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Research ArticleDEVELOPMENT AND HORMONE ACTION
Open Access

Strigolactones Are Involved in Root Response to Low Phosphate Conditions in Arabidopsis

Einav Mayzlish-Gati, Carolien De-Cuyper, Sofie Goormachtig, Tom Beeckman, Marnik Vuylsteke, Philip B. Brewer, Christine A. Beveridge, Uri Yermiyahu, Yulia Kaplan, Yael Enzer, Smadar Wininger, Natalie Resnick, Maja Cohen, Yoram Kapulnik, Hinanit Koltai
Einav Mayzlish-Gati
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Carolien De-Cuyper
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Sofie Goormachtig
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Tom Beeckman
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Marnik Vuylsteke
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Philip B. Brewer
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Christine A. Beveridge
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Uri Yermiyahu
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Yulia Kaplan
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Yael Enzer
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Smadar Wininger
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Natalie Resnick
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Maja Cohen
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Yoram Kapulnik
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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Hinanit Koltai
Institute of Plant Sciences, Agricultural Research Organization, Bet Dagan 50250, Israel (E.M.-G., Y.K., Y.E., S.W., N.R., M.C., Y.K., H.K.); Department of Plant Systems Biology and Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (C.D.-C., S.G., T.B., M.V.); School of Biological Sciences, The University of Queensland, St Lucia, Brisbane 4072, Australia (P.B.B., C.A.B.); Gilat Research Center, Agricultural Research Organization, Negev 2 85280, Israel (U.Y.); and Mina and Everard Goodman Faculty of Life Sciences, Bar-ilan University, Ramat Gan 52900, Israel (M.C.)
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  • For correspondence: hkoltai@volcani.agri.gov.il

Published November 2012. DOI: https://doi.org/10.1104/pp.112.202358

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Abstract

Strigolactones (SLs) are plant hormones that suppress lateral shoot branching, and act to regulate root hair elongation and lateral root formation. Here, we show that SLs are regulators of plant perception of or response to low inorganic phosphate (Pi) conditions. This regulation is mediated by MORE AXILLARY GROWTH2 (MAX2) and correlated with transcriptional induction of the auxin receptor TRANSPORT INHIBITOR RESPONSE1 (TIR1). Mutants of SL signaling (max2-1) or biosynthesis (max4-1) showed reduced response to low Pi conditions relative to the wild type. In max4-1, but not max2-1, the reduction in response to low Pi was compensated by the application of a synthetic strigolactone GR24. Moreover, AbamineSG, which decreases SL levels in plants, reduced the response to low Pi in the wild type, but not in SL-signaling or biosynthesis mutants. In accordance with the reduced response of max2-1 to low Pi relative to the wild type, several phosphate-starvation response and phosphate-transporter genes displayed reduced induction in max2-1, even though Pi content in max2-1 and the wild type were similar. Auxin, but not ethylene, was sufficient to compensate for the reduced max2-1 response to low Pi conditions. Moreover, the expression level of TIR1 was induced under low Pi conditions in the wild type, but not in max2-1. Accordingly, the tir1-1 mutant showed a transient reduction in root hair density in comparison with the wild type under low Pi conditions. Therefore, we suggest that the response of plants to low Pi is regulated by SLs; this regulation is transmitted via the MAX2 component of SL signaling and is correlated with transcriptional induction of the TIR1 auxin receptor.

  • Glossary

    SL
    strigolactone
    LR
    lateral root
    RH
    root hair
    P
    phosphorus
    PI
    inorganic phosphate
    PSI
    inorganic phosphate starvation-induced
    PHT
    phosphate transporter
    PR
    primary root
    IAA
    indole-3-acetic acid
    Col-0
    Columbia-0
    hpg
    h post germination
    dpg
    d post germination
    ACC
    1-aminocyclopropane-1-carboxylic acid
    REML
    residual maximum likelihood
    qPCR
    quantitative PCR
    Ct
    threshold cycle
    • Received June 21, 2012.
    • Accepted September 10, 2012.
    • Published September 11, 2012.

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    Strigolactones Are Involved in Root Response to Low Phosphate Conditions in Arabidopsis
    Einav Mayzlish-Gati, Carolien De-Cuyper, Sofie Goormachtig, Tom Beeckman, Marnik Vuylsteke, Philip B. Brewer, Christine A. Beveridge, Uri Yermiyahu, Yulia Kaplan, Yael Enzer, Smadar Wininger, Natalie Resnick, Maja Cohen, Yoram Kapulnik, Hinanit Koltai
    Plant Physiology Nov 2012, 160 (3) 1329-1341; DOI: 10.1104/pp.112.202358

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    Strigolactones Are Involved in Root Response to Low Phosphate Conditions in Arabidopsis
    Einav Mayzlish-Gati, Carolien De-Cuyper, Sofie Goormachtig, Tom Beeckman, Marnik Vuylsteke, Philip B. Brewer, Christine A. Beveridge, Uri Yermiyahu, Yulia Kaplan, Yael Enzer, Smadar Wininger, Natalie Resnick, Maja Cohen, Yoram Kapulnik, Hinanit Koltai
    Plant Physiology Nov 2012, 160 (3) 1329-1341; DOI: 10.1104/pp.112.202358
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