Analysis of peptide PSY1 responding transcripts in the two Arabidopsis plant lines: wild type and psy1r receptor mutant

BMC Genomics

Anja T Fuglsang²  Kirsten Jørgensen¹  Rubini Kannangara¹  Khalid Mahmood² 

[1] Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark;PUMPKIN, Centre for membrane pumps in cells and disease, Copenhagen, Denmark

关键词: Small signaling peptides;    Signaling cascade;    Microarray;    Gene enrichment analysis;    Cellular functions;   

Others  :  1216660
DOI  :  10.1186/1471-2164-15-441

 received in 2013-12-20, accepted in 2014-05-20,  发布年份 2014

【 摘 要 】

Background

Small-secreted peptides are emerging as important components in cell-cell communication during basic developmental stages of plant cell growth and development. Plant peptide containing sulfated tyrosine 1 (PSY1) has been reported to promote cell expansion and differentiation in the elongation zone of roots. PSY1 action is dependent on a receptor PSY1R that triggers a signaling cascade leading to cell elongation. However little is known about cellular functions and the components involved in PSY1-based signaling cascade.

Results

Differentially expressed genes were identified in a wild type plant line and in a psy1r receptor mutant line of Arabidopsis thaliana after treatment with PSY1. Seventy-seven genes were found to be responsive to the PSY1 peptide in wild type plants while 154 genes were responsive in the receptor mutant plants. PSY1 activates the transcripts of genes involved in cell wall modification. Gene enrichment analysis revealed that PSY1-responsive genes are involved in responses to stimuli, metabolic processes and biosynthetic processes. The significant enrichment terms of PSY1-responsive genes were higher in psy1r mutant plants compared to in wild type plants. Two parallel responses to PSY1 were identified, differing in their dependency on the PSY1R receptor. Promoter analysis of the differentially expressed genes identified a light regulatory motif in some of these.

Conclusion

PSY1-responsive genes are involved in cellular functions and stimuli responses suggesting a crosstalk between developmental cues and environmental stimuli. Possibly, two parallel responses to PSY1 exist. A motif involved in light regulation was identified in the promoter region of the differentially expressed genes. Reduced hypocotyl growth was observed in etiolated receptor mutant seedlings.

【 授权许可】

   
2014 Mahmood et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Sparks E, Wachsman G, Benfey PN: Spatiotemporal signalling in plant development. Nat Rev Genet 2013, 14(9):631-644.
• [2]Murphy E, Smith S, De Smet I: Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 2012, 24(8):3198-3217.
• [3]Wang YH, Irving HR: Developing a model of plant hormone interactions. Plant Signal Behav 2011, 6(4):494-500.
• [4]Zan Y, Ji Y, Zhang Y, Yang S, Song Y, Wang J: Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes. BMC Genomics 2013, 14:318. BioMed Central Full Text
• [5]Walker JC, Zhang R: Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 1990, 345(6277):743-746.
• [6]Lee JS, Torii KU: A tale of two systems: peptide ligand-receptor pairs in plant development. Cold Spring Harb Symp Quant Biol 2012, 77:83-89.
• [7]Matsubayashi Y: Ligand-receptor pairs in plant peptide signaling. J Cell Sci 2003, 116:3863-3870.
• [8]Kholodenko BN: Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 2006, 7(3):165-176.
• [9]Xiong L, Schumaker KS, Zhu JK: Cell signaling during cold, drought, and salt stress. Plant Cell 2002, 14(Suppl):S165-S183.
• [10]Chow B, McCourt P: Plant hormone receptors: perception is everything. Genes Dev 2006, 20(15):1998-2008.
• [11]Harashima H, Schnittger A: The integration of cell division, growth and differentiation. Curr Opin Plant Biol 2010, 13(1):66-74.
• [12]Gray WM: Hormonal regulation of plant growth and development. PLoS Biol 2004, 2(9):E311.
• [13]Mitchell CA, Myers PN: Mechanical stress regulation of plant growth and development. Hortic Rev 1995, 17:1-42.
• [14]Montgomery BL: Right place, right time: Spatiotemporal light regulation of plant growth and development. Plant Signal Behav 2008, 3(12):1053-1060.
• [15]Czyzewicz N, Yue K, Beeckman T, Smet ID: Message in a bottle: small signalling peptide outputs during growth and development. J Exp Bot 2013, 64(17):5281-5296.
• [16]Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y: Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci U S A 2007, 104(46):18333-18338.
• [17]Mosher S, Kemmerling B: PSKR1 and PSY1R-mediated regulation of plant defense responses. Plant Signal Behav 2013, 8(5):e24119.
• [18]Mosher S, Seybold H, Rodriguez P, Stahl M, Davies KA, Dayaratne S, Morillo SA, Wierzba M, Favery B, Keller H, Tax FE, Kemmerling B: The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J 2013, 73(3):469-482.
• [19]Du Z, Zhou X, Ling Y, Zhang Z, Su Z: agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38:64-70.
• [20]Muller K, Linkies A, Vreeburg RA, Fry SC, Krieger-Liszkay A, Leubner-Metzger G: In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 2009, 150(4):1855-1865.
• [21]Willats WG, Orfila C, Limberg G, Buchholt HC, van Alebeek GJ, Voragen AG, Marcus SE, Christensen TM, Mikkelsen JD, Murray BS, Knox JP: Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem 2001, 276(22):19404-19413.
• [22]Yu L, Sun J, Li L: PtrCel9A6, an Endo-1,4-beta-Glucanase, Is Required for Cell Wall Formation during Xylem Differentiation in Populus. Mol Plant 2013, 6(6):1904-1917.
• [23]Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Nakamura Y, Tabata S, Shibata D: Role of the putative membrane-bound endo-1,4-beta-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 2001, 42(3):251-263.
• [24]Hayashi T: The primary wall controls plant cell growth. Tanpakushitsu kakusan koso Protein, nucleic acid, enzyme 1992, 37(15):2968-2976.
• [25]Karin M: Signal transduction and gene control. Curr Opin Cell Biol 1991, 3(3):467-473.
• [26]Giehl RF, Lima JE, von Wiren N: Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 2012, 24(1):33-49.
• [27]Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L: The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 2004, 279(15):15348-15355.
• [28]Xin Z, Wang A, Yang G, Gao P, Zheng ZL: The Arabidopsis A4 subfamily of lectin receptor kinases negatively regulates abscisic acid response in seed germination. Plant Physiol 2009, 149(1):434-444.
• [29]Fan J, Hill L, Crooks C, Doerner P, Lamb C: Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions. Plant Physiol 2009, 150(4):1750-1761.
• [30]Chandler J, Wilson A, Dean C: Arabidopsis mutants showing an altered response to vernalization. Plant J 1996, 10(4):637-644.
• [31]Gremski K, Ditta G, Yanofsky MF: The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 2007, 134(20):3593-3601.
• [32]Alvarez JP, Goldshmidt A, Efroni I, Bowman JL, Eshed Y: The NGATHA distal organ development genes are essential for style specification in Arabidopsis. Plant Cell 2009, 21(5):1373-1393.
• [33]Toufighi K, Brady SM, Austin R, Ly E, Provart NJ: The Botany Array Resource: e-Northerns, Expression Angling, and promoter analyses. Plant J 2005, 43(1):153-163.
• [34]Hobson GM, Mitchell MT, Molloy GR, Pearson ML, Benfield PA: Identification of a novel TA-rich DNA binding protein that recognizes a TATA sequence within the brain creatine kinase promoter. Nucleic Acids Res 1988, 16(18):8925-8944.
• [35]Hudson ME, Quail PH: Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 2003, 133(4):1605-1616.
• [36]Lee YK, Kim GT, Kim IJ, Park J, Kwak SS, Choi G, Chung WI: LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development 2006, 133(21):4305-4314.
• [37]Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4(2):249-264.