Hostname: page-component-5d84bcc8dc-cszgk Total loading time: 0 Render date: 2026-09-15T20:35:58.137Z Has data issue: false hasContentIssue false
  • English
  • Français

Transcriptomics of host-specific interactions in natural populations of the parasitic plant purple witchweed (Striga hermonthica)

Published online by Cambridge University Press:  10 June 2019

Lua Lopez Open the ORCID record for Lua Lopez [Opens in a new window] ,
Emily S. Bellis ,
Eric Wafula ,
Sarah J. Hearne ,
Loren Honaas ,
Paula E. Ralph ,
Michael P. Timko ,
Nnanna Unachukwu ,
Claude W. dePamphilis  and
Jesse R. Lasky
Lua Lopez*
Affiliation:
Postdoctoral Research Associate, The Pennsylvania State University, University Park, PA, USA; Research Assistant Professor, Binghamton University, State University of New York, Binghamton, NY, USA
Emily S. Bellis
Affiliation:
Postdoctoral Research Fellow, The Pennsylvania State University, University Park, PA, USA
Eric Wafula
Affiliation:
Bioinformatics Programmer, The Pennsylvania State University, University Park, PA, USA
Sarah J. Hearne
Affiliation:
Research Scientist, International Institute of Tropical Agriculture, Ibadan, Nigeria Principal Research Scientist, International Maize and Wheat Improvement Center, Texcoco, Mexico
Loren Honaas
Affiliation:
Research Molecular Biologist, Physiology and Pathology of Tree Fruits Research, USDA-ARS, Wenatchee, WA, USA
Paula E. Ralph
Affiliation:
Lab Manager, The Pennsylvania State University, University Park, PA, USA
Michael P. Timko
Affiliation:
Professor, University of Virginia, Charlottesville, VA, USA
Nnanna Unachukwu
Affiliation:
Senior Research Supervisor, International Institute of Tropical Agriculture, Ibadan, Nigeria
Claude W. dePamphilis
Affiliation:
Professor, The Pennsylvania State University, University Park, PA, USA
Jesse R. Lasky
Affiliation:
Assistant Professor, The Pennsylvania State University, University Park, PA, USA
*
Author for correspondence: Lua Lopez, Email: lopezperez.lua@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Host-specific interactions can maintain genetic and phenotypic diversity in parasites that attack multiple host species. Host diversity, in turn, may promote parasite diversity by selection for genetic divergence or plastic responses to host type. The parasitic weed purple witchweed [Striga hermonthica (Delile) Benth.] causes devastating crop losses in sub-Saharan Africa and is capable of infesting a wide range of grass hosts. Despite some evidence for host adaptation and host-by-Striga genotype interactions, little is known about intraspecific Striga genomic diversity. Here we present a study of transcriptomic diversity in populations of S. hermonthica growing on different hosts (maize [Zea mays L.] vs. grain sorghum [Sorghum bicolor (L.) Moench]). We examined gene expression variation and differences in allelic frequency in expressed genes of aboveground tissues from populations in western Nigeria parasitizing each host. Despite low levels of host-based genome-wide differentiation, we identified a set of parasite transcripts specifically associated with each host. Parasite genes in several different functional categories implicated as important in host–parasite interactions differed in expression level and allele on different hosts, including genes involved in nutrient transport, defense and pathogenesis, and plant hormone response. Overall, we provide a set of candidate transcripts that demonstrate host-specific interactions in vegetative tissues of the emerged parasite S. hermonthica. Our study shows how signals of host-specific processes can be detected aboveground, expanding the focus of host–parasite interactions beyond the haustorial connection.

Keywords

Allele frequencygene expressionhost–parasite interactionsparasitic plantRNAseq

Information

Type
Research Article
Information
Weed Science , Volume 67 , Issue 4 , July 2019 , pp. 397 - 411
Copyright
© Weed Science Society of America, 2019 

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.)

Article purchase

Temporarily unavailable

Footnotes

Associate Editor: Sara Martin, Agriculture and Agri-Food Canada

References

Ahmed, S, Stephen, GC, Roger, KB, Philip, MG (2009) Wind-borne insects mediate directional pollen transfer between desert fig trees 160 kilometers apart. Proc Natl Acad Sci USA 106:20342–20347CrossRefGoogle ScholarPubMed
Albrecht, H, Yoder, JI, Phillips, DA (1999) Flavonoids promote haustoria formation in the root parasite Triphysaria versicolor. Plant Physiol 119:585–592CrossRefGoogle ScholarPubMed
Amusan, OI, Patrick, JR, Menkir, A, Housley, T, Ejeta, G (2008) Resistance to Striga hermonthica in a maize inbred line derived from Zea diploperennis. New Phytol 178:157–166CrossRefGoogle Scholar
Antonova, TS, Terborg, SJ (1996) The role of peroxidase in the resistance of sunflower against Orobanche cumana in Russia. Weed Res 36:113–121CrossRefGoogle Scholar
Archie, AE, Ezenwa, OV (2011) Population genetic structure and history of a generalist parasite infecting multiple sympatric host species. Int J Parasitol 41:89–98CrossRefGoogle ScholarPubMed
Ashburner, M, Ball, AC, Blake, JA, Botstein, D, Butler, H, Cherry, JM, Davis, AP, Dolinski, K, Dwight, SS, Eppig, JT, Harris, MA, Hill, DP, Issel-Tarver, L, Kasarskis, A, Lewis, S, et al. (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25CrossRefGoogle ScholarPubMed
Atera, E, Itoh, K, Azuma, T, Ishii, T (2012) Farmers’ perception and constraints to the adoption of weed control option: the case of Striga asiatica in Malawi. J Agric Sci 4:5Google Scholar
Bailey, FS, Hinz, A, Kassen, R (2014) Adaptive synonymous mutations in an experimentally evolved Pseudomonas fluorescens population. Nat Commun 5:4076CrossRefGoogle Scholar
Bandaranayake, PCG, Filappova, T, Tomilov, A, Tomilova, NB, Jamison-McClung, D, Ngo, Q, Inoue, K, Yoder, JI (2010) A single-electron reducing quinone oxidoreductase is necessary to induce haustorium development in the root parasitic plant Triphysaria. Plant Cell 22:1404–1419CrossRefGoogle ScholarPubMed
Bashey, F (2015) Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philos Trans R Soc Lond B Biol Sci 370:20140301CrossRefGoogle ScholarPubMed
Bethke, G, Thao, A, Xiong, G, Li, B, Soltis, NE, Hatsugai, N, Hillmer, RA, Katagiri, F, Kliebenstein, DJ, Pauly, M, Glazebrook, J (2016) Pectin biosynthesis is critical for cell wall integrity and immunity in Arabidopsis thaliana. Plant Cell 28:537–556CrossRefGoogle ScholarPubMed
Bolger, MA, Lohse, M, Usadel, B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle ScholarPubMed
Bourdin, B, Adenier, H, Perrin, Y (2007) Carnitine is associated with fatty acid metabolism in plants. Plant Physiol Biochem 45:926–931CrossRefGoogle ScholarPubMed
Bozkurt, ML, Muth, P, Parzies, HK, Haussmann, BIG (2015) Genetic diversity of East and West African Striga hermonthica populations and virulence effects on a contrasting set of sorghum cultivars. Weed Res 55:71–81CrossRefGoogle Scholar
Chamary, JV, Hurst, LD (2005) Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol 6:R75CrossRefGoogle ScholarPubMed
Conesa, A, Götz, S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832CrossRefGoogle ScholarPubMed
Conesa, A, Götz, S, García-Gómez, JM, Terol, J, Talón, M, Robles, M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefGoogle ScholarPubMed
Conn, CE, Bythell-Douglas, R, Neumann, D, Yoshida, S, Whittington, B, Westwood, JH, Shirasu, K, Bond, CS, Dyer, KA, Nelson, DC (2015) Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:540–543CrossRefGoogle ScholarPubMed
Cui, J, Bahrami, AK, Pringle, EG, Hernandez-Guzman, G, Bender, CL, Pierce, NE, Ausubel, FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci USA 102:1791–1796CrossRefGoogle ScholarPubMed
Durrant, WE, Dong, X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209.CrossRefGoogle ScholarPubMed
Ejeta, G (2007) Breeding for Striga resistance in sorghum: exploitation of an intricate host–parasite biology. Crop Sci 47:216–227CrossRefGoogle Scholar
Finn, RD, Attwood, TK, Babbitt, PC, Bateman, A, Bork, P, Bridge, AJ, Chang, H-Y, Dosztányi, Z, El-Gebali, S, Fraser, M, Gough, J, Haft, D, Holliday, GL, Huang, H, Huang, X, et al. (2017) InterPro in 2017–beyond protein family and domain annotations. Nucleic Acids Res 45:D190–D199CrossRefGoogle ScholarPubMed
Frank, SA (1993) Evolution of host-parasite diversity. Evolution 47:1721–1732CrossRefGoogle ScholarPubMed
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 Environ 20:483–492CrossRefGoogle Scholar
Fu, ZQ, Dong, X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863CrossRefGoogle ScholarPubMed
Geiger, R (1954) Klassifikation der klimate nach W. Köppen. Pages 603–607 in Landolt, HH, Börnstein, R, eds. Zahlenwerte Und Funktionen Aus Physik, Chemie, Astronomie, Geophysik Und Technik, Alte Serie. Berlin: SpringerGoogle Scholar
Gene Ontology Consortium (2017) Expansion of the Gene Ontology knowledgebase and resources. Nucleic Acids Res 45:331–338CrossRefGoogle Scholar
Grabherr, MG, Brian, JH, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q, Chen, Z, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol 29:644CrossRefGoogle ScholarPubMed
Griffiths-Jones, S, Bateman, A, Marshall, M, Khanna, A, Eddy, SR (2003) Rfam: an RNA family database. Nucleic Acids Res 31:439–41CrossRefGoogle Scholar
Guo, M, Tian, F, Wamboldt, Y, Alfano, JR (2009) The majority of the type III effector inventory of Pseudomonas syringae Pv. Tomato DC3000 can suppress plant immunity. Mol Plant-Microbe Interact 22:1069–1080CrossRefGoogle ScholarPubMed
Haussmann, BIG, Hess, DE, Omanya, GO, Folkertsma, RT, Reddy, BVS, 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 109:1005–1016CrossRefGoogle ScholarPubMed
Heese, M, Gansel, X, Sticher, L, Wick, P, Grebe, M, Granier, F, Jürgens, G (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 155:239–250CrossRefGoogle ScholarPubMed
Hess, DE, Ejeta, G, Butler, LG (1992) Selecting sorghum genotypes expressing a quantitative biosynthetic trait that confers resistance to Striga. Phytochemistry 31:493–497CrossRefGoogle Scholar
Hoffman, GE, Schadt, EE (2016) VariancePartition: interpreting drivers of variation in complex gene expression studies. BMC Bioinformatics 17:483CrossRefGoogle ScholarPubMed
Honaas, LA, Wafula, EK, Yang, Z, Der, JP, Wickett, NJ, Altman, NS, Taylor, CG, Yoder, JI, Timko, MP, Westwood, JH, dePamphilis, CW (2013) Functional genomics of a generalist parasitic plant: laser microdissection of host–parasite interface reveals host-specific patterns of parasite gene expression. BMC Plant Biol 13:9CrossRefGoogle ScholarPubMed
Hunt, RC, Simhadri, VL, Iandoli, M, Sauna, ZE, Kimchi-Sarfaty, C (2014). Exposing synonymous mutations. Trends Genet 30:308–321CrossRefGoogle ScholarPubMed
Ichihashi, Y, Mutuku, JM, Yoshida, S, Shirasu, K (2015) Transcriptomics exposes the uniqueness of parasitic plants. Brief Funct Genomics 14:275–282CrossRefGoogle ScholarPubMed
Ingvarsson, PK (2010) Natural selection on synonymous and nonsynonymous mutations shapes patterns of polymorphism in Populus tremula. Mol Biol Evol 27:650–660CrossRefGoogle ScholarPubMed
Kaci-Chaouch, T, Verneau, O, Desdevises, Y (2008) Host specificity is linked to intraspecific variability in the genus Lamellodiscus (Monogenea). Parasitology 135:607–616CrossRefGoogle Scholar
Kanehisa, M, Goto, S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30CrossRefGoogle ScholarPubMed
Karger, DN, Conrad, O, Böhner, J, Kawohl, T, Kreft, H, Soria-Auza, RW, Zimmermann, NE, Linder, PH, Kessler, M (2017) Climatologies at high resolution for the earth’s land surface areas. Sci Data 4:170122CrossRefGoogle ScholarPubMed
Konczal, M, Koteja, P, Stuglik, MT, Radwan, J, Babik, W (2013) Accuracy of allele frequency estimation using pooled RNA-Seq. Mol Ecol Res 14:381–392CrossRefGoogle ScholarPubMed
Koyama, ML (2000) Genetic variability of Striga hermonthica and effect of resistant cultivars on Striga population dynamics. Pages 247–260 in Rattunde, HFW, Geiger, HH, Haussman, BIG, Hess, DE, Koyama, ML, Grivet, L, eds. Breeding for Striga Resistance in Cereals. Weikersheim, Germany: Margraf VerlagGoogle Scholar
Kudla, G, Murray, AW, Tollervey, D, Plotkin, JB (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science 324:255–258CrossRefGoogle ScholarPubMed
Lajeunesse, MJ, Forbes, MR (2002) Host range and local parasite adaptation. Proc R Soc Lond B Biol Sci 269:703–710CrossRefGoogle ScholarPubMed
Lane, JA, Child, DV, Moore, THM, Arnold, GM, Bailey, JA (1997) Phenotypic characterization of resistance in Zea diploperennis to Striga. Maydica 42:45–51Google Scholar
Lawand, S, Dorne, AJ, Long, D, Coupland, G, Mache, R, Carol, P (2002) Arabidopsis A BOUT DE SOUFFLE, which is homologous with mammalian carnitine acyl carrier, is required for postembryonic growth in the light. Plant Cell 14:2161–2173CrossRefGoogle Scholar
Lechat, MM, Pouvreau, JB, Péron, T, Gauthier, M, Montiel, G, Véronési, C, Todoroki, Y, Le Bizec, B, Monteau, F, Macherel, D, Simier, P, Thoiron, S, Delavault, P (2012) PrCYP707A1, an ABA catabolic gene, is a key component of Phelipanche ramosa seed germination in response to the strigolactone analogue GR24. J Exp Bot 63:5311–5322CrossRefGoogle ScholarPubMed
Leggett, HC, Benmayor, R, Hodgson, DJ, Buckling, A (2013) Experimental evolution of adaptive phenotypic plasticity in a parasite. Curr Biol 23:139–142CrossRefGoogle Scholar
Li, H, Durbin, R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760CrossRefGoogle ScholarPubMed
Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G, Durbin, R, and 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079CrossRefGoogle ScholarPubMed
Liu, N, Sun, Y, Pei, Y, Zhang, X, Wang, P, Li, X, Li, F, Hou, Y (2018) A pectin methylesterase inhibitor enhances resistance to Verticillium Wilt. Plant Physiol 176:2202–2220CrossRefGoogle ScholarPubMed
Liu, Y (2012) Comparing and contrasting two plant pathogens provide a unique window into the differences in the innate immune responses between dicots and monocots. Ph.D dissertation. Atlanta, GA: Emory University. 173 pGoogle Scholar
Losner-Goshen, D, Portnoy, V, Mayer, A, Joel, D (1998) Pectolytic activity by the haustorium of the parasitic plant Orobanche L. (Orobanchaceae) in host roots. Ann Bot 81:319–326CrossRefGoogle Scholar
Maiti, RK, Ramaiah, KV, Bisen, SS, Chidley, VL (1984) A comparative study of the haustorial development of Striga asiatica (L.) Kuntze on Sorghum cultivars. Ann Bot 54:447–457CrossRefGoogle Scholar
McGill, BJ, Enquist, BJ, Weiher, E, Westoby, M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185CrossRefGoogle ScholarPubMed
Musselman, LJ (1980) The biology of Striga, Orobanche, and other root-parasitic weeds. Annu Rev Phytopathol 18:463–489CrossRefGoogle Scholar
Mutinda, SM, Masanga, J, Mutuku, JM, Runo, S, Alakonya, A (2018) KSTP 94, an open-pollinated maize variety has postattachment resistance to purple witchweed (Striga hermonthica). Weed Sci 66:525–529CrossRefGoogle Scholar
Mutuku, JM, Yoshida, S, Shimizu, T, Ichihashi, Y, Wakatake, T, Takahashi, A, Seo, M, Shirasu, K (2015) The WRKY45-dependent signaling pathway is required for resistance against Striga hermonthica parasitism. Plant Physiol 168:1152–1163CrossRefGoogle ScholarPubMed
Nei, M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225–233CrossRefGoogle ScholarPubMed
Ngo, QA, Albrecht, H, Tsuchimatsu, T, Grossniklaus, U (2013) The differentially regulated genes TvQR1 and TvPirin of the parasitic plant Triphysaria exhibit distinctive natural allelic diversity. BMC Plant Biol 13:28CrossRefGoogle ScholarPubMed
Nishiguchi, M, Yoshida, K, Sumizono, T, Tazaki, K (2002) A receptor-like protein kinase with a lectin-like domain from Lombardy poplar: gene expression in response to wounding and characterization of phosphorylation activity. Mol Genet Genomics 267:506–514CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, GF, Kindt, R, Legendre, P, Minchin, P, O’Hara, RB, Simpson, G, Solymos, P, Stevens, MHH, Wagner, HH (2013) Vegan: Community ecology package. R Package v. 2.0–10.Google Scholar
Olivier, A, Glaszmann, JC, Lanaud, C, Leroux, GD (1998) Population structure, genetic diversity and host specificity of the parasitic weed Striga hermonthica (Scrophulariaceae) in Sahel. Plant Syst Evol. 209:33–45CrossRefGoogle Scholar
Pageau, K, Simier, P, Le Bizec, B, Robins, RJ, Fer, A (2003) Characterization of nitrogen relationships between Sorghum bicolor and the root–hemiparasitic angiosperm Striga hermonthica (Del.) Benth. using K15NO3 as isotopic tracer. J Exp Bot 54:789–99CrossRefGoogle Scholar
Panter, RA, Mudd, JB (1969) Carnitine levels in some higher plants. FEBS Lett 5:169–170CrossRefGoogle ScholarPubMed
Patro, R, Duggal, G, Love, MI, Irizarry, RA, Kingsford, C (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14:417–419CrossRefGoogle ScholarPubMed
Pérez-de-Luque, A (2013) Haustorium invasion into host tissues. Pages 75–86 in Joel, DM, Gressel, J, Musselman, LJ, eds. Parasitic Orobanchaceae: Parasitic Mechanisms and Control Strategies. Berlin: SpringerCrossRefGoogle Scholar
Pouvreau, JB, Gaudin, Z, Auger, B, Lechat, MM, Gauthier, M, Delavault, P, Simier, P (2013) A high-throughput seed germination assay for root parasitic plants. Plant Methods 9:32CrossRefGoogle ScholarPubMed
Pruitt, KD, Tatusova, T, Maglott, DR (2007) NCBI Reference Sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:61–65CrossRefGoogle ScholarPubMed
Ranjan, A, Ichihashi, Y, Farhi, M, Zumstein, K, Townsley, B, David-Schwartz, R, Sinha, NR (2014) De novo assembly and characterization of the transcriptome of the parasitic weed dodder identifies genes associated with plant parasitism. Plant Physiol 166:1186–1199CrossRefGoogle ScholarPubMed
Riopel, Jl, Timko, MP (1992) Signals and regulation in the development of Striga and other parasitic angiosperms. Pages 493–507 in Verma, DPS, ed. Molecular Signals in Plant-Microbe Communications. Boca Raton, FL: CRC PressGoogle Scholar
Robinson, MD, McCarthy, DJ, Smyth, GK (2010) EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140CrossRefGoogle ScholarPubMed
Rodenburg, J, Demont, M, Zwart, SJ, Bastiaans, L (2016) Parasitic weed incidence and related economic losses in rice in Africa. Agric Ecosyst Environ 235:306–317CrossRefGoogle Scholar
Roppolo, D, Boeckmann, B, Pfister, A, Boutet, E, Rubio, MC, Dénervaud-Tendon, V, Vermeer, JE, Gheyselinck, J, Xenarios, I, Geldner, N (2014) Functional and evolutionary analysis of the CASPARIAN STRIP MEMBRANE DOMAIN PROTEIN family. Plant Physiol 165:1709–1722CrossRefGoogle ScholarPubMed
Runo, S, Kuria, EK (2018) Habits of a highly successful cereal killer, Striga. PLoS Pathog 14:e1006731CrossRefGoogle ScholarPubMed
Safa, SB, Jones, BMG, Musselman, LJ (1984) Mechanisms favouring outbreeding in Striga hermonthica (Scrofulariaceae). New Phytol 96:299–305CrossRefGoogle Scholar
Saucet, SB, Shirasu, K (2016) Molecular parasitic plant–host interactions. PLoS Pathog 12:e1005978CrossRefGoogle ScholarPubMed
Singh, A, Singh, M (1993) Cell wall degrading enzymes in Orobanche aegyptiaca and its host Brassica campestris. Physiol Plant 89:177–181CrossRefGoogle Scholar
Spallek, T, Mutuku, M, Shirasu, K (2013) The genus Striga: a witch profile. Mol Plant Pathol 14:861–869CrossRefGoogle ScholarPubMed
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 179:515–529CrossRefGoogle ScholarPubMed
Swenson, NG, Iida, Y, Howe, R, Wolf, A, Umaña, MN, Petprakob, K, Turner, BL, Ma, K (2017) Tree co-occurrence and transcriptomic response to drought. Nat Commun 8:1996CrossRefGoogle ScholarPubMed
Tomilov, AA, Tomilova, NB, Abdallah, I, Yoder, JI (2005) Localized hormone fluxes and early haustorium development in the hemiparasitic plant Triphysaria versicolor. Plant Physiol 138:1469–1480CrossRefGoogle ScholarPubMed
Unachukwu, NN, Menkir, A, Rabbi, IY, Oluoch, M, Muranaka, S, Elzein, A, Odhiambo, G, Farombi, EO, Gedil, M (2017) Genetic diversity and population structure of Striga hermonthica populations from Kenya and Nigeria. Weed Res 57:293–302CrossRefGoogle Scholar
Vogler, RK, Ejeta, G, Butler, LG (1996) Inheritance of low production of Striga germination stimulant in sorghum. Crop Sci 36:1185–1191CrossRefGoogle Scholar
Watson, IA (1970) Changes in virulence and population shifts in plant pathogens. Annu Rev Phytopathol 8:209–230CrossRefGoogle Scholar
Welsh, B, Mohamed, KI (2011) Genetic diversity of Striga hermonthica populations in Ethiopia: evaluating the role of geography and host specificity in shaping population structure. Int J Plant Sci 172:773–782CrossRefGoogle Scholar
Westwood, JH, dePamphilis, CW, Das, M, Fernández-Aparicio, M, Honaas, LA, Timko, MP, Wafula, EK, Wickett, NJ, Yoder, JI (2012) The Parasitic Plant Genome Project: new tools for understanding the biology of Orobanche and Striga. Weed Sci 60:295–306CrossRefGoogle Scholar
Wick, P, Gansel, X, Oulevey, C, Page, V, Studer, I, Dürst, M, Sticher, L (2003) The expression of the T-SNARE AtSNAP33 is induced by pathogens and mechanical stimulation. Plant Physiol 132:343–351CrossRefGoogle ScholarPubMed
Yang, Z, Wafula, EK, Honaas, LA, Zhang, H, Das, M, Fernandez-Aparicio, M, Huang, K, Bandaranayake, PCG, Wu, B, Der, JP, Clarke, CD, Ralph, PE, Landherr, L, Altman, NS, Timko, MP, et al. (2015). Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol Bio Evol 32:767–790CrossRefGoogle ScholarPubMed
Young, ND, Debellé, F, Oldroyd, GED, Geurts, R, Cannon, SB, Udvardi, MK, Benedito, VA, Mayer, KF, Gouzy, J, Schoof, H, Van de Peer, Y, Proost, S, Cook, DR, Meyers, BC, Spannagl, M, et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520CrossRefGoogle ScholarPubMed
Zdobnov, EM, Tegenfeldt, F, Kuznetsov, D, Waterhouse, RM, Simão, FA, Ioannidis, P, Seppey, M, Loetscher, A, Kriventseva, EV (2017) OrthoDB v9.1: cataloging evolutionary and functional annotations for animal, fungal, plant, archaeal, bacterial and viral orthologs. Nucleic Acids Res 45:744–749CrossRefGoogle ScholarPubMed
Zheng, X, Levine, D, Shen, J, Gogarten, SM, Laurie, C, Weir, BS (2012a) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328CrossRefGoogle ScholarPubMed
Zheng, XY, Spivey, NW, Zeng, W, Liu, PP, Fu, ZQ, Klessig, DF, He, SY, Dong, X (2012b) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–596CrossRefGoogle ScholarPubMed
Zouari, I, Salvioli, A, Chialva, M, Novero, M, Miozzi, L, Tenore, GG, Bagnaresi, P, Bonfante, P (2014) From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics 15:221CrossRefGoogle ScholarPubMed
Supplementary material: File

Lopez et al. supplementary material

Lopez et al. supplementary material

Download Lopez et al. supplementary material(File)
File 1.3 MB