Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T14:47:25.518Z Has data issue: false hasContentIssue false
  • English
  • Français

Host Resistance and Parasite Virulence in Striga–Host Plant Interactions: A Shifting Balance of Power

Published online by Cambridge University Press:  20 January 2017

Michael P. Timko ,
Kan Huang  and
Karolina E. Lis
Michael P. Timko*
Affiliation:
Department of Biology, University of Virginia, Charlottesville, VA 22903
Kan Huang
Affiliation:
Department of Biology, University of Virginia, Charlottesville, VA 22903
Karolina E. Lis
Affiliation:
Department of Biology, University of Virginia, Charlottesville, VA 22903
*
Corresponding author's E-mail: mpt9g@virginia.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The witchweeds, members of the genus Striga, are noxious and persistent pests in farmers' fields and serious constraints to crop productivity throughout Africa, India, and Southeast Asia. Among the primary hosts for Striga are the major cereals (maize, sorghum, rice, and millet) and grain legumes (cowpea) that are important food staples worldwide. The negative impact of parasitic plants on crop productivity increases globally each year, and their potential for affecting domestic agriculture looms larger as the movement of seed resources expands on a global scale. At the present time there is a limited understanding of how Striga and other parasitic plants select a suitable host and overcome the innate defense responses of the host in order to complete their life-cycle. In the grasses most reported resistance to Striga appears to be polygenic with a large genotype by environment interaction. In contrast, resistance to S. gesnerioides in cowpea is conferred by single dominant genes functioning in a race-specific manner suggesting that a gene-for-gene mechanism similar to effector-triggered immunity (ETI) described in other host–pathogen interactions is likely operating in these parasite-host associations. A hallmark of ETI is the direct or indirect recognition of parasite-derived avirulence (Avr) factors and other effectors that interfere with plant innate immunity by host sensors (or R proteins) leading to activation of defense responses. The recent cloning and functional characterization of a race-specific R gene from cowpea encoding a canonical coiled-coil (CC)-nucleotide binding site (NBS)-leucine-rich repeat (LRR) type R-protein opens the door for further exploration of the mechanism of host resistance and provides a focal point for studies aimed at uncovering the molecular and genetic factors underlying parasite virulence and host selection. The potential for the development of novel strategies for parasite control and eradication based on parasite virulence factors is discussed.

Keywords

Cowpea, Vigna unguiculata L. WalpersCowpea witchweedStriga gesnerioides (Willd.) Vatke STGE2purple witchweedStriga hermonthica, (Del.) Benth. STRfinger millet, Eleusine coracana Lmaize, Zea mays Lpearl millet, Pennisetum glaucum (L.) R. Brrice, Oryza sativa Lsorghum, Sorghum bicolor (L.) Moenchavirulenceeffectorimmunityparasitewitchweed
Type
Symposium
Information
Weed Science , Volume 60 , Issue 2 , June 2012 , pp. 307 - 315
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abramovitch, R. B., Anderson, J. C., and Martin, G. B. 2006. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Bio. 7:601–611.CrossRefGoogle ScholarPubMed
Aggarwal, V. D., Haley, S. D., and Broockman, F. E. 1986. Present status of breeding cowpea for resistance to Striga at IITA. Pages 176–180 in ter Borg, S. J., ed. Proceedings of a Workshop on Biology and Control of Orobanche . Wageningen, the Netherlands LH/VPO.Google Scholar
Aggarwal, V. D., Muleba, N., Drabo, I., Souma, J., and Mbewe, M. 1984. Inheritance of Striga gesnerioides resistance in cowpea. Pages 143–147 in Parker, C., Musselman, L. J., Polhill, R. M., and Wilson, A. K., eds. Proceedings of the Third International Symposium on Parasitic Weeds, Aleppo, Syria 7–11 May 1984. Aleppo, Syria ICARDA-IPSPRG.Google Scholar
Aly, R., Cholakh, H., Joel, D. M., Leibman, D., Steinitz, B., Zelcer, A., Naglis, A., Yarden, O., and Gal-On, A. 2009. Gene silencing of mannose 6-phosphate reductase in the parasitic weed Orobanche aegyptiaca through the production of homologous dsRNA sequences in the host plant. Plant Biotechnol. J. 7:487–498.CrossRefGoogle ScholarPubMed
Amusan, I. O., Rich, P. J., Menkir, A., Housley, T., and Ejeta, G. 2008. Resistance to Striga hermonthica in a maize inbred line derived from Zea diploperennis . New Phytol. 178:157–166.CrossRefGoogle Scholar
Atokple, I. D. K., Singh, B. B., and Emechebe, A. M. 1995. Genetics of resistance to Striga and Alectra in cowpea. J. Hered. 86:45–49.Google Scholar
Baxter, L., Tripathy, S., Ishaque, N., et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science. 330:1549–1551.Google Scholar
Bent, A. F. and Mackey, D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399–436.Google Scholar
Boller, T. and Felix, G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406.Google Scholar
Boller, T. and He, S -Y. 2009. Innate immunity in plants: an arms race between pattern recognition receptors and effectors in microbial pathogens. Science. 324:742–744.Google Scholar
Botanga, C. J. and Timko, M. P. 2005. Genetic structure and analysis of host and nonhost interactions of Striga gesnerioides (Witchweed) from Central Florida. Phytopathology. 95:1166–1173.Google Scholar
Botanga, C. J. and Timko, M. P. 2006. Phenetic relationships among different races of Striga gesnerioides (Willd.) Vatke from West Africa. Genome. 49:1351–1365.CrossRefGoogle ScholarPubMed
Bowen, J. K., Mesarich, C. H., Rees-George, J., Cui, W., Fitzgerald, A., Win, J., Plummer, K. M., and Templeton, M. D. 2009. Candidate effector gene identification in the ascomycete fungal phytopathogen Venturia inaequalis by expressed sequence tag analysis. Molec. Plant Pathol. 10:431–448.Google Scholar
Cameron, D. C., Coats, A. M., and Seel, W. E. 2006. Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor . Ann. Bot.-London. 98:1289–1299.Google Scholar
Caplan, J., Padmanabhan, M., and Dinesh-Kumar, S. P. 2008. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe. 3:126–135.CrossRefGoogle ScholarPubMed
Chandrasekharan, S. N. and Parthasarathy, S. V., eds. 1953. Cytogenetics and Plant Breeding. Madras, India P Varadchary and Co. 589 p.Google Scholar
Cramer, R. A., La Rota, C. M., Cho, Y., Thon, M., Craven, K. D., Knudson, D. L., Mitchell, T. L., and Lawrence, C. B. 2006. Bioinformatic analysis of expressed sequence tags derived from a compatible Alternaria brassicicola–Brassica oleracea interaction. Mol. Plant Pathol. 7:113–124.Google Scholar
de Framond, A., Rich, P. J., McMillan, J., and Ejeta, G. 2007. Effects of Striga parasitism of transgenic maize armed with RNAi constructs targeting essential S. asiatica genes. Pages 185–196 in Ejeta, G. and Gressel, J., eds. Integrating New Technologies for Striga Control, Towards Ending the Witch-hunt. Singapore World Scientific Publishing.CrossRefGoogle Scholar
de Wit, P. J. and Stergiopoulos, I. 2009. Fungal effector proteins. Annu. Rev. Phytopathol. 47:233–263.Google Scholar
Ejeta, G. 2007. Breeding for Striga resistance in sorghum: exploitation of an intricate host–parasite biology. Crop Sci. 47:S216–S227.CrossRefGoogle Scholar
Ellis, J. G., Dodds, P. N., and Lawrence, G. J. 2007. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu. Rev. Phytopathol. 45:289–306.Google Scholar
Ellis, J. G., Rafiqi, M., Gan, P., Chakrabarti, A., and Dodds, P. N. 2009. Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Curr. Opin. Plant Biol. 12:399–405.Google Scholar
Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–296.CrossRefGoogle Scholar
Göhre, V. and Robatzek, S. 2008. Breaking the barriers: microbial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46:189–215.Google Scholar
Gowda, B. S., Riopel, J. L., and Timko, M. P. 1999. NRS1: a resistance gene homolog expressed in roots of nonhost plants following parasitism by Striga asiatica (witchweed). Plant J. 20:217–230.Google Scholar
Greenshield, D. L. and Jones, J. D. G. 2008. Plant pathogen effectors: getting mixed messages. Curr. Biol. 18:R128–R130.Google Scholar
Grenier, C., Ibrahim, Y., Haussmann, B. I. G., Kiambi, D., and Ejeta, G. 2007. Marker-assisted selection for Striga resistance in sorghum. Pages 159–172 in Ejeta, G. and Gressel, J., eds. Integrating New Technologies for Striga Control, Towards Ending the Witch-hunt. Singapore World Scientific Publishing.CrossRefGoogle Scholar
Gurney, A. L., Grimanelli, D., Kanampiu, F., Hoisington, D., Scholes, J. D., and Press, M. C. 2003. Novel sources of resistance to Striga hermonthica in Tripsacum dactyloides, a wild relative of maize. New Phytol. 160:557–568.Google Scholar
Gurney, A. L., Slate, J., Press, M. C., and Scholes, J. D. 2006. A novel form of resistance in rice to the angiosperm parasite Striga hermonthica . New Phytol. 169:199–208.Google Scholar
Haussmann, B. I. G., Hess, D. E., Omanya, G. O., Folkertsma, R. T., Reddy, B. V. S., Kayentao, M., Welz, H. G., and Geiger, H. H. 2004. Genomic regions influencing resistance to the parasitic weed Striga hermonthica in two recombinant inbred populations of sorghum. Theor. Appl. Genet. 109:1005–1016.Google Scholar
Haussmann, B. I. G., Hess, D. E., Omanya, O., Reddy, B. V. S., Welz, H. G., and Geiger, H. H. 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.CrossRefGoogle Scholar
Hearne, S. J. 2009. Control: the Striga conundrum. Pest Manag. Sci. 65:603–614.CrossRefGoogle ScholarPubMed
Hiraoka, Y. and Sugimoto, Y. 2008. Molecular responses of sorghum to purple witchweed (Striga hermonthica) parasitism. Weed Sci. 56:356–363.CrossRefGoogle Scholar
Hiraoka, Y., Ueda, H., and Sugimoto, Y. 2009. Molecular responses of Lotus japonicus to parasitism by the compatible species Orobanche aegyptiaca and the incompatible species Striga hermonthica . J. Exp. Bot. 60:641–650.Google Scholar
Hood, M. E., Condon, J. M., Timko, M. P., and Riopel, J. L. 1998. Primary haustorial development of Striga asiatica on host and nonhost species. Phytopathology. 88:70–75.Google Scholar
Jones, J. D. G. and Dangl, J. L. 2006. The plant immune system. Nature. 444:323–329.Google Scholar
Kuijt, J. 1969. The Biology of Parasitic Flowering Plants. Berkeley, CA University of California Press. 246 p.Google Scholar
Kusumoto, D., Goldwasser, Y., Xie, X., Yoneyama, K., and Takeuchi, Y. 2007. Resistance of red clover (Trifolium pratense) to the root parasitic plant Orobanche minor is activated by salicylate but not by jasmonate. Ann. Bot. 100:537–544.Google Scholar
Lane, J. A., Bailey, J. A., Butler, R. C., and Terry, P. J. 1993. Resistance of cowpea [Vigna unguiculata (L.) Walp.] to Striga gesnerioides (Willd.) Vatke, a parasitic angiosperm. New Phytol. 125:405–412.Google Scholar
Lane, J. A., Child, D. V., Reiss, G. C., Entcheva, V., and Bailey, J. A. 1997a. Crop resistance to parasitic plants. Pages 81–97 in Crute, I. R., Holub, E. B., and Burton, J. J., eds. The Gene-for-Gene Relationship in Plant-Parasite Interactions. Wallingford, Oxon, UK CAB International.Google Scholar
Lane, J. A., Moore, T. H. M., Child, D. V., and Bailey, J. A. 1997b. Variation in virulence of Striga gesnerioides on cowpea: new sources of resistance. Pages 225–230 in Singh, B. B., Mohan Raj, D. R., Dashiell, K. E., and Jakai, L. E. N., eds. Advances in Cowpea Research. Co-publication of International Institute of Tropical Agriculture (IITA) and Japan International Research Center for Agricultural Sciences (JIRCAS). Ibadan, Nigeria IITA Press.Google Scholar
Lane, J. A., Moore, T. H. M., Child, D. V., and Cardwell, K. F. 1996. Characterization of virulence and geographic distribution of Striga gesnerioides on cowpea in West Africa. Plant Dis. 80:299–301.Google Scholar
Lane, J. A., Moore, T. H. M., Child, D. V., Cardwell, K. F., Singh, B. B., and Bailey, J. A. 1994. Virulence characteristics of a new race of the parasitic angiosperm Striga gesnerioides from southern Benin on cowpea (Vigna unguiculata). Euphytica. 72:183–188.Google Scholar
Li, J., Lis, K. E., and Timko, M. P. 2009. Molecular genetics of race-specific resistance of cowpea to Striga gesnerioides (Willd.). Pest Manag. Sci. 65:520–527.CrossRefGoogle ScholarPubMed
Li, J. and Timko, M. P. 2009. Gene-for-gene resistance in Striga-cowpea associations. Science. 325:1094.CrossRefGoogle ScholarPubMed
Maiti, R. K., Ramaiah, K. V., Bisen, S. S., and Chidley, V. L. 1984. A comparative study of the haustorial development of Striga asiatica (L.) Kuntze on sorghum cultivars. Ann. Bot. Fenn. 54:447–457.Google Scholar
McDowell, J. M. and Simon, S. A. 2008. Molecular diversity at the plant-pathogen interface. Dev. Comp. Immunol. 32:736–744.Google Scholar
Mohamed, A., Ellicott, A., Housley, T. L., and Ejeta, G. 2003. Hypersensitive response to Striga infection in sorghum. Crop Sci. 43:1320–1324.Google Scholar
Mohamed, A. H., Housley, T. L., and Ejeta, G. 2010. Inheritance of hypersensitive response to Striga parasitism in sorghum [Sorghum bicolor (L.) Moench]. Afr. J. Agric. Res. 19:2720–2729.Google Scholar
Mohamed, K. I., Musselman, L. J., and Riches, C. R. 2001. The genus Striga (Scrophulariaceae) in Africa. Ann. Mo. Bot. Gard. 88:60–103.Google Scholar
Mur, L., Kenton, P., Atzorn, R., Miersch, O., and Wasternack, C. 2006. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140:249–262.Google Scholar
Nabayaogo, P. 1984. Heritabilite de quelques characters chez le sorgho. Memoir presente en vue de l'obtention du Diplome d'Ingenieur des Techniques du Developpement Rural. University de Ouagafougou, Institut Superieur Polytechnique, Burkina Faso.Google Scholar
Narasimhamurty, B. L. and Sivaramakrishnaiah, M. 1963. Modern trends of agricultural research with reference to Striga resistant sorghum types for maximum food production. Andhra Agric. J. 10:6–11.Google Scholar
Oliva, R., Win, J., Raffaele, S., et al. 2010. Recent developments in effector biology of filamentous plant pathogens. Cell. MicroBiol. 12:705–715.CrossRefGoogle ScholarPubMed
Olivier, A., Benhamou, N., and Leroux, G. D. 1991a. Cell surface interactions between sorghum roots and the parasitic weed Striga hermonthica: cytochemical aspects of cellulose distribution in resistant and susceptible host tissues. Can. J. Bot. 69:1679–1690.Google Scholar
Olivier, A., Ramaiah, K. V., and Leroux, G. D. 1991b. Selection of sorghum (Sorghum bicolor Moench) varieties resistant to the parasitic weed Striga hermonthica (Del) Benth. Weed Res. 31:219–225.Google Scholar
Ouédraogo, J. T., Gowda, B. S., Jean, M., et al. 2002b. An improved genetic linkage map for cowpea (Vigna unguiculata L.) combining AFLP, RFLP, RAPD and biochemical markers and biological resistance traits. Genome. 45:175–188.Google Scholar
Ouédraogo, J. T., Maheshwari, V., Berner, D. K., St-Pierre, C-A., Belzile, F., and Timko, M. P. 2001. Identification of AFLP markers linked to resistance of cowpea (Vigna unguiculata L.) to parasitism by Striga gesnerioides . Theor. Appl. Genet. 102:1029–1036.Google Scholar
Ouédraogo, J. T., Olivier, A., Timko, M. P., and Belzile, F. J. 2002a. AFLP markers for resistance against Striga gesnerioides race 1 in cowpea (Vigna unguiculata). Genome. 45:787–793.Google Scholar
Parker, C. and Polniaszek, T. I. 1990. Parasitism of cowpea by Striga gesnerioides: variation in virulence and discovery of a new source of host resistance. Ann. Appl. Biol. 116:305–311.CrossRefGoogle Scholar
Parker, C. and Riches, C. R. 1993. Parasitic Weeds of the World. Biology and Control. Wallingford, UK CAB International. 332 p.Google Scholar
Parker, C. J. 2009. Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag. Sci. 65:453–459.Google Scholar
Pérez-de-Luque, A., Moreno, M. T., and Rubiales, D. 2008. Host plant resistance against broomrapes (Orobanche spp.): defence reactions and mechanisms of resistance. Ann. Appl. Biol. 152:131–141.Google Scholar
Press, M. C. and Graves, J. D., editors. 1995. Parasitic Plants. London Chapman & Hall. 292 p.Google Scholar
Raffaele, S., Farrer, R. A., Cano, L. M., et al. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science. 330:1540–1543.Google Scholar
Ramaiah, K. V. 1984. Patterns of Striga resistance in sorghums and millets with special emphasis on Africa. Pages 71–92 in Striga Biology and Control, Proceedings of the Workshop on the Biology and Control of Striga, 14–17 November 1983. Dakar, Senegal ICSU Press/IDCR.Google Scholar
Ramaiah, K. V. 1987. Control of Striga and Orobanche species: a review. Pages 637–664 in Chr. Weber, H. and Forstreuter, W., eds. Parasitic Flowering Plants, Proceedings of the 4th International Symposium on Parasitic Flowering Plants, Marburg, F.R.G. Google Scholar
Ramaiah, K. V. and Parker, C. 1982. Striga and other weeds in sorghum. Pages 291–302 in Sorghum in the Eighties: Proceedings of the International Symposium on Sorghum, 2–7 November 1981, Patancheru, A.P., India. ICRISAT, Patancheru P.O., Andhra Pradesh 502 324, India.Google Scholar
Rao, M. J. V., Chidley, V. L., Ramaiah, K. V., and House, L. R. 1983. Breeding sorghum genotypes with resistance to Striga asiatica at the ICRISAT Center. Pages 61–76 in Proceedings of the 2nd International Workshop on Striga, 5–8 October 1981, Ouagadougou, Upper Volta. ICRISAT, Patancheru P.O., Andhra Pradesh 502 324, India.Google Scholar
Rich, P. J., Grenier, C., and Ejeta, G. 2004. Striga resistance in the wild relatives of sorghum. Crop Sci. 4:2221–2229.Google Scholar
Riopel, J. L. and Timko, M. P. 1995. Haustorial initiation and differentiation. Pages 39–73 in Press, M. C. and Graves, J. D., eds. Parasitic Plants. London Chapman & Hall.Google Scholar
Rispail, N., Dita, M. A., Gonzalez-Verdejo, C., Pérez -de-Luque, A., Castillejo, M. A., Prats, E., Roman, B., Jorrin, J., and Rubiales, D. 2007. Plant resistance to parasitic plants: molecular approaches to an old foe. New Phytol. 173:703–712.Google Scholar
Rodenburg, J., Riches, C. R., and Kayeke, J. M. 2010. Addressing current and future problems of parasitic weeds in rice. Crop Prot. 29:210–221.Google Scholar
Ronald, P. C. and Beutler, B. 2010. Plant and animal sensors of conserved microbial signatures. Science. 330:1061–1064.Google Scholar
Roze, E., Hanse, B., Mitreva, M., et al. 2008. Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes. Mol. Plant Pathol. 9:1–10.Google Scholar
Runo, S., Alakonya, A., Machuka, J., and Sinha, N. 2010. RNA interference as a resistance mechanism against crop parasites in Africa: a “Trojan horse” approach. Pest Manag. Sci. 67:129–136.Google Scholar
Runyon, J., Mescher, M., Felton, G., and de Morales, C. 2010. Parasitism by Cuscuta pentagona sequentially induces JA and SA defense pathways in tomato. Plant Cell Environ. 33:290–303.Google Scholar
Ryu, H., Han, M., Lee, S., et al. 2006. A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep. 25:836–847.Google Scholar
Saunders, A. R. 1933. Studies on phanerogamic parasitism with particular reference to Striga lutea Lour. So. African Department of Agriculture Science Bulletin No. 128.56 p.Google Scholar
Schirawski, J., Mannhaupt, G., Munch, K., et al. 2010. Pathogenicity determinants in smut fungi revealed by genome comparisons. Science. 330:1546–1548.Google Scholar
Scholes, J. D. and Press, M. C. 2008. Striga infestation of cereal crops: an unsolved problem in resource limited agriculture. Curr. Opin. Plant Biol. 11:180–186.Google Scholar
Shinde, V. K. and Kulkarni, N. 1982. Genetics of resistance to Striga asiatica in sorghum. Pages 134–141 in Proceedings of the ICRISAT-ICAR Working Group Meeting on Striga Control, 30 September–1 October, 1982, ICRISAT, Patancheru P.O., Andhra Pradesh 502 324, India.Google Scholar
Singh, B. B. and Emechebe, A. M. 1990. Inheritance of Striga resistance in cowpea genotype B301. Crop Sci. 30:879–881.Google Scholar
Spanu, P. D., Abbott, J. C., Amselem, J., et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science. 330:1543–1546.CrossRefGoogle ScholarPubMed
Swarbrick, P. J., Huang, K., Liu, G., Slate, J., Press, M. C., and Scholes, J. D. 2008. Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica . New Phytol. 179:515–529.Google Scholar
Takken, F. L., Albrecht, M., and Tameling, W. I. 2006. Resistance proteins: molecular switches of plant defence. Curr. Opin. Plant Biol. 9:383–390.Google Scholar
Tameling, W. I. L. and Joosten, M. H. A. J. 2007. The diverse roles of NB-LRR proteins in plants. Physiol. Mol. Plant P. 71:126–134.Google Scholar
Thordal-Christensen, H. 2003. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6:351–357.Google Scholar
Timko, M. P., Gowda, B. S., Ouédraogo, J., and Ousmane, B. 2007. Molecular markers for analysis of resistance to Striga gesnerioides in cowpea. Pages 115–128 in Ejeta, G. and Gressel, J., eds. Integrating New Technologies for Striga Control, Towards Ending the Witch-hunt. Singapore World Scientific Publishing.Google Scholar
Timko, M. P., Rushton, P. J., Laudeman, T. W., Bokowiec, M. T., Chipumuro, E., Cheung, F., Town, C. D., and Chen, X. 2008. Sequencing and analysis of the gene-rich space of cowpea. BMC Genomics. 9:103.Google Scholar
Timko, M. P. and Singh, B. B. 2008. Cowpea, a multifunctional legume. Pages 227–258 in Moore, P. H. and Ming, R., eds. Genomics of Tropical Crop Plants. New York Springer Science + Business Media.Google Scholar
Tomilov, A., Tomilova, N. and Yoder, J. I. 2006. Agrobacterium tumefaciens and Agrobacterium rhizogenes transformed roots of the parasitic plant Triphysaria versicolor retain parasitic competence. Planta. 225:1059–1071.Google Scholar
Torto-Alalibo, T., Collmer, C. W., Lineberg, M., Bird, D., Collmer, A., and Tyler, B. M. 2009. Common and contrasting themes in host cell-targeted effectors from bacterial, fungal, oomycete and nematode plant symbionts described using the Gene Ontology. BMC MicroBiol. 9(Suppl 1):S3.Google Scholar
Touré, M., Olivier, A., Ntare, B. R., Lane, J. A., and St.-Pierre, C-A. 1997. Inheritance of resistance to Striga gesnerioides biotypes from Mali and Niger in cowpea (Vigna unguiculata (L.) Walp.). Euphytica. 94:273–278.Google Scholar
Tyler, B. M. 2009. Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell. MicroBiol. 11:13–20.Google Scholar
van der Hoorn, R. A. L. and Kamoun, S. 2008. From guard to decoy: A new model for perception of plant pathogen effectors. Plant Cell. 20:2009–2017.Google Scholar
Vieira Dos Santos, C., Delavault, P., Letousey, P., and Thalouarn, P. 2003. Identification by suppression subtractive hybridization and expression analysis of Arabidopsis thaliana putative defence genes during Orobanche ramosa infection. Physiol. Mol. Plant P. 62:297–303.Google Scholar
Vogler, R. K., Ejeta, G., and Butler, L. G. 1996. Inheritance of low production of Striga germination stimulant in sorghum. Crop Sci. 36:1185–1191.Google Scholar
Westwood, J. H., dePamphilis, C. W., Das, M., Fernandez-Aparicio, M., Honaas, L. A., Timko, M. P., Wickett, N. J., and Yoder, J. I. 2011. The Parasitic Plant Genome Project: new tools for understanding the biology of Orobanche and Striga . Weed Sci. 60:295–306.CrossRefGoogle Scholar
Westwood, J. H., Yoder, J. I., Timko, M. P., and dePamphilis, C. W. 2010. The evolution of parasitism in plants. Trends Plant Sci. 15:227–235.Google Scholar
Wilson, J. P., Hess, D. E., and Hanna, W. W. 2000. Resistance to Striga hermonthica in wild accessions of the primary gene pool of Pennisetum glaucum . Phytopathology. 90:1169–1172.Google Scholar
Wilson, J. P., Hess, D. E., Hanna, W. W., Kumar, K. A., and Gupta, S. C. 2004. Pennisetum glaucum subsp. monodii accessions with Striga resistance in West Africa. Crop Prot. 23:865–870.Google Scholar
Yoshida, S. and Shirasu, K. 2009. Multiple layers of incompatibility to the parasitic witchweed, Striga hermonthica . New Phytol. 183:180–189.Google Scholar