use efficiency in tropical maize cultivated in a low P soil. Crop Sci 54:1530–1538. doi:10.2135/cropsci2013.11.0755
Muehlig-Versen B, Buerkert A, Bationo A, Roemheld V (2003) Phosphorus placement on acid arenosols of the West African Sahel. Exp Agric 39:307–325
Nepolean T, Blümmel M, Hash CT (2009) Improving straw quality traits through QTL mapping and marker-assisted selection in pearl millet. In: Forage symposium 2009—emerging trends in forage research and livestock production, February 16–17, p 12
Nepolean T, Gupta SK, Dwivedi SL, Bhattacharjee R, Rai KN, Hash CT (2012) Genetic diversity in maintainer and restorer lines of pearl millet. Crop Sci 52:2555–2563
Oumar I, Mariac C, Pham JL, Vigouroux Y (2008) Phylogeny and origin of pearl millet (Pennisetum glaucum [L.] R. Br.) as revealed by microsatellite loci. Theor Appl Genet 117:489–497
Parentoni S, de Souza Jr C, de Carvalho Alves V et al (2010) Inheritance and breeding strategies for phosphorus efficiency in tropical maize (Zea mays L.). Maydica 55:1–15
Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA, Haseneyer G, Kilian B, Graner A (2012) Genome-wide association studies for agronomical traits in a world-wide spring barley collection. BMC Plant Biol 12:16. http://www.biomedcentral.com/1471-2229/12/16
Payne WA, Lascano RJ, Hossner LR, Wendt CW, Onken AB (1991) Pearl millet growth as affected by phosphorus and water. Agron J 83:942–948
Payne WA, Hossner LR, Onken AB, Wendt CW (1995) Nitrogen and phosphorus uptake in pearl millet and its relation to nutrient and transpiration efficiency. Agron J 87:425–431
Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/darwin
Piepho H-P, Möhring J (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177:1881–1888
Piepho H-P, Möhring J, Schulz-Streeck T, Ogutu JO (2012) A stage-wise approach for the analysis of multi-environment trials. Biom J 54(6):844–860
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multi-locus genotype data. Genetics 155:945–959
Pucher A, Hogh-Jensen H, Gondah J, Hash CT, Haussmann BIG (2014) Micronutrient density and stability in West African pearl millet—potential for biofortification. Crop Sci 54:1709–1720
Pucher A, Sy O, Angarawai II, Gondah J, Zangre R, Ouedraogo M, Sanogo MD, Boureima S, Hash CT, Haussmann BIG (2015) Agro-morphological characterization of West and Central African pearl millet accessions. Crop Sci. doi:10.2135/cropsci2014.06.0450
Rai KN, Rao AS, Hash CT (1995) Registration of pearl millet parental lines ICMA 88004 and ICMB 88004. Crop Sci 35:1242
Rai KN, Hash CT, Singh AK, Velu G (2008) Adaptation and quality traits of a germplasm-derived commercial seed parent of pearl millet. Plant Genet Resour Newsl 154:20–24
Raman R, Cowley RB, Raman H, Luckett DJ (2014) Analyses using SSR and DArT molecular markers reveal that Ethiopian accessions of white lupin (Lupinus albus L.) represent a unique genepool. Open J Genet 4:87–98. doi:10.4236/ojgen.2014.42012
Ramdoss Y, Oak ME, Holmberg KJ, Stevens N, Zhang Y (2011) User manual for TASSEL-Trait Analysis by aSSociation, evolution and linkage version 3.0. The Buckler Lab at Cornell, 73 pp
Rebafka F-P, Hebel A, Bationo A, Stahr K, Marschner S (1994) Short- and long-term effects of crop residues and of phosphorus fertilization on pearl millet yield on an acid sandy soil in Niger, West Africa. Field Crops Res 36:113–124
Reiter RS, Coors JG, Sussman MR, Gabelman WH (1991) Genetics analysis of tolerance to low-phosphorus stress in maize using RFLP. Theor Appl Genet 82:561–568
Rose TJ, Pariasca-Tanaka J, Rose MT, Fukuta Y, Wissuwa M (2010) Genotypic variation in grain phosphorus concentration, and opportunities to improve P-use efficiency in rice. Field Crop Res 119:154–160
Sabadin PK, Malosetti M, Boer MP, Tardin FD, Santos FG, Guimarães CT, Gomide RL, Andrade CLT, Albuquerque PEP, Caniato FF, Mollinari M, Margarido GRA, Oliveira BF, Schaffert RE, Garcia AAF, van Eeuwijk FA, Magalhaes JV (2012) Studying the genetic basis of drought tolerance in sorghum by managed stress trials and adjustments for phonological and plant height differences. Theor Appl Genet 124:1389–1402. doi:10.1007/s00122-012-1795-9
Saidou AA, Mariac C, Luong V, Pham J-L, Bezancon G et al (2009) Association studies identify natural variation at PHYC linked to flowering time and morphological variation in pearl millet. Genetics 182:899–910
Saidou AA, Clotault J, Couderc M, Mariac C, Katrien M, Devos KM, Thuillet AC, Ibrahim A, Amoukou IA, Vigouroux Y (2014) Association mapping, patterns of linkage disequilibrium and selection in the vicinity of the PHYTOCHROME C gene in pearl millet. Theor Appl Genet 127:19–32. doi:10.1007/s00122-013-2197-3
SAS Institute (2015) SAS Institute Inc., SAS Campus Drive, Cary, North Carolina 27513-2414
Sawaya WN, Khalil JK, Safi WJ (1984) Nutritional quality of pearl-millet flour and bread. Plant Foods Hum Nutr 34:117–125
Schaffert RE, Alves VMC, Parentoni SN, Raghothama KG (2000) Genetic control of phosphorus uptake and utilization efficiency in maize and sorghum under marginal soil conditions. In: Ribaut JM, Poland D (eds) Molecular approaches for the genetic improvement of cereals for stable production in water-limited environments. A strategic planning workshop held at CIMMYT, El Batan, Mexico, 21–25 June 1999. International Maize and Wheat Improvement Center (CIMMYT), Mexico, DF, Mexico, pp 79–85
Sehgal D, Rajaram V, Armstead IP, Vadez V, Yadav YP, Hash CT, Yadav RS (2012) Integration of gene-based markers in a pearl millet genetic map for identification of candidate genes underlying drought tolerance quantitative trait loci. BMC Plant Biol 12:9. http://www.biomedcentral.com/1471-2229/12/9
Serraj R, Hash CT, Rizvi SMH, Sharma A, Yadav RS, Bidinger FR (2005) Recent advances in marker-assisted selection for drought tolerance in pearl millet. Plant Prod Sci 8:332–335
Sharma PC, Singh D, Sehgal D, Singh G, Hash CT, Yadav RS (2014) Further evidence that a terminal drought tolerance QTL of pearl millet is associated with reduced salt uptake. Environ Exp Bot 102:48–57. doi:10.1016/j.envexpbot.2014.01.013
Stegmeier WD, Andrews DJ, Rai KN (1998a) Pearl millet parental lines 842A and 842B. Int Sorghum Millets Newsl 39:128–129
Stegmeier WD, Andrews DJ, Rai KN, Hash CT (1998b) Pearl millet parental lines 843A and 843B. Int Sorghum Millets Newsl 39:129–130
Stich B, Möhring J, Piepho H-P, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754. doi:10.1534/genetics.107.079707
Stich B, Haussmann BIG, Pasam R, Bhosale S, Hash CT, Melchinger AE, Parzies HK (2010) Patterns of molecular and phenotypic diversity in pearl millet [Pennisetum glaucum (L.) R. Br.] from West and Central Africa and their relation to geographical and environmental parameters. BMC Plant Biol 10:1–10. doi:10.1186/1471-2229-10-216
Su JY, Zheng Q, Li HW, Li B, Jing RL, Tong YP, Li ZS (2009) Detection of QTLs for phosphorus use efficiency in relation to agronomic performance in wheat grown under phosphorus sufficient and limited conditions. Plant Sci 176:824–836
Subbarao GV, Renard C, Payne WA, Batiano A (2000) Longterm effects of tillage, phosphorus fertilization and crop rotation on pearl millet–cowpea productivity in the West-African Sahel. Exp Agric 36:243–264
Supriya A, Senthilvel S, Nepolean T, Eshwar K, Rajaram V, Shaw R, Hash CT, Kilian A, Yadav RC, Narasu ML (2011) Development of a molecular linkage map of pearl millet integrating DArT and SSR markers. Theor Appl Genet 123:239–250. doi:10.1007/s00122-011-1580-1
Tinker NA, Kilian A, Wight CP, Heller-Uszynska K, Wenzl P, Rines HW, Bjørnstad A, Howarth CJ, Jannink JL, Anderson JM, Rossnage BG, Stuthman DD, Sorrells ME, Jackson EW, Tuvesson S, Kolb FL, Olsson O, Federizzi LC, Carson ML, Ohm HW, Molnar SJ, Scoles GJ, Eckstein PE, Bonman JM, Ceplitis A, Langdon T (2009) New DArT markers for oat provide enhanced map coverage and global germplasm characterization. BMC Genomics 10:39
Tostain S (1992) Enzyme diversity in pearl millet (Pennisetum glaucum L.) 3. Wild millet. Theor Appl Genet 83:733–742
Tostain S, Riandley MF, Marchais L (1987) Enzyme diversity in pearl millet (Pennisetum glaucum). 1. West Africa. Theor Appl Genet 74:188–193
Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol Biol 48:697–712
Valluru R, Vadez V, Hash CT, Karanam P (2010) A minute phosphorus application contributes to a better establishment of pearl millet (Pennisetum glaucum (L.) R.Br.) seedling in phosphorus deficient soils. Soil Use Manag 26:36–43
VDLUFA (2011) Umweltanalytik. VDLUFA-Verlag, Darmstadt
Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD et al (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217
Vigouroux Y, Mitchell S, Matsuoka Y, Hamblin M, Kresovich S, Smith JS, Jaqueth J, Smith OS, Doebley J (2005) An analysis of genetic diversity across the maize genome using microsatellites. Genetics 169:1617–1630
Weir CC (1972) Phosphate studies on the Jamaican bauxite soils. Trop Agric (Trinidad) 49:89–96
Weir CC (1977) Phosphate fixation in Jamaican latosolic soils. Soil Sci Soc Am Proc 30:653–655
Wenzl P, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity arrays technology (DArT) for whole genome profiling of barley. Proc Natl Acad Sci USA 101(26):9915–9920
Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777–783
Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor Appl Genet 105:890–897
Xia L, Peng K, Yang S, Wenzl P, Carmen de Vicente M, Fregene M, Kilian A (2005) DArT for high-throughput genotyping of cassava (Manihot esculenta) and its wild relatives. Theor Appl Genet 110:1092–1098
Yadav RS, Hash CT, Bidinger FR, Cavan GP, Howarth CJ (2002) Quantitative trait loci associated with traits determining grain and stover yield in pearl millet under terminal drought-stress conditions. Theor Appl Genet 104(1):67–83
Yadav RS, Bidinger FR, Hash CT, Yadav YP, Yadav OP, Bhatnagar SK, Howarth CJ (2003) Mapping and characterisation of QTL × E interactions for traits determining grain and stover yield in pearl millet. Theor Appl Genet 106(3):512–520
Yadav RS, Hash CT, Bidinger FR, Devos KM, Howarth CJ (2004) Genomic regions associated with grain yield and aspects of post-flowering drought tolerance in pearl millet across stress environments and tester background. Euphytica 136:265–277
Yadav R, Sehgal D, Vadez V (2011) Using genetic mapping and genomics approaches in understanding and improving drought tolerance in pearl millet. J Exp Bot 62:397–408
Yan W, Kang MS (2002) GGE biplot analysis: a graphical tool for breeders, geneticists, and agronomists, 1st edn. CRC Press, Boca Raton
Yan X, Liao L, Trull MC, Beebe SE, Lynch JP (2001) Induction of a major leaf acid phosphatase does not confer adaptation to low phosphorus availability in common bean. Plant Physiol 125:1901–1911
Yang S, Pang W, Harper J, Carling J, Wenzl P, Huttner E, Zong X, Kilian A (2006) Low level of genetic diversity in cultivated pigeon pea compared to its wild relatives is revealed by diversity arrays technology. Theor Appl Genet 113:585–595
Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zaongo CGL, Hossner LR, Wendt CW (1994) Root distribution, water use and nutrient uptake of millet and grain sorghum on West African soils. Soil Sci 157:379–388
Zhang D, Cheng H, Geng L, Kan G, Cui S, Meng Q, Gai J, Yu D (2009) Detection of quantitative trait loci for phosphorus deficiency tolerance at soybean seedling stage. Euphytica 167:313–322
Zhang L, Liu D, Guo X, Yang W, Sun J, DaoWen Wang D, Sourdille P, AiMin Zhang A (2011) Investigation of genetic diversity and population structure of common wheat cultivars in northern China using DArT markers. BMC Genetics 12:42. http://www.biomedcentral.com/1471-2156/12/42
Zhang H, Uddin MS, Zou C, Xie C, Xu Y, Li WX (2014) Meta analysis and candidate gene mining of low phosphorus tolerance in maize. J Integr Plant Biol 56:262–270. doi:10.1111/jipb.12168
Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C et al (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:71–82
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20. doi:10.3835/plantgenome2008.02.0089
Acknowledgments
The financial support from the German Federal Ministry for Economic Cooperation and Development (BMZ) through the BMZ-Abiotic Stress project (GIZ Project Number 09.7860.1-001.00) based at ICRISAT West Africa-Niamey, from Foundation ‘Fiat Panis’ through the Food Security Centre at University of Hohenheim to DC Gemenet and from the McKnight Foundation Collaborative Crop Research Program to BIG Haussmann is gratefully appreciated. We thank Mr. Hamadou Adamou, Mr. Ada Abarchi and Mr. Issa Karimou (all at ISC-Sadoré) for preparing and coordinating the field trials within the region. Our sincere appreciation is extended to the technical staff at collaborating NARs in Burkina Faso, Mali and Senegal for conducting trials in their respective countries. The publication is an output of a scholarship from the Food Security Centre from the University of Hohenheim, which is part of the DAAD (German Academic Exchange Service) program ‘exceed’ and is supported by DAAD and BMZ. The work was finalized as part of the CGIAR Research Program on Dryland Cereals.
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Gemenet, D.C., Leiser, W.L., Zangre, R.G. et al. Association analysis of low-phosphorus tolerance in West African pearl millet using DArT markers. Mol Breeding 35, 171 (2015). https://doi.org/10.1007/s11032-015-0361-y
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DOI: https://doi.org/10.1007/s11032-015-0361-y