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PMID: 26494758 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination.

Science (New York, N.Y.) ·Vol. 350 ·No. 6259 ·2015-10-23 ·Pages 438-41

Hamilton ES, Jensen GS, Maksaev G, Katims A, Sherp AM, Haswell ES

Abstract

Pollen grains undergo dramatic changes in cellular water potential as they deliver the male germ line to female gametes, and it has been proposed that mechanosensitive ion channels may sense the resulting mechanical stress. Here, we identify and characterize MscS-like 8 (MSL8), a pollen-specific, membrane tension-gated ion channel required for pollen to survive the hypoosmotic shock of rehydration and for full male fertility. MSL8 negatively regulates pollen germination but is required for cellular integrity during germination and tube growth. MSL8 thus senses and responds to changes in membrane tension associated with pollen hydration and germination. These data further suggest that homologs of bacterial MscS have been repurposed in eukaryotes to function as mechanosensors in multiple developmental and environmental contexts.

MeSH Terms
Animals Arabidopsis/genetics,physiology Arabidopsis Proteins/genetics,physiology Germination/genetics,physiology Ion Channel Gating Ion Channels/genetics,physiology Mechanotransduction, Cellular/genetics,physiology Oocytes Osmotic Pressure/physiology Pollination/genetics,physiology Surface Tension Water/physiology Xenopus laevis
Chemicals
Arabidopsis Proteins Ion Channels MSL8 protein, Arabidopsis Water
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Hamilton Eric S
Department of Biology, Washington University in Saint Louis, Saint Louis, MO 63130, USA.
Jensen Gregory S
Department of Biology, Washington University in Saint Louis, Saint Louis, MO 63130, USA.
Maksaev Grigory
Department of Biology, Washington University in Saint Louis, Saint Louis, MO 63130, USA.
Katims Andrew
Department of Biology, Washington University in Saint Louis, Saint Louis, MO 63130, USA.
Sherp Ashley M
Department of Biology, Washington University in Saint Louis, Saint Louis, MO 63130, USA.
Haswell Elizabeth S
Department of Biology, Washington University in Saint Louis, Saint Louis, MO 63130, USA. ehaswell@wustl.edu.
References (23)
23 references, click to expand
  1. Widespread mechanosensing controls the structure behind the architecture in plants.
    Curr Opin Plant Biol. 2013 Oct;16(5):654-60 PMID: 23830994
  2. The rate of osmotic downshock determines the survival probability of bacterial mechanosensitive channel mutants.
    J Bacteriol. 2015 Jan 1;197(1):231-7 PMID: 25349158
  3. Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility.
    PLoS One. 2013;8(2):e55277 PMID: 23424627
  4. Two families of mechanosensitive channel proteins.
    Microbiol Mol Biol Rev. 2003 Mar;67(1):66-85, table of contents PMID: 12626684
  5. Pollen and stigma structure and function: the role of diversity in pollination.
    Plant Cell. 2004;16 Suppl:S84-97 PMID: 15075396
  6. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14531-6 PMID: 17726111
  7. Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root.
    Curr Biol. 2008 May 20;18(10):730-4 PMID: 18485707
  8. Water status and associated processes mark critical stages in pollen development and functioning.
    Ann Bot. 2012 Jun;109(7):1201-14 PMID: 22523424
  9. The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves.
    J Bacteriol. 2012 Sep;194(18):4802-9 PMID: 22685280
  10. Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in Capsella grandiflora.
    Mol Biol Evol. 2013 Nov;30(11):2475-86 PMID: 23997108
  11. The interplay between cell signalling and mechanics in developmental processes.
    Nat Rev Genet. 2013 Oct;14(10):733-44 PMID: 24045690
  12. Feeling the hidden mechanical forces in lipid bilayer is an original sense.
    Proc Natl Acad Sci U S A. 2014 Jun 3;111(22):7898-905 PMID: 24850861
  13. The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm.
    Int J Dev Biol. 2009;53(8-10):1609-22 PMID: 19247955
  14. Recent characterizations of MscS and its homologs provide insight into the basis of ion selectivity in mechanosensitive channels.
    Channels (Austin). 2013 May-Jun;7(3):215-20 PMID: 23590902
  15. Flowers under pressure: ins and outs of turgor regulation in development.
    Ann Bot. 2014 Nov;114(7):1517-33 PMID: 25288632
  16. The pollen tube paradigm revisited.
    Curr Opin Plant Biol. 2012 Dec;15(6):618-24 PMID: 23000432
  17. Expression and characterization of the bacterial mechanosensitive channel MscS in Xenopus laevis oocytes.
    J Gen Physiol. 2011 Dec;138(6):641-9 PMID: 22084416
  18. Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes.
    Plant J. 2009 Aug;59(4):528-39 PMID: 19392698
  19. Identification and characterization of stretch-activated ion channels in pollen protoplasts.
    Plant Physiol. 2004 Jul;135(3):1398-406 PMID: 15247410
  20. Pollen and seed desiccation tolerance in relation to degree of developmental arrest, dispersal, and survival.
    J Exp Bot. 2011 Nov;62(15):5267-81 PMID: 21831844
  21. United in diversity: mechanosensitive ion channels in plants.
    Annu Rev Plant Biol. 2015;66:113-37 PMID: 25494462
  22. Transient expression of chimeric genes delivered into pollen by microprojectile bombardment.
    Plant Physiol. 1989 Dec;91(4):1270-4 PMID: 16667175
  23. RNA-seq of Arabidopsis pollen uncovers novel transcription and alternative splicing.
    Plant Physiol. 2013 Jun;162(2):1092-109 PMID: 23590974
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2015-10-23
Pages
438-41
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC4764502
Subset
IM
Grants
NIGMS NIH HHS · R01 GM084211 · United States
NIGMS NIH HHS · 2R01GM084211 · United States
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