Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T15:10:46.814Z Has data issue: false hasContentIssue false
  • English
  • Français

The Parasitic Plant Genome Project: New Tools for Understanding the Biology of Orobanche and Striga

Published online by Cambridge University Press:  20 January 2017

James H. Westwood ,
Claude W. dePamphilis ,
Malay Das ,
Mónica Fernández-Aparicio ,
Loren A. Honaas ,
Michael P. Timko ,
Eric K. Wafula ,
Norman J. Wickett  and
John I. Yoder
James H. Westwood*
Affiliation:
Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA 24061
Claude W. dePamphilis
Affiliation:
Department of Biology, Institute of Molecular Evolutionary Genetics, and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802
Malay Das
Affiliation:
Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA 24061
Mónica Fernández-Aparicio
Affiliation:
Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA 24061 Additional address: Institute for Sustainable Agriculture, IAS-CSIC, Dept. of Plant Breeding, Córdoba, 14080, Spain
Loren A. Honaas
Affiliation:
Department of Biology, Institute of Molecular Evolutionary Genetics, and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802
Michael P. Timko
Affiliation:
Department of Biology, University of Virginia, Charlottesville, VA 22904
Eric K. Wafula
Affiliation:
Department of Biology, Institute of Molecular Evolutionary Genetics, and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802
Norman J. Wickett
Affiliation:
Department of Plant Sciences, University of California, Davis, CA 95616
*
Corresponding author's E-mail: westwood@vt.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The Parasitic Plant Genome Project has sequenced transcripts from three parasitic species and a nonparasitic relative in the Orobanchaceae with the goal of understanding genetic changes associated with parasitism. The species studied span the trophic spectrum from free-living nonparasite to obligate holoparasite. Parasitic species used were Triphysaria versicolor, a photosynthetically competent species that opportunistically parasitizes roots of neighboring plants; Striga hermonthica, a hemiparasite that has an obligate need for a host; and Orobanche aegyptiaca, a holoparasite with absolute nutritional dependence on a host. Lindenbergia philippensis represents the closest nonparasite sister group to the parasitic Orobanchaceae and was included for comparative purposes. Tissues for transcriptome sequencing from each plant were gathered to identify expressed genes for key life stages from seed conditioning through anthesis. Two of the species studied, S. hermonthica and O. aegyptiaca, are economically important weeds and the data generated by this project are expected to aid in research and control of these species and their relatives. The sequences generated through this project will provide an abundant resource of molecular markers for understanding population dynamics, as well as provide insight into the biology of parasitism and advance progress toward understanding parasite virulence and host resistance mechanisms. In addition, the sequences provide important information on target sites for herbicide action or other novel control strategies such as trans-specific gene silencing.

Keywords

Egyptian broomrape, Orobanche aegyptiaca (Pers.) (Syn. Phelipanche aegyptiaca) ORAAELindenbergia philippensis (Cham. & Schltdl.) Benth. LINPHyellowbeak owl's-clover, Triphysaria versicolor (Fisch. & C.A. Mey) TRVEVpurple witchweed, Striga hermonthica, (Del.) Benth. STRHEEST sequencinggene expressionhaustoriumparasitic plant evolutionparasitic weedsRNA-seqtranscriptome sequencingweed genomics
Type
Symposium
Information
Weed Science , Volume 60 , Issue 2 , June 2012 , pp. 295 - 306
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.)

Footnotes

Current address: Institute of Biochemical Plant Pathology, Helmholtz Zentrum Munchen, 85764 Neuherberg, Germany.

References

Literature Cited

Alfano, J. R. 2009. Roadmap for future research on plant pathogen effectors. Mol. Plant Pathol. 10:805–813.CrossRefGoogle ScholarPubMed
Alonso, L. C., Fernandez-Escobar, J., Lopez, G., Rodriguez-Ojeda, M. I., and Sallago, F. 1996. New highly virulent sunflower broomrape (Orobanche cernua Loefl.) pathotypes in Spain. Pages 639–644 in Moreno, M. T., Cubero, J. I., Berner, D., Joel, D., Musselman, L. J., and Parker, C., eds. Advances in Parasitic Plant Research. Cordoba, Spain. Junta de Andalucia.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
Barker, E. R., Press, M. C., Scholes, J. D., and Quick, W. P. 1996. Interactions between the parasitic angiosperm Orobanche aegyptiaca and its tomato host: growth and biomass allocation. New Phytol. 133:637–642.CrossRefGoogle Scholar
Baulcombe, D. C. 1996. Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell. 8:1833–1844.CrossRefGoogle ScholarPubMed
Baum, J. A., Bogaert, T., Clinton, W., et al. 2007. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25:1322–1326.CrossRefGoogle ScholarPubMed
Baxter, L., Tripathy, S., Ishaque, N., et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science. 330:1549–1551.CrossRefGoogle ScholarPubMed
Benharrat, H., Boulet, C., Theodet, C., and Thalouarn, P. 2005. Virulence diversity among branched broomrape (O. ramosa L.) populations in France. Agron. Sust. Dev. 25:123–128.CrossRefGoogle Scholar
Bernhard, R. H., Jensen, J. E., and Andreasen, C. 1998. Prediction of yield loss caused by Orobanche spp. in carrot and pea crops based on the soil seedbank. Weed Res. 38:191–197.CrossRefGoogle Scholar
Block, A., Li, G., Fu, Z. Q., and Alfano, J. R. 2008. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11:396–403.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. Mol. Plant Pathol. 10:431–448.CrossRefGoogle ScholarPubMed
Brault, M., Betsou, F., Jeune, B., Tuquet, C., and Sallé, G. 2007. Variability of Orobanche ramosa populations in France as revealed by cross infestations and molecular markers. Environ. Exp. Bot. 61:272–280.CrossRefGoogle Scholar
Cardoso, C., Ruyter-Spira, C., and Bouwmeester, H. J. 2011. Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. Plant Sci. 180:414–420.CrossRefGoogle ScholarPubMed
Chuang, T. I. and Heckard, L. R. 1991. Generic realignment and synopsis of subtribe Castillejinae (Scrophulariaceae—tribe Pediculareae). Syst. Bot. 16:644–666.CrossRefGoogle Scholar
Cramer, R. A., La Rota, C. M., Cho, Y., Thon, M., Craven, K. D., Knudson, D. L., Mitchell, T. K., 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.CrossRefGoogle ScholarPubMed
Das, M., Reichman, J., Haberer, G., et al. 2010. A composite transcriptional signature differentiates responses toward closely related herbicides in Arabidopsis thaliana and Brassica napus . Plant Mol. Biol. 72:545–556.CrossRefGoogle Scholar
Davis, E. L., Hussey, R. S., Mitchum, M. G., and Baum, T. J. 2008. Parasitism proteins in nematode–plant interactions. Curr. Opin. Plant Biol. 11:360–366.CrossRefGoogle ScholarPubMed
de Framond, A., Rich, P., McMillan, J., and Ejeta, G. 2007. Effects on 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: Toward Ending the Witch-Hunt. Hackensack, NJ World Scientific.CrossRefGoogle Scholar
Díaz-Ruiz, R., Torres, A., Satovic, Z., Gutierrez, M., Cubero, J., and Román, B. 2009. Validation of QTLs for Orobanche crenata resistance in faba bean (Vicia faba L.) across environments and generations. Theor. Appl. Genet. 120:909–919.CrossRefGoogle ScholarPubMed
Die, J. V., Dita, M. A., Krajinski, F., Gonzalez-Verdejo, C. I., Rubiales, D., Moreno, M. T., and Roman, B. 2007. Identification by suppression subtractive hybridization and expression analysis of Medicago truncatula putative defence genes in response to Orobanche crenata parasitization. Physiol. Mol. Plant Path. 70:49–59.CrossRefGoogle Scholar
Dita, M. A., Die, J. V., Román, B., Krajinski, F., Küster, H., Moreno, M. T., Cubero, J. I., and Rubiales, D. 2009. Gene expression profiling of Medicago truncatula roots in response to the parasitic plant Orobanche crenata . Weed Res. 49:66–80.CrossRefGoogle Scholar
Duarte, J., Wall, P. K., Edger, P., Landherr, L., Ma, H., Pires, J. C., Leebens-Mack, J., and dePamphilis, C. 2010. Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol. Biol. 10:61.CrossRefGoogle ScholarPubMed
Ejeta, G. 2007. The Striga scourge in Africa: a growing pandemic. Pages 3–16 in Ejeta, G., and Gressel, J., eds. Integrating New Technologies for Striga Control: Toward Ending the Witch-Hunt. Singapore World Scientific.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Eplee, R. E. 1992. Witchweed (Striga asiatica): an overview of management strategies in the USA. Crop Protec. 11:3–7.CrossRefGoogle Scholar
Fernández-Martínez, J. M., Domínguez, J., Pérez-Vich, B., and Velasco, L. 2009. Current research strategies for sunflower broomrape control in Spain. Helia. 32:47–55.CrossRefGoogle Scholar
Frost, C. C. and Musselman, L. J. 1980. Clover broomrape (Orobanche minor) in the United States. Weed Sci. 28:119–122.CrossRefGoogle Scholar
Goldwasser, Y. and Kleifeld, Y. 2004. Recent approaches to Orobanche management: a review. Pages 439–566 in Inderjit, . ed. Weed Biology and Management. Dordrecht Kluwer.CrossRefGoogle Scholar
Goldwasser, Y., Westwood, J. H., and Yoder, J. I. 2002. The use of Arabidopsis to study interactions between parasitic angiosperms and their plant hosts. in Somerville, C. R., and Meyerowitz, E. M., eds. The Arabidopsis Book. 1:Page e0035. DOI:10.1199/tab.0035 Rockville, MD American Society of Plant Biologists.Google Scholar
Gressel, J. 2009. Crops with target-site herbicide resistance for Orobanche and Striga control. Pages 560–565 John Wiley & Sons CrossRefGoogle Scholar
Gressel, J., Segel, L., and Ransom, J. K. 1996. Managing the delay of evolution of herbicide resistance in parasitic weeds. Int. J. Pest Manag. 42:113–129.CrossRefGoogle Scholar
Hall, M. C. and Willis, J. H. 2005. Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence. Genetics. 170:375–386.CrossRefGoogle ScholarPubMed
Hamamouch, N., Westwood, J. H., Banner, I., Cramer, C. L., Gepstein, S., and Aly, R. 2005. A peptide from insects protects transgenic tobacco from a parasitic weed. Transgen. Res. 14:227–236.CrossRefGoogle ScholarPubMed
Hearne, S. J. 2009. Control—the Striga conundrum. Pest Manag. Sci. 65:603–614.CrossRefGoogle ScholarPubMed
Helliwell, C. A. and Waterhouse, P. M. 2005. Constructs and methods for hairpin RNA-mediated gene silencing in plants. Methods Enzymol. 392:24–35.CrossRefGoogle ScholarPubMed
Hickman, J. C. 1993. The Jepson Manual; Higher Plants of California. 1400 p.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Huang, G., Allen, R., Davis, E., Baum, T., and Hussey, R. 2006. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. USA. 103:14302–14306.CrossRefGoogle ScholarPubMed
Imelfort, M. and Edwards, D. 2009. De novo sequencing of plant genomes using second-generation technologies. Brief. Bioinform. 10:609–618.CrossRefGoogle ScholarPubMed
Joel, D. M., Steffens, J. C., and Matthews, D. E. 1995. Germination of weedy root parasites. Pages 567–597 in Kigel, J., and Galili, G., eds. Seed Development and Germination. New York Marcel Dekker.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.CrossRefGoogle Scholar
Letousey, P., De Zélicourt, A., Vieira Dos Santos, C., Thoiron, S., Monteau, F., Simier, P., Thalouarn, P., and Delavault, P. 2007. Molecular analysis of resistance mechanisms to Orobanche cumana in sunflower. Plant Pathol. 56:536–546.CrossRefGoogle Scholar
Li, J. and Timko, M. P. 2009. Gene-for-gene resistance in Striga-cowpea associations. Science. 325:1094.CrossRefGoogle ScholarPubMed
Manabe, Y., Tinker, N., Colville, A., and Miki, B. 2007. CSR1, the sole target of imidazolinone herbicide in Arabidopsis thaliana . Plant Cell Physiol. 48:1340–1358.CrossRefGoogle ScholarPubMed
Mangnus, E. M., Stommen, P. L. A., and Zwanenburg, B. 1992. A standardized bioassay for evaluation of potential germination stimulants for seeds of parasitic weeds. J. Plant Growth Regul. 11:91–98.CrossRefGoogle Scholar
Marguerat, S. and Bähler, J. 2010. RNA-seq: from technology to biology. Cell. Mol. Life Sci. 67:569–579.CrossRefGoogle ScholarPubMed
Mohamed, K. I., Musselman, L. J., and Riches, C. R. 2001. The genus Striga (Scrophulariaceae) in Africa. Ann. Missouri Bot. Gard. 88:60–103.CrossRefGoogle Scholar
Molinero-Ruiz, M. L., Melero-Vara, J. M., Garcia-Ruiz, R., and Dominguez, J. 2006. Pathogenic diversity within field populations of Orobanche cumana and different reactions on sunflower genotypes. Weed Res. 46:462–469.CrossRefGoogle Scholar
Ohtsu, K., Smith, M. B., Emrich, S. J., Borsuk, L. A., Zhou, R., Chen, T., Zhang, X., Timmermans, M. C. P., Beck, J., Buckner, B., Janick-Buckner, D., Nettleton, D., Scanlon, M. J., and Schnable, P. S. 2007. Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant J. 52:391–404.CrossRefGoogle ScholarPubMed
Olmstead, R. G., DePamphilis, C. W., Wolfe, A. D., Young, N. D., Elisons, W., and Reeves, P. A. 2001. Disintegration of the Scrophulariaceae. Am. J. Bot. 88:348–361.CrossRefGoogle ScholarPubMed
Parker, C. 1991. Protection of crops against parasitic weeds. Crop Protect. 10:6–22.CrossRefGoogle Scholar
Parker, C. 2009. Observations on the current status of Orobanche and Striga problems worldwide. Pest Man. Sci. 65:453–459.CrossRefGoogle ScholarPubMed
Parker, C. and Riches, C. R. 1993. Parasitic Weeds of the World: Biology and Control. Wallingford, CT CAB International. Pp. 111–164.Google Scholar
Paterson, A. H., Bowers, J. E., Bruggmann, R., et al. Nature. 457:551–556.CrossRefGoogle Scholar
Peng, Y., Abercrombie, L. L. G., Yuan, J. S., Riggins, C. W., Sammons, R. D., Tranel, P. J., and Stewart, C. N. 2010. Characterization of the horseweed (Conyza canadensis) transcriptome using GS-FLX 454 pyrosequencing and its application for expression analysis of candidate nontarget herbicide resistance genes. Pest Manag. Sci. 66:1053–1062.CrossRefGoogle ScholarPubMed
Perez-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.CrossRefGoogle Scholar
Pérez-Vich, B., Akhtouch, B., Knapp, S. J., Leon, A. J., Velasco, L., Fernández-Martínez, J. M., and Berry, S. T. 2004. Quantitative trait loci for broomrape (Orobanche cumana Wallr.) resistance in sunflower. Theor. Appl. Genet. 109:92–102.CrossRefGoogle ScholarPubMed
Radwan, O., Gandhi, S., Heesacker, A., et al. 2008. Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol. Genet. Genom. 280:111–125.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Raghavan, C., Ong, E. K., Dalling, M. J., and Stevenson, T. W. 2005. Effect of herbicidal application of 2,4-dichlorophenoxyacetic acid in Arabidopsis . Funct. Integr. Genomics. 5:4–17.CrossRefGoogle ScholarPubMed
Ransom, J., Kanampiu, F., Gressel, J., Groote, H. D., Burnet, M., and Odhiambo, G. 2012. Herbicides applied to the seed of IR-maize as a Striga control option for small-scale African farmers. Weed Sci. 60:283–289.CrossRefGoogle Scholar
Riggins, C. W., Peng, Y., Stewart, C. N., and Tranel, P. J. 2010. Characterization of de novo transcriptome for waterhemp (Amaranthus tuberculatus) using GS-FLX 454 pyrosequencing and its application for studies of herbicide target-site genes. Pest Manag. Sci. 66:1042–1052.CrossRefGoogle ScholarPubMed
Rispail, N., Dita, M. A., González-Verdejo, C., Pérez-de-Luque, A., Castillejo, M. A., Prats, E., Román, B., Jorrín, J., and Rubiales, D. 2007. Plant resistance to parasitic plants: molecular approaches to an old foe. New Phytol. 173:703–712.CrossRefGoogle Scholar
Román, B., Satovic, Z., Alfaro, C., Moreno, M. T., Kharrat, M., Pérez-de-Luque, A., and Rubiales, D. 2007. Host differentiation in Orobanche foetida Poir. Flora. 202:201–208.CrossRefGoogle Scholar
Roze, E., Hanse, B., Mitreva, M., Vanholme, B., Bakker, J., and Smant, G. 2008. Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes. Mol. Plant Pathol. 9:1–10.CrossRefGoogle ScholarPubMed
Rubiales, D., Fernández-Aparicio, M., Perez-de-Luque, A., Castillejo, M. A., Prats, E., Sillero, J. C., Rispail, N., and Fondevilla, S. 2009. Breeding approaches for crenate broomrape (Orobanche crenata Forsk.) management in pea (Pisum sativum L.). Pest Manag. Sci. 65:553–559.CrossRefGoogle ScholarPubMed
Rubiales, D., Perez-de-Luque, A., Fernández-Aparico, M., Sillero, J. C., Roman, B., Kharrat, M., Khalil, S., Joel, D. M., and Riches, C. 2006. Screening techniques and sources of resistance against parasitic weeds in grain legumes. Euphytica. 147:187–199.CrossRefGoogle Scholar
Sanford, J. C. and Johnston, S. A. 1985. The concept of parasite-derived resistance—deriving resistance genes from the parasite's own genome. J. Theor. Biol. 113:395–405.CrossRefGoogle Scholar
Sauerborn, J. 1991. The economic importance of the phytoparasites Orobanche and Striga . Proceedings of the 5th International Symposium of Parasitic Weeds, Nairobi, Kenya. CIMMYT.Google Scholar
Schirawski, J., Mannhaupt, G., Münch, K., et al. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science. 330:1546–1548.CrossRefGoogle ScholarPubMed
Schnable, P. S., Ware, D., Fulton, R. S., et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science. 326:1112–1115.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Spanu, P. D., Abbott, J. C., Amselem, J., et al. Science. 330:1543–1546.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Thorogood, C. J. and Hiscock, S. J. 2010. Compatibility interactions at the cellular level provide the basis for host specificity in the parasitic plant Orobanche . New Phytol. 186:571–575.CrossRefGoogle ScholarPubMed
Thorogood, C. J., Rumsey, F. J., Harris, S. A., and Hiscock, S. J. 2008. Host-driven divergence in the parasitic plant Orobanche minor Sm. (Orobanchaceae). Mol. Ecol. 17:4289–4303.CrossRefGoogle Scholar
Thorogood, C. J., Rumsey, F. J., and Hiscock, S. J. 2009. Host-specific races in the holoparasitic angiosperm Orobanche minor: implications for speciation in parasitic plants. Ann. Bot. 103:1005–1014.CrossRefGoogle ScholarPubMed
Timko, M., Gowda, B., Ouedraogo, 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.CrossRefGoogle Scholar
Tinoco, M. L. P., Dias, B. B. A., Dall'Astta, R. C., Pamphile, J. A., and Aragao, F. J. L. 2010. In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol. 8.CrossRefGoogle ScholarPubMed
Tomilov, A. A., Tomilova, N. B., Wroblewski, T., Michelmore, R., and Yoder, J. I. 2008. Trans-specific gene silencing between host and parasitic plants. Plant J. 56:389–397.CrossRefGoogle ScholarPubMed
Torres, M., Tomilov, A., Tomilova, N., Reagan, R., and Yoder, J. 2005. Pscroph, a parasitic plant EST database enriched for parasite associated transcripts. BMC Plant Biol. 5:24.CrossRefGoogle ScholarPubMed
Tyler, B. M. 2009. Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell. MicroBiol. 11:13–20.CrossRefGoogle ScholarPubMed
van Frankenhuyzen, K. 2009. Insecticidal activity of Bacillus thuringiensis crystal proteins. J. Invert. Pathol. 101:1–16.CrossRefGoogle ScholarPubMed
Velasco, L., Pérez-Vich, B., Jan, C. C., and Fernández-Martínez, J. M. 2007. Inheritance of resistance to broomrape (Orobanche cumana Wallr.) race F in a sunflower line derived from wild sunflower species. Plant Breed. 126:67–71.CrossRefGoogle Scholar
Voinnet, O. 2002. RNA silencing: small RNAs as ubiquitous regulators of gene expression. Curr. Opin. Plant Biol. 5:444–451.CrossRefGoogle ScholarPubMed
Vrânceanu, A. V., Tudor, V. A., Stoenescu, F. M., and Pirvu, N. 1980. Virulence group of O. cumana Wallr., differential host and resistance sources and genes in sunflower. Proceedings of the IXth International Sunflower Conference. 2:74–82 Torremolinos, Madrid, Spain. Ministerio de Agricultura.Google Scholar
Wall, P. K., Leebens-Mack, J., Chanderbali, A. S., et al. 2009. Comparison of next generation sequencing technologies for transcriptome characterization. BMC Genomics. 10:347.CrossRefGoogle ScholarPubMed
Wall, P. K., Leebens-Mack, J., Müller, K. F., Field, D., Altman, N. S., and dePamphilis, C. W. 2008. PlantTribes: a gene and gene family resource for comparative genomics in plants. Nucleic Acids Res. 36:D970–D976.CrossRefGoogle ScholarPubMed
Westwood, J. H. 2000. Characterization of the Orobanche–Arabidopsis system for studying parasite–host interactions. Weed Sci. 48:742–748.CrossRefGoogle Scholar
Westwood, J. H. 2001. Parasitic plant research in the era of genomics. Pages 82–87 in Proceedings of the 7th International Parasitic Weed Symposium, Nantes, France. University of Nantes.Google 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.CrossRefGoogle ScholarPubMed
Wickett, N. J., Honaas, L. A., Wafula, E. K., et al. 2011. Transcriptomes of the Parasitic Plant Family Orobanchaceae Reveal Surprising Conservation of Chlorophyll Synthesis. Curr. Biol. 21:2098–2104.Google Scholar
Wu, C. A., Lowry, D. B., Cooley, A. M., Wright, K. M., Lee, Y. W., and Willis, J. H. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity. 100:220–230.CrossRefGoogle ScholarPubMed
Yin, C. T., Jurgenson, J. E., and Hulbert, S. H. 2011. Development of a host-induced RNAi system in the wheat stripe rust fungus Puccinia striiformis f. sp tritici. Mol. Plant Microbe Interact. 24:554–561.CrossRefGoogle ScholarPubMed
Yoder, J. I. 2001. Host-plant recognition by parasitic Scrophulariaceae. Curr. Opin. Plant Biol. 4:359–365.CrossRefGoogle ScholarPubMed
Yoder, J. I. and Scholes, J. D. 2010. Host plant resistance to parasitic weeds; recent progress and bottlenecks. Curr. Opin. Plant Biol. 13:478–484.CrossRefGoogle ScholarPubMed
Yoneyama, K., Xie, X., Sekimoto, H., Takeuchi, Y., Ogasawara, S., Akiyama, K., Hayashi, H., and Yoneyama, K. 2008. Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol. 179:484–494.CrossRefGoogle ScholarPubMed
Zhang, J., Chiodini, R., Badr, A., and Zhang, G. 2011. The impact of next-generation sequencing on genomics. J. Gen. Genom. 38:95–109.CrossRefGoogle ScholarPubMed
Zhou, J-M. and Chai, J. 2008. Plant pathogenic bacterial type III effectors subdue host responses. Curr. Opin. MicroBiol. 11:179–185.CrossRefGoogle ScholarPubMed
Zhulidov, P. A., Bogdanova, E. A., Shcheglov, A. S., et al. 2004. Simple cDNA normalization using kamchatka crab duplex-specific nuclease. Nucleic Acids Res. 32:e37.CrossRefGoogle ScholarPubMed