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Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis

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Abstract

Strigolactones (SLs) have been proposed as a new group of plant hormones, inhibiting shoot branching, and as signaling molecules for plant interactions. Here, we present evidence for effects of SLs on root development. The analysis of mutants flawed in SLs synthesis or signaling suggested that the absence of SLs enhances lateral root formation. In accordance, roots grown in the presence of GR24, a synthetic bioactive SL, showed reduced number of lateral roots in WT and in max3-11 and max4-1 mutants, deficient in SL synthesis. The GR24-induced reduction in lateral roots was not apparent in the SL signaling mutant max2-1. Moreover, GR24 led to increased root-hair length in WT and in max3-11 and max4-1 mutants, but not in max2-1. SLs effect on lateral root formation and root-hair elongation may suggest a role for SLs in the regulation of root development; perhaps, as a response to growth conditions.

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Abbreviations

CCD7:

Carotenoid cleavage dioxygenase 7

CCD8:

Carotenoid cleavage dioxygenase 8

SL:

Strigolactone

WT:

Wild type

References

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bainbridge K, Sorefan K, Ward S, Leyser O (2005) Hormonally controlled expression of the Arabidopsis MAX4 shoot branching regulatory gene. Plant J 44:569–580

    Article  CAS  PubMed  Google Scholar 

  • Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16:553–563

    Article  CAS  PubMed  Google Scholar 

  • Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, RouxC Bécard G, Séjalon-Delmas N (2006) Mitochondrial activity and presymbiotic growth of arbuscular mycorrhizal fungi are strongly stimulated by strigolactones. PloS Biol 4:1239–1247

    Article  CAS  Google Scholar 

  • Besserer A, Bécard G, Roux C, Jauneau A, Séjalon-Delmas N (2008) GR24, a synthetic analogue of strigolactones, stimulates mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energetic metabolism. Plant Physiol 148:402–413

    Article  CAS  PubMed  Google Scholar 

  • Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493

    Article  CAS  PubMed  Google Scholar 

  • Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852

    Article  CAS  PubMed  Google Scholar 

  • Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171

    Article  CAS  PubMed  Google Scholar 

  • Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Physiol 36:77–115

    Article  CAS  Google Scholar 

  • Delbarre A, Muller P, Imhoff V, Guern J (1996) Comparison of mechanisms controlling uptake and accumulation of 2, 4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198:532–541

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Evans ML, Ishikawa H, Estalle M (1994) Responses of Arabidopsis roots to auxin studied with high temporal resolution: comparison of wild type and auxin-response mutants. Planta 194:215–222

    Article  CAS  Google Scholar 

  • Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin and strigolactone in regulating shoot branching. Plant Physiol 149:1929–1944

    Article  CAS  PubMed  Google Scholar 

  • Floss DS, Walter MH (2009) Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited. Plant Signal Behav 4:172–175

    Article  CAS  PubMed  Google Scholar 

  • García-Garrido JM, Lendzemo V, Castellanos-Morales V, Steinkellner S, Vierheilig H (2009) Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 19:449–459

    Article  PubMed  Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60

    Article  CAS  PubMed  Google Scholar 

  • Goldwasser Y, Yoneyama K, Xie X, Yoneyama K (2008) Production of strigolactones by Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant Growth Regul 55:21–28

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412

    Article  CAS  PubMed  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture method used in the study of plant nutrition, The Eastern Press, 2nd edn. Commonwealth Agricultural Bureau, London

    Google Scholar 

  • Hu Z, Yan H, Yang J, Yamaguchi S, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51:1136–1142

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Johnson AW, Gowda G, Wassanali A, Knox J, Monaco S, Razawi Z, Roseberry G (1981) The preparation of synthetic analogues of strigol. J Chem Soc Perkin Trans 1:1734–1743

    Article  Google Scholar 

  • Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HM, Grierson CS (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11:78–84

    Article  CAS  PubMed  Google Scholar 

  • Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bahattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136

    Article  CAS  Google Scholar 

  • Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant Cell Environ 32:694–703

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  Google Scholar 

  • López-Ráez JA, Bouwmeester H (2008) Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal Behav 3:963–965

    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

    Article  PubMed  Google Scholar 

  • Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    CAS  PubMed  Google Scholar 

  • Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073

    Article  CAS  PubMed  Google Scholar 

  • Matusova R, Rani K, Verstappen FW, Franssen MC, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    Article  CAS  PubMed  Google Scholar 

  • Mouchel CF, Leyser O (2007) Novel phytohormones involved in long-range signaling. Curr Opin Plant Biol 10:473–476

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419

    Article  PubMed  Google Scholar 

  • Ongaro V, Leyser O (2008) Hormonal control of shoot branching. J Exp Bot 59:67–74

    Article  CAS  PubMed  Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560

    Article  CAS  PubMed  Google Scholar 

  • Prusinkiewicz P, Crawford S, Smith RS, Ljung K, Bennett T, Ongaro V, Leyser O (2009) Control of bud activation by an auxin transport switch. Proc Natl Acad Sci USA 106:17431–17436

    Article  CAS  PubMed  Google Scholar 

  • Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46:617–626

    Article  CAS  PubMed  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  CAS  PubMed  Google Scholar 

  • Stirnberg P, Furner IJ, Leyser O (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94

    Article  CAS  PubMed  Google Scholar 

  • Stirnberg P, Ward S, Leyser O (2010) Auxin and strigolactones in shoot branching: intimately connected? Biochem Soc Trans 38:717–722

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    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

    Article  CAS  PubMed  Google Scholar 

  • Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ (2009) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311

    Article  PubMed  Google Scholar 

  • Xie X, Yoneyama K, Kusumoto D, Yamada Y, Yokota T, Takeuchi Y, Yoneyama K (2008) Isolation and identification of alectrol as (+)-orobanchyl acetate, a germination stimulant for root parasitic plants. Phytochemistry 69:427–431

    Article  CAS  PubMed  Google Scholar 

  • Yokota T, Sakal 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, 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

    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

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Bruria Ben-Dor, Smadar Hai, Yulia Kaplan, Natalie Sakman, Maja Cohen and Niv Faig for technical help and Ori Cheshin for consultation. Pierre-Marc Delaux was granted by Grant Award No. CIFRE0391/2008 from Bayer CropScience; Einav Mayzlish-Gati was supported by Research Grant Award No. IS-4211-09F from BARD, The United States—Israel Binational Agricultural Research and Development Fund.

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Authors and Affiliations

  1. Institute of Plant Sciences, Agricultural Research Organization (ARO), The Volcani Center, PO Box 6, Bet Dagan, 50250, Israel

    Yoram Kapulnik, Natalie Resnick, Einav Mayzlish-Gati, Smadar Wininger, Chaitali Bhattacharya, Eduard Belausov & Hinanit Koltai

  2. Surfaces Cellulaires et Signalisation chez les Végétaux, Université de Toulouse, UPS, UMR 5546, BP 42617, 31326, Castanet-Tolosan, France

    Pierre-Marc Delaux, Nathalie Séjalon-Delmas, Jean-Philippe Combier & Guillaume Bécard

  3. UMR 5546, BP 42617, 31326, Castanet-Tolosan, France

    Pierre-Marc Delaux, Nathalie Séjalon-Delmas, Jean-Philippe Combier & Guillaume Bécard

  4. Department of Plant Systems Biology, VIB, Technologiepark 927, 9052, Ghent, Belgium

    Tom Beeckman

  5. Department of Plant Biotechnology and Genetics, Ghent University, Technologiepark 927, 9052, Ghent, Belgium

    Tom Beeckman

  6. Department of Phytopathology and Weed Research, Newe-Ya’ar Research Center, PO Box 1021, Ramat-Yishay, Israel

    Evgenia Dor & Joseph Hershenhorn

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  1. Yoram Kapulnik
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  2. Pierre-Marc Delaux
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  3. Natalie Resnick
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  4. Einav Mayzlish-Gati
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Correspondence to Hinanit Koltai.

Additional information

Y. Kapulnik and P.-M. Delaux have equal contribution.

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Supplementary Fig. 1

Lateral root formation in wild-type Arabidopsis (Col-0, WT) and max3-1 mutant grown under 10−8 M GR24 and control treatments after 12 days of seedling incubation (n = 40). Error bars indicate ± SE. Different letters (a, b) indicate statistically significant different means according to Kruskal–Wallis test and box-plot analysis (PPT 133 kb)

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Kapulnik, Y., Delaux, PM., Resnick, N. et al. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis . Planta 233, 209–216 (2011). https://doi.org/10.1007/s00425-010-1310-y

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