Oscillatory Growth in Lily Pollen Tubes Does Not Require Aerobic Energy Metabolism

Caleb M Rounds,Peter K Hepler,Lawrence J Winship,Sasha J Fuller

doi:10.1104/pp.109.150896

Caleb M Rounds, Peter K Hepler + Show 2 more

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https://doi.org/10.1104/pp.109.150896

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Journal: Plant Physiology	Publication Date: Dec 9, 2009
Citations: 37	License type: CC BY 4.0

Affiliation: University of Massachusetts Amherst

Abstract

Oscillatory tip growth in pollen tubes depends on prodigious amounts of energy. We have tested the hypothesis that oscillations in the electron transport chain lead to growth oscillations in lily (Lilium formosanum). Using three respiratory inhibitors, oligomycin, antimycin A, and cyanide, we find that pollen tube growth is much less sensitive to respiratory inhibition than respiration is. All three block respiration at concentrations severalfold lower than necessary to inhibit growth. Mitochondrial NAD(P)H and potentiometric JC-1 fluorescence, employed as markers for electron transport chain activity, rise rapidly in response to oligomycin, as expected. Pollen tube growth stops for several minutes before resuming. Subsequent growth has a lower mean rate, but continues to oscillate, albeit with a longer period. NAD(P)H fluorescence no longer exhibits coherent oscillations, and mitochondria no longer congregate directly behind the apex: they distribute evenly throughout the cell. Postinhibition growth relies on aerobic fermentation for energy production as revealed by an increase in ethanol in the media. These data suggest that oscillatory growth depends not on a single oscillatory pacemaker but rather is an emergent property arising from a number of stable limit cycles.

Highlights

Oscillatory tip growth in pollen tubes depends on prodigious amounts of energy
We investigated whether oscillations in the electron transport chain (ETC) lead to growth oscillations
To test the hypothesis that NAD(P)H/NAD(P)+ oscillations were leading to growth oscillations, we examined the effects of three inhibitors of the major complexes of the ETC

Summary

Introduction

Oscillatory tip growth in pollen tubes depends on prodigious amounts of energy. We have tested the hypothesis that oscillations in the electron transport chain lead to growth oscillations in lily (Lilium formosanum). The search for the factors leading to oscillatory growth has led to the observation that several underlying cellular processes oscillate in the growing pollen tube (Holdaway-Clarke et al, 1997, 2003; Moreno et al, 2007). One approach has been to rank the oscillatory phenomenon through crosscorrelation analysis This procedure exploits variations in the amplitude and periodicity to determine which processes precede growth and which follow (Holdaway-Clarke et al, 1997; Cardenas et al, 2006, 2008; Lovy-Wheeler et al, 2006). Recent work showed that oscillations in NAD(P)H/ NAD(P)+ fluorescence lead growth oscillations in lily pollen tubes by 50° to 110° (Cardenas et al, 2006). Combined with the data from other organisms, it has seemed plausible that oscillations in the mitochondrial ETC might be a good candidate for the oscillatory pacemaker (Cardenas et al, 2006)

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