Abstract
Main conclusion
New transgenic and biotechnological approaches may serve as a key component in achieving crop resistance to root parasitic weeds.
Abstract
Root parasitic weeds inflict severe damage to numerous crops, reducing yield quantity and quality. A lack of new sources of resistance limits our ability to manage newly developing, more virulent races. Having no effective means to control the parasites in most crops, innovative biotechnological solutions are needed. Several novel biotechnological strategies using regulatory RNA molecules, the CRISPR/Cas9 system, and T-DNA insertions have been acknowledged for engineering resistance against parasitic weeds. Significant breakthroughs have been made over the years in deciphering the plant genome and its functions, including the genomes of parasitic weeds. However, the basis of biotechnological strategies to generate host resistance to root parasitic weeds needs to be further developed. Gene-silencing and editing tools should be used to target key processes of host–parasite interactions, such as strigolactone biosynthesis and signaling, haustorium development, and degradation and penetration of the host cell wall. In this review, we summarize and discuss the main areas of research leading to the discovery and functional analysis of genes involved in host-induced gene silencing that target key parasite genes, transgenic host modification, and host gene editing to generate sustainable resistance to root parasitic weeds.
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References
Alakonya A, Kumar R, Koenig D et al (2012) Interspecific RNA interference of SHOOT MERISTEMLESS-like disrupts Cuscuta pentagona plant parasitism. Plant Cell 24:3153–3166
Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186
Albrecht H, Yoder JI, Phillips DA (1999) Flavonoids promote haustoria formation in the root parasite Triphysaria versicolor. Plant Physiol 119:585–591
Aly R (2007) Conventional and biotechnological approaches for control of parasitic weeds. Vitro Cell Dev Biol Plant 43:304–317
Aly R, Plakhin D, Achdari G (2006) Expression of sarcotoxin IA gene via a root-specific tob promoter enhanced host resistance against parasitic weeds in tomato plants. Plant Cell Rep 25:297–303
Aly R, Cholakh H, Joel DM et al (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
Aly R, Hamamouch N, Abu-Nassar J et al (2011) Movement of protein and macromolecules between host plants and the parasitic weed Phelipanche aegyptiaca Pers. Plant Cell Rep 30:2233–2241
Aly R, Dubey NK, Yahyaa M, Abu-Nassar J, Ibdah M (2014) Gene silencing of CCD7 and CCD8 in Phelipanche aegyptiaca by tobacco rattle virus system retarded the parasite development on the host. Plant Signal Behav 9:e29376
Auldridge ME, Block A, Vogel JT et al (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993
Aviv D, Amsellem Z, Gressel J (2002) Transformation of carrots with mutant acetolactate synthase for Orobanche (broomrape) control. Pest Manag Sci 58:1187–1193
Bandaranayake PC, 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 22:1404–1419
Bari VK, Nassar JA, Kheredin SM et al (2019) CRISPR/Cas9-mediated mutagenesis of CAROTENOID CLEAVAGE DIOXYGENASE 8 in tomato provides resistance against the parasitic weed Phelipanche aegyptiaca. Sci Rep 9:e11438
Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84
Benfey PN, Chua NH (1989) Regulated genes in transgenic plants. Science 244:174–181
Benhod G, Losner D, Joel DM, Mayer AM (1993) Pectin methylesterase in calli and germinating-seeds of Orobanche aegyptiaca. Phytochemistry 32:1399–1402
Bouwmeester HJ, Matusova R, Sun ZK, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364
Brewer PB, Yoneyama K, Filardo F et al (2016) LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc Natl Acad Sci 113:6301–6306
Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166:1292–1297
Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550–553
Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–746
Butt H, Jamil M, Wang JY, Al-Babili S, Mahfouz M (2018) Engineering plant architecture via CRISPR/Cas9-mediated alteration of strigolactone biosynthesis. BMC Plant Biol 18:174
Cameron DD, Coats AM, Seel WE (2006) Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor. Ann Bot 98:1289–1299
Cheng X, Flokova K, Bouwmeester H, Ruyter-Spira C (2017) The role of endogenous strigolactones and their interaction with ABA during the infection process of the parasitic weed Phelipanche ramosa in tomato plants. Front Plant Sci 8:392
Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190
Cui S, Wada S, Tobimatsu Y et al (2018) Host lignin composition affects haustorium induction in the parasitic plants Phtheirospermum japonicum and Striga hermonthica. New Phytol 218:710–723
Cui S, Kubota T, Nishiyama T, Ishida JK, Shigenobu S, Shibata TF, Toyoda A, Hasebe M, Shirasu K, Yoshida S (2020) Ethylene signaling mediates host invasion by parasitic plants. Sci Adv 6:eabc2385
de Framond ARP, McMillan J, Ejeta G (2007) Effects on Striga parasitism of transgenic maize armed with RNAi constructs targeting essential S. asiatica genes. In: Ejeta G, Gressel J (eds) Integrating new technologies for Striga control: towards ending the witch-hunt. World Scientific, Singapore, pp 185–196
Delavault P, Simier P, Thoiron S, Veronesi C, Fer A, Thalouarn P (2002) Isolation of mannose 6-phosphate reductase cDNA, changes in enzyme activity and mannitol content in broomrape (Orobanche ramosa) parasitic on tomato roots. Physiol Plant 115:48–55
Dorr I, Kollmann R (1995) Symplasmic sieve element continuity between Orobanche and its host. Bot Acta 108:47–55
Dubey NK, Eizenberg H, Leibman D et al (2017) Enhanced host-parasite resistance based on down-regulation of Phelipanche aegyptiaca target genes is likely by mobile small RNA. Front Plant Sci 8:1574
Duriez P, Vautrin S, Auriac MC et al (2019) A receptor-like kinase enhances sunflower resistance to Orobanche cumana. Nat Plants 5:1211–1215
Everard JD, Cantini C, Grumet R, Plummer J, Loescher WH (1997) Molecular cloning of mannose-6-phosphate reductase and its developmental expression in celery. Plant Physiol 113:1427–1435
Fernandez-Aparicio M, Rubiales D, Bandaranayake PC, Yoder JI, Westwood JH (2011) Transformation and regeneration of the holoparasitic plant Phelipanche aegyptiaca. Plant Methods 7:36
Fernandez-Aparicio M, Flores F, Rubiales D (2016) The effect of Orobanche crenata infection severity in faba bean, field pea, and grass pea productivity. Front Plant Sci 7:1409
Fernández-Martínez JM, Domínguez J, Pérez-Vich B (2008) Update on breeding for resistance to sunflower broomrape. Helia 31:73–84
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811
Foy CL, Jain R, Jacobsohn R (1989) Recent approaches for chemical control of broomrape (Orobanche spp.). Rev Weed Sci 4:123–152
Franke AC, van den Brand GJ, Vanlauwe B, Giller KE (2018) Sustainable intensification through rotations with grain legumes in Sub-Saharan Africa: a review. Agric Ecosyst Environ 261:172–185
Frizzi A, Huang S (2010) Tapping RNA silencing pathways for plant biotechnology. Plant Biotechnol J 8:655–677
Gobena D, Shimels M, Rich PJ, Ruyter-Spira C, Bouwmeester H, Kanuganti S, Mengiste T, Ejeta G (2017) Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. Proc Natl Acad Sci 114:4471–4476
Goldwasser Y, Kleifeld Y (2004) Recent approaches to Orobanche management—a review. In: Inderjit (ed) Weed biology and management. Kluwer Academic, Dordrecht, pp 439–466
Gonzalez-Verdejo CI, Barandiaran X, Moreno MT, Cubero JI, Di Pietro A (2006) A peroxidase gene expressed during early developmental stages of the parasitic plant Orobanche ramosa. J Exp Bot 57:185–192
Hamamouch N, Westwood JH, Banner I, Cramer CL, Gepstein S, Aly R (2005) A peptide from insects protects transgenic tobacco from a parasitic weed. Transgenic Res 14:227–236
Hasegawa S, Tsutsumi T, Fukushima S et al (2018) Low infection of Phelipanche aegyptiaca in micro-tom mutants deficient in CAROTENOID CLEAVAGE DIOXYGENASE 8. Int J Mol Sci 19:2645
Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170
Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322
Jaganathan D, Ramasamy K, Sellamuthu G, Jayabalan S, Venkataraman G (2018) CRISPR for crop improvement: an update review. Front Plant Sci 9:985
Joel DM, Losnergoshen D (1994) The attachment organ of the parasitic angiosperms Orobanche cumana and O. aegyptiaca and its development. Can J Bot 72:564–574
Joel DM, Steffens JC, Matthews DE (1995) Germination of weedy root parasites. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, New York, pp 567–598
Joel DM, Gressel J, Musselman LJ (2013) Parasitic Orobanchaceae: parasitic mechanisms and control strategies. Springer Edition, Heidelberg, Germany
Johnsen HR, Striberny B, Olsen S, Vidal-Melgosa S, Fangel JU, Willats WGT, Rose JKC, Krause K (2015) Cell wall composition profiling of parasitic giant dodder (Cuscuta reflexa) and its hosts: a priori differences and induced changes. New Phytol 207:805–816
Kaiser B, Vogg G, Fürst UB, Albert M (2015) Parasitic plants of the genus Cuscuta and their interaction with susceptible and resistant host plants. Front Plant Sci 6:45
Keyes W, Taylor J, Apkarian R, Lynn D (2001) Dancing together: social controls in parasitic plant development. Plant Physiol 127:1508–1512
Kirigia D, Runo S, Alakonya A (2014) A virus-induced gene silencing (VIGS) system for functional genomics in the parasitic plant Striga hermonthica. Plant Methods 10:16
Kohlen W, Charnikhova T, Lammers M et al (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547
Koltai C, Prandi C (2019) Strigolactones: biology and applications. Springer Nature, Switzerland
Kountche BA, Jamil M, Yonli D et al (2019) Suicidal germination as a control strategy for Striga hermonthica (Benth.) in smallholder farms of sub-Saharan Africa. Plants People Planet 1:107–118
Kretzschmar T, Kohlen W, Sasse J et al (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344
Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley
Kusumoto D, Goldwasser Y, Xie X, Yoneyama K, Takeuchi Y, Yoneyama K (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
LeBlanc M, Kim G, Westwood JH (2012) RNA trafficking in parasitic plant systems. Front Plant Sci 3:203
Lechat MM, Pouvreau JB, Peron T et al (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 63:5311–5322
Letousey P, De Zelicourt A, Vieira Dos Santos C, Thoiron S, Monteau F, Simier P, Thalouarn P, Delavault P (2007) Molecular analysis of resistance mechanisms to Orobanche cumana in sunflower. Plant Pathol 56:536–546
Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691
Liang Z, Zhang K, Chen KL, Gao CX (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom 41:63–68
Libiakova D, Ruyter-Spira C, Bouwmeester HJ, Matusova R (2018) Agrobacterium rhizogenes transformed calli of the holoparasitic plant Phelipanche ramosa maintain parasitic competence. Plant Cell Tiss Org Cult 135:321–329
Lin H, Wang R, Qian Q et al (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525
Lopez-Raez JA, Bouwmeester H (2008) Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal Behav 3:963–965
Losner-Goshen D, Portnoy VH, Mayer AM, Joel DM (1998) Pectolytic activity by the haustorium of the parasitic plant Orobanche L. (Orobanchaceae) in host roots. Ann Bot 81:319–326
Ma X, Zhu Q, Chen Y, Liu YG (2016) CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Mol Plant 9:961–974
Mansoor S, Amin I, Hussain M, Zafar Y, Briddon RW (2006) Engineering novel traits in plants through RNA interference. Trends Plant Sci 11:559–565
Martin-Pizarro C, Pose D (2018) Genome editing as a tool for fruit ripening manipulation. Front Plant Sci 9:1415
Matvienko M, Torres MJ, Yoder JI (2001) Transcriptional responses in the hemiparasitic plant Triphysaria versicolor to host plant signals. Plant Physiol 127:272–282
Mutuku JM, Cui S, Yoshida S, Shirasu K (2020) Orobanchaceae parasite–host interactions. New Phytol. https://doi.org/10.1111/nph.17083
Nandula VK, Foy CL, Orcutt DM (1999) Glyphosate for Orobanche aegyptiaca control in Vicia sativa and Brassica napus. Weed Sci 47:486–491
Nandula VK, Foster JG, Foy CL (2000) Impact of Egyptian broomrape (Orobanche aegyptiaca (Pers.) parasitism on amino acid composition of carrot (Daucus carota L.). J Agric Food Chem 48:3930–3934
Palauqui JC, Elmayan T, Pollien JM, Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–4745
Palmer AG, Gao R, Maresh J, Erbil WK, Lynn DG (2004) Chemical biology of multi-host/pathogen interactions: chemical perception and metabolic complementation. Annu Rev Phytopathol 42:439–464
Perez-de-Luque A, Gonzalez-Verdejo CI, Lozano MD et al (2006) Protein cross-linking, peroxidase and beta-1,3-endoglucanase involved in resistance of pea against Orobanche crenata. J Exp Bot 57:1461–1469
Perez-de-Luque A, Fondevilla S, Perez-Vich B et al (2009) Understanding Orobanche and Phelipanche–host plant interactions and developing resistance. Weed Res 49:8–22
Ransom J, Kanampiu F, Gressel J, De Groote H, Burnet M, Odhiambo G (2012) Herbicides applied to the seed of imidazolinone-resistant maize as a Striga control option for small-scale African farmers. Weed Sci 60:283–289
Rasmussen A, Mason MG, de Cuyper C et al (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158:1976–1987
Rubiales D, Perez-De-Luque A, Fernandez-Aparicio M et al (2006) Screening techniques and sources of resistance against parasitic weeds in grain legumes. Euphytica 147:187–199
Runyon JB, Mescher MC, Felton GW, De Moraes CM (2010) Parasitism by Cuscuta pentagona sequentially induces JA and SA defence pathways in tomato. Plant Cell Environ 33:290–303
Schneeweiss GM, Colwell A, Park JM, Jang CG, Stuessy TF (2004) Phylogeny of holoparasitic Orobanche (Orobanchaceae) inferred from nuclear ITS sequences. Mol Phylogenet Evol 30:465–478
Senseman SA (2007) Herbicide handbook. KS, Weed Weed Science Society of America, Lawrence, p 458
Singh A, Singh M (1993) Cell-wall degrading enzymes in Orobanche aegyptiaca and its host Brassica campestris. Physiol Plant 89:177–181
Slavov S, Valkov V, Batchvarova R, Atanassova S, Alexandrova M, Atanassov A (2005) Chlorsulfuron resistant transgenic tobacco as a tool for broomrape control. Transgenic Res 14:273–278
Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67
Surov T, Aviv D, Aly R, Joel DM, Goldman-Guez T, Gressel J (1998) Generation of transgenic asulam-resistant potatoes to facilitate eradication of parasitic broomrapes (Orobanche spp.), with the sul gene as the selectable marker. Theor Appl Genet 96:132–137
Tomilov AA, Tomilova NB, Wroblewski T, Michelmore R, Yoder JI (2008) Trans-specific gene silencing between host and parasitic plants. Plant J 56:389–397
Trusov Y, Botella JR (2006) Silencing of the ACC synthase gene ACACS2 causes delayed flowering in pineapple [Ananas comosus (L.) Merr.]. J Exp Bot 57:3953–4396
Uraguchi D, Kuwata K, Hijikata Y et al (2018) A femtomolar-range suicide germination stimulant for the parasitic plant Striga hermonthica. Science 6420:1301–1305
Vogel JT, Walter MH, Giavalisco P et al (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311
Wada S, Cui S, Yoshida S (2019) Reactive oxygen species (ROS) generation is indispensable for haustorium formation of the root parasitic plant Striga hermonthica. Front Plant Sci 10:328
Wakabayashi T, Hamana M, Mori A et al (2019) Direct conversion of carlactonoic acid to orobanchol by cytochrome P450 CYP722C in strigolactone biosynthesis. Sci Adv 5:eaax9067
Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J-L (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951
Westwood JH, Yu X, Foy CL, Cramer CL (1998) Expression of a defense-related 3-hydroxy-3-methylglutaryl CoA reductase gene in response to parasitization by Orobanche spp. Mol Plant Microbe Interact 11:530–536
Westwood JH, Yoder JI, Timko MP, Depamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235
Westwood JH, Depamphilis CW, Das M et al (2012) The parasitic plant genome project: new tools for understanding the biology of Orobanche and Striga. Weed Sci 60:295–306
Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117
Yang Z, Wafula EK, Honaas LA et al (2015) Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol Biol Evol 32:767–790
Yao R, Ming Z, Yan L et al (2016) DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536:469–473
Yoder JI (1999) Parasitic plant responses to host plant signals: a model for subterranean plant-plant interactions. Curr Opin Plant Biol 2:65–70
Yoder JI, Gunathilake P, Wu B, Tomilova N, Tomilov AA (2009) Engineering host resistance against parasitic weeds with RNA interference. Pest Manag Sci 65:460–466
Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ (2004) A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000
Yoshida S, Cui S, Ichihashi Y, Shirasu K (2016) The haustorium, a specialized invasive organ in parasitic plants. Annu Rev Plant Biol 67:643–667
Zhao B, Wu TT, Ma SS, Jiang DJ, Bie XM, Sui N, Zhang XS, Wang F (2019) TaD27-B gene controls the tiller number in hexaploid wheat. Plant Biotechnol J 18:513–525
Acknowledgements
The authors thank Jonathan Gressel and Harry S. Paris for their valuable comments. Vinay Kumar Bari is grateful to the ARO—Volcani Center, Israel Ministry of Agriculture, for providing a postdoctoral fellowship.
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Aly, R., Matzrafi, M. & Bari, V.K. Using biotechnological approaches to develop crop resistance to root parasitic weeds. Planta 253, 97 (2021). https://doi.org/10.1007/s00425-021-03616-1
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DOI: https://doi.org/10.1007/s00425-021-03616-1