Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T14:36:37.307Z Has data issue: false hasContentIssue false

Differences in seed germination response of two populations of Phelipanche ramosa (L.) Pomel to a set of GR24 concentrations and durations of stimulation

Published online by Cambridge University Press:  15 September 2021

Stéphanie Gibot-Leclerc*
Affiliation:
Agroécologie, AgroSup Dijon, INRAE, Univ. Bourgogne, Univ. Bourgogne-Franche-Comté, Dijon F-21000, France
Manon Connault
Affiliation:
Agroécologie, AgroSup Dijon, INRAE, Univ. Bourgogne, Univ. Bourgogne-Franche-Comté, Dijon F-21000, France
Rémi Perronne
Affiliation:
IGEPP, INRAE, Institut Agro, Univ. de Rennes, Le Rheu F-35653, France
Fabrice Dessaint
Affiliation:
Agroécologie, AgroSup Dijon, INRAE, Univ. Bourgogne, Univ. Bourgogne-Franche-Comté, Dijon F-21000, France
*
Author for Correspondence: Stéphanie Gibot-Leclerc, E-mail: stephanie.gibot-leclerc@inrae.fr

Abstract

Phelipanche ramosa is a major weed holoparasite characterized by a broad host range with a suboptimal development on numerous hosts, suggesting inter- or intra-species specificities. Seeds of P. ramosa germinate after exposure to exogenous chemicals exuded by surrounding host roots such as strigolactones, the concentrations of these germination stimulants varying between hosts. In France, P. ramosa is characterized by genetically differentiated populations presenting varying germination rates and a host specificity. The objective of our study was to investigate the sensitivity of seeds of two P. ramosa populations harvested on tobacco and oilseed rape, to a set of GR24 concentrations, a synthetic strigol analogue. The assessment of the germination rate was based on in vitro experiments. Seeds of P. ramosa were placed in Petri dishes with various concentrations of GR24. The cumulative number of germinated seeds of P. ramosa was counted several times after application of the treatment. Cumulative germination curves were analysed using a three-parameter log-logistic model and a time-to-event approach. The results show that the germination rate of P. ramosa seeds depends on the GR24 concentration and the duration of stimulation, but also that the response to these two factors varies greatly according to the origin of the P. ramosa seeds. The difference in germination speed between P. ramosa populations further shows distinct responses at the intraspecific level, thus suggesting that the specialization of P. ramosa probably occurs at least from the first stage of the holoparasite cycle.

Type
Short Communication
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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.)

References

Auger, B, Pouvreau, JB, Pouponneau, K, Yoneyama, K, Montiel, G, Le Bizec, B, Yoneyama, K, Delavault, P, Delourme, R and Simier, P (2012) Germination stimulants of Phelipanche ramosa in the rhizosphere of Brassica napus are derived from the glucosinolate pathway. Molecular Plant-Microbe Interactions 25, 9931004. doi:10.1094/MPMI-01-12-0006-R.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. Environmental and Experimental Botany 61, 272280. doi:10.1016/j.envexpbot.2007.06.009.CrossRefGoogle Scholar
Brun, G, Braem, L, Thoiron, S, Gevaert, K, Goormachtig, S and Delavault, P (2018) Seed germination in parasitic plants: what insights can we expect from strigolactone research? Journal of Experimental Botany 69, 22652280. doi:10.1093/jxb/erx472.CrossRefGoogle ScholarPubMed
Brun, G, Thoiron, S, Braem, L, Pouvreau, JB, Montiel, G, Lechat, MM, Simier, P, Gevaert, K, Goormachtig, S and Delavault, P (2019) CYP707As are effectors of karrikin and strigolactone signalling pathways in Arabidopsis thaliana and parasitic plants. Plant Cell & Environment 42, 26122626. doi:10.1111/ pce.13594.CrossRefGoogle ScholarPubMed
Bürger, M and Chory, J (2020) The many models of strigolactones signaling. Trends in Plant Science 25, 395405. doi:10.1016/j.tplants.2019.12.009.CrossRefGoogle ScholarPubMed
Clarke, CR, Timko, MP, Yoder, JI, Axtell, MJ and Westwood, JH (2019) Molecular dialog between parasitic plants and their hosts. Annual Review of Phytopathology 57, 279299. doi:10.1146/annurev-phyto-082718-100043.CrossRefGoogle ScholarPubMed
Dor, E, Plakhine, D, Joel, DM, Larose, H, Westwood, JH, Smirnov, E, Ziadna, H and Hershenhorn, J (2020) A new race of sunflower broomrape (Orobanche cumana) with a wider host range due to changes in seed response to strigolactones. Weed Science 68, 134142. doi:10.1017/wsc.2019.73.CrossRefGoogle Scholar
Fernández-Aparicio, M, Flores, F and Rubiales, D (2009) Recognition of root exudates by seeds of broomrape (Orobanche and Phelipanche) species. Annals of Botany 103, 423431. doi:10.1093/aob/mcn236.CrossRefGoogle ScholarPubMed
Fernández-Aparicio, M, Yoneyama, K and Rubiales, D (2011) The role of strigolactones in host specificity of Orobanche and Phelipanche seed germination. Seed Science Research 21, 5561. doi:10.1017/S0960258510000371.CrossRefGoogle Scholar
Gauthier, M, Véronési, C, El-Halmouch, Y, Leflon, M, Jestin, C, Labalette, F, Simier, P, Delourme, R and Delavault, P. (2012) Characterisation of resistance to branched broomrape, Phelipanche ramosa, in winter oilseed rape. Crop Protection 42, 5663. doi:10.1016/J.CROPRO.2012.07.002.CrossRefGoogle Scholar
Gibot-Leclerc, S, Corbineau, F, Sallé, G and 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 Regulation 43, 6371. doi:10.1023/B:GROW.0000038242.77309.73.CrossRefGoogle Scholar
Gibot-Leclerc, S, Sallé, G, Reboud, X and 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 – Morphology, Distribution, Functional Ecology of Plants 207, 512521. doi:10.1016/j.flora.2012.06.011.CrossRefGoogle Scholar
Gibot-Leclerc, S, Dessaint, F, Reibel, C and Le Corre, V (2013) Phelipanche ramosa (L.) Pomel populations differ in life-history and infection response to hosts. Flora – Morphology, Distribution, Functional Ecology of Plants 208, 247252. doi:10.1016/j.flora.2013.03.007.CrossRefGoogle Scholar
Gibot-Leclerc, S, Perronne, R, Dessaint, F, Reibel, C and Le Corre, V (2016) Assessment of phylogenetic signal in the germination ability of Phelipanche ramosa on Brassicaceae hosts. Weed Research 56, 452461. doi:10.1111/wre.12222.CrossRefGoogle Scholar
Huet, S, Pouvreau, JB, Delage, E, Delgrange, S, Marais, C, Bahut, M, Delavault, P, Simier, P and Poulin, L (2020) Populations of the parasitic plant Phelipanche ramosa influence their seed microbiota. Frontiers in Plant Sciences 11, 1075. doi:10.3389/fpls.2020.01075.CrossRefGoogle ScholarPubMed
Joel, DM (2009) The new nomenclature of Orobanche and Phelipanche. Weed Research 49, 67. doi:10.1111/j.1365-3180.2009.00748.x.CrossRefGoogle Scholar
Kokla, A and Melnyk, CW (2018) Developing a thief: haustoria formation in parasitic plants. Developmental Biology 442, 5359. doi:10.1016/j.ydbio.2018.06.013.CrossRefGoogle ScholarPubMed
Le Corre, V, Reibel, C and Gibot-Leclerc, S (2014) Development of microsatellite markers in the branched broomrape Phelipanche ramosa L. (Pomel) and evidence for host-associated genetic divergence. International Journal of Molecular Science 15, 9941002. doi:10.3390/ijms15010994.CrossRefGoogle ScholarPubMed
Mangnus, EM, Dommerholt, FJ, De Jong, RLP and Zwanenburg, B (1992a) Improved synthesis of strigol analog GR24 and evaluation of the biological activity of its diastereomers. Journal of Agricultural and Food Chemistry 40, 12301235. doi:10.1021/jf00019a031.CrossRefGoogle Scholar
Mangnus, EM, Stommen, PLA and Zwanenburg, B (1992b) A standardized bioassay for evaluation of potential germination stimulants for seeds of parasitic weeds. Journal of Plant Growth Regulation 11, 91. doi:10.1007/BF00198020.CrossRefGoogle Scholar
Matusova, R, Kullacova, D and Tóth, P (2014) Response of weedy and non-weedy broomrapes to synthetic strigolactone analogue GR24. Journal of Central European Agriculture 15, 7282. doi:10.5513/JCEA01/15.4.1511.CrossRefGoogle Scholar
Onofri, A, Gresta, F and Tei, F (2010) A new method for the analysis of germination and emergence data of weed species. Weed Research 50, 187198. doi:10.1111/j.1365-3180.2010.00776.x.CrossRefGoogle Scholar
Parker, C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Management Science 65, 453459. doi:10.1002/ps.1713.CrossRefGoogle ScholarPubMed
Perronne, R, Gibot-Leclerc, S, Dessaint, F, Reibel, C and Le Corre, V (2017) Is induction ability of seed germination of Phelipanche ramosa phylogenetically structured among hosts? A case study on Fabaceae species. Genetica 145, 481489. doi:10.1007/s10709-017-9990-x.CrossRefGoogle ScholarPubMed
Pointurier, O, Gibot-Leclerc, S, Le Corre, V, Reibel, C, Strbik, F and Colbac, N (2019) Intraspecific seasonal variation of dormancy and mortality of Phelipanche ramosa seeds. Weed Research 50, 407418. doi:10.1111/wre.12378.CrossRefGoogle Scholar
R Core Team (2020) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from: http://www.R-project.org/.Google Scholar
Ritz, C, Pipper, CB and Streibig, JC (2013) Analysis of germination data from agricultural experiments. European Journal of Agronomy 45, 16. doi:10.1016/j.eja.2012.10.003.CrossRefGoogle Scholar
Ritz, C, Baty, F, Streibig, JC and Gerhard, D (2015) Dose-response analysis using R. PLoS One 10, e0146021. doi:10.1371/journal.pone.0146021.CrossRefGoogle ScholarPubMed
Stojanova, B, Delourme, R, Duffé, P, Delavault, P and Simier, P (2019) Genetic differentiation and host preference reveal non-exclusive host races in the generalist parasitic weed Phelipanche ramosa. Weed Research 59, 107118. doi:10.1111/wre.12353.CrossRefGoogle Scholar
Thorogood, CJ, Rumsey, FJ, Harris, SA and Hiscock, SJ (2008) Host-driven divergence in the parasitic plant Orobanche minor Sm. (Orobanchaceae). Molecular Ecology 17, 42894303. doi:10.1111/j.1365-294X.2008.03915.x.CrossRefGoogle Scholar
Thorogood, CJ, Rumsey, FJ, Harris, SA and Hiscock, SJ (2009) Gene flow between alien and native races of the holoparasitic angiosperm Orobanche minor (Orobanchaceae). Plant Systematics and Evolution 282, 3142. doi:10.1007/s00606-009-0204-6.CrossRefGoogle Scholar
Wang, Y and Bouwmeester, HJ (2018) Structural diversity in the strigolactones. Journal of Experimental Botany 69, 22192230. doi:10.1093/jxb/ery091.CrossRefGoogle ScholarPubMed
Xie, X, Kusumoto, D, Takeuchi, Y, Yoneyama, K, Yamada, Y and Yoneyama, K (2007) 2'-epi-orobanchol and solanacol, two unique strigolactones, germination stimulants for root parasitic weeds, produced by tobacco. Journal of Agricultural and Food Chemistry 55, 80678072. doi:10.1021/jf0715121.CrossRefGoogle ScholarPubMed
Yoshida, S, Cui, S, Ichihashi, Y and Shirasu, K (2006) The haustorium, a specialized invasive organ in parasitic plants. Annual Review of Plant Biology 67, 643667. doi:10.1146/annurev-arplant-043015-111702.CrossRefGoogle Scholar
Zehhar, N, Labrousse, P, Arnaud, MC, Boulet, C, Bouya, D and Fer, A (2003) Study of resistance to Orobanche ramosa in host (oilseed rape and carrot) and non-host (maize) plants. European Journal of Plant Pathology 109, 7582. doi:10.1023/A:1022060221283.CrossRefGoogle Scholar