First Report of the Parasitic Plant Phelipanche ramosa on Berseem Clover (Trifolium alexandrinum) in Tunisia

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1 Short Communication First Report of the Parasitic Plant Phelipanche ramosa on Berseem Clover (Trifolium alexandrinum) in Tunisia Moez Amri, Centre Régional de Recherche en Grandes Cultures de Béja, Laboratoire des Grandes Cultures, Université Carthage, Route de Tunis, km 5, 9000 Béja, Tunisia, Zouhaier Abbes, Meriam Bouhadida, and Mohamed Kharrat, Institut National de la Recherche Agronomique de Tunisie, Laboratoire des Grandes Cultures, Université Carthage, Rue Hédi Karray, 2080 Ariana, Tunisia ABSTRACT Amri, M., Abbes, Z., Bouhadida, M., and Kharrat, M First report of the parasitic plant Phelipanche ramosa on berseem clover (Trifolium alexandrinum) in Tunisia. Tunisian Journal of Plant Protection 8: Branched broomrape (Phelipanche ramosa) is a parasitic plant that has been described as an agricultural problem on many host crops in the world. In Tunisia, this broomrape was found parasitizing berseem clover (Trifolium alexandrinum) in some commercial fields in Beja region in north of Tunisia. P. ramosa attachments on the roots of berseem clover plants were observed and the number of tubers in different berseem clover fields varied from 0.83 ± 1.33 to 3 ± 3.69 tubers/m². This situation can be considered a further threat for many potential host crops cultivated in these fields at the Beja region. Keywords: Attachment, broomrape, Phelipanche ramosa, Trifolium alexandrinum, Tunisia Broomrapes (Orobanche spp. and Phelipanche spp.) are destructive holoparasitic flowering plants that completely depend on their host for all nutritional requirements. Under natural conditions, interactions between parasitic plants and their hosts first occur at the underground level following seed germination of the parasite in response to specific chemical root exudates released from the host plant (1). Broomrapes attack many crop species over the world. Among all identified species only five are Corresponding author: Moez Amri amrmoez@gmail.com Accepted for publication 25 October 2013 noxious pests of economically important crops. These are O. crenata, O. cumana, O. minor, Phelipanche aegyptiaca and P. ramosa (10). Musselman (18) has reported that the branched broomrape P. ramosa is the most widespread broomrape in the world, spreading from Central Europe to North Africa, Pakistan, Afghanistan, north India, China and South Africa. The parasitic weed has also been found in USA (7), Cuba (17), Chile (19) and Australia (20). P. ramosa parasitizes a number of host species belonging to various botanical families (20) and represents a real threat for many host crops. The main parasitized crops belong to the Solanaceae family, including tomato (4), potato (12) and Tunisian Journal of Plant Protection 127 Vol. 8, No. 2, 2013

2 tobacco (2). Other hosts include species from Cruciferae and Leguminosae families (Parker 1994), cannabis (Canabis sativa) and rapeseed (Brassica napus) from Cannabaceae and Brassicaceae families, respectively (3, 11). Berseem clover (Trifolium alexandrinum) is an erect cool-season forage legume crop. It can grow cm tall and can be mowed several times for forage then ploughed as green manure, yielding kg/ha of nitrogen (16). Inter-cropping berseem clover with cereals, such as oats, provide high quality silage or hay, increases yield and quality of cereal forage crops and reduces fertilizer needs (22). In Tunisia, O. crenata (syn. O. speciosa) and O. foetida are known as the two major important Orobanche species that cause a serious problem for legume crops (13). However, P. ramosa has been reported only in very limited infestation levels in some regions of Tunisia (14). During a survey conducted in March 2011, P. ramosa was found for the first time parasitizing berseem clover cultivars in different fields in the region of Beja in north of Tunisia (Fig. 1). The broomrape morphology and biology were typical of P. ramosa plant with branched stems (Figs. 2 and 3), bract and bracteoles equaling a lanceolated division calyx, corolla blue-purple with curved tube, bilobed and ciliated upper and lower lips with three spreading lobes and hairy external face, four hairy stamens in the basis with glabrous anthers or shortly haired, and unilocular capsule with two valves adherent at the basis. To confirm the attachments of the parasitic plant to the host roots, berseem clover plants were gently dug up and the root systems were washed. Clear P. ramosa attachments were observed (Fig. 4). In order to determine the level of infestation, six plots of 1 m² each were randomly chosen in three berseem clover infested fields for which the number of P. ramosa tubers was determined. Results showed that the numbers of P. ramosa tubers varied among the plots and were 0.83 ± 1.33, 1.33 ± 1.03 and 3.0 ± Berseem clover was reported to be parasitized by O. foetida in an infested field in Tunisia (15) and by O. crenata in a pot experiment (5). Other studies have reported berseem clover to be a catch crop, effective in reducing O. crenata emergence in faba bean and to have potential for broomrape control in rotations (6) which explains and confirms reductions of O. crenata infestations on faba bean or pea intercropped with berseem clover (8). Fernandez et al. (9) demonstrated that P. ramosa seeds germinate with berseem clover root exudates. However, this is the first report of P. ramosa infecting berseem clover in Tunisia and that could be, especially in the region of Beja, a further threat for potential host cultivated crops in this area such as potato, tomato and pepper. RESUME Amri M., Abbes Z., Bouhadida, M. et Kharrat, M Premier signalement de la plante parasite Phelipanche ramosa sur le trèfle d'alexandrie (Trifolium alexandrinum) en Tunisie. Tunisian Journal of Plant Protection 8: L orobanche ramifiée (Phelipanche ramosa) est une plante parasite qui a été décrite comme un problème majeur pour plusieurs cultures dans le monde. En Tunisie, cette espèce a été trouvée parasitant le trèfle d'alexandrie (Trifolium alexandrinum) dans certains champs de la région de Béja Tunisian Journal of Plant Protection 128 Vol. 8, No. 2, 2013

3 Fig. 1. Phelipanche ramosa broomrape parasitizing berseem clover plant (Trifolium alexandrinum) in a commercial field. Fig. 2. Lateral view of Phelipanche ramosa blue-purple flower showing the corolla and the calyx. Fig. 3. The Phelipanche ramosa reproductive organs (the pistil on the left and the 4 stamens). Tunisian Journal of Plant Protection 129 Vol. 8, No. 2, 2013

4 Fig. 4. a: Attachment of Phelipanche ramosa to berseem clover (Trifoliumm alexandrinum) roots, b: Magnification 10. Tunisian Journal of Plant Protection 130 Vol. 8, No. 2, 2013

5 dans le Nord de la Tunisie. L attachement de P. ramosa aux racines des plantes de trèfle d'alexandrie a été observé et le nombre de tubercules dans les différents champs cultivés de trèfle d'alexandrie variait entre 0,83 ± 1,33 et 3 ± 3,69 tubercules/m². Cette situation peut être considérée comme une nouvelle menace pour plusieurs espèces cultivées dans les champs de la région de Beja. Mots clés: Attachement, Orobanche, Phelipanche ramosa, Trifolium alexandrinum, Tunisie اي وزھ س و ة و ااط أول "! (ت ا'&% Phelipanche.-+" %. (Trifolium alexandrinum) +تا*, ramosa Tunisian Journal of Plant Protection 8: اك اع Phelipanche ramosa م زرا ة ا' م& ا%رات #" م! أء ا). و#"-/ -) ا'ر ھ+اا*عم&اكم 01 تا 2 ) alexandrinum) (Trifolium #" 8: ا 9 ل 91*8 #" 78 6 ل ا 0 د ا 3. -? م 0 <= ا>قاك 2 ) و-او<? أ Aاد 2 ا Aرت #" < 9 لا 2 )ا!م& 0,83 1,33± إ 3 3,69± در/م. & ارھ+اا DE - AAاإ #E Aة أاعم&ا GHا Fاا%رو #"ھ+ها 9 ل #"م* تم<: ا>ق -/ ھك ramosa Trifolium alexandrinum Phelipanche LITERATURE CITED 1. Bouwmeester, H.J., Matusova, R., Zhongkui, S., and Beale, M.H Secondary metabolite signalling in host parasitic plant interactions. Curr. Opin. Plant Biol. 6: Buschmann, H., Gonsior, G., and Sauerborn, J. 2005a. Pathogenicity of branched broomrape (O. ramosa) population on tobacco cultivars. Plant Pathol. 54: Buschmann, H., Komle, S., Gonsior, G., and Sauerborn, J. 2005b. Susceptibility of rapeseed (Brassica napus ssp. napus) to branched broomrape (O. ramosa L.). J. Plant Dis. Prot. 112: Cagan, L. and Toth P A decrease in tomato yield caused by branched broomrape parasitization. Acta Fytotech. Zootech. 6: Chabrolin, C Contribution à l étude de la germination des graines de l orobanche de la fève. Extrait des Annales du Service Botanique et Agronomique de la Tunisie 15-16: Cooke, D Control of Branched Broomrape: A literature review. Animal and Plant Control Commission of SA (ed.). Department of water, Land and Biodiversity Conservation, Adelaide, Australia, 39 pp. 7. Eplee, R.E Orobanche ramosa in the United States. Pages In: Proceedings of the Third International Symposium on Parasitic Weeds, Parker, C., Musselman, L.J., Polhilland, R.M., and Wilson, A.K. (Ed.). May, 7-11, 1984, Aleppo, Syria. 8. Fernandez Aparicio, M., Emeran, A.A., and Rubiales, D Inter-cropping with berseem clover (Trifolium alexandrinum) reduces infection by Orobanche crenata in legumes. Crop Prot. 29: Fernandez Aparicio, M., Flores, F., and Rubiales, D Recognition of root exudates by seeds of broomrape (Orobanche and Phelipanche) species. Annals of Botany 103: Garcia-Torres, L Progress in Orobanche control, an overview. Biology and Management of Orobanche. Pages In: Proceedings of the Third International Workshop on Orobanche and related Striga Research. Pieterse, A.H., Verkleij, J.A.C., and Ter Borg, S.J. (Ed.). Royal Tropical Institute. November, 08-12, 1993, Amsterdam, The Netherlands. 11. Gonsior, G., Buschmann, H., Szinicz, G., Otmar, S., and Sauerborn, J Induced resistance: An innovative approach to manage branched broomrape (Orobanche ramosa) in hemp and tobacco. Weed Science 52: Haidar, M.A., Bibi, W., and Sidahmed, M.M Response of branched broomrape (Orobanche ramosa) growth and Tunisian Journal of Plant Protection 131 Vol. 8, No. 2, 2013

6 development to various soil amendments in potato. Crop Prot. 22: Kharrat, M. and Souissi, T Research on Orobanche foetida and O. crenata in Tunisia. Integrated management of orobanche in food legumes in the Near East and North Africa. Pages In: Proceedings of the expert consultation on IPM for Orobanche in Food Legume Systems in the Near East and North Africa. Dahan, R., and El Mourid, M. (Ed.). April, 7-9, 2003, Rabat, Morocco. 14. Kharrat, M., Ayadi, N., Belhadj, R., Amraoui, S., Kouki, C., Ben Othmen, K., and Ben Saad, A L expérience tunisienne pour la lutte contre l Orobanche sur les fèves à travers la formation des agriculteurs dans les écoles champ. Pages In: Progress on framer training in parasitic weed management, Labrada, R. (Ed). 2007, FAO, Rome, Italy, 156 pp. 15. Kharrat, M Etude de la virulence de l écotype de Béja d Orobanche foetida sur différentes espèces de légumineuses. Devenir des légumineuses alimentaires dans le Maghreb. Page 89. In: Proceeding du 2 ème séminaire du réseau REMAFEVE/REMALA. Kharrat, M., Abbad Andaloussi, F., Maatougui, M.E.H., Sadiki, M., and Bertenbreiter, W. (Ed.), 30 Janvier 2 Février, 2002, Hammamet, Tunisie. 16. Knight, W.E Miscellaneous annual clovers. Pages In: Clover Science and Technology, Taylor, N.L. (Ed.), N 25. Series Agronomy. American Society of Agronomy, Inc., Crop Science Society of America, Inc., Soil Science Society of America, Publishers, Madison, Wisconsin, USA. 17. Labrada, R Occurrence and control of Orobanche ramosa L. in Cuba. Biology and Management of Orobanche. Pages In: Proceedings of the Third International Workshop on Orobanche and related Striga Research. Pieterse, A.H., Verkleij, J.A.C., and Ter Borg, S.J. (Ed.). Royal Tropical Institute, November, 08-12, 1993, Amsterdam, The Netherlands. 18. Musselman, L.J Taxonomy and spread of Orobanche. Biology and Management of Orobanche. Pages In: Proceedings of the Third International Workshop on Orobanche and related Striga Research. Pieterse, A.H., Verkleij, J.A.C., and ter Borg, S.J., (Ed.). Royal Tropical Institute, November, 08-12, 1993, Amsterdam, The Netherlands. 19. Norambuena, H., Kroschel, J., and Klein, O Introduction of Phytomyza orobanchia for biocontrol of Orobanche spp. in Chile. Pages In: Advances in Parasitic Weed Control at On-farm Level. vol. II. Joint Action to Control Orobanche in the WANA Region. Kroschel, J., Abderabihi, M., and Betz, H. (Ed.). Margraf Verlag, Weikersheim, Germany, 324 pp. 20. Parker, C. and Riches, C.A Parasitic Weeds of the World: Biology and Control. CAB International, Wallingford, UK, 332 pp. 21. Parker, C Orobanche control: State of the art after the Third International Workshop on Orobanche. Biology and Management of Orobanche. Page 727. In: Proceedings of the Third International Workshop on Orobanche and Related Striga Research, Pieterse, A.H., Verkleijand, J.A.C., and Ter Borg, S.J., (Ed.). Royal Tropical Institute, November, 08-12, 1993, Amsterdam, The Netherlands. 22. Ross, S.M., King, J.R., O Donovan, J.T., and Spaner, D Forage potential of intercropping berseem clover with barley, oat or triticale. Agron. J. l96: Tunisian Journal of Plant Protection 132 Vol. 8, No. 2, 2013

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