31, 285289. 58, 11871193. Resistance and avoidance against Orobanche crenata in pea (Pisum spp.) (2007a). Variability of interactions between barrel medic (Medicago truncatula) genotypes and Orobanche species. Phytopathol. Kuijt, J. A. S. Lpez, E. I. Martnez, T. R. Blas, M. C. Lpez, and J. P. Sestelo (A Corua: Dario Prada-Rodrguez of University of A Corua), 688. 38, 343349. Res. B., Thoiron, S., Leduc, N., et al. 58, 29022907. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. (1999). However, it is a long-term strategy due to the long viability of seed bank (Rubiales et al., 2009b), which requires at least a nine-course rotation in order to prevent broomrape seed bank increases (Grenz et al., 2005). Germination response of Orobanche seeds subjected to conditioning temperature, water potential and growth regulator treatments. Hot air temperature and clear skies are required during the solarization period. Plant Prot. This approach would inhibit parasitism by killing the young seedling before it attaches to the host root. MF-A wrote the paper. (1996). Mol. This would open the work on parasitism toward more community ecology and what can be considered the realistic nature of parasitism. 2018 Aug;102(8):1477-1488. doi: 10.1094/PDIS-01-18-0020-FE. Sholmer-Ilan, A. Paris: Mmoires du Museum dHistoire Naturelle, 261273. Therefore, decisions on the date of sowing has to be well-adjusted in order to balance the loss of productivity due to shorter growing period with gain of productivity due to reduced parasitism. 8600 Rockville Pike 14, 227236. Effects of environment and sowing date on the competition between faba bean (Vicia faba) and the parasitic weed Orobanche crenata. There have been some known cases in the Sacramento Valley, but I think its more than reported, Hanson said. (2013). Until now, difficulties of purification at industrial scale have hampered the field experimentation with such metabolites (Vurro et al., 2009) despite their interesting potential. (2010). In addition, some modifications of host biochemistry have been described in tolerant crops inducing low performance of the parasite when attached. Resistance of red clover (Trifolium pratense) to the root parasitic plant Orobanche minor is activated by salicylate but not by jasmonate. In recent years, a new, aggressive race designated as race F (called biotype D in Russia) has . Dev. doi: 10.1038/nature07272, USEPA (2004). Ecological aspects of nitrogen assimilation. The parasitic plant genome project: new tools for understanding the biology of Orobanche and Striga. Accumulation of ammonium can be toxic to plants and its detoxification occurs via incorporation into organic compounds. Tetrahedron Lett. J. Agric. and their current disposition. Effect of fungal and plant metabolites on broomrapes (Orobanche and Phelipanche spp.) Foy, C. L., Jain, R., and Jacobsohn, R. (1989). With target-site resistance, the herbicide translocates unmetabolised to the underground broomrape via the haustorium inflicting its suppressive action in the parasite (Gressel, 2009). Bot. An official website of the United States government. Food Chem. Ecological of weed seed size and persistence in the soil under different tilling systems: implications for weed management. It allows the parasite to quickly start tapping carbohydrates, amino acids, and organic acids from its host (Drr and Kollmann, 1995; Nandula et al., 2000; Abbes et al., 2009). Bioinspired chitinous material solutions for environmental sustainability and medicine. Imazamox application timing for small broomrape (Orobanche minor) control in red clover. doi: 10.4236/ajps.2015.68120. Resistance in AB-VL-8 is . In addition, their mixed traits of weed and underground pathogen, make their control tricky. This gene remains silenced during conditioning phase and its activation occurs mediated by host-encoded germination stimulants, i.e., strigolactones, only after the conditioning phase is complete. Because the haustorial organ in broomrape radicle is terminal and its growth is not resumed unless it can immediately penetrate the host, cessation of radicle elongation and haustorial induction in the absence of a host is lethal to the parasite. (2010). Expression of a defense-related 3-hydroxy-3-methylglutaryl CoA reductase gene in response to parasitism by Orobanche spp. (1995). Biochem. Transgenic Res. in Mediterranean agriculture. Ghersa, C. M., and Martinez-Ghersa, M. A. known genetic relationship between HA-267, LIV-10, LIV-17, and AB-VL-8. doi: 10.1093/jxb/50.331.211, Kebreab, E., and Murdoch, A. J. The apical cells in the radicle apex develop into intrusive cells, which successively invade host root cortex, endodermis, and the central cylinder. Post-germination development in broomrape could be probably regulated by their own broomrape-encoded strigolactones as it occurs in the close related parasite Striga hermonthica or in non-parasitic plants (Liu et al., 2014; Das et al., 2015). The efficient action of the biological control agent will depend on its ability to remain active over a large range of ecological conditions (Aly, 2007). not been previously reported. Sci. FIGURE 2. and other fungi as biological control agents of broomrape (Orobanche ramosa). Biotic inducers of systemic resistance have also proved being successful against broomrape parasitism under experimental conditions. Weed Sci. Persistence of GR7 and Striga germination stimulant(s) from Euphorbia aegyptiaca Boiss. 25, 402411. doi: 10.1016/S0031-9422(00)90779-9, Bar-Nun, N., and Mayer, A. M. (2002). broomrape and bursage relationship. The model was developed in greenhouse studies and validated in the field during three growing seasons. Lpez-Granados, F., and Garca-Torres, L. (1996). In addition it also varies considerably in crops growing under different physiological status, growth stages and growing seasons, allowing broomrape to synchronize its germination with physiologically suitable hosts (Lpez-Granados and Garca-Torres, 1996; Yoneyama et al., 2007a,b; Fernndez-Aparicio et al., 2009b, 2014; Xie et al., 2010). doi: 10.1046/j.1365-3040.1999.00462.x, Hiraoka, Y., Ueda, H., and Sugimoto, Y. Although broomrape pre-vascular connections benefits from host nutrients, the growth of broomrape in its way toward vascular cylinder is mainly sustained by consumption of seed reserves (Aber et al., 1983; Joel and Losner-Goshen, 1994; Joel, 2000). Chlorsulfuron resistant transgenic tobacco as a tool for broomrape control. Although the effect of jasmonic-acid-dependent induced systemic resistance (ISR) against parasitic plants is less clear (Kusumoto et al., 2007; Hiraoka et al., 2009; Yoder and Scholes, 2010), strains of Pseudomonas sp. A reduced content of broomrape germination-inducing factors in root exudates of mycorrhizal plants has been demonstrated (Lpez-Rez et al., 2011). Due to their physical and metabolic overlap with the crop, their underground parasitism, their achlorophyllous nature, and hardly destructible seed bank, broomrape weeds are usually not controlled by management strategies designed for non-parasitic weeds. doi: 10.1002/ps.1738. buca di bacco meaning. This kind of resistance is more interesting than other mechanisms of resistance that usually involve translocation and enhanced metabolism, resulting in lower herbicide concentration in the sap of the host plant. Proceedings of the International Workshop on Orobanche Research, eds K. Wegmann and L. J. Musselman (Obermarchtal, FRG: Eberhard Karls Universitt), 147156. Preventing the movement of parasitic seeds from infested to non-infested agricultural fields, by contaminated machinery or seed lots, is crucial (Panetta and Lawes, 2005). doi: 10.1093/jxb/erv119, Lechat, M. M., Pouvreau, J. Flavonoids promote haustoria formation in the root parasite Triphysaria versicolor. Musselman, L. J. doi: 10.1111/nph.12692, Logan, D., and Stewart, G. R. (1995). Researchers are conducting the germination studies to develop a model for the right application time in the UC Davis Contained Research Facility, which is designed to prevent escape of the weed. doi: 10.3732/ajb.93.7.1039, Berner, D. K., Schaad, N. W., and Volksch, B. J. Agric. B., Pouponneau, K., Yoneyama, K., Montiel, G., Le Bizec, B., et al. (2009). Westwood, J. H., dePamphilis, C. W., Das, M., Fernndez-Aparicio, M., Honaas, L. A., Timko, M. P., et al. Sauerborn, J. A novel metabolite, ryecyanatine-A recently isolated from rye (Secale cereale L.), presents potential for broomrape control by promoting rapid cessation of broomrape radicle growth and therefore inhibiting its ability to reach the host. (2009). This site needs JavaScript to work properly. Mller-Stver, D., Buschmann, H., and Sauerborn, J. inducers of ISR (Gozzo, 2003) and commercially available as Proradix can reduce broomrape parasitism by 80% in susceptible cultivars of hemp and tobacco without phytotoxic effect on the crop (Gonsior et al., 2004). Plant Growth Regul. Inhibition of shoot branching by new terpenoid plant hormones. doi: 10.1139/b94-075, Joel, D. M., and Portnoy, V. H. (1998). Pectolytic activity by the haustorium of the parasitic plant Orobanche L. (Orobanchaceae) in host roots. Sauerborn, J., Linke, K. H., Saxena, M. C., and Koch, W. (1989). Bethesda, MD 20894, Web Policies Curr. Appl. Signalling organogenesis in parasitic angiosperms: xenognosin generation, perception, and response. This parasitic weed, unable to produce its own chlorophyll, survives only by attaching to the roots of a host plant, often with severe consequences. We are trying to predict the timing of germination of broomrape based on the soil temperature and moisture, Mesgaran said. Crop Sci. Abbes Z., Kharrat M., Pouvreau J. Control 2, 291296. Eizenberg, H., Aly, R., and Cohen, Y. The presence of strigolactone biosynthetic system in broomrapes raises the question on how the parasite performs diversified stimulant recognition in order to set the timing of germination. The site is secure. Biological traits in broomrape such as achlorophyllous nature, underground parasitism, the physical connection and growth synchronization with the crop, and the exclusive uptake of resources via crop vascular system rather than from the soil make broomrape control a challenging agricultural task. doi: 10.1016/j.tetlet.2009.09.142, Fernandez, J., and Ingber, D. (2013). The best studied group of germination-inducing factors are strigolactones, a group of terpenoid lactones. 93, 300313. seedbank by soil solarization and organic supplementation. 28 Articles, This article is part of the Research Topic, Specialized Mechanisms in Broomrape Weeds for a Parasitic Mode of Life, Control Strategies Targeting Underground Broomrape Stages, http://www.terresinovia.fr/orobanche/carte.php, www.fao.org/ag/AGP/AGPP/IPM/Weeds/Issues/orobanche.htm, www.epa.gov/opprd001/inerts_list4Bname.pdf, Creative Commons Attribution License (CC BY). Adv. The seedling absorbs water both from the soil and from the seed endothelium, the later ensuring radicle development even in dry soil (Joel et al., 2012). 65, 492496. broomrape and bursage relationship. Each broomrape species show specificity not only for root exudates in order to germinate but also for host species to invade and feed on, being the germination-stimulatory range usually broader than the actual host range (Fernndez-Aparicio et al., 2009b). 112, 297308. The flowers are irregularly shaped and produce single-chambered capsules that contain numerous minute seeds. *Correspondence: Mnica Fernndez-Aparicio, monica.fernandez@dijon.inra.fr, View all
This work was cofunded by the European Union and INRA, in the framework of the Marie-Curie FP7 COFUND People Program, through the award of an AgreenSkills fellowship (under grant agreement n PCOFUND-GA-2010-267196) to MF-A with additional support by the INRA Division Sant des Plantes et Environnement., Abbasher, A. Sources of natural resistance based on reduced release of haustorium-inducing factors is a doubly interesting strategy to inhibit broomrape parasitism because not only it prevents broomrape parasitism in the current crop, but also it promotes the demise of the seed bank by promoting suicidal germination. Rhizobium leguminosarum induces defense mechanisms based on elevated induction of the phenylpropanoid pathway conferring mechanical and chemical barriers to the parasite penetration (Mabrouk et al., 2007a,b,c, 2010). Besides the effects of fertilization management on pre-attached broomrape stages described in previous sections, high soil fertility can induce crops to endure broomrape parasitism by helping the host to maintain a favorable osmotic potential that reduces the parasitic sink strength (Gworgwor and Weber, 1991). Food Chem. However, selecting for high phenolic varieties is likely to induce many other side changes altering agronomic performance. Epub 2018 Jul 3. Please also list any non-financial associations or . Bot. Original article from AgAlert, California Farm Bureau Federation.). Broomrapes produce little or no chlorophyll; instead, they draw nourishment from the roots of other plants by means of small suckers called haustoria. Symbiosis 15, 6170. Host plant resistance to parasitic weeds; recent progress and bottlenecks. Please refer to the appropriate style manual or other sources if you have any questions. J. Nematol. doi: 10.1093/jxb/err246, Fernndez-Aparicio, M., Sillero, J. C., and Rubiales, D. (2007). doi: 10.1006/anbo.1996.0385, Drr, I., and Kollmann, R. (1995). doi: 10.1111/j.0031-9317.2004.0243.x, Cimmino, A., Fernandez-Aparicio, M., Andolfi, A., Basso, S., Rubiales, D., and Evidente, A. As a nurse plant, the bursage provides protection from hungry animals, shade from the relentless sun and additional nutrients and water that collect under the plant. The metabolic activity of the seed conditioning in broomrape has been characterized in terms of patterns of respiration, synthesis and turnover of proteins, metabolism of nitrogen, carbohydrates and lipids and hormonal balance. doi: 10.1002/ps.1706, Keywords: integrated pest management, Orobanche, Phelipanche, parasitism, germination, haustorium, plant recognition, seed bank, Citation: Fernndez-Aparicio M, Reboud X and Gibot-Leclerc S (2016) Broomrape Weeds. 10.1016/1049-9644(92)90021-5 (2007). Prez-de-Luque, A., Fondevilla, S., Prez-Vich, B., Aly, R., Thoiron, S., Simier, P., et al. TABLE 1. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). Host specificity in broomrape species is usually indirectly related to the predictability of nutritive resources. The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. Mol. Control strategies designed for non-parasitic weeds such as cultural and chemical methods do not necessarily achieve the required level of control for broomrape due to its mixed traits as weed and as root parasite. Bandaranayake, P. C. G., and Yoder, J. I. 1, 139146. Although hard seed coat has been described as dormancy mechanism in newly formed broomrape seeds (Lpez-Granados and Garca-Torres, 1996), water uptake and imbibition are performed quickly by mature seeds through the micropyle without the need of scarification (Bar-Nun and Mayer, 1993; Joel et al., 2012). 11, 240246. doi: 10.1111/j.1365-3180.2007.00583.x, Mabrouk, Y., Zourgui, L., Sifi, B., Delavault, P., Simier, P., and Belhadj, O. doi: 10.1002/ps.993, Tank, D. C., Beardsley, P. M., Kelchner, S. A., and Olmstead, R. G. (2006). Weed Res. Purification of pectin methylesterase from Orobanche aegyptiaca. MeSH 3rd class relic of the true cross. Sci. -, Abbes Z., Kharrat M., Delavault P., Chabi W., Simier P. (2009). operate at different developmental stages of the parasite. doi: 10.1614/WS-06-135, Evidente, A., Cimmino, A., Fernndez-Aparicio, M., Andolfi, A., Rubiales, D., and Motta, A. Exogenous amino acids inhibit seed germination and tubercle formation by Orobanche ramosa (broomrape): potential application for management of parasitic weeds. Pest Manag. (2012). Delayed sowing date is a traditional method that can show high degree of success on inhibiting parasitism if implemented correctly (Lpez-Granados and Garca-Torres, 1996; Rubiales et al., 2003a; Prez-de-Luque et al., 2004; Grenz et al., 2005). Mater. Breeding for broomrape resistance stands out as the most economic, easy to adopt and environmentally friendly practice. Parasitic Weeds of the World: Biology and Control. Effects of environmental factors on dormancy and germination of crenate broomrape (Orobanche crenata). Striga seed avoidance by deep planting and no-tillage in sorghum and maize. Westwood, J. H., Yu, X., Foy, C. L., and Cramer, C. L. (1998). Plant 43, 304317. Plant Cell Environ. doi: 10.1007/s00425-006-0410-1, Zehhar, N., Ingouff, M., Bouya, D., and Fer, A. When resistant crops impose barriers to stop the parasitic development at this stage, broomrape exhausts and parasitism is quickly aborted. Solar heating (solarization) control of soilborne pests. The concept of trap crops refers to the cultivation of crop species whose root exudates exhibit high germination-inducing activity on broomrape seeds, but these species do not become infected because they are resistant to later stages of the parasitic process indirectly leading to the killing of the young broomrape seedlings due to the lack of proper host. Possibilities of biological control of Orobanche crenata and O. cumana with Ulocladium botrytis and Fusarium oxysporum f. sp. Orobanche crenata in UK- an update. Ilustration of broomrape life stages and mechanisms of control. doi: 10.1560/ETEL-C34X-Y6MG-YT0M, Veronesi, C., Bonnin, E., Calvez, S., Thalouarn, P., and Simier, P. (2007). Control 28, 110. Evaluation of Fusarium spp. 60, 316323. (2001). Among the reviewed strategies are those aimed (1) to reduce broomrape seed bank viability, such as fumigation, herbigation, solarization and use of broomrape-specific pathogens; (2) diversion strategies to reduce the broomrape ability to timely detect the host such as those based on promotion of suicidal germination, on introduction of allelochemical interference, or on down-regulating host exudation of germination-inducing factors; (3) strategies to inhibit the capacity of the broomrape seedling to penetrate the crop and connect with the vascular system, such as biotic or abiotic inhibition of broomrape radicle growth and crop resistance to broomrape penetration either natural, genetically engineered or elicited by biotic- or abiotic-resistance-inducing agents; and (4) strategies acting once broomrape seedling has bridged its vascular system with that of the host, aimed to impede or to endure the parasitic sink such as those based on the delivery of herbicides via haustoria, use of resistant or tolerant varieties and implementation of cultural practices improving crop competitiveness. Once broomrape germination has occurred, chemicals that reduce the growth of broomrape radicle reduce the chances of reaching the host and therefore parasitism. As the tubercle matures a crown of adventitious roots will emerge from this tubercle carrying capacity of developing lateral haustorial connections. (2006). 28, 16. Vaucher, J. P. (1823). Afr. (2009a). doi: 10.1017/S001447970100401X. For each broomrape-crop association, broomrape germination potential is defined by the combination of both, the stimulatory capability of crop root exudates and the sensitivity of parasitic receptors to recognize specific forms of germination-inducing factors (Fernndez-Aparicio et al., 2008a, 2009b, 2011). Their absolute dependence on host-derived nutritive resources for successful seedling establishment and consequent growth makes necessary the synchronization of parasitic germination with the growth of its host. Instead, broomrapes are in current state of intensification and spread due to lack of broomrape-specific control programs, unconscious introduction to new areas and may be decline of herbicide use and global warming to a lesser degree. doi: 10.1023/B:GROW.0000038242.77309.73, Goldwasser, Y., Kleifeld, Y., Golan, S., Bargutti, A., and Rubin, B. doi: 10.1614/WS-07-049.1, Liu, Q., Zhang, Y., Matusova, R., Charnikhova, T., Amini, M., Jamil, M., et al. Nutrients influence the crop-parasite pre-attached interaction in several ways. Plant Growth Regul. Structure and function of natural and synthetic signaling molecules in parasitic weed germination. Depending on the genetic background of the resistant host, the intrusive cells of broomrape seedling can be stopped at three different levels in their way of penetration through the root layers to achieve connection with the host vascular system. Sci. Plant Sci. Available at: www.fao.org/ag/AGP/AGPP/IPM/Weeds/Issues/orobanche.htm, Acharya, B. D., Khattri, B. G., Chettri, M. K., and Srivastava, X. Orobanche crenata in Ethiopia. Thidiazuron stimulates germination and ethylene production in Striga hermonthica comparison with the effects of GR24, ethylene and 1-aminocyclopropane-1-carboxylic acid. J. Eur. The regulatory consequences of having this quarantine pest discovered are so draconian there may be a temptation to keep the finding secret, Hanson said. (1991). Broomrape seed has been documented to last in the soil for at . (2005). Weed Res. Agron. 43, 6371. If this works, it will be easy to implement through the fertilizer system.. (2013). Weed Res. (2009). This treatment in the lab mimics the soil conditions in climatically suitable regions for broomrape such as Mediterranean non-irrigated agrosystems where the onset of warm and wet season coincides with the growth of juvenile stages of many annual crops (Lpez-Granados and Garca-Torres, 1996; Grenz and Sauerborn, 2007). Rubiales, D., Alcntara, C., Prez-de-Luque, A., Gil, J., and Sillero, J. C. (2003a). "Broomrape is easily spread by equipment, boots and water," he said. Crop Prot. Bot. Plant J. doi: 10.2478/jppr-2014-0023, Hearne, S. J. Joel, D. M. (2000). A swelling of the host root at the penetration point is also observed due the parasitic stimulation of host tissue proliferation; (G) tubercle develops a crown of adventicious roots; (H) tubercle differentiates apical shoot meristem (single shoot meristem for Orobanche species and several shoot meristems for Phelipanche species); (I) the underground shoot eventually emerges through the root surface; (J) flowering and pollination occur. Wallingford: CAB International. doi: 10.1111/j.1365-3180.1996.tb01669.x. (2009). Imidazolinone-tolerant crops: history, current status and future. doi: 10.1021/jf504609w, Cimmino, A., Fernandez-Aparicio, M., Avolio, F., Andolfi, A., Rubiales, D., Yoneyama, K., et al. The differentiation of xylem elements in the parasite are under the control of polar auxin transport (Harb et al., 2004; Bar-Nun et al., 2008). 13, 478484. Fertilization can induce soil suppressiveness to initiation of broomrape parasitism. The reduction of ABA:GA ratio induced by stratification (conditioning) is enough to break dormancy and promote germination in dormant seeds of non-parasitic weeds but it is not enough for broomrape, which requires a further decrease in ABA levels induced by the activation of the ABA catabolic gene PrCYP707A1 (Lechat et al., 2012). The timing of germination is the most crucial event that obligated parasitic plants face along their life cycle (Figure 2C). The development of the solutions has usually not been conducted to their end so that many potential ways of controlling broomrape are not on the market. Annu. The points of vulnerability of some underground events, key for their parasitism such as crop-induced germination or haustorial development are reviewed as inhibition targets of the broomrape-crop association.