RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis

Significance Regulation of growth is crucial for overall plant development and its adaptation to environment. Peptide rapid alkalinization factors 1 (RALF1) and phytohormone auxin are key growth regulators with characteristic both rapid and long-term effects. However, the underlying mechanism and coordination of these signals are unclear. Our study reveals that those two signals trigger rapid growth inhibition (<1 min) by rapidly alkalinizing the apoplast, a result of rapid net H+ influx across the plasma membrane; nonetheless, their signaling mechanisms are independent. RALF1 sustains root growth inhibition long term by inducing auxin biosynthesis and signaling. These discoveries contribute to the understanding of rapid plant growth responses and hormone-peptide cross-talk for optimization of plant growth and architecture also relevant for agriculture applications.

[1]  Zhenbiao Yang,et al.  TMK-based cell-surface auxin signalling activates cell-wall acidification , 2021, Nature.

[2]  J. Merrin,et al.  Cell surface and intracellular auxin signalling for H+ fluxes in root growth , 2021, Nature.

[3]  J. Friml Fourteen Stations of Auxin. , 2021, Cold Spring Harbor perspectives in biology.

[4]  Shivani Dubey,et al.  No Time for Transcription-Rapid Auxin Responses in Plants. , 2021, Cold Spring Harbor perspectives in biology.

[5]  C. Schwechheimer,et al.  Naphthylphthalamic acid associates with and inhibits PIN auxin transporters , 2020, Proceedings of the National Academy of Sciences.

[6]  J. Friml,et al.  Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants , 2020, Science Advances.

[7]  Sha Li,et al.  FERONIA mediates root nutating growth. , 2020, The Plant journal : for cell and molecular biology.

[8]  S. Shabala,et al.  Evidence for multiple receptors mediating RALF-triggered Ca2+ signaling and proton pump inhibition. , 2020, The Plant journal : for cell and molecular biology.

[9]  Xiaojuan Li,et al.  The RALF1-FERONIA interaction modulates endocytosis to mediate control of root growth in Arabidopsis , 2020, Development.

[10]  L. Strader,et al.  Old Town Roads: routes of auxin biosynthesis across kingdoms. , 2020, Current opinion in plant biology.

[11]  W. Gray,et al.  Rapid Auxin-Mediated Cell Expansion. , 2020, Annual review of plant biology.

[12]  M. Haruta,et al.  Twenty Years of Progress in Physiological and Biochemical Investigation of RALF Peptides1[OPEN] , 2020, Plant Physiology.

[13]  Weiman Xing,et al.  A phosphorylation-based switch controls TAA1-mediated auxin biosynthesis in plants , 2020, Nature Communications.

[14]  Rongfeng Huang,et al.  Noncanonical auxin signaling regulates cell division pattern during lateral root development , 2019, Proceedings of the National Academy of Sciences.

[15]  J. Friml,et al.  TMK1-mediated auxin signalling regulates differential growth of the apical hook , 2019, Nature.

[16]  Qingkun Dong,et al.  FERONIA regulates auxin‐mediated lateral root development and primary root gravitropism , 2019, FEBS letters.

[17]  S. Assmann,et al.  A kinase‐dead version of FERONIA receptor‐like kinase has dose‐dependent impacts on rosette morphology and RALF1‐mediated stomatal movements , 2018, FEBS letters.

[18]  M. Sussman,et al.  Probing a Plant Plasma Membrane Receptor Kinase's Three-Dimensional Structure Using Mass Spectrometry-Based Protein Footprinting. , 2018, Biochemistry.

[19]  R. Sormani,et al.  Receptor Kinase THESEUS1 Is a Rapid Alkalinization Factor 34 Receptor in Arabidopsis , 2018, Current Biology.

[20]  M. Sussman,et al.  Comparison of the effects of a kinase‐dead mutation of FERONIA on ovule fertilization and root growth of Arabidopsis , 2018, FEBS letters.

[21]  J. Merrin,et al.  Rapid and reversible root growth inhibition by TIR1 auxin signalling , 2018, Nature Plants.

[22]  X. Dumont,et al.  Uncovering pH at both sides of the root plasma membrane interface using noninvasive imaging , 2018, Proceedings of the National Academy of Sciences.

[23]  J. Friml,et al.  Real-time Analysis of Auxin Response, Cell Wall pH and Elongation in Arabidopsis thaliana Hypocotyls , 2018, Bio-protocol.

[24]  S. Braybrook,et al.  Acid growth: an ongoing trip. , 2018, Journal of experimental botany.

[25]  M. Silva-Filho,et al.  Arabidopsis thaliana rapid alkalinization factor 1–mediated root growth inhibition is dependent on calmodulin-like protein 38 , 2017, The Journal of Biological Chemistry.

[26]  M. Silva-Filho,et al.  BAK1 is involved in AtRALF1-induced inhibition of root cell expansion , 2017, PLoS genetics.

[27]  Huw A. Ogilvie,et al.  Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. , 2017, Molecular plant pathology.

[28]  J. Friml,et al.  Live tracking of moving samples in confocal microscopy for vertically grown roots , 2017, eLife.

[29]  W. Busch,et al.  Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana , 2017, Proceedings of the National Academy of Sciences.

[30]  S. Turner,et al.  A Comprehensive Analysis of RALF Proteins in Green Plants Suggests There Are Two Distinct Functional Groups , 2017, Front. Plant Sci..

[31]  M. Estelle,et al.  Mechanisms of auxin signaling , 2016, Development.

[32]  T. Kinoshita,et al.  The Plasma Membrane H+-ATPase AHA1 Plays a Major Role in Stomatal Opening in Response to Blue Light1 , 2016, Plant Physiology.

[33]  David Turrà,et al.  A fungal pathogen secretes plant alkalinizing peptides to increase infection , 2016, Nature Microbiology.

[34]  Teva Vernoux,et al.  Reporters for sensitive and quantitative measurement of auxin response , 2015, Nature Methods.

[35]  M. Sussman,et al.  SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in Arabidopsis[C][W] , 2014, Plant Cell.

[36]  Josh T. Cuperus,et al.  New Generation of Artificial MicroRNA and Synthetic Trans-Acting Small Interfering RNA Vectors for Efficient Gene Silencing in Arabidopsis1[W][OPEN] , 2014, Plant Physiology.

[37]  Y. Kamiya,et al.  Yucasin is a potent inhibitor of YUCCA, a key enzyme in auxin biosynthesis. , 2014, The Plant journal : for cell and molecular biology.

[38]  M. Sussman,et al.  A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion , 2014, Science.

[39]  J. Friml,et al.  Local Auxin Sources Orient the Apical-Basal Axis in Arabidopsis Embryos , 2013, Current Biology.

[40]  K. Ljung,et al.  Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. , 2012, The Plant journal : for cell and molecular biology.

[41]  H. Nozaki,et al.  Rational design of an auxin antagonist of the SCF(TIR1) auxin receptor complex. , 2012, ACS chemical biology.

[42]  Jun Cao,et al.  Evolution of the RALF Gene Family in Plants: Gene Duplication and Selection Patterns , 2012, Evolutionary bioinformatics online.

[43]  A. Cheung,et al.  THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases? , 2011, Current opinion in plant biology.

[44]  Zhenbiao Yang,et al.  A Small-Molecule Screen Identifies l-Kynurenine as a Competitive Inhibitor of TAA1/TAR Activity in Ethylene-Directed Auxin Biosynthesis and Root Growth in Arabidopsis[C][W] , 2011, Plant Cell.

[45]  H. Kawaide,et al.  The main auxin biosynthesis pathway in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[46]  P. Benfey,et al.  Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching , 2010, Science.

[47]  Jan Petrásek,et al.  Auxin transport routes in plant development , 2009, Development.

[48]  M. Sussman,et al.  A cytoplasmic Ca2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: identification of AtRALF1 peptide. , 2008, Biochemistry.

[49]  Johan Trygg,et al.  High-throughput data analysis for detecting and identifying differences between samples in GC/MS-based metabolomic analyses. , 2005, Analytical chemistry.

[50]  Masashi Yamada,et al.  Plant development is regulated by a family of auxin receptor F box proteins. , 2005, Developmental cell.

[51]  M. Sjöström,et al.  Design of experiments: an efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. , 2004, Analytical biochemistry.

[52]  O. Leyser,et al.  AXR3 and SHY2 interact to regulate root hair development , 2003, Development.

[53]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[54]  G. Pearce,et al.  RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. Friml,et al.  Evaluation of Gravitropism in Non-seed Plants. , 2022, Methods in molecular biology.

[56]  S. Persson,et al.  Faculty of 1000 evaluation for SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H -ATPases to Promote Cell Expansion in Arabidopsis. , 2015 .