Hostname: page-component-6587cd75c8-6qszs Total loading time: 0 Render date: 2025-04-23T15:18:28.089Z Has data issue: false hasContentIssue false
  • English
  • Français

Primary metabolic profiling of four broomrapes belonging to Orobanche and Phelipanche species

Published online by Cambridge University Press:  30 October 2024

Evgenia Dor ,
Aviv Guy ,
Rachel Amir Open the ORCID record for Rachel Amir [Opens in a new window]  and
Yael Hacham
Evgenia Dor
Affiliation:
Researcher, Newe Ya’ar Research Center, Agricultural Research Organization, Ramat Yishay, Israel
Aviv Guy
Affiliation:
Graduate student, Laboratory of Plant Science, MIGAL–Galilee Technology Center, Kiryat Shmona, Israel Graduate student, Tel-Hai College, Upper Galilee, Israel
Rachel Amir*
Affiliation:
Professor, Laboratory of Plant Science, MIGAL–Galilee Technology Center, Kiryat Shmona, Israel Professor, Tel-Hai College, Upper Galilee, Israel
Yael Hacham
Affiliation:
Researcher, Laboratory of Plant Science, MIGAL–Galilee Technology Center, Kiryat Shmona, Israel Researcher, Tel-Hai College, Upper Galilee, Israel
*
Corresponding author: Rachel Amir; Email: rachel@migal.org.il
Get access Rights & Permissions [Opens in a new window]

Abstract

Genera of the Orobanchaceae family are holoparasites that parasitize various hosts. Several members of this family cause severe damage to diverse crop plants. While the biological and life cycles of these parasites have been studied, their metabolism has received little attention, most of which focused on Egyptian broomrape [Orobanche aegyptiaca Pers.; syn.: Phelipanche aegyptiaca (Pers.) Pomel]. This study aimed at obtaining more knowledge about the primary metabolic profiling of four parasite species belonging to the Orobanchaceae family—sunflower broomrape (Orobanche cumana Wallr.), Orobanche cernua, P. aegyptiaca, and branched broomrape [Orobanche ramosa L.; syn.: Phelipanche ramosa (L.) Pomel.]—that developed on tomato (Solanum lycopersicum L.) as a host. Gas chromatography–mass spectrometry analysis demonstrated that significant differences in metabolite content occur between species belonging to Orobanche compared with those belonging to Phelipanche. This finding adds another layer to the separation of these two genera in addition to morphological separation. Moreover, each of these four species exhibits different metabolic profiles, indicating that the parasites can absorb the host’s metabolites but also have the ability to self-regulate their metabolites in order to grow and develop.

Keywords

GC-MS analysisholoparasitic plantprimary metabolic profiling
Type
Research Article
Information
Weed Science , Volume 72 , Issue 6 , November 2024 , pp. 714 - 722
Check for updates
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of Weed Science Society of America

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

*

These authors contributed equally to this work.

Associate Editor: William Vencill, Univ of Georgia-Crop/Soils

References

Abbes, Z, Kharrat, M, Delavault, P, Chaïbi, W, Simier, P (2009) Osmoregulation and nutritional relationships between Orobanche foetida and faba bean. Plant Signal Behav 4:336–338 CrossRefGoogle ScholarPubMed
Aly, R, Cholakh, H, Joel, DM, Leibman, D, Steinitz, B, Zelcer, A, Naglis, A, Yarden, O, Gal-On, A (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 CrossRefGoogle ScholarPubMed
Aly, R, Matzrafi, M, Bari, VK (2021) Using biotechnological approaches to develop crop resistance to root parasitic weeds. Planta 253:1–11 CrossRefGoogle ScholarPubMed
Basheer, L, Niv, D, Cohen, A, Gutman, R, Hacham, Y, Amir, R (2024) Egyptian broomrape (Phelipanche aegyptiaca): from foe to friend? Evidence of high nutritional value and potential suitability for food use. Future Food 10:100413 CrossRefGoogle Scholar
Casadesús, A, Munné-Bosch, S (2021) Holoparasitic plant-host interactions and their impact on Mediterranean ecosystems. Plant Physiol 185:1325–1338 CrossRefGoogle ScholarPubMed
Cechin, I, Press, MC (1993) Nitrogen relations of the sorghum-Striga hermonthica hostparasite association: growth and photosynthesis. Plant Cell Environ 16:237–247 CrossRefGoogle Scholar
Clermont, K, Wang, Y, Liu, S, Yang, Z, dePamphilis, CW, Yoder, JI (2019) Comparative metabolomics of early development of the parasitic plants Phelipanche aegyptiaca and Triphysaria versicolor . Metabolites 9:114–133 CrossRefGoogle ScholarPubMed
Cochavi, A, Rapaport, T, Gendler, T, Karnieli, A, Eizenberg, H, Rachmilevitch, S, Ephrath, EJ (2017) Recognition of Orobanche cumana below-ground parasitism through physiological and hyper spectral measurements in sunflower (Helianthus annuus L.). Front Plant Sci 8:1–12 CrossRefGoogle ScholarPubMed
Delavault, P (2015) Knowing the parasite: biology and genetics of Orobanche . Helia 38:15–29 CrossRefGoogle Scholar
Delavault, P, Thalouarn, P (2002) The obligate root parasite Orobanche cumana exhibits several rbcL sequences. Gene 297:85–92 CrossRefGoogle ScholarPubMed
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 8:1–15 CrossRefGoogle ScholarPubMed
Emran, S, Nawade, B, Yahyaa, M, Abu Nassar, J, Tholl, D, Eizenberg, H, Ibdah, M (2020) Broomrape infestation in carrot (Daucus carota): changes in carotenoid gene expression and carotenoid accumulation in the parasitic weed Phelipanche aegyptiaca and its host. Sci Rep 10:2–11 CrossRefGoogle ScholarPubMed
En-nahli, Y, El Arroussi, H, Kumar, S, Bouhlal, O, Mentag, R, Hejjaoui, K, Douaik, A, Abbes, I, Eddine, N, Es-Safi, I, Amri, M (2021) Resistance to Orobanche crenata Forsk. in lentil (Lens culinaris Medik.): exploring some potential altered physiological and biochemical defense mechanisms. J Plant Interact 16:321–331 CrossRefGoogle Scholar
Farrokhi, Z, Alizadeh, Ha, Alizadeh, H (2019) Developmental patterns of enzyme activity, gene expression, and sugar content in sucrose metabolism of two broomrape species. Plant Physiol Biochem 142:8–14 CrossRefGoogle ScholarPubMed
Farrokhi, Z, Alizadeh, Ha, Alizadeh, H (2021) Egyptian broomrape sucrose metabolism in response to different host plants. Weed Res 61:137–145 CrossRefGoogle Scholar
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 7:21–25 CrossRefGoogle ScholarPubMed
Flores-Sánchez, IJ, Garza-Ortiz, A (2019) Is there a secondary/specialized metabolism in the genus Cuscuta and which is the role of the host plant? Phytochem Rev 18:5–9 CrossRefGoogle Scholar
Guo, C, Qin, L, Ma, Y, Qin, J (2022) Integrated metabolomic and transcriptomic analyses of the parasitic plant Cuscuta japonica Choisy on host and non-host plants. BMC Plant Biol 22:1–16 CrossRefGoogle ScholarPubMed
Habimana, S, Nduwumuremyi, A, Chinama, RJD (2014) Management of Orobanche in field crops—a review. J Soil Sci Plant Nutr 14:43–62 Google Scholar
Hacham, Y, Hershenhorn, J, Dor, E, Amir, R (2016) Primary metabolic profiling of Egyptian broomrape (Phelipanche aegyptiaca) compared to its host tomato roots. J Plant Physiol 205:11–19 CrossRefGoogle ScholarPubMed
Hacham, Y, Matityahu, I, Amir, R (2017) Transgenic tobacco plants having a higher level of methionine are more sensitive to oxidative stress. Physiol Plant 160:242–252 CrossRefGoogle ScholarPubMed
Hershenhorn, J, Eizenberg, H, Dor, E, Kapulnik, Y, Goldwasser, Y (2009) Phelipanche aegyptiaca management in tomato. Weed Res 49:34–47 CrossRefGoogle Scholar
Igbinnosa, I, Thalouarn, P (1996) Nitrogen assimilation enzyme activities in witchweed (Striga) in hosts presence and absence. Weed Sci 44:224–232 CrossRefGoogle Scholar
Irving, LJ, Cameron, DD (2009) You are what you eat. Interactions between root parasitic plants and their hosts. Pages 87–138 in Kader, J-C, Delseny, M, eds. Advances in Botanical Research. Volume 50. Amsterdam: Elsevier Google Scholar
Joel, DM (2007) Direct infection of potato tubers by the root parasite Orobanche aegyptiaca . Weed Res 47:276–279 CrossRefGoogle Scholar
Joel, DM (2009) The new nomenclature of Orobanche and Phelipanche . Weed Res 49:6–7 CrossRefGoogle Scholar
Kumar, K, Amir, R (2021) The effect of a host on the primary metabolic profiling of Cuscuta campestris’ main organs, haustoria, stem and flower. Plants 10:1–13 CrossRefGoogle ScholarPubMed
Kumar, K, Hacham, Y, Amir, R (2022) The effect of 10 crop plants that served as hosts on the primary metabolic profile of the parasitic plant Phelipanche aegyptiaca . Metabolites 12:1195–1210 CrossRefGoogle ScholarPubMed
Li, L, Lietz, G, Seal, CJ (2021) Phenolic, apparent antioxidant and nutritional composition of quinoa (Chenopodium quinoa Willd.) seeds. Int J Food Sci Technol 56:3245–3254 CrossRefGoogle Scholar
Mutuku, JM, Cui, S, Yoshida, S, Shirasu, K (2021) Orobanchaceae parasite–host interactions. New Phytol 230:46–59 CrossRefGoogle ScholarPubMed
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 CrossRefGoogle ScholarPubMed
Nativ, N, Hacham, Y, Hershenhorn, J, Dor, E, Amir, R (2017) Metabolic investigation of Phelipanche aegyptiaca reveals significant changes during developmental stages and in its different organs. Front Plant Sci 8:491–504 CrossRefGoogle ScholarPubMed
Nguyen, HC, Hoefgen, R, Hesse, H (2012) Improving the nutritive value of rice seeds: elevation of cysteine and methionine contents in rice plants by ectopic expression of a bacterial serine acetyltransferase. J Exp Bot 63:5991–6001 CrossRefGoogle ScholarPubMed
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 54:789–799 CrossRefGoogle Scholar
Piwowarczyk, R, Denysenko-Bennett, M, Góralski, G, Kwolek, D, Pedraja, ÓS, Mizia, P, Pedraja, SO, Mizia, P, Cygan, M, Joachimiak, A (2018) Phylogenetic relationships within orobanche and phelipanche (orobanchaceae) from central Europe, focused on problematic aggregates, taxonomy, and host ranges. Acta Biol Crac Ser Bot 60:45–64 Google Scholar
Rispail, N, Dita, MA, González-Verdejo, C, Pérez-De-Luque, A, Castillejo, MA, Prats, E, Román, B, Jorrín, J, Rubiales, D (2007) Plant resistance to parasitic plants: molecular approaches to an old foe: research review. New Phytol 173:703–712 CrossRefGoogle Scholar
Rubiales, D, Verkleij, J, Vurro, M, Murdoch, AJ, Joel, DM (2009) Parasitic plant management in sustainable agriculture. Weed Res 49:1–5 CrossRefGoogle Scholar
Scharenberg, F, Zidorn, C (2018) Genuine and sequestered natural products from the genus Orobanche (Orobanchaceae, Lamiales). Molecules 23:2821–2851 CrossRefGoogle ScholarPubMed
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 8:1–16 CrossRefGoogle ScholarPubMed
Sim, SYJ, Srv, A, Chiang, JH, Henry, CJ (2021) Plant proteins for future foods: a roadmap. Foods 10:1–31 CrossRefGoogle ScholarPubMed
Sisou, D, Tadmor, Y, Plakhine, D, Ziadna, H, Hübner, S, Eizenberg, H (2021) Biological and transcriptomic characterization of pre-haustorial resistance to sunflower broomrape (Orobanche cumana w.) in sunflowers (Helianthus annuus). Plants 10:1810–1824 CrossRefGoogle ScholarPubMed
Sun, M, Li, S, Yu, H, Gong, Q, Zhang, B, Liu, G, Xiao, Y, Peng, F (2023) Effects of valine and urea on carbon and nitrogen accumulation and lignin content in peach trees. Plants 12:1596–1619 CrossRefGoogle ScholarPubMed
Wakabayashi, T, Joseph, B, Yasumoto, S, Akashi, T, Aoki, T, Harada, K, Muranaka, S, Bamba, T, Fukusaki, E, Takeuchi, Y (2015) Planteose as a storage carbohydrate required for early stage of germination of Orobanche minor and its metabolism as a possible target for selective control. J Exp Bot 66:3085–3097 CrossRefGoogle ScholarPubMed
Westwood, JH (2013) The physiology of the established parasite–host association. Pages 87–114 in Joel, DM, Gressel, J, Musselman, LJ, eds. Parasitic Orobanchaceae. Berlin: Springer CrossRefGoogle Scholar
Westwood, JH, dePamphilis, CW, Das, M, Fernández-Aparicio, M, Honaas, LA, Timko, MP, Wafula, EK, Wickett, JN, Yoder, IJ (2012) The parasitic plant genome project: new tools for understanding the biology of Orobanche and Striga. Weed Sci 60:295–306 CrossRefGoogle Scholar
Xia, J, Sinelnikov, IV, Han, B, Wishart, DS (2015) MetaboAnalyst 3.0-making metabolomics more meaningful. Nucleic Acids Res 43:W251–W257 CrossRefGoogle ScholarPubMed
Yoshida, S, Shirasu, K (2012) Plants that attack plants: Molecular Elucidation of plant parasitism. Curr Opin Plant Bio 15:708–713 CrossRefGoogle ScholarPubMed
Supplementary material: File

Dor et al. supplementary material 1

Dor et al. supplementary material
Download Dor et al. supplementary material 1(File)
File 25.6 KB
Supplementary material: File

Dor et al. supplementary material 2

Dor et al. supplementary material
Download Dor et al. supplementary material 2(File)
File 566.8 KB