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RALF34 is a Paracrine Signal to Trigger Pollen Tubes Burst and Sperm Release

  • Zengxiang GeEmail author
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Part of the Springer Theses book series (Springer Theses)

Abstract

During the delivery of sperm cells, pollen tubes maintain the cell integrity via RALF4/19-BUPS/ANX signaling complex when they grow in the maternal tissues. After arriving at the female gametophyte, pollen tubes should rupture timely to release the sperm cells for successful double fertilization, the mechanism of which remains unknown. Here, we show that RALF34 could induce pollen tubes burst in a paracrine manner. RALF34 shares high sequence identity with RALF4 and RALF19, but it shows distinct expression pattern from RALF4/19 in that RALF34 is mainly expressed in the ovule while RALF4/19 are pollen-expressed. RALF34 is distributed in the inner integument cells. Furthermore, RALF34 peptide could not only interact with BUPS1/2 but also be able to bind to ANX1/2, which is consistent with the pull-down results of RALF4/19 and BUPS1/2–ANX1/2, suggesting RALF34 is another ligand of BUPS–ANX receptor complex. In the competition assay, RALF34 peptide could compete with RALF4 for BUPS/ANX binding. Therefore, our results suggest that RALF34 peptide might act as a paracrine signal to bind BUPS1/2–ANX1/2 complex and participates in regulating pollen tubes rupture and sperm cell release in the female tissues.

Keywords

RALF peptides Paracrine signals Pollen tubes burst Sperm release 

References

  1. 1.
    Qu L-J, Li L, Lan ZJ, Dresselhaus T (2015) Peptide signalling during the pollen tube journey and double fertilization. J Exp Bot 66:5139–5150CrossRefGoogle Scholar
  2. 2.
    Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue BPA (2015) The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27:2095–2118CrossRefGoogle Scholar
  3. 3.
    Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336CrossRefGoogle Scholar
  4. 4.
    Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–411CrossRefGoogle Scholar
  5. 5.
    Li C, Wu H-M, Cheung AY (2016) FERONIA and her pals: functions and mechanisms. Plant Physiol 171:2379–2392PubMedPubMedCentralGoogle Scholar
  6. 6.
    Ma XY, Xu GY, He P, Shan L (2016) SERKing coreceptors for receptors. Trends Plant Sci 21:1017–1033CrossRefGoogle Scholar
  7. 7.
    Meng X, Zhou J, Tang J, Li B, de Oliveira Marcos VV, Chai J, He P, Shan L (2016) Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep 14:1330–1338Google Scholar
  8. 8.
    Song W, Han ZF, Wang JZ, Lin GZ, Chai JJ (2017) Structural insights into ligand recognition and activation of plant receptor kinases. Curr Opin Struct Biol 43:18–27CrossRefGoogle Scholar
  9. 9.
    Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293Google Scholar
  10. 10.
    Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–244CrossRefGoogle Scholar
  11. 11.
    Lee JS, Hnilova M, Maes M, Lin Y-CL, Putarjunan A, Han S-K, Avila J, Torii KU (2015) Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522:439–443CrossRefGoogle Scholar
  12. 12.
    Lin GZ, Zhang L, Han ZF, Yang XR, Liu WJ, Li ET, Chang JB, Qi YJ, Shpak ED, Chai JJ (2017) A receptor-like protein acts as a specificity switch for the regulation of stomatal development. Genes Dev 31:927–938CrossRefGoogle Scholar
  13. 13.
    Muschietti J, Dircks L, Vancanneyt G, McCormick S (1994) LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 6:321–338CrossRefGoogle Scholar
  14. 14.
    Tang W, Ezcurra I, Muschietti J, McCormick S (2002) A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14:2277–2287CrossRefGoogle Scholar
  15. 15.
    Tang W, Kelley D, Ezcurra I, Cotter R, McCormick S (2004) LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J 39:343–353CrossRefGoogle Scholar
  16. 16.
    Dresselhaus T, Franklin-Tong N (2013) Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6:1018–1036CrossRefGoogle Scholar
  17. 17.
    Bircheneder S, Dresselhaus T (2016) Why cellular communication during plant reproduction is particularly mediated by CRP signalling. J Exp Bot 67:4849–4861CrossRefGoogle Scholar
  18. 18.
    Dresselhaus T, Sprunck S, Wessel GM (2016) Fertilization mechanisms in flowering plants. Curr Biol 26:R125–R139CrossRefGoogle Scholar
  19. 19.
    Zhang J, Wei B, Yuan R, Wang J, Ding M, Chen Z, Yu H, Qin G (2017) The Arabidopsis RING-type E3 ligase TEAR1 controls leaf development by targeting the TIE1 transcriptional repressor for degradation. Plant Cell 29:243–259CrossRefGoogle Scholar
  20. 20.
    Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel C (2017) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–289CrossRefGoogle Scholar
  21. 21.
    Ge Z, Bergonci T, Zhao YL, Zou YJ, Du S, Liu MC, Luo XJ, Ruan H, Garcia-Valencia LE, Zhong S et al (2017) Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358:1596–1599CrossRefGoogle Scholar
  22. 22.
    Lee JS, De Smet I (2016) Fine-tuning development through antagonistic peptides: an emerging theme. Trends Plant Sci 21:991–993CrossRefGoogle Scholar
  23. 23.
    Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16:537–552CrossRefGoogle Scholar
  24. 24.
    Murphy E, Vu LD, Van den Broeck L, Lin Z, Ramakrishna P, van de Cotte B, Gaudinier A, Goh T, Slane D, Beeckman T et al (2016) RALFL34 regulates formative cell divisions in Arabidopsis pericycle during lateral root initiation. J Exp Bot 67:4863–4875CrossRefGoogle Scholar
  25. 25.
    Duan QH, Kita D, Li C, Cheung AY, Wu H-M (2010) FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci USA 107:17821–17826CrossRefGoogle Scholar
  26. 26.
    Marmiroli N, Maestri E (2014) Plant peptides in defense and signaling. Peptides 56:30–44CrossRefGoogle Scholar
  27. 27.
    Grienenberger E, Fletcher JC (2015) Polypeptide signaling molecules in plant development. Curr Opin Plant Biol 23:8–14CrossRefGoogle Scholar
  28. 28.
    Huang Q, Dresselhaus T, Gu H, Qu L-J (2015) Active role of small peptides in Arabidopsis reproduction: expression evidence. J Integr Plant Biol 57:518–521CrossRefGoogle Scholar
  29. 29.
    Mouline K, Very AA, Gaymard F, Boucherez J, Pilot G, Devic M, Bouchez D, Thibaud JB, Sentenac H (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes Dev 16:339–350CrossRefGoogle Scholar
  30. 30.
    Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719CrossRefGoogle Scholar
  31. 31.
    Tunc-Ozdemir M, Rato C, Brown E, Rogers S, Mooneyham A, Frietsch S, Myers CT, Poulsen LR, Malho R, Harper JF (2013) Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility. PLoS One 8:e55277CrossRefGoogle Scholar
  32. 32.
    Duan QH, Kita D, Johnson EA, Aggarwal M, Gates L, Wu H-M, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129Google Scholar
  33. 33.
    Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106CrossRefGoogle Scholar
  34. 34.
    Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U (2015) Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. Proc Natl Acad Sci USA 112:12211–12216CrossRefGoogle Scholar
  35. 35.
    Liao HZ, Zhu MM, Cui HH, Du XY, Tang Y, Chen LQ, Ye D, Zhang XQ (2016) MARIS plays important roles in Arabidopsis pollen tube and root hair growth. J Integr Plant Biol 58:927–940Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  1. 1.School of Life SciencesPeking UniversityBeijingRepublic of China

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