Sulfinylated azadecalins act as functional mimics of a pollen germination stimulant in Arabidopsis pistils

Yuan Qin, Ronald J. Wysocki, Arpad Somogyi, Yelena Feinstein, Jessica Y. Franco, Tatsuya Tsukamoto, Damayanthi Dunatunga, Clara Levy, Steven E Smith, Robert Simpson, David Gang, Mark A. Johnson, Ravishankar Palanivelu

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Polarized cell elongation is triggered by small molecule cues during development of diverse organisms. During plant reproduction, pollen interactions with the stigma result in the polar outgrowth of a pollen tube, which delivers sperm cells to the female gametophyte to effect double fertilization. In many plants, pistils stimulate pollen germination. However, in Arabidopsis, the effect of pistils on pollen germination and the pistil factors that stimulate pollen germination remain poorly characterized. Here, we demonstrate that stigma, style, and ovules in Arabidopsis pistils stimulate pollen germination. We isolated an Arabidopsis pistil extract fraction that stimulates Arabidopsis pollen germination, and employed ultra-high resolution electrospray ionization (ESI), Fourier-transform ion cyclotron resonance (FT-ICR) and MS/MS techniques to accurately determine the mass (202.126 Da) of a compound that is specifically present in this pistil extract fraction. Using the molecular formula (C 10H 19NOS) and tandem mass spectral fragmentation patterns of the m/z (mass to charge ratio) 202.126 ion, we postulated chemical structures, devised protocols, synthesized N-methanesulfinyl 1- and 2-azadecalins that are close structural mimics of the m/z 202.126 ion, and showed that they are sufficient to stimulate Arabidopsis pollen germination in vitro (30 μm stimulated approximately 50% germination) and elicit accession-specific response. Although N-methanesulfinyl 2-azadecalin stimulated pollen germination in three species of Lineage I of Brassicaceae, it did not induce a germination response in Sisymbrium irio (Lineage II of Brassicaceae) and tobacco, indicating that activity of the compound is not random. Our results show that Arabidopsis pistils promote germination by producing azadecalin-like molecules to ensure rapid fertilization by the appropriate pollen.

Original languageEnglish (US)
Pages (from-to)800-815
Number of pages16
JournalPlant Journal
Volume68
Issue number5
DOIs
StatePublished - Dec 2011

Fingerprint

pollen germination
pistil
Germination
Pollen
Arabidopsis
ions
germination
Brassicaceae
stigma
Sisymbrium
Ions
pollen
Fertilization
plant reproduction
extracts
fertilization (reproduction)
pollen tubes
ovules
Pollen Tube
chemical structure

Keywords

  • chemical biology
  • functional mimic
  • germination
  • pistil
  • pollen
  • stimulant

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology
  • Genetics

Cite this

Sulfinylated azadecalins act as functional mimics of a pollen germination stimulant in Arabidopsis pistils. / Qin, Yuan; Wysocki, Ronald J.; Somogyi, Arpad; Feinstein, Yelena; Franco, Jessica Y.; Tsukamoto, Tatsuya; Dunatunga, Damayanthi; Levy, Clara; Smith, Steven E; Simpson, Robert; Gang, David; Johnson, Mark A.; Palanivelu, Ravishankar.

In: Plant Journal, Vol. 68, No. 5, 12.2011, p. 800-815.

Research output: Contribution to journalArticle

Qin, Y, Wysocki, RJ, Somogyi, A, Feinstein, Y, Franco, JY, Tsukamoto, T, Dunatunga, D, Levy, C, Smith, SE, Simpson, R, Gang, D, Johnson, MA & Palanivelu, R 2011, 'Sulfinylated azadecalins act as functional mimics of a pollen germination stimulant in Arabidopsis pistils', Plant Journal, vol. 68, no. 5, pp. 800-815. https://doi.org/10.1111/j.1365-313X.2011.04729.x
Qin, Yuan ; Wysocki, Ronald J. ; Somogyi, Arpad ; Feinstein, Yelena ; Franco, Jessica Y. ; Tsukamoto, Tatsuya ; Dunatunga, Damayanthi ; Levy, Clara ; Smith, Steven E ; Simpson, Robert ; Gang, David ; Johnson, Mark A. ; Palanivelu, Ravishankar. / Sulfinylated azadecalins act as functional mimics of a pollen germination stimulant in Arabidopsis pistils. In: Plant Journal. 2011 ; Vol. 68, No. 5. pp. 800-815.
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abstract = "Polarized cell elongation is triggered by small molecule cues during development of diverse organisms. During plant reproduction, pollen interactions with the stigma result in the polar outgrowth of a pollen tube, which delivers sperm cells to the female gametophyte to effect double fertilization. In many plants, pistils stimulate pollen germination. However, in Arabidopsis, the effect of pistils on pollen germination and the pistil factors that stimulate pollen germination remain poorly characterized. Here, we demonstrate that stigma, style, and ovules in Arabidopsis pistils stimulate pollen germination. We isolated an Arabidopsis pistil extract fraction that stimulates Arabidopsis pollen germination, and employed ultra-high resolution electrospray ionization (ESI), Fourier-transform ion cyclotron resonance (FT-ICR) and MS/MS techniques to accurately determine the mass (202.126 Da) of a compound that is specifically present in this pistil extract fraction. Using the molecular formula (C 10H 19NOS) and tandem mass spectral fragmentation patterns of the m/z (mass to charge ratio) 202.126 ion, we postulated chemical structures, devised protocols, synthesized N-methanesulfinyl 1- and 2-azadecalins that are close structural mimics of the m/z 202.126 ion, and showed that they are sufficient to stimulate Arabidopsis pollen germination in vitro (30 μm stimulated approximately 50{\%} germination) and elicit accession-specific response. Although N-methanesulfinyl 2-azadecalin stimulated pollen germination in three species of Lineage I of Brassicaceae, it did not induce a germination response in Sisymbrium irio (Lineage II of Brassicaceae) and tobacco, indicating that activity of the compound is not random. Our results show that Arabidopsis pistils promote germination by producing azadecalin-like molecules to ensure rapid fertilization by the appropriate pollen.",
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