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The PSI family of nuclear proteins is required for growth in arabidopsis

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Abstract

PSI1 was identified as a gene that is co-expressed with the phytosulfokine (PSK) receptor genes PSKR1 and PSKR2 in Arabidopsis thaliana. It represents a plant-specific protein family of unknown function with six members in two clades. Clade 1 members PSI1, PSI2 and PSI3 were characterized in this study. All three are nuclear localized. A predicted N-terminal myristoylation site was functionally analyzed. psi1-1 seedlings have shorter roots and hypocotyls. This growth-retarded phenotype was restored by expression of either wildtype PSI1 or PSI1 G2A with a mutated myristate attachment site in the psi1-1 background suggesting that myristate attachment was not essential for PSI1 function. psi2-1 and psi3-1 seedlings have a wildtype phenotype but overexpression of PSI1 or PSI2 promoted seedling growth. PSI2 activity appears to be linked to PSK signaling as psi2-1 and psi2-1 psi3-1 roots are unresponsive to PSK. PSI3 functions in vegetative plant growth synergistic with PSI2. psi3-1 and particularly psi2-1 psi3-1 rosettes are small. Overexpression of PSI3 promoted plant growth indicating that PSI3 is limiting at the vegetative stage. Severe dwarfism of psi2-1 psi3-1 plants results from reduced cell growth and proliferation and premature leaf growth arrest. Plants further display reduced fertility and premature senescence revealing a crucial function of PSI proteins in vegetative growth and reproduction. Psi single and double knock-out plants have less and PSI3ox plants have more starch compared to wt and growth retardation is partially rescued by sucrose. Our studies reveal a crucial function of the nuclear-localized PSI proteins in growth possibly through metabolic control.

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References

  • Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci USA 104:18333–18338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branchs: a fast, accurate and powerful alternative. Syst Biol 55:539–552

    Article  PubMed  Google Scholar 

  • Bailey JM, Whelan WJ (1961) Physical properties of starch. I. Relationship between iodine stain and chain length. J Biol Chem 236:969–973

    CAS  PubMed  Google Scholar 

  • Boisson B, Giglione C, Meinnel T (2003) Unexpected protein families including cell defense components feature in the N-myristoylome of a higher eukaryote. J Biol Chem 278:43418–43429

    Article  CAS  PubMed  Google Scholar 

  • Brameier M, Krings A, MacCallum RM (2007) NucPred- predicting nuclear localization of proteins. Bioinformatics 23:1159–1160

    Article  CAS  PubMed  Google Scholar 

  • Braun P, Carvunis AR, Charloteaux B, Dreze M, Ecker JR, Hill DE, Roth FP, Vidal M, Galli M, Balumuri P, Bautista V, Chesnut JD, Kim RC, de los Reyes C, Gilles P, Kim CJ, Matrubutham U, Mirchandani J, Olivares E, Patnaik S, Quan R, Ramaswamy G, Shinn P, Swamilingiah GM, Wu S, Ecker JR, Dreze M, Byrdsong D, Dricot A, Duarte M, Gebreab F, Gutierrez BJ, MacWilliams A, Monachello D, Mukhtar MS, Poulin MM, Reichert P, Romero V, Tam S, Waaijers S, Weiner EM, Vidal M, Hill DE, Braun P, Galli M, Carvunis AR, Cusick ME, Dreze M, Romero V, Roth FP, Tasan M, Yazaki J, Braun P, Ecker JR, Carvunis AR, Ahn YY, Barabási AL, Charloteaux B, Chen H, Cusick ME, Dangl JL, Dreze M, Ecker JR, Fan C, Gai L, Galli M, Ghoshal G, Hao T, Hill DE, Lurin C, Milenkovic T, Moore J, Mukhtar MS, Pevzner SJ, Przulj N, Rabello S, Rietman EA, Rolland T, Roth FP, Santhanam B, Schmitz RJ, Spooner W, Stein J, Tasan M, Vandenhaute J, Ware D, Braun P, Vidal M (2011) Evidence for network evolution in an arabidopsis interactome map. Arabidopsis interactome mapping consortium. Science 333:601–607

  • Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM (2009) Plant peptides in signalling: looking for new partners. Trends Plant Sci 14:255–263

    Article  CAS  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Chevenet F, Brun C, Banuls AL, Jacq B, Chisten R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439

    Article  PubMed Central  PubMed  Google Scholar 

  • Clough S, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Damm B, Willmitzer L (1988) Regeneration of fertile plants from protoplasts of different Arabidopsis thaliana genotypes. Mol Gen Genet 213:15–20

    Article  Google Scholar 

  • Damm B, Schmidt R, Willmitzer L (1989) Efficient transformation of Arabidopsis thaliana using direct gene transfer to protoplasts. Mol Gen Genet 217:6–12

    Article  CAS  PubMed  Google Scholar 

  • De Vylder J, Vandenbussche F, Hu Y, Philips W, van der Straeten D (2013) Rosette tracker: an open source image analysis tool for automatic quantification of genotype effects. Plant Physiol 160:1149–1159

    Article  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469

  • Dereeper A, Audic S, Claverie J, Blanc G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10:8

    Article  PubMed Central  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ (2013) STRING v9.1: protein–protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808–D815

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:295–305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gräf P, Weiler EW (1989) ATP-driven Ca2+-transport in sealed plasma membrane vesicles prepared by aqueous two-phase partitioning from leaves of Commelia communis. Physiol Plant 75:469–478

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hartmann J, Stührwohldt N, Dahlke RI, Sauter M (2013) Phytosulfokine control of growth occurs in the epidermis, is likely non-cell autonomous and dependent on brassinosteroids. Plant J 73:579–590

    Article  CAS  PubMed  Google Scholar 

  • Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed Central  PubMed  Google Scholar 

  • Jun JH, Fiume E, Fletcher JC (2008) The CLE family of plant polypeptide signaling molecules. Cell Mol Life Sci 65:743–755

    Article  CAS  PubMed  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  CAS  PubMed  Google Scholar 

  • Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106:15067–15072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kutschmar A, Rzewuski G, Stührwohldt N, Beemster GTS, Inzé D, Sauter M (2009) PSK-α promotes root growth in Arabidopsis. New Phytol 181:820–831

    Article  CAS  PubMed  Google Scholar 

  • Lorbiecke R, Sauter M (2002) Comparative analysis of PSK peptide growth factor precursor homologs. Plant Sci 163:321–332

    Article  CAS  Google Scholar 

  • Marré E (1979) Fusicoccin: a tool in plant physiology. Annual Rev Plant Physiol 30:273–288

    Article  Google Scholar 

  • Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93:7623–7627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y (2006) Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol 142:45–53

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Plant Physiol 15:473–497

    Article  CAS  Google Scholar 

  • Saiga S, Furumizu C, Yokoyama R, Kurata T, Sato S, Kato T, Tabata S, Suzuki M, Komeda Y (2008) The Arabidopsis OBERON1 and OBERON2 genes encode plant homeodomain finger proteins and are required for apical meristem maintenance. Development 135:1751–1759

    Article  CAS  PubMed  Google Scholar 

  • Snel B, Lehmann G, Bork P, Huynen MA (2000) STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 28:3442–3444

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Srinivasasainagendra V, Page GP, Mehta T, Coulibaly I, Loraine AE (2008) CressExpress: a tool for large-scale mining of expression data from Arabidopsis. Plant Physiol 147:1004–1016

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Srivastava R, Liu JX, Howell S (2009) Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J 56:219–227

    Article  Google Scholar 

  • Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved geentic modules. Science 302:249–255

    Article  CAS  PubMed  Google Scholar 

  • Stührwohldt N, Dahlke RI, Steffens B, Johnson A, Sauter M (2011) Phytosulfokine-α controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS ONE 6:e21054

    Article  PubMed Central  PubMed  Google Scholar 

  • Thomas CL, Schmidt D, Bayer EM, Dreos R, Maule AJ (2009) Arabidopsis plant homeodomain finger proteins operate downstream of auxin accumulation in specifying the vasculature and primary root meristem. Plant J 59:426–436

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi S, Fusada N, Hayashi H, Utsumi T, Uozumi N, Endo Y, Tozawa Y (2010) The consensus motif for N-myristoylation of plant proteins in a wheat germ cell-free translation system. FEBS J 277:3596–3607

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Matsubayashi Y, Hagani H, Sakagami Y (2000) Phytosulfokine-α, a peptide growth factor found in higher plants: its structure, functions and receptors. Plant Cell Physiol 41:825–830

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (2001) Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol 127:842–851

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

Authors acknowledge expert technical assistance by Timo Staffel. We are grateful to Christina Pielke for help in generating psi1-1 psi3-1 and psi2-1 psi3-1 double mutants.

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Authors and Affiliations

  1. Plant Developmental Biology and Plant Physiology, University of Kiel, Am Botanischen Garten 5, 24118, Kiel, Germany

    Nils Stührwohldt, Jens Hartmann, Renate I. Dahlke & Margret Sauter

  2. Center for Plant Molecular Biology, Plant Physiology, University of Tübingen, Auf der Morgenstelle 5, 72076, Tübingen, Germany

    Claudia Oecking

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  1. Nils Stührwohldt
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  2. Jens Hartmann
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  3. Renate I. Dahlke
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  4. Claudia Oecking
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  5. Margret Sauter
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Correspondence to Margret Sauter.

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Stührwohldt, N., Hartmann, J., Dahlke, R.I. et al. The PSI family of nuclear proteins is required for growth in arabidopsis. Plant Mol Biol 86, 289–302 (2014). https://doi.org/10.1007/s11103-014-0229-2

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  • DOI: https://doi.org/10.1007/s11103-014-0229-2

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