Abstract
Phelipanche ramosa is a weed holoparasite which became a major agronomic problem for several crops in France. The yield and quality losses may be complete and lead to the abandonment of crops in the most infested fields. Chemical weed control using synthetic herbicides does not have a direct effect on this weed because the first half of its reproductive cycle occurs on the root system of its host. The aim of this study is to contribute to the definition of an integrated weed management program of P. ramosa, especially focusing on the use of the possible direct effect of amino acids on seed of broomrapes as a potential biocontrol solution. We studied a set of 14 amino acids in in vitro conditions to investigate whether some amino acids can have an inhibitory effect on the germination of the P. ramosa seeds, whether this effect may be permanent after the removal of the amino acid, and whether some amino acids can cause a high dormancy or seed mortality rate. Our main results showed (1) a strong inhibitory effect of four amino acids on the seed germination concerning arginine, lysine, phenylalanine and tryptophan, and (2) that this effect appeared temporary for arginine and lysine, but permanent for phenylalanine and tryptophan. Our study thus highlighted the interest of phenylalanine and tryptophan as they caused both high inhibition of germination and high seed mortality of P. ramosa. Based on these results, we suggest three options for the use of these amino acids that could provide concrete answers to farmers.
Similar content being viewed by others
Data availability
The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Alila S, Boufi S (2009) Removal of organic pollutants from water by modified cellulose fibres. Ind Crops Prod 30:93–104. https://doi.org/10.1016/j.indcrop.2009.02.005
Auger B, Pouvreau JB, Pouponneau K, Yoneyama K, Montiel G, Le Bizec B, Yoneyama K, Delavault P, Delourme R, Simier P (2012) Germination stimulants of Phelipanche ramosa in the rhizosphere of Brassica napus are derived from the glucosinolate pathway. Mol Plant-Microbe Interact 25:993–1004. https://doi.org/10.1094/MPMI-01-12-0006-R
Boari A, Vurro M (2004) Evaluation of Fusarium spp. and other fungi as biological control agents of broomrape (Orobanche ramosa). Biol Control 30:212–219. https://doi.org/10.1016/j.biocontrol.2003.12.003
Bourguet D, Guillemaud T (2016) The hidden and external costs of pesticide use. In: Lichtfouse E (ed) Sustainable agriculture reviews. Springer, Berlin, pp 35–120
Brault M, Betsou F, Jeune B, Tuquet C, Sallé G (2007) Variability of Orobanche ramosa populations in France as revealed by cross infestations and molecular markers. Environm Exp Bot 61:272–280. https://doi.org/10.1016/j.envexpbot.2007.06.009
Cimmino A, Masi M, Rubiales D, Evidente A, Fernández-Aparicio M (2018) Allelopathy for parasitic plant management. Nat Prod Commun 13:289–294. https://doi.org/10.1177/1934578X1801300307
Cordeau S, Triolet M, Wayman S, Steinberg C, Guillemin JP (2016) Bioherbicides: dead in the water? A review of the existing products for integrated weed management. Crop Prot 87:44–49. https://doi.org/10.1016/j.cropro.2016.04.016
Dor E, Galili S, Smirnov E, Hacham Y, Amir R, Hershenhorn J (2017) The effects of herbicides targeting aromatic and branched chain amino acid biosynthesis support the presence of functional pathways in broomrape. Front Plant Sci 8:707. https://doi.org/10.3389/fpls.2017.00707
Duru M, Therond O, Martin G, Martin-Clouaire R, Magne MA, Justes E, Journet EP, Aubertot JN, Savary S, Bergez JE, Sarthou JP (2015) How to implement biodiversity-based agriculture to enhance ecosystem services: a review. Agron Sustain Dev 35:1259–1281. https://doi.org/10.1007/s13593-015-0306-1
Fernández-Aparicio M, Sillero JC, Rubiales D (2007) Intercropping with cereals reduces infection by Orobanche crenata in legumes. Crop Prot 26:1166–1172. https://doi.org/10.1016/j.cropro.2006.10.012
Fernández-Aparicio M, Emeran AA, Rubiales D (2010) Inter-cropping with berseem clover (Trifolium alexandrinum) reduces infection by Orobanche crenata in legumes. Crop Prot 29:867–871. https://doi.org/10.1016/j.cropro.2010.03.004
Fernández-Aparicio M, Yoneyama K, Rubiales D (2011) The role of strigolactones in host specificity of Orobanche and Phelipanche seed germination. Seed Sci Res 21:55–61. https://doi.org/10.1017/S0960258510000371
Fernández-Aparicio M, Reboud X, Gibot-Leclerc S (2016) Broomrape weeds. Underground mechanisms of parasitism and associated strategies for their control: a review. Front Plant Sci 7:135. https://doi.org/10.3389/fpls.2016.00135
Fernández-Aparicio M, Bernard A, Falchetto L, Marget P, Chauvel B, Steinberg C, Morris CE, Gibot-Leclerc S, Boari A, Vurro M, Bohan DA, Sands DC, Reboud X (2017) Investigation of amino acids as herbicides for control of Orobanche minor parasitism in red clover. Front Plant Sci 8:842. https://doi.org/10.3389/fpls.2017.00842
Fernández-Aparicio M, Delavault P, Timko MP (2020) Management of infection by parasitic weeds: a review. Plants 9:1184. https://doi.org/10.3390/plants9091184
Fernández-Pérez M, Garrido-Herrera FJ, Gonzalez-Pradas E (2011) Alginate and lignin-based formulations to control pesticides leaching in a calcareous soil. J Hazard Mater 190:794–801. https://doi.org/10.1016/j.jhazmat.2011.03.118
Flores-Cespedes F, Villafranca-Sanchez M, Perez-Gracia S, Fernandez-Perez M (2007) Modifying sorbents in controlled release formulations to prevent herbicides pollution. Chemosphere 69:785–794. https://doi.org/10.1016/j.chemosphere.2007.05.005
Gaba S, Perronne R, Fried G, Gardarin A, Bretagnolle F, Biju-Duval L, Colbach N, Cordeau S, Gauvrit C, Gibot-Leclerc S, Guillemin JP, Moreau D, Munier-Jolain N, Strbik F, Reboud X (2017) Response and effect traits of arable weeds in agro-ecosystems: a review of current knowledge. Weed Res 57:123–147. https://doi.org/10.1111/wre.12245
Galili G, Amir R, Fernie AR (2016) The regulation of essential amino acid synthesis and accumulation in plants. Annu Rev Plant Biol 67:153–178. https://doi.org/10.1146/annurev-arplant-043015-112213
Gibot-Leclerc S, Brault M, Pinochet X, Sallé G (2003) Potential role of winter rape weeds in the extension of broomrape in Poitou-Charentes. CR Biol 326:645–658. https://doi.org/10.1016/S1631-0691(03)00169-0
Gibot-Leclerc S, Corbineau F, Sallé G, Côme D (2004) Responsiveness of Orobanche ramosa L. seeds to GR 24 as related to temperature, oxygen availability and water potential during preconditioning and subsequent germination. Plant Growth Regul 43:63–71. https://doi.org/10.1023/B:GROW.0000038242.77309.73
Gibot-Leclerc S, Sallé G, Reboud X, Moreau D (2012) What are the traits of Phelipanche ramosa (L.) Pomel that contribute to the success of its biological cycle on its host Brassica napus L.? Flora 207:512–521. https://doi.org/10.1016/j.flora.2012.06.011
Gibot-Leclerc S, Perronne R, Dessaint F, Reibel C, Le Corre V (2016) Assessment of phylogenetic signal in the germination ability of Phelipanche ramosa on Brassicaceae hosts. Weed Res 56:452–461. https://doi.org/10.1111/wre.12222
Gibot-Leclerc S, Connault M, Perronne R, Dessaint F (2021) Differences in seed germination response of two populations of Phelipanche ramosa (L.) Pomel. to a set of GR24 concentrations and durations of stimulation. Seed Sci Res 31:243–248. https://doi.org/10.1017/S0960258521000143
Gibot-Leclerc S, Guinchard L, Edel-Hermann V, Dessaint F, Cartry D, Reibel C, Gautheron N, Bernaud E, Steinberg C (2022) Screening for potential mycoherbicides within the endophyte community of Phelipanche ramosa parasitizing tobacco. FEMS Microbiol Ecol 98:1–16. https://doi.org/10.1093/femsec/fiac024
Hemmati R, Gholizadeh R (2019) Talaromyces trachyspermus a potential biocontrol agent for branched broomrape (Orobanche ramosa). Australasian Plant Pathol 48:217–219. https://doi.org/10.1007/s13313-019-0620-1
Joel DM (2009) The new nomenclature of Orobanche and Phelipanche. Weed Res 49:6–7. https://doi.org/10.1111/j.1365-3180.2009.00748.x
Julio E, Malpica A, Cotucheau J, Bachet S, Volpatti R, Dorlhac de Borne F (2020) RNA-Seq analysis of Orobanche resistance in Nicotiana tabacum: development of molecular markers for breeding recessive tolerance from ‘Wika’ tobacco variety. Euphytica 216:6. https://doi.org/10.1007/s10681-019-2544-9
Kato-Noguchi H, Mizutani J, Hasegawa K (1994) Allelopathy of oats. II. Allelochemical effect of L-tryptophan and its concentration in oat root exudates. J Chem Ecol 20:315–319. https://doi.org/10.1007/BF02064440
Kuruma M, Suzuki T, Seto Y (2021) Tryptophan derivatives regulate the seed germination and radicle growth of a root parasitic plant, Orobanche minor. Bioorganic Med Chem Lett 43:128085. https://doi.org/10.1016/j.bmcl.2021.128085
Loyce C, Meynard JM, Bouchard C, Rolland B, Lonnet P, Bataillon P, Bernicot MH, Bonnefoy M, Charrier X, Debote B, Demarquet T, Duperrier B, Félix I, Heddadj D, Leblanc O, Leleu M, Mangin P, Méausoone M, Doussinault G (2012) Growing winter wheat cultivars under different management intensities in France: a multicriteria assessment based on economic, energetic and environmental indicators. Field Crops Res 125:167–178. https://doi.org/10.1016/j.fcr.2011.08.007
Mangnus EM, Dommerholt FJ, De Jong RLP, Zwanenburg B (1992) Improved synthesis of strigol analog GR24 and evaluation of the biological activity of its diastereomers. J Agric Food Chem 40:1230–1235. https://doi.org/10.1021/jf00019a031
Navasivayam SKR, Pandian UK, Chava V, Bharani RSA, Kavisri M, Moovendhan M (2023) Chitosan nanocomposite as an effective carrier of potential herbicidal metabolites for noteworthy phytotoxic effect against major aquatic invasive weed water hyacinth (Eichhornia crassipes). Int J Biol Macromol 226:1597–1610. https://doi.org/10.1016/j.ijbiomac.2022.11.272
Nzioki HS, Oyosi F, Morris CE, Kaya E, Pilgeram AL, Baker CS, Sands DC (2016) Striga biocontrol on a toothpick: a readily deployable and inexpensive method for smallholder farmers. Front Plant Sci 7:1121. https://doi.org/10.3389/fpls.2016.01121
Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459. https://doi.org/10.1002/ps.1713
Pérez-De-Luque A, Fondevilla S, Pérez-Vich B, Aly R, Thoiron S, Simier P, Castillejo MA, Fernández-Martinez JM, Jorrin J, Rubiales D, Delavault P (2009) Understanding Orobanche and Phelipanche -host plant interactions and developing resistance. Weed Res 49:8–22. https://doi.org/10.1111/j.1365-3180.2009.00738.x
Petit S, Cordeau S, Chauvel B, Bohan D, Guillemin JP, Steinberg C (2018) Biodiversity-based options for arable weed management: a review. Agron Sustain Dev 38:1–21. https://doi.org/10.1007/s13593-018-0525-3
Pointurier O, Gibot-Leclerc S, Le Corre V, Reibel C, Strbik F, Colbach N (2019) Intraspecific seasonal variation of dormancy and mortality of Phelipanche ramosa seeds. Weed Res 50:407–418. https://doi.org/10.1111/wre.12378
Qasem JR, Issa NN (2018) Germination and growth management of some common annual weeds by phytotoxicity of selected vegetable crops. Sci Hortic 233:431–445. https://doi.org/10.1016/j.scienta.2017.12.023
R Core Team (2020) R: A language and environment for statistical computing. Vienna, Austria, R foundation for statistical computing. Retrieved from http://www.R-proje ct.org/
Ramos-Campos EV, de Oliveira JL, Fraceto LF, Singh B (2015) Polysaccharides as safer release systems for agrochemicals. Agron Sustain Dev 35:47–66. https://doi.org/10.1007/s13593-014-0263-0
Rubiales D, Fernández-Aparicio M (2012) Innovations in parasitic weeds management in legume crops. A Review. Agron Sustain Dev 32:433–449. https://doi.org/10.1007/s13593-011-0045-x
Rubiales D, Fernández-Aparicio M, Vurro M, Eizenberg H (2018) Editorial: advances in parasitic weed research. Front Plant Sci 9:236. https://doi.org/10.3389/fpls.2018.00236
Shilo T, Rubin B, Plakhine D, Gal S, Amir R, Hacham Y, Wolf S, Eizenberg H (2017) Secondary effects of glyphosate action in Phelipanche aegyptiaca: inhibition of solute transport from the host plant to the parasite. Front Plant Sci 8:255. https://doi.org/10.3389/fpls.2017.00255
Sopeña F, Maqueda C, Morillo E (2009) Controlled release formulations of herbicides based on micro-encapsulation. Cienca e Investigation Agraria 35:27–42. https://doi.org/10.4067/S0718-16202009000100002
van Bruggen AHC, He MM, Shin K, Mai V, Jeong KC, Finckh MR, Morris JG Jr (2018) Environmental and health effects of the herbicide glyphosate. Sci Total Environ 616:255–268. https://doi.org/10.1016/j.scitotenv.2017.10.309
van der Werf HM (1996) Assessing the impact of pesticides on the environment. Agric Ecosyst Environ 60:81–96. https://doi.org/10.1016/S0167-8809(96)01096-1
Vila-Aiub MM (2019) Fitness of herbicide-resistant weeds: Current knowledge and implications for management. Plants 8:469. https://doi.org/10.3390/plants8110469
Vurro M, Boari A, Pilgeram AL, Sands DC (2006) Exogenous amino acids inhibit seed germination and tubercle formation by Orobanche ramosa (Broomrape): potential application for management of parasitic weeds. Biol Control 36:258–265. https://doi.org/10.1016/j.biocontrol.2005.09.017
Vurro M, Boari A, Casella F, Zonno MC (2018) Fungal phytotoxins in sustainable weed management. Curr Med Chem 25:268–286. https://doi.org/10.2174/0929867324666170426152331
Wang Y, Caruso F (2005) Mesoporous silica spheres as supports for enzyme immobilization and encapsulation. Chem Mater 17:953–961. https://doi.org/10.1021/cm0483137
Acknowledgements
We thank Lucie Guinchard and Carole Reibel for their technical assistance. We thank Lucien Gatard (CT2F) for the supply of broomrape seeds. This work was supported by CASDAR FAM 201939 ELIOT.
Author information
Authors and Affiliations
Contributions
SGL and FD conceived and designed the experiments. SGL and MC performed the experiments. FD and RP analyzed the data. SGL, FD, MC, and RP wrote the paper. SGL and FD supervised the work. SGL acquired funding.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gibot-Leclerc, S., Dessaint, F., Connault, M. et al. Can amino acids be used to inhibit germination or deplete the soil seedbank of Phelipanche ramosa (L.) Pomel?. J Plant Dis Prot 131, 91–99 (2024). https://doi.org/10.1007/s41348-023-00797-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-023-00797-7