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Overexpression of phytosulfokine-α induces male sterility and cell growth by regulating cell wall development in Arabidopsis

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Abstract

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Over-production of functional PSK-α in Arabidopsis caused increases in both plant cell growth and biomass and induced male sterility by regulating cell wall development.

Abstract

Phytosulfokine-α (PSK-α) is a novel disulfated pentapeptide hormone that is involved in promoting plant cell growth. Although a role for PSK-α in stimulating protoplast expansion has been suggested, how PSK-α regulates cell growth in planta remains poorly understood. In this study, we found that overexpression of the normal PSK-α precursor gene AtPSK4, which resulted in high levels of PSK-α, caused longer roots and larger leaves with enlarged cells. As expected, these changes were not observed in transgenic plants overexpressing mutated AtPSK4, which generated unsulfated PSK-α. These findings confirmed the role of PSK-α in promoting plant cell growth. Furthermore, we found that overexpressing AtPSK4, but not mutated AtPSK4, induced a phenotype of male sterility that resulted from the failure of fibrous cell wall development in the endothecium. In addition, overexpressing AtPSK4 enhanced expression of a number of genes encoding expansins, which are involved in cell wall loosening. Accordingly, in addition to its role in cell growth, we propose a novel function for PSK-α signaling in the modulation of plant male sterility via regulation of cell wall development.

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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  PubMed Central  Google Scholar 

  • Becnel J, Natarajan M, Kipp A, Braam J (2006) Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol Biol 61:451–467

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, 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 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol Plant 4:199–211

    Article  CAS  PubMed  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanai H, Matsuno T, Yamamoto M, Matsubayashi Y, Kobayashi T, Kamada H, Sakagami Y (2000) A secreted peptide growth factor, phytosulfokine, acting as a stimulatory factor of carrot somatic embryo formation. Plant Cell Physiol 41:27–32

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hartmann J, Fischer C, Dietrich P, Sauter M (2014) Kinase activity and calmodulin binding are essential for growth signaling by the phytosulfokine receptor PSKR1. Plant J 78:192–202

    Article  CAS  PubMed  Google Scholar 

  • Igarashi D, Tsuda K, Katagiri F (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71:194–204

    Article  CAS  PubMed  Google Scholar 

  • Igasaki T, Akashi N, Ujino-Ihara T, Matsubayashi Y, Sakagami Y, Shinohara K (2003) Phytosulfokine stimulates somatic embryogenesis in Cryptomeria japonica. Plant Cell Physiol 44:1412–1416

    Article  CAS  PubMed  Google Scholar 

  • Keijzer CJ (1987) The processes of anther dehiscence and pollen dispersal. New Phytol 105:487–498

    Article  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  PubMed Central  Google Scholar 

  • Kutschmar A, Rzewuski G, Stuhrwohldt N, Beemster GT, Inze D, Sauter M (2009) PSK-alpha promotes root growth in Arabidopsis. New Phytol 181:820–831

    Article  CAS  PubMed  Google Scholar 

  • Kwezi L, Ruzvidzo O, Wheeler JI, Govender K, Iacuone S, Thompson PE, Gehring C, Irving HR (2011) The phytosulfokine (PSK) receptor is capable of guanylate cyclase activity and enabling cyclic GMP-dependent signaling in plants. J Biol Chem 286:22580–22588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladwig F, Dahlke RI, Stuhrwohldt N, Hartmann J, Harter K, Sauter M (2015) Phytosulfokine regulates growth in arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1. Plant Cell 27:1718–1729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo L (2012) Plant cytokine or phytocytokine. Plant Signal Behav 7:1513–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahmood K, Kannangara R, Jorgensen K, Fuglsang AT (2014) Analysis of peptide PSY1 responding transcripts in the two Arabidopsis plant lines: wild type and psy1r receptor mutant. BMC Genom 15:441

    Article  CAS  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  PubMed Central  Google Scholar 

  • Matsubayashi Y, Sakagami Y (2006) Peptide hormones in plants. Annu Rev Plant Biol 57:649–674

    Article  CAS  PubMed  Google Scholar 

  • Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y (1999) The endogenous sulfated pentapeptide phytosulfokine-alpha stimulates tracheary element differentiation of isolated mesophyll cells of zinnia. Plant Physiol 120:1043–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472

    Article  CAS  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  PubMed Central  Google Scholar 

  • Mosher S, Seybold H, Rodriguez P, Stahl M, Davies KA, Dayaratne S, Morillo SA, Wierzba M, Favery B, Keller H, Tax FE, Kemmerling B (2013) The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J 73:469–482

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Sauter M (2015) Phytosulfokine peptide signalling. J Exp Bot 66:5161–5169

    Article  CAS  PubMed  Google Scholar 

  • Shani Z, Dekel M, Roiz L, Horowitz M, Kolosovski N, Lapidot S, Alkan S, Koltai H, Tsabary G, Goren R, Shoseyov O (2006) Expression of endo-1,4-beta-glucanase (cel1) in Arabidopsis thaliana is associated with plant growth, xylem development and cell wall thickening. Plant Cell Rep 25:1067–1074

    Article  CAS  PubMed  Google Scholar 

  • Shinohara H, Ogawa M, Sakagami Y, Matsubayashi Y (2007) Identification of ligand binding site of phytosulfokine receptor by on-column photoaffinity labeling. J Biol Chem 282:124–131

    Article  CAS  PubMed  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava R, Liu JX, Howell SH (2008) Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J 56:219–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuhrwohldt N, Dahlke RI, Kutschmar A, Peng X, Sun MX, Sauter M (2015) Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana. Physiol Plant 153:643–653

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Yu H, Zhang Z, Yu L, Xu X, Hong Z, Luo L (2015a) Phytosulfokine is involved in positive regulation of Lotus japonicus nodulation. Mol Plant Microbe Interact 28:847–855

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J (2015b) Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265–268

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (1999) Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants. Proc Natl Acad Sci USA 96:13560–13565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L, Sun J, Li L (2013) PtrCel9A6, an endo-1,4-beta-glucanase, is required for cell wall formation during xylem differentiation in populus. Mol Plant 6:1904–1917

    Article  CAS  PubMed  Google Scholar 

  • Yu L, Chen H, Sun J, Li L (2014) PtrKOR1 is required for secondary cell wall cellulose biosynthesis in Populus. Tree Physiol 34:1289–1300

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Professor Xiangyang Hu for critical reading of the manuscript and Ms. Jiqin Li and Mr. Xiaoyan Gao at Shanghai Institute of Plant Physiology and Ecology (CAS) for assistance with the scanning electron microscopy. This work was supported by the National Natural Science Foundation of China (31500197) and Shanghai Sailing Program (15YF1403800) to L. Yu; and Shanghai Key Projects of Basic Research (14JC1402300) and Shanghai Key Program of Supporting (15230500100) to L. Luo.

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  1. Shanghai Key Lab of Bio-energy Crops, School of Life Sciences, Shanghai University, Shanghai, 200444, China

    Liangliang Yu, Yan Liu, Yumin Liu, Qiong Li, Guirong Tang & Li Luo

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  1. Liangliang Yu
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  2. Yan Liu
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  3. Yumin Liu
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  6. Li Luo
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Correspondence to Li Luo.

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Communicated by C-Hai Dong.

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299_2016_2050_MOESM1_ESM.tif

Supplemental Fig. 1Transgenic Arabidopsis lines with high AtPSK4 expression levels demonstrated reduced fertility rates. Five individual AtPSK4-OX and AtPSK4-OXm transgenic Arabidopsis lines are shown. Arrowheads indicate unfertilized siliques. Bar = 2 cm (TIFF 38598 kb)

299_2016_2050_MOESM2_ESM.tif

Supplemental Fig. 2 Transgenic Arabidopsis with a reduced fertility rate had functional pollen grains and pistils. a Pollen grains from manually opened anthers of OX_4 and OX_6 transgenic lines were able to germinate and grow normally on pollen-germination medium, as were wild-type and OXm_1 anthers. Bar = 200 μm. b OX_4 and OX_6 transgenic lines were cross-fertilized with the pollen grains of Col-0. Three flowers in an inflorescence were used for cross-fertilization. Arrowheads indicate fertilized siliques. Bar = 2 cm (TIFF 34130 kb)

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Yu, L., Liu, Y., Liu, Y. et al. Overexpression of phytosulfokine-α induces male sterility and cell growth by regulating cell wall development in Arabidopsis. Plant Cell Rep 35, 2503–2512 (2016). https://doi.org/10.1007/s00299-016-2050-7

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  • DOI: https://doi.org/10.1007/s00299-016-2050-7

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