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Shoot-derived signals other than auxin are involved in systemic regulation of strigolactone production in roots

Abstract

Main conclusion

Nitrogen and phosphorus fertilization in one side of split-root sorghum plants systemically reduced root contents of strigolactones in both sides of the split roots. Shoot-derived signals other than auxin appeared to be involved in this process.

Strigolactones (SLs) are a novel class of plant hormones regulating both shoot and root architectures and suggested to be functioning downstream of auxin. The levels of SLs in plant tissues and root exudates are regulated by nutrients, especially phosphorus (P) and nitrogen (N); however, the underlying mechanism remains elusive. We examined the effects of N and P fertilization on root contents of two SLs, sorgomol and 5-deoxystrigol, in sorghum plants pre-incubated under N and P free conditions using a split-root system. N and P fertilization to one side of the split-root plants systemically reduced root contents of SLs in both sides of the split roots. The shoot N and P levels increased when one side of the split-root plants was fertilized, while N and P levels in the non-fertilized split roots were unaffected. N fertilization decreased shoot and root IAA (indole-3-acetic acid) levels, while P fertilization did not affect them. IAA applied to the shoot apices increased root contents of 5-deoxystrigol but not that of sorgomol only when the plants were grown under P free conditions. Shoot (leaf) removal dramatically decreased the root contents of SLs but did not affect root IAA levels, and IAA applied to the stumps of leaves could not restore root contents of SLs. Consequently, shoot-derived signals other than auxin are suggested to be involved in the regulation of SL production in roots.

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Abbreviations

AM:

Arbuscular mycorrhizal

HPLC:

High performance liquid chromatography

IAA:

Indole-3-acetic acid

LC–MS/MS:

Liquid chromatography/tandem mass spectrometry

NPA:

N-naphthylphthalamic acid

SL:

Strigolactone

References

  • Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108:20242–20247. doi:10.1073/pnas.1111902108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. doi:10.1038/nature03608

    Article  CAS  PubMed  Google Scholar 

  • Alvarez JM, Vidal EA, Gutierrez RA (2012) Integration of local and systemic signaling pathways for plant N responses. Curr Opin Plant Biol 15:185–191. doi:10.1016/j.pbi.2012.03.009

    Article  CAS  PubMed  Google Scholar 

  • Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029. doi:10.1111/j.1365-313X.2007.03210.x

    Article  CAS  PubMed  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. doi:10.1007/s10725-006-0009-3

    CAS  Google Scholar 

  • Balzergue C, Puech-Pagès V, Bécard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 62:1049–1060. doi:10.1093/jxb/erq335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhard D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017. doi:10.1111/j.1365-313X.2010.04385.x

    Article  CAS  PubMed  Google Scholar 

  • Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749. doi:10.1111/j.1365-313X.2007.03368.x

    Article  CAS  PubMed  Google Scholar 

  • Chiou T-J, Lin S-I (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206. doi:10.1146/annurev-arplant-042110-103849

    Article  CAS  PubMed  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. doi:10.1126/science.154.3753.1189

    Article  CAS  PubMed  Google Scholar 

  • Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14:364–372. doi:10.1016/j.tplants.2009.04.003

    Article  CAS  PubMed  Google Scholar 

  • Ejeta G, Gressel J (eds) (2007) Integrating new technologies for Striga control: towards ending the witch-hunt. World Scientific Publishing Co. Pte. Ltd., Singapore

    Google Scholar 

  • Foo E (2013) Auxin influences strigolactones in pea mycorrhizal symbiosis. J Plant Physiol 170:523–528. doi:10.1016/j.jplph.2012.11.002

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234:1073–1081. doi:10.1007/s00425-011-1516-7

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17:464–474. doi:10.1105/tpc.104.026716

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87. doi:10.1093/mp/sss115

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Chiou T-J, Lin S-I, Aung K, Zhu J-K (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043. doi:10.1016/j.cub.2005.10.016

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194. doi:10.1038/nature07271

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1016/S0176-1617(11)80497-9

    Article  CAS  Google Scholar 

  • Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22:4523–4533

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144:232–247. doi:10.1104/pp.106.092130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jamil M, Kanampiu FK, Karaya H, Charnikhova T, Bouwmeester HJ (2012) Striga hermonthica parasitism in maize in response to N and P fertilisers. Field Crops Res 134:1–10. doi:10.1016/j.fcr.2012.03.015

    Article  Google Scholar 

  • Johnson X, Brcich T, Dun EA, Goussot M, Haurogné K, Beveridge CA, Rameau C (2006) Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142:1014–1026. doi:10.1104/pp.106.087676

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kapulnik Y, Delaux P-M, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier J-P, Bécard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216. doi:10.1007/s00425-010-1310-y

    Article  CAS  PubMed  Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918

    Article  CAS  PubMed  Google Scholar 

  • Koegel S, Boller T, FL M, Wiemken A, Courty PE (2013) Rapid nitrogen transfer in the Sorghum bicolor-Glomus mosseae arbuscular mycorrhizal symbiosis. Plant Signal Behav 8:e25229. doi:10.4161/psb.25229

    Article  PubMed Central  PubMed  Google Scholar 

  • Koltai H, Cohen M, Chesin O, Mayzlish-Gati E, Bécard G, Puech-Pagès V, Dor BB, Resnick N, Wininger S, Kapulnik Y (2011) Light is a positive regulator of strigolactone levels in tomato roots. J Plant Physiol 168:1993–1996. doi:10.1016/j.jplph.2011.05.022

    Article  CAS  PubMed  Google Scholar 

  • López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874. doi:10.1111/j.1469-8137.2008.02406.x

    Article  PubMed  Google Scholar 

  • Marzec M, Muszynska A, Gruszka D (2013) The role of strigolactones in nutrient-stress responses in plants. Int J Mol Sci 14:9286–9304. doi:10.3390/ijms14059286

    Article  PubMed Central  PubMed  Google Scholar 

  • Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci USA 111:6092–6097. doi:10.1073/pnas.1322045111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nanamori M, Shinano T, Wasaki J, Yamamura T, Rao IM, Osaki M (2004) Low phosphorus tolerance mechanisms: phosphorus recycling and photosynthate partitioning in the tropical forage grass, Brachiaria hybrid cultivar Mulato compared with rice. Plant Cell Physiol 45:460–469. doi:10.1093/pcp/pch056

    Article  CAS  PubMed  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible W-R (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738. doi:10.1111/j.1365-313X.2007.03363.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556. doi:10.1038/nature07723

    Article  CAS  PubMed  Google Scholar 

  • Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734. doi:10.1104/pp.110.166645

    Article  PubMed Central  CAS  PubMed  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. doi:10.1021/jf00033a025

    Article  CAS  Google Scholar 

  • Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, Carcía-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385. doi:10.1016/j.soilbio.2009.11.007

    Article  CAS  Google Scholar 

  • Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot. doi:10.1093/jxb/eru029 (in press)

    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 

  • Toh S, Kamiya Y, Kawakami N, Nambara E, McCourt P, Tsuchiya Y (2012) Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol 53:107–117. doi:10.1093/pcp/pcr176

    Article  CAS  PubMed  Google Scholar 

  • Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6:741–749. doi:10.1038/nchembio.435

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200. doi:10.1038/nature07272

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126. doi:10.1093/pcp/pcq084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. doi:10.1016/j.cell.2009.01.046

    Article  CAS  PubMed  Google Scholar 

  • Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xie X, Yoneyama K, Kusumoto D, Yamada Y, Takeuchi Y, Sugimoto Y, Yoneyama K (2008) Sorgomol, germination stimulant for root parasitic plants, produced by Sorghum bicolor. Tetrahedron Lett 49:2066–2068. doi:10.1016/j.tetlet.2008.01.131

    Article  CAS  Google Scholar 

  • Xie X, Yoneyama K, Kisugi T, Uchida K, Ito S, Akiyama K, Hayashi H, Yokota T, Nomura T, Yoneyama K (2013) Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol Plant 6:153–163. doi:10.1093/mp/sss139

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:399–408. doi:10.1007/s00425-014-2096-0

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) 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. doi:10.1007/s00425-007-0600-5

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038. doi:10.1007/s00425-006-0410-1

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2011) Characterization of strigolactones exuded by Asteraceae plants. Plant Growth Regul 65:495–504. doi:10.1007/s10725-011-9620-z

    Article  CAS  Google Scholar 

  • Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207. doi:10.1007/s00425-011-1568-8

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kisugi T, Nomura T, Yoneyama K (2013) Nitrogen and phosphorus fertilization negatively affects strigolactone production and exudation in sorghum. Planta 238:885–894. doi:10.1007/s00425-013-1943-8

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We acknowledge Prof. Tadao Asami (University of Tokyo), and Dr. Hiroyuki Kasahara (RIKEN) for their generous gifts of 5-deoxystrigol-d6 and [13C6]IAA, respectively. This work was supported by KAKENHI (22-9996) from the Japan Society for the Promotion of Science (JSPS) and by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry. Kaori Yoneyama was supported by a JSPS Research Fellowship for young scientists

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The authors declare that they have no conflict of interest.

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Yoneyama, K., Kisugi, T., Xie, X. et al. Shoot-derived signals other than auxin are involved in systemic regulation of strigolactone production in roots. Planta 241, 687–698 (2015). https://doi.org/10.1007/s00425-014-2208-x

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Keywords

  • Auxin transport inhibitor
  • Indole-3-acetic acid
  • Nitrogen deficiency
  • Phosphorus deficiency
  • Shoot-derived signal
  • Sorghum
  • Strigolactone