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A phosphoinositide hub connects CLE peptide signaling and polar auxin efflux regulation

Author

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  • Qian Wang

    (University of Lausanne)

  • A. Cecilia Aliaga Fandino

    (University of Lausanne)

  • Moritz Graeff

    (University of Lausanne)

  • Thomas A. DeFalco

    (University of Zurich, Zurich-Basel Plant Science Center
    Western University)

  • Cyril Zipfel

    (University of Zurich, Zurich-Basel Plant Science Center)

  • Christian S. Hardtke

    (University of Lausanne)

Abstract

Auxin efflux through plasma-membrane-integral PIN-FORMED (PIN) carriers is essential for plant tissue organization and tightly regulated. For instance, a molecular rheostat critically controls PIN-mediated auxin transport in developing protophloem sieve elements of Arabidopsis roots. Plasma-membrane-association of the rheostat proteins, BREVIS RADIX (BRX) and PROTEIN KINASE ASSOCIATED WITH BRX (PAX), is reinforced by interaction with PHOSPHATIDYLINOSITOL-4-PHOSPHATE-5-KINASE (PIP5K). Genetic evidence suggests that BRX dampens autocrine signaling of CLAVATA3/EMBRYO SURROUNDING REGION-RELATED 45 (CLE45) peptide via its receptor BARELY ANY MERISTEM 3 (BAM3). How excess CLE45-BAM3 signaling interferes with protophloem development and whether it does so directly or indirectly remains unclear. Here we show that rheostat polarity is independent of PIN polarity, but interdependent with PIP5K. Catalytically inactive PIP5K confers rheostat polarity without reinforcing its localization, revealing a possible PIP5K scaffolding function. Moreover, PIP5K and PAX cooperatively control local PIN abundance. We further find that CLE45-BAM3 signaling branches via RLCK-VII/PBS1-LIKE (PBL) cytoplasmic kinases to destabilize rheostat localization. Our data thus reveal antagonism between CLE45-BAM3-PBL signaling and PIP5K that converges on auxin efflux regulation through dynamic control of PAX polarity. Because second-site bam3 mutation suppresses root as well as shoot phenotypes of pip5k mutants, CLE peptide signaling likely modulates phosphoinositide-dependent processes in various developmental contexts.

Suggested Citation

  • Qian Wang & A. Cecilia Aliaga Fandino & Moritz Graeff & Thomas A. DeFalco & Cyril Zipfel & Christian S. Hardtke, 2023. "A phosphoinositide hub connects CLE peptide signaling and polar auxin efflux regulation," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36200-0
    DOI: 10.1038/s41467-023-36200-0
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    References listed on IDEAS

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    1. Shunsuke Miyashima & Pawel Roszak & Iris Sevilem & Koichi Toyokura & Bernhard Blob & Jung-ok Heo & Nathan Mellor & Hanna Help-Rinta-Rahko & Sofia Otero & Wouter Smet & Mark Boekschoten & Guido Hooivel, 2019. "Mobile PEAR transcription factors integrate positional cues to prime cambial growth," Nature, Nature, vol. 565(7740), pages 490-494, January.
    2. Bernard Moret & Petra Marhava & Ana Cecilia Aliaga Fandino & Christian S. Hardtke & Kirsten H. W. ten Tusscher, 2020. "Local auxin competition explains fragmented differentiation patterns," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Martin Bonke & Siripong Thitamadee & Ari Pekka Mähönen & Marie-Theres Hauser & Ykä Helariutta, 2003. "APL regulates vascular tissue identity in Arabidopsis," Nature, Nature, vol. 426(6963), pages 181-186, November.
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