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Abstract
Ectoapyrase enzymes remove the terminal phosphate from extracellular nucleoside tri- and diphosphates. In Arabidopsis (Arabidopsis thaliana), two ectoapyrases, AtAPY1 and AtAPY2, have been implicated as key modulators of growth. In fibers of cotton (Gossypium hirsutum), transcript levels for GhAPY1 and GhAPY2, two closely related ectoapyrases that have high sequence similarity to AtAPY1 and AtAPY2, are up-regulated when fibers enter their rapid growth phase. In an ovule culture system, fibers release ATP as they grow, and when their ectoapyrase activity is blocked by the addition of polyclonal anti-apyrase antibodies or by two different small molecule inhibitors, the medium ATP level rises and fiber growth is suppressed. High concentrations of the poorly hydrolyzable nucleotides ATPgammaS and ADPbetaS applied to the medium inhibit fiber growth, and low concentrations of them stimulate growth, but treatment with adenosine 5'-O-thiomonophosphate causes no change in the growth rate. Both the inhibition and stimulation of growth by applied nucleotides can be blocked by an antagonist that blocks purinoceptors in animal cells, and by adenosine. Treatment of cotton ovule cultures with ATPgammaS induces increased levels of ethylene, and two ethylene antagonists, aminovinylglycine and silver nitrate, block both the growth stimulatory and growth inhibitory effects of applied nucleotides. In addition, the ethylene precursor, 1-aminocyclopropane-1-carboxylic acid, lowers the concentration of nucleotide needed to promote fiber growth. These data indicate that ectoapyrases and extracellular nucleotides play a significant role in regulating cotton fiber growth and that ethylene is a likely downstream component of the signaling pathway.
Highlights
Ectoapyrase enzymes remove the terminal phosphate from extracellular nucleoside tri- and diphosphates
In this study we found that the expression of two cotton apyrases that most resemble AtAPY1 and AtAPY2 is highest during the rapid growth phase of the fibers, and that inhibition of apyrase activity by the addition of chemical apyrase inhibitors or anti-APY1/APY2 antibodies to cotton ovule cultures can inhibit cotton fiber growth
An alignment of the deduced amino acid sequence of the coding regions of GhAPY1, GhAPY2, AtAPY1, and AtAPY2 shows that GhAPY1 and GhAPY2 are very closely related with 86% identity (Supplemental Fig. S1)
Summary
Ectoapyrase enzymes remove the terminal phosphate from extracellular nucleoside tri- and diphosphates. The ethylene precursor, 1-aminocyclopropane-1-carboxylic acid, lowers the concentration of nucleotide needed to promote fiber growth These data indicate that ectoapyrases and extracellular nucleotides play a significant role in regulating cotton fiber growth and that ethylene is a likely downstream component of the signaling pathway. A recent review summarizes the evidence that eATP and the ectoapyrases that lower its concentration can regulate growth and other responses in plants (Roux and Steinebrunner, 2007). These findings led us to hypothesize that ectoapyrase activity could affect the growth of cotton fibers. Our results indicate that extracellular nucleotides and ectoapyrases play an important regulatory role during cotton fiber growth
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