Abstract
Plant derived sesquiterpene strigolactones, which have previously been characterized as germination stimulants for root parasitic plants, have recently been identified as the branching factors which induce hyphal branching morphogenesis, a critical step in host recognition by arbuscular mycorrhizal (AM) fungi. We show here that, in red clover plants (Trifolium pratense L.), which is known as a host for both AM fungi and the root holoparasitic plant Orobanche minor Sm., reduced supply of phosphorus (P) but not of other elements examined (N, K, Mg, Ca) in the culture medium significantly promotes the release of a strigolactone, orobanchol, by the roots of this plant. In red clover plants, the level of orobanchol exudation appeared to be regulated by P availability and was in good agreement with germination stimulation activity of the root exudates. This implies that under P deficiency, plant roots attract not only symbiotic fungi but also root parasitic plants through the release of strigolactones. This is the first report demonstrating that nutrient availability influences both symbiotic and parasitic interactions in the rhizosphere.
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References
Abu-Irmaileh BE (1981) Response of hemp broomrape (Orobanche ramosa) infestation to some nitrogenous compounds. Weed Sci 29: 8–10
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
Amijee F, Tinker PB, Stribley DP (1989) The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on colonization. New Phytol 111:453–446
Awad AA, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K (2006) Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche, produced by maize, millet and sorghum. Plant Growth Regul 48:221–227
Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252
Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signaling in host–parasitic plant interactions. Curr Opin Plant Biol 6:358–364
Chae SH, Yoneyama K, Takeuchi Y, Joel DM (2004) Fluridone and norflurazon, carotenoid-biosynthesis inhibitors, promote seed conditioning and germination of the holoparasite Orobanche minor. Physiol Plant 120:328–337
Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154: 1189–1190
Cook CE, Whichard LP, Wall ME, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. II. The structure of strigol– a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94: 6198–6199
Gworgwor NA, Weber HC (2003) Arbuscular mycorrhizal fungi-parasite-host interaction for the control of Striga hermonthica (Del.) Benth. in sorghum [Sorghum bicolor (L.) Moench]. Mycorrhiza 13:277–281
Haidar MA, Sidahmed MM (2000) Soil solarization and chiken manure for the control of Orobanche crenata and other weeds in Lebanon. Crop Prot 19: 169–173
Haidar MA, Bibi W, Sidahmed MM (2003) Response of branched broomrape (Orobanche ramose) growth and development to various soil amendments in potato. Crop Prot 22:291–294
Hauck C, Müller S, Schildknecht H (1992) A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. J Plant Physiol 139:474–478
Joel DM, Steffens JC, Matthews DE (1995) Germination of weedy root parasites. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, New York, pp 567–597
Lendzemo VW, Kuyper TW (2001) Effects of arbuscular mycorrhizal fungi on damage by Striga hermonthica on two contrasting cultivars of sorghum, Sorghum bicolor. Agric Ecosyst Environ 87:29–35
Lendzemo VW, Kuyper TW, Kropff MJ, van Ast A (2005) Field inoculation with arbuscular mycorrhizal fungi reduces Striga hermonthica performance on cereal crops and has the potential to contribute to integrated Striga management. Field Crops Res 91:51–61
Marschner H, Römheld V (1983) In vivo measurement of root-induced pH changes at the soil-root interface. Z Pflanzenphysiol 111:241–251
Müller S, Hauck C, Schildknecht H (1992) Germination stimulants produced by Vigna unguiculata Walp cv. Saunders upright. J Plant Growth Regul 11:77–84
Nagahashi G, Douds DD (2000) Partial separation of root exudates components and their effects upon the growth of germinated spores of AM fungi. Mycol Res 104:1453–1464
Raju PS, Osman MA, Soman P, Peacock JM (1990) Effects of N, P and K on Striga asiatica (L.) Kuntze seed germination and infestation of sorghum. Weed Res 30:139–144
Sato D, Awad AA, Chae SH, Yokota T, Sugimoto Y, Takeuchi Y, Yoneyama K (2003) Analysis of strigolactones, germination stimulants for Striga and Orobanche, by high-performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 51:1162–1168
Sato D, Awad AA, Takeuchi Y, Yoneyama K (2005) Confirmation and quantification of strigolactones, germination stimulants for root parasitic plants Striga and Orobanche, produced by cotton. Biosci Biotechnol Biochem 69:98–102
Siame BP, Weerasuriya Y, Wood K, Ejeta G, Butler LG (1993) Isolation of strigol, a germination stimulant for Striga asiatica, from host plants. J Agric Food Chem 41:1486–1491
Southwood OR (1971) The effects of superphosphate application, 2,4-DB and grazing on broomrape (Orobanche minor Sm.) in a subterranean clover pasture. Weed Res 11:240–246
Tadano T, Tanaka A (1980) The effect of low phosphate concentrations in culture medium on early growth of several crop plants (in Japanese, translated by the authors). Jpn J Soil Sci Plant Nutr 51: 399–404
Tinker PB, Jones MD, Durall DM (1992) A functional comparison of ecto and endomycorrhizas. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wellingfgord, pp 303–310
Xu QF, Tsai CL, Tsai CY (1992) Interaction of potassium with the form and amount of nitrogen nutrition on growth and nitrogen uptake of maize. J Plant Nutr 15:23–33
Yokota T, Sakai H, Okuno K, Yoneyama K, Takeuchi Y (1998) Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49:1967–1973
Yoneyama K, Takeuchi Y, Yokota T (2001) Production of clover broomrape seed germination stimulants by red clover root requires nitrate but is inhibited by phosphate and ammonium. Physiol Plant 112:25–30
Yoneyama K, Sato D, Takeuchi Y, Sekimoto H, Yokota T, Sassa T (2006) Search for germination stimulants and inhibitors for root parasitic weeds. In: Duke SO, Rimando A (eds) Natural products for pest management. ACS, Washington, pp 88–98
Acknowledgments
We thank Dr. D. M. Joel (ARO, Israel) for numerous advices, discussions, and critical reading of the manuscript. A part of this study was supported by the Sasakawa Scientific Research Grant from The Japan Science Society, Grants-in-Aid for Scientific Research (15380079, 1820810) from the Japan Society for the Promotion of Science (JSPS), and a grant for Eminent Research at Utsunomiya University (2003–2006).
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Yoneyama, K., Yoneyama, K., Takeuchi, Y. et al. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225, 1031–1038 (2007). https://doi.org/10.1007/s00425-006-0410-1
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DOI: https://doi.org/10.1007/s00425-006-0410-1