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Plant Physiol, June 2002, Vol. 129, pp. 391-392

EDITORIAL

Plant Physiology's Best Paper Award 2001


It is a pleasure to announce Dr. Frans J.M. Maathuis as the winner of the second annual Plant Physiology Best Paper Award. The paper for which he is receiving this award---a contribution that he co-authored with Dr. Dale Sanders (see Plant Physiology 127: 1617-1625)---is entitled "Sodium Uptake in Arabidopsis Roots Is Regulated by Cyclic Nucleotides." In this paper the authors, both of the University of York, present evidence, based on a diversity of techniques, to support the idea that a cyclic nucleotide-gated channel is involved in allowing Na+ influx into Arabidopsis roots under high salt conditions. This highly original finding will undoubtedly have broad implications for understanding the basic biology of salt stress in glycophytic plants and may conceivably lead to the genetic engineering of increased salt resistance in agricultural crops.

Soil salinization is an expanding agricultural problem. Around 6% of global land area suffers from salinization, either naturally or through human activities such as irrigation. Because most crop species are salt sensitive, salinization places a major strain on agricultural production, particularly in marginal, semi-arid areas. Indeed, it is estimated that irrigation-related salinization leads to the abandonment of 107 ha of agricultural land annually. Na+ uptake from the soil is a major cause of salinity toxicity in plants, yet little is known about the mechanisms that underlie Na+ uptake by plant cells. It is clear that successful strategies to limit Na+ uptake by crop species will have to involve an understanding of Na+ uptake pathways.

The general research interests of Dr. Maathuis are in plant nutrition and abiotic stress, with particular emphasis on ion transport across plant membranes. In particular, he has pioneered the application of electrophysiological techniques to address fundamental questions in plant physiology. During his PhD studies at the University of Groningen in the 1980s, he set up the first plant patch-clamp facility in The Netherlands to compare the vacuolar membrane transport properties of salt-sensitive and salt-tolerant Plantago spp. He continued this work while he was a postdoctoral fellow at the University of Sussex in the United Kingdom, this time studying the role of the slow vacuolar channel in salt tolerance of the halophyte Suaeda maritima.

In 1992, Dr. Maathuis started work in the Biology Department of the University of York, United Kingdom, as a postdoctoral fellow with Dr. Dale Sanders. During the ensuing years, he studied the mechanisms of low- and high-affinity K+ uptake in plants. K+, as the major cationic constituent of fertilizers, has been the subject of longstanding plant physiological research, and Dr. Maathuis's studies helped define the energizing principles regarding the mechanisms of high- and low-affinity K+ uptake in plant roots. Using Arabidopsis as a model, the main conclusions of this work were that low-affinity K+ uptake is mainly mediated by a specific inward-rectifying K+ channel and that high-affinity K+ uptake is energized via coupling to the H+ gradient with a 1:1 stoichiometry. The latter is now generally accepted as the mechanism for high-affinity K+ uptake in terrestrial plants.

Since 1998, Dr. Maathuis has worked as an independent research fellow in York. His research interest has returned to the area of plant salt tolerance, where a key question concerns the identification of pathways for Na+ entry into plant roots. Using a patch-clamp approach, he successfully characterized non-selective cation channels in Arabidopsis root cells. Although these channels were prime candidates for contributing significantly to a plant Na+ load, nothing was known about the modulation of their activity. Dr. Maathuis discovered that in some root cells the activity of a voltage-independent class of transporter is inhibited by cyclic nucleotides, providing a putative mechanism for regulation of non-selective cation channels in plants. In addition, he showed that Na+ influx in intact roots is down-regulated by cyclic nucleotides and that these compounds enhance plant growth in salinized conditions. These findings suggest that cyclic nucleotides improve salt tolerance through inhibition of uptake of Na+ through these voltage-independent channels (VICs). If this is indeed the case, then externally supplied cyclic nucleotides should reduce the amount of Na+ that is accumulated in plants. Accordingly, Na+ contents of plants subjected to salinity in the presence and absence of membrane-permeable cyclic nucleotides were measured and found to be lower in the presence of cyclic nucleotides. These rather long-term experiments might be subject to the criticism that cyclic nucleotides are decreasing Na+ content through one of a number of secondary effects, and therefore short-term unidirectional Na+ uptake was measured. The results demonstrated a clear inhibitory effect of cGMP and, to a lesser extent, cAMP on Na+ uptake, again in accord with the notion that cyclic nucleotide-inhibitable VICs provide a major route for uptake of Na+. The results in this study open up several hitherto unexpected but highly exciting avenues. First, they suggest that previously described channels that exhibit VIC activity might be encoded by the Cyclic Nucleotide-Gated Channel (CNGC) family. Patch-clamp studies are now taking place on cngc knockout mutants to resolve this issue. Second, the physiological functions of VICs now need to be more intensely investigated: It is unlikely that their function is to allow Na+ into plants, since the ion has little nutritional relevance. It seems possible that these channels form a pathway for Ca2+ uptake and therefore constitute a junction in Ca2+- and cyclic nucleotide-based signaling pathways. Finally, the results imply that it might be possible to engineer a degree of salt tolerance in plants by blocking cyclic nucleotide-gated channels. Subsequent to the acceptance of this groundbreaking paper in Plant Physiology, Maathuis and Sanders have found that a knockout mutant in one cyclic nucleotide-gated channel isoform is, under some conditions, more salt resistant.

An article summarizing Dr. Maathuis's work is scheduled for the May/June 2002 issue of the ASPB News, the Society's membership newsletter. Dr. Maathuis will be honored at the ASPB Annual Awards Ceremony, to be held Saturday, August 3, the opening day of the Plant Biology 2002 meeting in Denver. At that time, ASPB president Vicki Chandler will present Dr. Maathuis with a check for $1,000. On Tuesday, August 6, he will present a talk at the "Membrane Transport" minisymposium. Congratulations, Frans!

    FOOTNOTES

www.plantphysiol.org/cgi/doi/10.1104/pp.900035.

Natasha V. Raikhel, Editor-in-Chief of Plant Physiology

Peter V. Minorsky, Science Writer

© 2002 American Society of Plant Physiologists




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