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Carbon dioxide and water use in forests

state of the doublet accommodates current in the ‘forward’ direction (the supercurrent usually observed in junctions), whereas the excited state corresponds to current in the ‘reverse’ direction. Importantly, the Andreev bound-state doublet is a system of spin-1/2 that is localized to the weak link and behaves as an internal degree of freedom associated with the Josephson effect. It is this internal feature that Bretheau et?al. detected directly using the technique of photon–absorption spectroscopy. The authors used several aspects of the Josephson effect to carry out photon-absorption spectroscopy of the Andreev doublet. First, to access the doublet from a single weak link, they used a mechanically controllable atomic break junction (a narrow bridge containing only a few atoms) formed on a flexible substrate5. By applying a mechanical force in situ to the cryogenically cooled break junction, the researchers could reduce the number of channels down to as low as a single weak link with a particular transmission probability. Second, to change the phase difference across the atomic junction and thereby tune the Andreevdoublet energies, Bretheau et?al. fabricated the break junction as part of a superconducting loop containing a much larger Josephson tunnel junction, thereby forming a sensitive magnetometer known as a superconducting quantum interference device. In this configuration, a magnetic field applied to the loop sets the phase difference across the atomic junction and makes the bound-state energies tunable. Third, to drive transitions between the ground and excited Andreev bound states, the authors used a separate tunnel junction as a spectrometer (Fig.?1). Applying a voltage to the spectrometer junction causes it to emit electromagnetic radiation at a frequency that is proportional to the applied voltage and is tunable over a wide range — up to around 80?gigahertz. Finally, owing to conservation of energy, a unidirectional (d.c.) current flows through the spectrometer junction that is proportional to the absorption rate of the radiation emitted by the atomic junction or the surrounding environment. Therefore, determining the spectrometer’s d.c. current is a measurement of the absorption rate. The spectrometer Josephson junction thus serves both as a microwave generator and a detector in this experiment. With this set-up, Bretheau et?al. carried out photon-absorption spectroscopy of the Andreev bound-state doublet, observing the expected trend in transition frequency as a function of the phase difference across the atomic junction. It should be noted that in several earlier experimental works (for example, ref.?6), the presence of Andreev bound states was required to explain the observed phenomena, serving as indirect evidence for their existence. More recently, direct evidence was provided by applying a technique called tunnelling spectroscopy to a carbon nanotube weak link7 and to a graphene quantum dot8?— complementary studies that observed alternative microscopic configurations of the bound states. Bretheau and colleagues’ experiment stands as the first photon-absorption spectroscopy of the spin-1/2 Andreev boundstate doublet. These doublets could be used as a quantum logic element or, in conjunction with interactions between the electron’s spin and orbital degrees of freedom, to realize a Majorana state?— an elusive spin-1/2 particle that is its own antiparticle. This experimental technique may also shed light on the perennial problem of quasi-particle poisoning in coherent superconducting devices. Indeed, by driving the bound-state transition, this work opens up experiments to a new level of Andreev physics. ■

Simon Gustavsson is in the Research Laboratory of Electronics, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139–4307, USA. William D. Oliver is in the Lincoln Laboratory, Massachusetts Institute of Technology, Lexington, Massachusetts 02420–9108, USA. e-mails: simongus@mit.edu; oliver@ll.mit.edu
1. Josephson, B. D. Phys. Lett. 1, 251 (1962). 2. Bretheau, L. et al. Nature 499, 312–315 (2013). 3. Feynman, R. P., Leighton, R. B. & Sands, M. The Feynman Lectures on Physics (Basic Books, 2011). 4. Hekking, F. W. J., Schon, G. & Averin, D. V. Proc. NATO Adv. Res. Workshop Mesoscopic Superconductivity (NATO-ASI, 1994). 5. van Ruitenbeek, J. M. et al. Rev. Sci. Instrum. 67, 108–111 (1996). 6. Fueschsle, M. et al. Phys. Rev. Lett. 102, 127001 (2009). 7. Pillet, J.-D. et al. Nature Phys. 6, 965–969 (2010). 8. Dirks, T. et al. Nature Phys. 7, 386–390 (2011).

Carbon dioxide and water use in forests
Plants are expected to respond to rising levels of atmospheric carbon dioxide by using water more efficiently. Direct evidence of this has been obtained from forests, but the size of the effect will prompt debate. See Letter p .324
B E L I N D A M E D LY N & M A R T I N D E K A U W E


n a study published on page 324 of this issue, Keenan et?al.1 report that the efficiency with which forests use water has increased over the past 20?years, and conclude that this is a consequence of rises in the concentration of atmospheric carbon dioxide.* The findings call for a reassessment of models of the terrestrial carbon cycle. The concentration of CO2 in the atmosphere is rising at an unprecedented rate. In May this year, it reached 400 parts per million, 43% above the pre-industrial concentration of 280?p.p.m. (ref.?2). Much of this increase has occurred in recent decades, with the rate of increase over the past 20?years being 5% per decade2. This drastic upsurge in atmospheric CO2 should have stimulated plant productivity worldwide, because we know from experiments that rising CO2 concentrations increase the rate of photosynthesis and reduce water use in plants3. Such effects are fundamental to our current understanding of the carbon cycle — for example, most terrestrial carboncycle models explain the current land sink for carbon by assuming that rising CO2 levels have enhanced plant productivity4. However, detecting the effects of rising
*This article and the paper under discussion1 were published online on 10 July 2013.

CO2 concentrations on terrestrial vegetation outside controlled experiments has proven remarkably difficult, provoking numerous debates about whether such effects are really occurring5–10. There are few high-quality, longterm records of plant productivity and water use that can be used to test for such effects. The main types of data come from plot surveys, tree-ring records, satellite images, aerial photographs and measurements of stream flow. Each of these is an indirect measurement and has a relatively coarse time resolution. Even where trends in these data have been detected, it has been extremely difficult to attribute them to rising CO2 levels, because simultaneous changes in many confounding factors — such as rainfall, temperature, land use and fire frequency — have occurred11. Keenan et?al. bring a new source of data to bear on this problem. The eddy-covariance technique, developed in the 1980s to quantify the exchange of gases between the atmosphere and land areas, has revolutionized plantecosystem science because it continuously monitors the functioning of whole ecosystems on an hourly timescale12. Using instruments mounted above a vegetation canopy, eddy covariance can be used to measure the carbon uptake and water use of whole ecosystems on a spatial scale of up to one square kilometre. Over the past 20?years, eddy-covariance towers
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CO2. Decades of controlled experiments13–15 have consistently found that the intercellular CO2 concentration (Ci) in photosynthesizing tissue is proportional to the atmospheric CO2 concentration (Ca) — that is, Ci/Ca is constant. The trend identified by Keenan et?al., however, implies that intercellular CO2 has remained constant, and so Ci/Ca has strongly decreased with increasing concentrations of atmospheric CO2. To put it another way, controlled experiments16,17 have found that the effect of increased atmospheric CO2 levels on water-use efficiency is roughly proportional to the increase in atmospheric CO2. By contrast, according to our calculations, the increase in water-use efficiency found by Keenan and co-workers in the eddy-covariance data is approximately six times larger than the corresponding increase in atmospheric CO2. Consequently, the authors show that current models of the terrestrial carbon cycle do not capture the magnitude of the trend obtained from eddy covariance. This is to be expected, because the models were developed from, and so are consistent with, data from controlled experiments17. Keenan and colleagues’ study thus provides an intriguing challenge to our understanding of ecosystem functioning — there is a significant increase in water-use efficiency that we cannot currently explain. The implication is either that plants are markedly more responsive to rising CO2 levels than we previously thought, or that there are other, unknown factors behind the observed trend in the eddycovariance data. Our view is that it is unlikely that the effect of CO2 on water-use efficiency is being underestimated by the magnitude that Keenan et al. suggest, because the response of water-use efficiency to CO2 is so predictable in controlled experiments16,17. Nevertheless, the authors have ruled out most other potential drivers for the trend. More research is clearly needed to understand these findings, including long-term studies with complementary observational data streams, such as measurements of changes in plant biomass and water use by whole ecosystems. ■ Belinda Medlyn and Martin De Kauwe are in the Department of Biological Science, Macquarie University, North Ryde, New South Wales 2109, Australia. e-mails: belinda.medlyn@mq.edu.au; mdekauwe@gmail.com
1. Keenan, T. F. et al. Nature 499, 324–327 (2013). 2. www.esrl.noaa.gov/gmd/ccgg/trends 3. Eamus, D. & Jarvis, P. G. Adv. Ecol. Res. 19, 1–55 (1989). 4. Arora, V. K. et al. J. Clim. http://dx.doi.org/10.1175/ JCLI-D-12-00494.1 (2013). 5. Lewis, S. L., Malhi, Y. & Phillips, O. L. Phil. Trans. R. Soc. Lond. B 359, 437–462 (2004). 6. Gedney, N. et al. Nature 439, 835–838 (2006). 7. Piao, S. L. et al. Proc. Natl Acad. Sci. USA 104, 15242–15247 (2007). 8. Wright, S. J. Glob. Change Biol. 19, 337–339 (2013).

Figure 1 | Vapour flux. Keenan et al.1 analysed the flux of water vapour and carbon dioxide above forests in the Northern Hemisphere, such as at Willow Creek, California (pictured).

have been established worldwide in a broad range of ecosystems, and high-quality longterm data sets are now becoming available12. The authors used these data to analyse longterm changes in ecosystem-scale water-use efficiency. Plants lose water through evaporation whenever they open their stomata to admit CO2 for photosynthesis, and water-use efficiency is a measurement of the rate at which the plant exchanges water for carbon. This measurement is expected to be a good indicator of the effects of rising CO2 concentrations on vegetation — because rising CO2 levels both increase carbon uptake by plants and reduce plant water use, the effects of higher levels of CO2 on water-use efficiency should be larger and more consistent than the effects on carbon gain or water use alone. Keenan and colleagues report that the wateruse efficiency of forest canopies in the Northern Hemisphere (Fig.?1) over the past two decades shows a remarkable upward trend. The trend was consistent, with no decreases at any
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of the 21 forest sites examined. The rates of increase across all sites were large (averaging about 3% per annum) and highly statistically significant. To prove that this rise was caused by increasing levels of atmospheric CO2, Keenan et?al. examined a suite of potential confounding factors. They found that, across all 21?sites, there were no trends in meteorological variables (precipitation, wind speed, temperature and humidity) or structural attributes of canopies (leaf area, leaf-nitrogen content and canopy roughness) that could explain the observed rise in water-use efficiency. The authors conclude that the trend was most consistent with a strong fertilization effect of increased CO2. This observation-based finding will probably stimulate considerable debate and further research because, although the reported trend is convincing, the magnitude of the trend is much larger than would be predicted from our existing knowledge of plant responses to
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9. Clark, D. A., Clark, D. B. & Oberbauer, S. F. J. Geophys. Res. 118, 1–12 (2013). 10. Silva, L. C. R. & Anand, M. Glob. Ecol. Biogeogr. 22, 83–92 (2013). 11. Donohue, R. J., McVicar, T. R. & Roderick, M. L. Glob. Change Biol. 15, 1025–1039 (2009). 12. Baldocchi, D. Aust. J. Bot. 56, 1–26 (2008). 13. Wong, S. C., Cowan, I. R. & Farquhar, G. D. Plant Physiol. 78, 821–825 (1985). 14. Drake, B. G., Gonzàlez-Meler, M. A. & Long, S. P. Annu. Rev. Plant Physiol. Plant Mol. Biol. 28, 609–639 (1996). 15. Ainsworth, E. A. & Rogers, A. Plant Cell Environ. 30, 258–270 (2007). 16. Barton C. V. M. et al. Glob. Change Biol. 18, 585–595 (2012). 17. De Kauwe, M. G. et al. Glob. Change Biol. 19,? 1759–1779 (2013).


50 Years Ago
A technique has been used with limited success to obtain simultaneous measurement of cosmic radiation at two different altitudes. The method consists of suspending two packets of nuclear emulsion plates from the one balloon, while maintaining a constant vertical separation of 10,000–27,000 ft. between the packets … in this way the two packets do not separate in latitude and longitude—a factor which enters if two separate independent balloons are flown. This has been achieved by carrying aloft a cone of nylon string which was allowed to unwind at a predetermined height, leaving one packet of plates suspended at the balloon while the other fell at the end of the string … As the alarm rings, the alarm winder releases the key … holding the lower packet and target, which then fall away freely, unwinding the string in the process. Twenty thousand feet of string unwinds in approximately 10 min. From Nature 20 July 1963

A three-state balancing act
How do pathogens survive temperature variations? At a molecular level, one bacterial species seems to regulate gene expression in response to temperature through structural equilibria in corresponding RNA sequences. See Letter p .355


n bacteria, many messenger RNA molecules carry a regulatory segment called a riboswitch. Specific binding of small ligand molecules, such as adenine, to this segment determine whether the riboswitch mRNA will be translated into a protein1–4. On page 355 of this issue, Reining et al.5 show that regulation of gene expression through such ‘riboswitching’ is coupled to temperature sensing. The authors investigate the adenine-sensitive riboswitch from the pathogenic bacterium Vibrio vulnificus6, and demonstrate that efficient RNA regulation at different temperatures — those of the bacterium’s marine habitat and its human host — requires a change in the riboswitch’s structural behaviour from a twostate pattern to a three-state one.* A typical riboswitch consists of two domains at the 5? end of the mRNA: a ligand-binding aptamer and an adjoining expression platform, which can have one of two mutually exclusive structures depending on whether the aptamer is in the ligand-bound or ligand-unbound state. The structural change in the expression platform signals that gene expression should be turned on or off. During gene transcription, a polymerase enzyme synthesizes first the aptamer and then the expression platform7. The sequential release of riboswitch domains from the polymerase is especially meaningful for transcription-controlling riboswitches, which act under kinetic control. To direct the folding of the expression platform, the aptamer domain of the growing RNA chain must bind rapidly to its ligand, which requires high ligand concentrations8; otherwise, the resulting fulllength mRNA becomes trapped in a default fold that cannot respond to the ligand9. In
*This article and the paper under discussion5 were published online on 10 July 2013.

transcription-controlling riboswitches, the two mutually exclusive structures are generally referred to as terminator and antiterminator folds, causing cessation of polymerase activity and continuation of mRNA synthesis, respectively. Bacterial transcription is tightly coupled to translation. In translation-controlling riboswitches, the molecular mechanism relies on either sequestration or liberation of the Shine–Dalgarno sequence — the mRNA site that binds to cellular organelles known as ribosomes to initiate translation. In contrast to transcription-controlling riboswitches, most translation-controlling riboswitches act under thermodynamic control9. Consequently, ligand-dependent control of translation is maintained even for a full-length mRNA. For these riboswitches, therefore, two states (ligand-bound and -unbound) seem sufficient to turn translation on and off. Reining and colleagues have found that, for robust functioning, their translation-controlling adenine-sensing riboswitch must occur in three structural states. The authors investigated the full-length (more than 100-nucleotide) riboswitch domain at single-nucleotide resolution. They also determined a complete set of thermodynamic and kinetic parameters for folding and ligand-binding of this RNA, under conditions that involved varying the concentrations of RNA, magnesium ions (a factor mediating structure formation) and adenine, as well as, importantly, temperature. The researchers find that a ligand-free (apo) form of the riboswitch exists in a pre-equilibrium of two structurally distinct aptamer folds (Fig.?1). One of the structures (apoA) can bind to the ligand, exhibiting a structure that resembles a third structural state — the adenine-bound holo form. The other structure (apoB) adopts a different fold and cannot interact with the ligand. But why does
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100 Years Ago
The Potato: A Compilation of Information from Every Available Source. By E. H. Grubb and W. S. Guilford. There are men who, having attained to wealth and fame by the agency of some humble instrument, basely repudiate and kick over the ladder by which they have risen. Not so the authors of the first book on our list. The potato has “made” them, and in return they proceed to “make” the potato … the authors are so evidently enthusiastic, and discourse so eloquently on the merits of their subject, that we are carried along with them, and forget that, after all, they are only talking about potatoes, and not about alpine plants or roses. From Nature 17 July 1913
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