State and Spectral Properties of Chloride Oscillations in Pollen

• Published in: Biophysical journal 2003-02, Vol.84 (2), p.1387-1398
• Main Authors: Zonia, Laura, Feijó, José A.
• Format: Article
• Language: English
• Subjects: 4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid - pharmacology; Cells, Cultured; Cellular biology; Chloride Channels - drug effects; Chloride Channels - physiology; Chlorine - pharmacokinetics; Electrophysiology; Fourier Analysis; Homeostasis - physiology; Inositol Phosphates - pharmacology; Ion Channel Gating - drug effects; Ion Channel Gating - physiology; Models, Biological; Nicotiana - physiology; Nonlinear Dynamics; Oscillometry - methods; Osmotic Pressure; Periodicity; Physical growth; Plant reproduction; Pollen; Pollen - physiology; Signal Processing, Computer-Assisted
• ISSN: 0006-3495; 1542-0086
• DOI: 10.1016/S0006-3495(03)74953-4

Pollen tube growth is a dynamic system expressing a number of oscillating circuits. Our recent work identified a new circuit, oscillatory efflux of Cl − anion from the pollen tube apex. Cl − efflux is the first ion signal found to be coupled in phase with growth oscillations. Functional analyses indicate an active role for Cl − flux in pollen tube growth. In this report the dynamical properties of Cl − efflux are examined. Phase space analysis demonstrates that the system trajectory converges on a limit cycle. Fourier analysis reveals that two harmonic frequencies characterize normal growth. Cl − efflux is inhibited by the channel blocker DIDS, is stimulated by hypoosmotic treatment, and is antagonized by the signal encoded in inositol 3,4,5,6-tetra kisphosphate. These perturbations induce transitions of the limit cycle to new metastable states or cause system collapse to a static attractor centered near the origin. These perturbations also transform the spectral profile, inducing subharmonic frequencies, transitions to period doubling and tripling, superharmonic resonance, and chaos. These results indicate that Cl − signals in pollen tubes display features that are characteristic of active oscillators that carry frequency-encoded information. A reaction network of the Cl − oscillator coupled to two nonlinear feedback circuits that may drive pollen tube growth oscillations is considered.