Abstract
Adenosine kinase (ADK) is a key enzyme that regulates intra- and extracellular levels of adenosine, thereby modulating methyltransferase reactions, production of polyamines and secondary compounds, and cell signaling in animals. Unfortunately, little is known about ADK's contribution to the regulation of plant growth and development. Here, we show that ADK is a modulator of root cap morphogenesis and gravitropism. Upon gravistimulation, soluble ADK levels and activity increase in the root tip. Mutation in one of two Arabidopsis (Arabidopsis thaliana) ADK genes, ADK1, results in cap morphogenesis defects, along with alterations in root sensitivity to gravistimulation and slower kinetics of root gravitropic curvature. The kinetics defect can be partially rescued by adding spermine to the growth medium, whereas the defects in cap morphogenesis and gravitropic sensitivity cannot. The root morphogenesis and gravitropism defects of adk1-1 are accompanied by altered expression of the PIN3 auxin efflux facilitator in the cap and decreased expression of the auxin-responsive DR5-GUS reporter. Furthermore, PIN3 fails to relocalize to the bottom membrane of statocytes upon gravistimulation. Consequently, adk1-1 roots cannot develop a lateral auxin gradient across the cap, necessary for the curvature response. Interestingly, adk1-1 does not affect gravity-induced cytoplasmic alkalinization of the root statocytes, suggesting either that ADK1 functions between cytoplasmic alkalinization and PIN3 relocalization in a linear pathway or that the pH and PIN3-relocalization responses to gravistimulation belong to distinct branches of the pathway. Our data are consistent with a role for ADK and the S-adenosyl-L-methionine pathway in the control of root gravitropism and cap morphogenesis.
Highlights
The primary roots of most plants perceive their orientation within the gravity field mainly through the sedimentation of starch-filled plastids within the columella cells of the root cap (Blancaflor and Masson, 2003)
We show that adenosine kinase (ADK; EC2.7.1.20; ATP: adenosine 5’phosphotransferase), an enzyme that converts adenosine (Ado) into adenosine 5’-monophosphate (5’-AMP), using one molecule of ATP (Moffatt et al, 2000), modulates root gravitropism and cap morphogenesis in Arabidopsis thaliana
Our data indicate that adk1-1 alters root gravitropism by affecting both gravitropic sensitivity and curvature kinetics
Summary
The primary roots of most plants perceive their orientation within the gravity field mainly through the sedimentation of starch-filled plastids within the columella cells of the root cap (Blancaflor and Masson, 2003). A lateral gradient of auxin forms across the root cap, which can be observed indirectly by the asymmetrical activation of expression of auxin-responsive reporters, such as DR5-GUS or DR5-GFP (Boonsirichai et al, 2003; Ottenschläger et al, 2003), at the bottom flank of the cap This gradient of auxin is transmitted basipetally through cell files, using a transport system that involves auxin influx and efflux carriers, such as the AUX1, PGP4 and AGR1/EIR1/PIN2/WAV6 proteins, respectively (Bennett et al, 1996; Chen et al, 1999; Terasaka et al, 2005). The gravity-induced auxin gradient, probably coupled with other signals, promotes a complex differential cellular elongation between upper and lower flanks, resulting in gravitropic curvature (Blancaflor and Masson, 2003) Other than those that affect starch synthesis or accumulation in columella amyloplasts, only a few genes have far been uncovered through genetic screens for their involvement in gravity signal transduction within the root statocytes (Blancaflor and Masson, 2003). ARL2, contributes to root and hypocotyl gravitropism, and appears to function in the same genetic pathway (Guan et al, 2003)
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