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The role of reactive oxygen species in pollen germination in Picea pungens (blue spruce)

  • Nikita Maksimov
  • Anastasia Evmenyeva
  • Maria Breygina
  • Igor Yermakov
Original Article

Key message

Endogenous ROS, including those produced by NADPH oxidase, are required for spruce pollen germination and regulate membrane potential in pollen tubes; \({\mathbf{O}}_{{\mathbf{2}}}^{{{\mathbf{ \cdot - }}}}\) and H 2 O 2 are unevenly distributed along the tube.

Abstract

Recently, the key role of reactive oxygen species (ROS) in plant reproduction has been decisively demonstrated for angiosperms. This paper is dedicated to the involvement of ROS in pollen germination of gymnosperms, which remained largely unknown. We found that ROS are secreted from pollen grains of blue spruce during the early stage of activation. The localization of different ROS in pollen tube initials and pollen tubes demonstrated the accumulation of H2O2 in pollen tube apex. Colocalization with mitochondria-derived \({\text{O}}_{2}^{ \cdot - }\) showed that H2O2 is produced in mitochondria and amyloplasts in addition to its apical gradient in the cytosol. The necessity of intracellular ROS and, particularly, \({\text{O}}_{2}^{ \cdot - }\) for pollen germination was demonstrated using different antioxidants. ·OH and extracellular ROS, on the contrary, were found to be not necessary for germination. Exogenous hydrogen peroxide did not affect the germination efficiency but accelerated pollen tube growth in a concentration-dependent manner. The optical measurements of membrane potential showed that in spruce pollen tubes there is a gradient which is controlled by H+-ATPase, potassium- and calcium-permeable channels, anion channels and ROS, as demonstrated by inhibitory analysis. An important role of NADPH oxidase in the regulation of ROS balance in particular, and in germination in general, has been demonstrated by inhibiting the enzyme, which leads to the reduction in ROS release, depolarization of pollen tube plasma membrane, and blocking of pollen germination.

Keywords

Pollen germination Pollen tube growth Gymnosperms Reactive oxygen species Hydrogen peroxide 

Notes

Acknowledgements

Authors are grateful to WSBS of Moscow State University and Prof. A. B. Tsetlin for providing the technical opportunity to conduct this study. Authors want to thank N. P. Matveyeva for the idea on which this study is based. The research was supported by Russian Foundation for Basic Research, project 18-34-00979.

References

  1. Breygina MA, Smirnova AV, Matveeva NP, Yermakov IP (2010a) Membrane potential changes during pollen germination and tube growth. Cell Tissue Biol 3:573–582.  https://doi.org/10.1134/S1990519X0906011X CrossRefGoogle Scholar
  2. Breygina M, Smirnova A, Maslennikov M et al (2010b) Effects of anion channel blockers NPPB and DIDS on tobacco pollen tube growth and its mitochondria state. Cell Tissue Biol 4:289–296.  https://doi.org/10.1134/S1990519X10030119 CrossRefGoogle Scholar
  3. Breygina MA, Abramochkin DV, Maksimov NM, Yermakov IP (2016) Hydrogen peroxide affects ion channels in lily pollen grain protoplasts. Plant Biol 18:761–767.  https://doi.org/10.1111/plb.12470 CrossRefPubMedGoogle Scholar
  4. Cárdenas L, McKenna ST, Kunkel JG, Hepler PK (2006) NAD(P)H oscillates in pollen tubes and is correlated with tip growth. Plant Physiol 142:1460–1468.  https://doi.org/10.1104/pp.106.087882 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Carol RJ, Takeda S, Linstead P et al (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–1016.  https://doi.org/10.1038/nature04198 CrossRefPubMedGoogle Scholar
  6. Coelho SMB, Brownlee C, Bothwell JHF (2008) A tip-high, Ca2 + -interdependent, reactive oxygen species gradient is associated with polarized growth in Fucus serratus zygotes. Planta 227:1037–1046.  https://doi.org/10.1007/s00425-007-0678-9 CrossRefPubMedGoogle Scholar
  7. Feijo JA, Sainhas J, Hackett GR et al (1999) Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144:483–496CrossRefPubMedPubMedCentralGoogle Scholar
  8. Foreman J, Demidchik V, Bothwell JHF et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446.  https://doi.org/10.1038/nature01485 CrossRefPubMedGoogle Scholar
  9. Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5:263–267.  https://doi.org/10.1016/S1360-1385(00)01649-6 CrossRefPubMedGoogle Scholar
  10. Lassig R, Gutermuth T, Bey TD et al (2014) Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106.  https://doi.org/10.1111/tpj.12452 CrossRefPubMedGoogle Scholar
  11. Lazzaro MD (1999) Microtubule organization in germinated pollen of the conifer Picea abies (Norway spruce, Pinaceae). Am J Bot 86:759–766.  https://doi.org/10.2307/2656696 CrossRefPubMedGoogle Scholar
  12. Lazzaro MD, Cardenas L, Bhatt AP et al (2005) Calcium gradients in conifer pollen tubes; dynamic properties differ from those seen in angiosperms. J Exp Bot 56:2619–2628.  https://doi.org/10.1093/jxb/eri256 CrossRefPubMedGoogle Scholar
  13. Liu P, Li RL, Zhang L et al (2009) Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 60:303–313.  https://doi.org/10.1111/j.1365-313X.2009.03955.x CrossRefPubMedGoogle Scholar
  14. Maeda H, Fukuyasu Y, Yoshida S et al (2004) Fluorescent probes for hydrogen peroxide based on a non-oxidative mechanism. Angew Chemie Int Ed 43:2389–2391.  https://doi.org/10.1002/anie.200452381 CrossRefGoogle Scholar
  15. Maksimov NM, Breigin MA, Ermakov IP (2016) Regulation of ion transport across the pollen tube plasmalemma by hydrogen peroxide. Cell Tissue Biol 10:69–75.  https://doi.org/10.1134/S1990519X16010077 CrossRefGoogle Scholar
  16. Michard E, Simon AA, Tavares B et al (2017) Signaling with ions: the keystone for apical cell growth and morphogenesis in pollen tubes. Plant Physiol 173:91–111.  https://doi.org/10.1104/pp.16.01561 CrossRefPubMedGoogle Scholar
  17. Monshausen GB, Bibikova TN, Messerli MA et al (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996–21001.  https://doi.org/10.1073/pnas.0708586104 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Potocky M, Jones MA, Bezvoda R et al (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751.  https://doi.org/10.1111/j.1469-8137.2007.02042.x CrossRefPubMedGoogle Scholar
  19. Potocký M, Pejchar P, Gutkowska M et al (2012) NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. J Plant Physiol 169:1654–1663.  https://doi.org/10.1016/j.jplph.2012.05.014 CrossRefPubMedGoogle Scholar
  20. Robinson KM, Janes MS, Beckman JS (2008) The selective detection of mitochondrial superoxide by live cell imaging. Nat Protoc 3:941–947.  https://doi.org/10.1038/nprot.2008.56 CrossRefPubMedGoogle Scholar
  21. Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858.  https://doi.org/10.1242/dev.132845 CrossRefPubMedGoogle Scholar
  22. Smirnova AV, Matveyeva NP, Polesskaya OG, Yermakov IP (2009) Generation of reactive oxygen species during pollen grain germination. Russ J Dev Biol 40:345–353.  https://doi.org/10.1134/S1062360409060034 CrossRefGoogle Scholar
  23. Smirnova A, Matveyeva N, Yermakov I (2013) Reactive oxygen species are involved in regulation of pollen wall cytomechanics. Plant Biol 16:252–257.  https://doi.org/10.1111/plb.12004 CrossRefPubMedGoogle Scholar
  24. Speranza A, Crinelli R, Scoccianti V, Geitmann A (2012) Reactive oxygen species are involved in pollen tube initiation in kiwifruit. Plant Biol 14:64–76.  https://doi.org/10.1111/j.1438-8677.2011.00479.x PubMedGoogle Scholar
  25. Tavares B, Dias PN, Domingos P et al (2011a) Calcium-regulated anion channels in the plasma membrane of Lilium longiflorum pollen protoplasts. New Phytol 192:45–60.  https://doi.org/10.1111/j.1469-8137.2011.03780.x CrossRefPubMedGoogle Scholar
  26. Tavares B, Domingos P, Dias PN et al (2011b) The essential role of anionic transport in plant cells: the pollen tube as a case study. J Exp Bot 62:2273–2298.  https://doi.org/10.1093/jxb/err036 CrossRefPubMedGoogle Scholar
  27. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616.  https://doi.org/10.1016/j.cell.2010.10.020 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Nikita Maksimov
    • 1
  • Anastasia Evmenyeva
    • 1
  • Maria Breygina
    • 1
    • 2
  • Igor Yermakov
    • 1
  1. 1.Lomonosov Moscow State UniversityMoscowRussia
  2. 2.Pirogov Russian National Research Medical UniversityMoscowRussia

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