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Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites

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Abstract

Strigolactones released from plant roots induce hyphal branching of symbiotic arbuscular mycorrhizal (AM) fungi and germination of root parasitic weeds, Striga and Orobanche spp. We already demonstrated that, in red clover plants (Trifolium pratense L.), 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, Ca, Mg) in the culture medium significantly promoted the secretion of a strigolactone, orobanchol, by the roots of this plant. Here we show that in the case of sorghum [Sorghum bicolor (L.) Moench], a host of both the root hemiparasitic plant Striga hermonthica and AM fungi, N deficiency as well as P deficiency markedly enhanced the secretion of a strigolactone, 5-deoxystrigol. The 5-deoxystrigol content in sorghum root tissues also increased under both N deficiency and P deficiency, comparable to the increase in the root exudates. These results suggest that strigolactones may be rapidly released after their production in the roots. Unlike the situation in the roots, neither N nor P deficiency affected the low content of 5-deoxystrigol in sorghum shoot tissues.

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Abbreviations

AM:

Arbuscular mycorrhizal

Mes:

4-Morpholineethanesulfonic acid

LC/MS/MS:

High performance liquid chromatography/tandem mass spectrometry

References

  • Abu Irmaileh BE (1994) Nitrogen reduces branched broomrape (Orobanche ramosa) seed germination. Weed Sci 42:57–60

    Google Scholar 

  • Akiyama, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931

    Article  PubMed  CAS  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Buee M, Rossignol M, Jauneau A, Ranjeva R, Beard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13:693–698

    Article  PubMed  CAS  Google Scholar 

  • Cechin I, Press MC (1993) Nitrogen relations of the sorghum-Striga hermonthica host–parasite association: germination, attachment and early growth. New Phytol 124:681–687

    Article  CAS  Google Scholar 

  • Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11:263–266

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 94:6198–9199

    Article  CAS  Google Scholar 

  • Epstein E, Bloom JA (2004) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Citernesi S A, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593

    Article  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Harrison JM (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Article  PubMed  CAS  Google Scholar 

  • Hauck C, Muller S, Schildknecht H (1992) A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. J Plant Physiol 139:474–478

    CAS  Google Scholar 

  • He HX, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567

    Article  Google Scholar 

  • Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411

    Article  PubMed  CAS  Google Scholar 

  • Jain R, Foy CL (1992) Nutrient effects on parasitism and germination of Egyptian broomrape (Orobanche aegyptiaca). Weed Technol 6:269–275

    CAS  Google Scholar 

  • Joel DM (2000) The long-term approach to parasitic weeds control: manipulation of specific developmental mechanisms of the parasite. Crop Prot 19:753–758

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Joel DM, Hershenhorm J, Eizenberg H, Aly R, Ejeta G, Rich P J, Ransom J K, Sauerborn J, Rubiales D (2007) Biology and management of weedy root parasites. In: Janick J (ed) Horticultural reviews, vol 33. Willey, New York, pp 267–350

    Chapter  Google Scholar 

  • Lendzemo VW, Kuyper TW, Kropff MJ, Ast AV (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

    Article  Google Scholar 

  • Marschner H (2002) Mineral nutrition of higher plants, 2nd edn. Academic, California

    Google Scholar 

  • Müller S, Hauck C, Schildknecht H (1992) Germination stimulants produced by Vigna unguiculata Walp cv. Saunders upright. J Plant Growth Regul 11:77–84

    Article  Google Scholar 

  • Mumera LM, Below FE (1993) Role of nitrogen in resistance to Striga parasitism of maize. Crop Sci 33:758–763

    Article  CAS  Google Scholar 

  • Muurinen S, Slafer GA, Peltonen-Sainio P (2006) Breeding effects on nitrogen use efficiency of spring cereals under northern conditions. Crop Sci 46:561–568

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Parker C, Riches R C (1993) Parasitic weeds of the world: biology and control. CAB International, Wallingford

    Google Scholar 

  • Raghothama GK (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the early Devonian. Mycologia 87:560–573

    Article  Google Scholar 

  • Wang X, Yost RS, Linquist BA (2001) Soil aggregate size affects phosphorus desorption from highly weathered soils and plant growth. Soil Sci Soc Am J 65:139–146

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge Dr. Kohki Akiyama (Osaka Prefecture University) for generous gift of synthetic (±)-5-deoxystrigol. We thank Dr. D. M. Joel (Agricultural Research Organization, Ramat Yishay, Israel) for critical reading of the manuscript. A part of this study was supported by the Sasakawa Scientific Research Grant from The Japan Science Society, a Grant-in Aid for Scientific Research (1820810) from Japan Society for the Promotion of Science (JSPS), and a grant for Eminent Research at Utsunomiya University (2006).

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Authors and Affiliations

  1. Weed Science Center, Utsunomiya University, 350 Mine-machi, Utsunomiya, 321-8505, Japan

    Kaori Yoneyama, Xiaonan Xie, Dai Kusumoto, Yasutomo Takeuchi & Koichi Yoneyama

  2. Department of Bioproductive Sciences, Faculty of Agriculture, Utsunomiya University, 350 Mine-machi, Utsunomiya, 321-8505, Japan

    Hitoshi Sekimoto

  3. Faculty of Agriculture, Kobe University, 1-1 Rokkodai-cho, Nada, Kobe, 657-8501, Japan

    Yukihiro Sugimoto

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  1. Kaori Yoneyama
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  2. Xiaonan Xie
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  3. Dai Kusumoto
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  4. Hitoshi Sekimoto
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  5. Yukihiro Sugimoto
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  6. Yasutomo Takeuchi
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  7. Koichi Yoneyama
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Correspondence to Koichi Yoneyama.

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Yoneyama, K., Xie, X., Kusumoto, D. et al. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227, 125–132 (2007). https://doi.org/10.1007/s00425-007-0600-5

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  • DOI: https://doi.org/10.1007/s00425-007-0600-5

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