Skip to main content
SpringerLink
Log in

Molecular tagging and validation of microsatellite markers linked to the low germination stimulant gene (lgs) for Striga resistance in sorghum [Sorghum bicolor (L.) Moench]

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Striga is a devastating parasitic weed in Africa and parts of Asia. Low Striga germination stimulant activity, a well-known resistance mechanism in sorghum, is controlled by a single recessive gene (lgs). Molecular markers linked to the lgs gene can accelerate development of Striga-resistant cultivars. Using a high density linkage map constructed with 367 markers (DArT and SSRs) and an in vitro assay for germination stimulant activity towards Striga asiatica in 354 recombinant inbred lines derived from SRN39 (low stimulant) × Shanqui Red (high stimulant), we precisely tagged and mapped the lgs gene on SBI-05 between two tightly linked microsatellite markers SB3344 and SB3352 at a distance of 0.5 and 1.5 cM, respectively. The fine-mapped lgs region was delimited to a 5.8 cM interval with the closest three markers SB3344, SB3346 and SB3343 positioned at 0.5, 0.7 and 0.9 cM, respectively. We validated tightly linked markers in a set of 23 diverse sorghum accessions, most of which were known to be Striga resistant, by genotyping and phenotyping for germination stimulant activity towards both S. asiatica and S. hermonthica. The markers co-segregated with Striga germination stimulant activity in 21 of the 23 tested lines. The lgs locus similarly affected germination stimulant activity for both Striga species. The identified markers would be useful in marker-assisted selection for introgressing this trait into susceptible sorghum cultivars. Examination of the sorghum genome sequence and comparative analysis with the rice genome suggests some candidate genes in the fine-mapped region (400 kb) that may affect strigolactone biosynthesis or exudation. This work should form a foundation for map-based cloning of the lgs gene and aid in elucidation of an exact mechanism for resistance based on low Striga germination stimulant activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  PubMed  CAS  Google Scholar 

  • Amusan I, Rich P, Housley T, Ejeta G (2011) An in vitro method for identifying post-attachment Striga resistance in maize and sorghum. Agron J 103:1472–1478

    Article  Google Scholar 

  • Awad A, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K (2006) Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche, produced by maize, millet and sorghum. Plant Growth Regul 48:221–227

    CAS  Google Scholar 

  • Bhattramakki D, Dong J, Chabra AK, Hart GE (2000) An integrated SSR and RFLP linkage map of Sorghum bicolor (L.) Moench. Genome 43:988–1002

    PubMed  CAS  Google Scholar 

  • Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a Cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449

    Article  PubMed  CAS  Google Scholar 

  • Cook CE, Whichard LP, Wall ME, Egley GH, Coggan P, Luhan PA, McPhail AT (1972) Germination stimulants II. The structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–6199

    Article  CAS  Google Scholar 

  • Cook D, Rimando AM, Clemente TE, Schroder J, Dayan FE, Nanayakkara NPD, Pan Z, Noonan BP, Fishbein M, Abe I, Duke SO, Baerson SR (2010) Alkylresorcinol synthases expressed in Sorghum bicolor root hairs play an essential role in the biosynthesis of the allelopathic benzoquinone sorgoleone. Plant Cell 22:867–887

    Article  PubMed  CAS  Google Scholar 

  • Ejeta G (2007a) The Striga scourge in Africa: a growing pandemic. In: Ejeta G, Gressel J (eds) Integrating new technologies for Striga control: towards ending the witch-hunt. World Scientific Publishing Company PTE LTD, Singapore, pp 3–16

    Chapter  Google Scholar 

  • Ejeta G (2007b) Breeding for Striga resistance in sorghum: exploitation of an intricate host-parasite biology. Crop Sci 47(S3):S216–S227

    Google Scholar 

  • Ejeta G, Butler LG (1993) Host plant resistance to Striga. In: Buxton DR, Shilbes R, Forsburg RA, Blad BL, Asay KH, Paulsen GM, Wilson RF (eds) International crop science I, vol 1. Crop Science Society of America, Madison, pp 561–569

    Google Scholar 

  • Erickson J, Schott D, Reverri T, Muhsin W, Ruttledge T (2001) GC–MS analysis of hydrophobic root exudates of Sorghum and implications on the parasitic plant Striga asiatica. J Agric Food Chem 49:5537–5542

    Article  PubMed  CAS  Google Scholar 

  • Frost DL, Gurney AL, Press MC, Scholes JD (1997) Striga hermonthica reduces photosynthesis in sorghum: the importance of stomatal limitations and a potential role for ABA. Plant Cell Env 20:492–4873

    Article  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  PubMed  CAS  Google Scholar 

  • Graves JD, Wylde A, Press MC, Stewart GR (1990) Growth and carbon allocation in Pennisetum typhoides infected with the parasitic angiosperm Striga hermonthica. Plant Cell Env 13:367–373

    Article  CAS  Google Scholar 

  • Grenier C, Rich PJ, Mohamed A, Ellicott A, Shaner C, Ejeta G (2001) Independent inheritance of lgs and IR genes in sorghum. In: 7th international parasitic weed symposium. Nantes, France, pp 220–223

    Google Scholar 

  • Hauck C, Muller S, Schilknecht H (1992) A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. J Plant Physiol 139:474–478

    Article  CAS  Google Scholar 

  • Haussmann BIG, Hess DE, Omanya GO, Reddy BVS, Welz HG, Geiger HH (2001) Major and minor genes for stimulation of Striga hermonthica seed germination in sorghum, and interaction with different Striga populations. Crop Sci 41:1507–1512

    Article  Google Scholar 

  • Haussmann BIG, Hess DE, Omanya GO, Folkertsma RT, Reddy BV, Kayentao M, Welz HG, Geiger HH (2004) Genomic regions influencing resistance to the parasitic weed Striga hermonthica in two recombinant inbred populations of sorghum. Theor Appl Genet 109:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Hess DE, Ejeta G (1992) Inheritance of resistance to Striga in sorghum genotype SRN39. Plant Breed 109:233–241

    Article  Google Scholar 

  • Hess DE, Ejeta G, Butler LG (1992) Selecting sorghum genotypes expressing a quantitative biosynthetic trait that confers resistance to Striga. Phytochem 31:493–497

    Article  CAS  Google Scholar 

  • Ibrahim YH (1999) A sorghum linkage map and predicted response to phenotypic and markers selection for resistance to Striga in sorghum. Dissertation, Purdue University

  • Joel DM, Hershenhorn J, Eizenberg H, Aly R, Ejeta G, Rich PJ, Ransom JK, Sauerborn J, Rubiales D (2007) Biology and management of weedy root parasites. In: Janick J (ed) Horticultural reviews. John Wiley & Sons, Inc., New York, pp 267–349

    Chapter  Google Scholar 

  • Kaewchumnong K, Price AH (2008) A study on the susceptibility of rice cultivars to Striga hermonthica and mapping of Striga tolerance quantitative trait loci in rice. New Phytol 180:206–216

    Article  PubMed  Google Scholar 

  • Kim JS, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005) Chromosome identification and nomenclature of Sorghum bicolor. Genetics 169:1169–1173

    Article  PubMed  CAS  Google Scholar 

  • Knoll J, Gunaratna N, Ejeta G (2008) QTL analysis of early-season cold tolerance in sorghum. Theor Appl Genet 116:577–587

    Article  PubMed  Google Scholar 

  • Li Q, Yang X, Bai G, Warburton ML, Mahuku G, Gore M, Dai J, Li J, Yan J (2010) Cloning and characterization of a putative GS3 ortholog involved in maize kernel development. Theor Appl Genet 120:753–763

    Article  PubMed  CAS  Google Scholar 

  • Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wanga Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice Tiller bud outgrowth. Plant Cell 21:1512–1525

    Article  PubMed  CAS  Google Scholar 

  • Mangombe N, Mabasa S, Obilana AT (2000) Breeding sorghum for Striga resistance in Zimbabwe. In: Haussmann BIG, Hess DE, Koyama ML, Grivet L, Rattunde HFW, Geiger HH (eds) Breeding for Striga resistance in cereals. Margraf, Ibadan, p 335

    Google Scholar 

  • Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    Article  PubMed  CAS  Google Scholar 

  • Mbwaga AM, Riches C, Ejeta G (2007) Integrated Striga management to meet sorghum demand in Tanzania. In: Ejeta G, Gressel J (eds) Integrating new technologies for Striga control: towards ending the witch-hunt. World Scientific Publishing Company PTE LTD, Singapore, pp 253–264

    Chapter  Google Scholar 

  • Michelmore RW, Paran I, Kessel RV (1991) Identification of markers linked to disease resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genome regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed  CAS  Google Scholar 

  • Mimmo T, Marzadori C, Gessa C (2009) Does the degree of pectin esterification influence aluminium sorption by the root apoplast? Plant and Soil. Springer, Netherlands, pp 159–168

    Google Scholar 

  • Mohamed KI, Musselman LJ, Riches CR (2001) The genus Striga (Scrophulariaceae) in Africa. Ann Missouri Bot Garden 88:60–103

    Article  Google Scholar 

  • Mutengwa CS, Tongoona PB, Sithole-Niang I (2005) Genetic studies and a search for molecular markers that are linked to Striga asiatica resistance in sorghum. Afr J Biotech 4:1355–1361

    CAS  Google Scholar 

  • Netzly DH, Riopel JL, Ejeta G, Butler LG (1988) Germination stimulants of witchweed (Striga asiatica) from hydrophobic root exudate of sorghum (Sorghum bicolor). Weed Sci 36:441–446

    CAS  Google Scholar 

  • Nimbal CI, Pedersen JF, Yerkes CN, Weston LA, Weller SC (1996) Phytotoxicity and distribuition of sorgoleone in grain sorghum. J Agric Food Chem 44:1343–1347

    Article  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  PubMed  CAS  Google Scholar 

  • Price AH (2006) Believe it or not, QTLs are accurate. Trends Plant Sci 11:213–216

    Article  PubMed  CAS  Google Scholar 

  • Ramaiah KV (1987) Breeding cereal grains for resistance to witchweed. In: Musselman LJ (ed) Parasitic weeds in agriculture, vol 1. CRC Press, Boca Raton, pp 227–242

    Google Scholar 

  • Ramaiah KV, Chidley VL, House LR (1990) Inheritance of Striga seed germination stimulant in sorghum. Euphytica 45:33–38

    Google Scholar 

  • Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46:617–626

    Article  PubMed  CAS  Google Scholar 

  • Rich PJ, Grenier C, Ejeta G (2004) Striga resistance in wild relatives of sorghum. Crop Sci 44:2221–2229

    Article  Google Scholar 

  • Rodenburg J, Bastiaans L, Kropff MJ, Van Ast A (2006) Effects of host plant genotype and seedbank density on Striga reproduction. Weed Res 46:251–263

    Article  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgenen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    Article  PubMed  CAS  Google Scholar 

  • Satish K, Srinivas G, Madhusudhana R, Padmaja PG, Nagaraja Reddy R, Murali Mohan S, Seetharama N (2009) Identification of quantitative trait loci for resistance to shoot fly in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 119(8):1425–1439

    Article  PubMed  CAS  Google Scholar 

  • Sauerborn J (1991) The economic importance of the phytoparasites Orobanche and Striga. In: 5th international symposium on parasitic weeds. Nairobi, Kenya, pp 137–143

    Google Scholar 

  • Saxton AM (1998) A macro for converting mean separation output to letter groupings in Proc Mixed. In: Proceedings of the 23rd SAS users group international. SAS Institute, Cary, pp 1243–1246

    Google Scholar 

  • Scholes JD, Press MC (2008) Striga infestation of cereal crops—an unsolved problem in resource limited agriculture. Curr Opin Plant Biol 11:180–186

    Article  PubMed  Google Scholar 

  • Siame BA, Weerasuriya Y, Wood K, Ejeta G, Buttler LG (1993) Isolation of strigol, a germination stimulant for Striga asiatica, from host plants. J Agric Food Chem 41:1486–1491

    Article  CAS  Google Scholar 

  • Swarbrick PJ, Huang K, Liu G, Slate J, Press MC, Scholes JD (2008) Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. New Phytol 179(2):515–529

    Article  PubMed  CAS  Google Scholar 

  • Swarbrick PJ, Scholes JD, Press MC, Slate J (2009) A major QTL for resistance of rice to the parasitic plant Striga hermonthica is not dependent on genetic background. Pest Manag Sci 65:528–532

    Article  PubMed  CAS  Google Scholar 

  • Tesso T, Deressa A, Gutema Z, Ejeta G (2007) An integrated Striga management (ISM) option offers effective control of Striga in Ethiopia. In: Ejeta G, Gressel J (eds) Integrating new technologies for Striga control: Towards ending the witch-hunt. World Scientific Publishing Company PTE LTD, Singapore, pp 199–212

    Chapter  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:U129–U195

    Article  Google Scholar 

  • Van Ooijen JW (2005) Map-QTL® 5: software for the mapping quantitative trait loci in mapping populations. Kyazma BV, Wageningen

    Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0® software for the calculation of genetic linkage maps. Plant Research International, Wageningen

    Google Scholar 

  • Vasudeva Rao MJ (1985) Techniques for screening sorghums for resistance to Striga. In: Musselman LJ (ed) Parasitic weeds in agriculture. CRC Press, Inc., Boca Raton, pp 281–304

    Google Scholar 

  • Vogler RK, Ejeta G, Butler LG (1996) Inheritance of low production of Striga germination stimulant in sorghum. Crop Sci 36:1185–1191

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTL. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Vu GTH, Wicker T, Buchmann JP, Chandler PM, Matsumoto T, Graner A, Stein N (2010) Fine mapping and syntenic integration of the semi-dwarfing gene sdw3 of barley. Funct Integr Genomics 10:509–521

    Article  PubMed  CAS  Google Scholar 

  • Weber WE, Wrickle G (1994) Genetic markers in plants breeding. Adv Plant Breed, Parey Scientific Publ., Berlin No. 16

    Google Scholar 

  • Williams CN (1959) Resistance of Sorghum to witchweed. Nature 184:1511–1512

    Article  Google Scholar 

  • Xie X, Yoneyama K, Kusumoto D, Yamada Y, Takeuchi Y, Sugimoto Y, Yoneyama K (2008) Sorgomol, germination stimulant for root parasitic plants, produced by Sorghum bicolor. Tetrahedron Lett 49:2066–2068

    Article  CAS  Google Scholar 

  • Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117

    Article  PubMed  CAS  Google Scholar 

  • Xin Z, Velten JP, Oliver MJ, Burke JJ (2003) High-throughput DNA extraction method suitable for PCR. BioTechniques 34:820–826

    PubMed  CAS  Google Scholar 

  • Yoder JI, Scholes JD (2010) Host plant resistance to parasitic weeds; recent progress and bottlenecks. Curr Opin Plant Biol 13:478–484

    Article  PubMed  CAS  Google Scholar 

  • Yonemaru J, Ando T, Mizubayashi T, Kasuga S, Matsumoto T, Yano M (2009) Development of genome-wide simple sequence repeat markers using whole-genome shotgun sequences of sorghum (Sorghum bicolor (L.) Moench). DNA Res 16:187–193

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama K, Awad AA, Xie X, Yoneyama K, Takeuchi Y (2010) Strigolactones as germination stimulants for root parasitic plants. Plant Cell Physiol 51:1095–1103

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge financial support from the United States Agency for International Development (USAID) INTSORMIL grant #EPP-A-0006-00016-00.

Author information

Authors and Affiliations

  1. Department of Agronomy, Purdue University, 915 W State Street, West Lafayette, IN, 47907-2054, USA

    Kanuganti Satish, Zenbaba Gutema, Cécile Grenier, Patrick J. Rich & Gebisa Ejeta

Authors
  1. Kanuganti Satish
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zenbaba Gutema
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cécile Grenier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrick J. Rich
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gebisa Ejeta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gebisa Ejeta.

Additional information

Communicated by A. Paterson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Satish, K., Gutema, Z., Grenier, C. et al. Molecular tagging and validation of microsatellite markers linked to the low germination stimulant gene (lgs) for Striga resistance in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 124, 989–1003 (2012). https://doi.org/10.1007/s00122-011-1763-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-011-1763-9

Keywords

Search

Navigation