Nature-De Wit-Mackey-2002 Comment
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Nature-De Wit-Mackey-2002 Comment

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nnews and viewsantimony atoms among all the silicon atoms clusters is random. This suggests that over- they will also be important in increasing ourcoming carrier saturation at very high dopantin the crystal is like searching for the prover- understanding of a wide range of complexbial needle in a haystack. To ‘see’ the anti- concentrations will be a major challenge. materials.Seeing is frequently the first step towardsmony dopant atoms, the researchers adapted Paul S. Peercy is at the College of Engineering,a powerful technique — scanning transmis- understanding. This first, unambiguous University of Wisconsin, 1415 Engineering Drive,5sion electron microscopy observation of single atoms bonded inside a— to image almost Madison, Wisconsin 53706-1691, USA.all the antimony atoms in the silicon crystal, bulk solid environment has wide-ranging e-mail: peercy@engr.wisc.eduimplications for the analysis of single atoms 1. Voyles, P. M., Muller, D. A., Grazul, J. L., Citrin, P. H. &even individual antimony atoms. Gossmann, H.-J. L. Nature 416, 826–829 (2002).The first critical step was to prepare thin and of clusters of two, three or four atoms —2. 2001 International Technology Roadmap for Semiconductorscrystals — only 9 or 11 atoms thick — lack- and for our efforts to understand the struc-(Semiconductor Industry Association, 2001);ing any surface or near-surface disorder that ture of impurities and alloy constituents in www.semichips.org/pre_technology.cfm 1 3. ...

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antimony atoms among all the silicon atoms clusters is random. This suggests that over- they will also be important in increasing our
coming carrier saturation at very high dopantin the crystal is like searching for the prover- understanding of a wide range of complex
bial needle in a haystack. To ‘see’ the anti- concentrations will be a major challenge. materials.
Seeing is frequently the first step towardsmony dopant atoms, the researchers adapted Paul S. Peercy is at the College of Engineering,
a powerful technique — scanning transmis- understanding. This first, unambiguous University of Wisconsin, 1415 Engineering Drive,
5sion electron microscopy observation of single atoms bonded inside a— to image almost Madison, Wisconsin 53706-1691, USA.
all the antimony atoms in the silicon crystal, bulk solid environment has wide-ranging e-mail: peercy@engr.wisc.edu
implications for the analysis of single atoms 1. Voyles, P. M., Muller, D. A., Grazul, J. L., Citrin, P. H. &even individual antimony atoms.
Gossmann, H.-J. L. Nature 416, 826–829 (2002).The first critical step was to prepare thin and of clusters of two, three or four atoms —
2. 2001 International Technology Roadmap for Semiconductors
crystals — only 9 or 11 atoms thick — lack- and for our efforts to understand the struc-
(Semiconductor Industry Association, 2001);
ing any surface or near-surface disorder that ture of impurities and alloy constituents in www.semichips.org/pre_technology.cfm
1 3. Gossmann, H.-J., Rafferty, C. S. & Keys, P M. at. Res. Soc. Symp.could scatter the incoming electron beam of crystalline solids. Voyles et al.’s results are
610, B1.2.1–B1.2.10 (2000).
the scanning transmission electron micro- important in understanding the distribution
4. Packan, P. A. Science 285, 2079–2080 (1999).
scope and prevent it from being guided of impurities in silicon at an atomic level; 5. Pennycook, S. J. & Narayan, JA. ppl. Phys. Lett.45, 385–387 (1984).
through the channels formed by the rows of
atoms in the lattice. The cross-section (or
probability) for electron scattering increases Plant biology
1.7with the atomic number Z, , as Z , so an anti-
mony atom, with Z451, scatters electrons On guard
nine times more strongly than a host silicon
atom with Z414. By detecting the intensity Pierre J. G. M. de Wit
1of the scattered electrons, Voyles et al. could
readily distinguish rows in the atomic lattice Microorganisms that infect plants must suppress their hosts’ defence
that contained a single antimony atom from mechanisms before they take up residence. But some plants use molecular
rows containing only silicon atoms (Fig. 1). guards to sense when they are being manipulated by pathogens.
From these elegant measurements, Voyles
et al. conclude that the electrically inactive s a rich source of sugars and amino nisms such as strengthened cell walls and
atoms are grouped in clusters containing two antimicrobial compounds, as well as activeacids, plants attract a variety of intrud-
antimony atoms. But their measurements Aers, from viruses, bacteria and fungi to healing responses. Only a few microbes can
also revealed that the basis on which impurity breach these ‘basal’ defences, and are theninsects. To protect themselves, plants have in
dopant atoms remain isolated or form small their armoury of passive defence mecha- fought by the plant’s innate immune system.
Agriculture
Champagne surprise
Pinot noir is an important grape their skin: using tissue culture, the
variety that is used for making wine, authors regenerated whole plants
including champagne. It is derived from Pinot Meunier L1 cells. As well
from an ancient strain that has been as having hairy leaves, these plants
cultivated for maybe 2,000 years. were semi-dwarfed — they were
Cultivated grapevines (Vitis vinifera ) shorter and stockier than usual. This
are usually reproduced from cuttings, provided a clue about which gene
so all individuals are genetically might be mutated. Sure enough, it
identical. But sometimes mutations turned out to be the grapevine
arise, and long ago this resulted in the equivalent of the gene that, when smaller. Of course this only occurs if this hormone may ensure that the
generation of another champagne mutated, causes dwarfing in wheat. all cells are mutant; if the mutation later-arising structures become
grape variety, Pinot Meunier (pictured Gene sequencing showed that the is limited to the epidermis the only tendrils rather than flowering stems.
here), from Pinot noir. Pinot Meunier gene had a similar mutation in the change seen is increased hairiness Gibberellic acid was known to
plants are genetically indistinguish- L1-cell plants and in dwarfed wheat. — gibberellic acid presumably also influence flowering in other plant
able from Pinot noir in most cells, but What does the gene do? It was suppresses hair growth. species, but this function is
their outer layer, the ‘L1’ epidermal first identified and cloned from the There was one more surprise apparently new. Interestingly, tendrils
cell layer, is different — meaning that thale cress Arabidopsis thaliana, and from Boss and Thomas’s study: in the in some plants such as peas have a
Pinot Meunier has a furry surface on named GA INSENSITIVE because of L1-cell plants, tendrils were replaced different origin — they are modified
its leaves whereas Pinot noir does the effect on the plant of mutating it. by flowering stems. Normally, a new leaflets rather than flowering stems.
not. Elsewhere in this issue ( Nature It is a regulatory gene that normally shoot produces several bunches of New knowledge about hormone-
416, 847–850; 2002), Paul K. Boss keeps a brake on plant growth; the flowers (and thus grapes) opposite response genes may allow us to
and Mark R. Thomas describe the brake is released by gibberellic acid the first few leaves, and tendrils fine-tune both the vegetative
precise mutation that causes this (GA). Thus the plant can regulate its opposite leaves that form later. The architecture of grapevines, and how
difference. Surprisingly, it is the growth by controlling the production tendrils anchor the vine as it grows in many bunches of grapes they
grapevine equivalent of the ‘dwarfing’ and location of this hormone. Some search of light. But in the semi- produce. David R. Smyth
mutations used to increase wheat mutations in the gene disrupt the dwarfed mutant, flowering stems David R. Smyth is in the School of
yields during the green revolution. encoded protein so that gibberellic continued to form in place of tendrils. Biological Sciences, Clayton
Boss and Thomas started by acid no longer releases the brake on Presumably, the explanation is again Campus, Monash University,
producing grapevines that carried growth. This means that the brake is that the plants cannot respond Victoria 3800, Australia; e-mail:
the mutation in all their cells, not just permanently on, and the plant is correctly to gibberellic acid. Normally, david.smyth@sci.monash.edu.au
NATURE | VOL 416| 25 APRIL 2002| www.nature.com 801
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CEPHAS/KEVIN JUDDnews and views Pseudomonas
a b syringaeSusceptible Resistant
DeliveryArabidopsis Arabidopsis
plant of Avr plant
proteins
RPM1 Inside
Avr AvrRIN4 RIN4 cell
100 YEARS AGO
Our present state of civilisation has of
necessity resulted in an annual increase in
RPM1the amount of capital borrowed by man from Avr InsideRIN4AvrRIN4the store of energy accumulated by our earth cell
in bygone times, and the diversion of this PP
capital to uses for which the world’s annual
income of solar energy was formerly Less pathogen growth
Suppress basal defences Hypersensitive responsedeemed adequate. An instance of this
More pathogen growth (local cell death)
tendency is afforded by the experiments of
Dr. Selim Lemström, of Helsingfors, on the
3uses of electricity in stimulating the growth Figure 1 At the crossroads of disease resistance and susceptibility. Mackeety al. studied the
of cereals, vegetables and other plants… The Arabidopsis thaliana resistance (R) protein RPM1, and the Pseudomonas syringaeavirulence (Avr)
investigation seems to have been suggested proteins AvrRpm1 and AvrB. (P. syringae infects A. thaliana leaves.) The authors found that the two
in the first instance by an attempt to connect bacterial proteins can bind to the plant protein RIN4, tag it with phosphate groups (circled ‘P’) and
the luxuriant growth of plants in high upregulate its concentration and its activity as a negative regulator of plant basal defence
latitudes with the influence of electric mechanisms. a, In susceptible plants, this downgrading of plant defences results in the spread of the
currents associated with the Aurora Borealis. bacterium. b, Resistant plants make use of the RPM1 protein to sense these manipulations of RIN4 by
The experiments showed that for plants the bacterial Avr proteins, activating the hypersensitive response which prevents bacterial spread.
growing on arable land of medium quality Figure modified from ref. 3.
an increase of 45 per cent. in the crops is
5
obtainable; but the better the field is The innate immune response is well descri- interactions , and so are expected to allow
ploughed and cared for the greater will be bed genetically by what is known as the R proteins to lock directly onto Avr proteins,
1
the increase. On poor soil the effect is trifling. gene-for-gene model , because it requires a although (despite much searching) so far this
Certain plants, such as peas, cabbages and pathogen protein encoded by an ‘avirulence’ has been shown only for the rice Pi-ta protein
turnips, only lend themselves to electrical (Avr) gene to be recognized by a plant pro- and the AvrPita protein from the rice-blast
6fungus Magnaporthe griseatreatment after being watered. It is, however, tein encoded by a resistance ( R) gene. This . LRRs may also
injurious to most, if not all, plants to submit activates an array of defence mechanisms, specify interactions with other plant proteins
2including the hypersensitive responsethem to the influence of electricity in hot , in (although the specificity of R proteins is not
7
sunshine... A further suggestion is that which a few plant cells at the site of infectiondetermined solely by their LRRs ). Some
we have here an explanation of the needle- die, thereby limiting the spread of disease. R proteins have LRRs in their extracellular
shaped leaves of coniferous plants which Although many Avr and R proteins have regions; here, the LRRs are assumed to be
been identified, we have still much to learnare well adapted to facilitate the passage involved in recognizing pathogens outside
8
of electricity, or in common parlance, about what they do. For example, do Avr pro-plant cells . By contrast, the A. thaliana
teins bind directly to R proteins? And what“attract electricity.” RPM1 protein resides wholly within plant
From Nature 24 April 1902. are the main functions of Avr proteins? They cells, associated with the plasma membrane,
are surely not there just to enable the plant towhere it was thought to interact directly with
50 YEARS AGO detect the intruder. Writing in Cell, Mackey Avr proteins like P. syringae AvrRpm1 and
3 9et al. AvrBCrystalline penicillin (sodium salt) was have proposed some answers. The . These Avr proteins are injected into
added at the rate of 12.6 gm. per ton to a authors studied the R protein RPM1 from theleaf cells by the tubular bacterial type III
10
standard turkey-rearing mash... The thale cress Arabidopsis thalianaand two Avr secretion machinery .
experiments briefly summarized show that proteins, AvrB and AvrRpm1, from the bac- But it seems that things are not so simple.
3terium Pseudomonas syringae. They showthe addition of small amounts of penicillin to Mackey et al. find that the A. thalianaRPM1
the diet of growing turkeys not only that RPM1 is a molecular guard that prevents and P. syringaeAvrRpm1 and AvrB proteins
the bacterial proteins from taking advantageproduced a significant increase in growth- interact not directly but indirectly, through
rate but also that it appeared to have a of another plant protein, RIN4, that down- the newly discovered plant protein RIN4 (for
grades plant basal defences. The results pro- ‘RPM1-interacting protein-4’). The authorsprofound effect in stimulating metabolism,
tiding chicks over a critical period of vide concrete support for the ‘guard hypoth- first identified RIN4 because of its interaction
esis’ of plant defence (reviewed in refs 2,4). with AvrB, and showed that it also interactssusceptibility to chilling and other non-
specific causes of mortality during the first Some predictions about the molecular with RPM1 and AvrRpm1. They then discov-
connections between Avr and R proteins ered that RIN4 suppresses the expression offew weeks of life. Rate of growth and
mortality during rearing are factors of have emerged from studies of their struc- plant genes needed for basal defence; more-
tures and amino-acid sequences. For the over, both AvrRpm1 and AvrB induce theprimary importance to the turkey industry
and largely determine the profitability of the most part, pathogen Avr proteins are struc- covalent addition of phosphate groups to
turally unrelated to each other. But most RIN4, possibly enhancing its ability to nega-undertaking... Its administration to birds
destined for the table within the shortest plant R proteins do have similar structures tively regulate plant defence. Conversely,
and contain sequences with a high propor- however, RIN4 is essential for RPM1 to acti-possible time would appear to be strongly
indicated. tion of leucine amino acids. vate the hypersensitive response to the two
These ‘leucine-rich repeats’ (LRRs) are P.syringae proteins, thereby inhibiting bacte-From Nature 26 April 1952.
thought to be involved in protein–protein rial growth — this response does not occur in
802 NATURE | VOL 416| 25 APRIL 2002| www.nature.com
© 2002 Macmillan Magazines Ltdn
news and views
12plants with low levels of RIN4. Reductions in Avr protein (Avr2) requires not only the cog- 1. Flor, H. H. Annu. Rev. Phytopathol.9, 275–296 (1971).
2. Dangl, J. L. & Jones, J. D. G. Nature 411, 826–833 (2001).RIN4 levels also cause reductions in RPM1 nate R protein (Cf-2) but also a further toma-
3. Mackey, D. et al. Cell108, 743–754 (2002).levels and (for as yet unknown reasons) resis- to protein (Rcr3), found outside cells, which
4. Van der Hoorn, R. A. L., Joosten, M. H. A. J. &
13tance to both P. syringae and, intriguingly, the might be a virulence-related target. Perhaps de Wit, P. J. G. M. Trends Plant Sci.7, 67–71 (2002).
unrelated fungus-like Peronospora parasitica . the R protein protects this target from the 5. Ellis, J., Dodds, P. & Pryor, TT. rends Plant Sci.5, 373–379
(2000).All of which suggests that RIN4 sits at a pathogen protein. Molecular guards may be
6. Jia, Y. et al. EMBO J.19, 4004–4014 (2000).crossroads between susceptibility and disease widely used to prevent plant proteins from
7. Luck, J. E. et al. Plant Cell12, 1367–1377 (2000).
4resistance, and that RPM1 guards A. thaliana being subverted for pathogenic purposes . 8. Joosten, M. H. A. J. & de Wit, P. J.G. M. Annu. Rev. Phytopathol.
against pathogens that use AvrRpm1 and Pierre J. G. M. de Wit is in the Laboratory of 37, 335–367 (1999).
3 9. Nimchuk, Z. et al. Cell101, 353–363 (2000).AvrB to manipulate RIN4 activity (Fig. 1). Phytopathology, Wageningen University,
10.Hueck, C. J. Microbiol. Mol. Biol. Rev62,. 379–433 (1998).
So, when susceptible plants are infected by Binnenhaven 5, 6709 PD Wageningen,
11.Leach, J. E. et al. Annu. Rev. Phytopathol. 39, 187–224 (2001).
P. syringae, the Avr proteins interact with The Netherlands. 12.Luderer, R. et al. Mol. Microbiol.(in the press).
13. Dixon, M. S. et al. Proc. Natl Acad. Sci USA 97, 8807–8814 (2000).RIN4, induce its phosphorylation, and e-mail: pierre.dewit@fyto.dpw.wag-ur.nl
increase its concentration, thereby inhibiting
basal defences and leading to susceptibility.
But in plants that are resistant toP . syringae, Relativity
these manipulations are somehow sensed
by RPM1, which launches a local cell-death Testing times in spaceprogramme that leads to resistance.
3So Mackey et al. have shown how one Steve K. Lamoreaux
R protein and two Avr proteins work at the
molecular and cellular levels, causing either We take for granted that physical ‘constants’, such as the speed of light,
disease or the hypersensitive response accord- are fixed values. But they might not be, and experiments in space may
ing to the balance of power between the pro- allow us to investigate this possibility.
teins. In so doing, the authors have answered
the questions (at least for this set of proteins) any violation of relativity can be correlatedbasic assumption of Einstein’s theory of
of how an R protein can sense the presence of relativity is that the fundamental physi- with some aspect of orientation or velocity.
its cognate Avr proteins — through their An example of a clock comparison exper-Acal laws and parameters do not depend
manipulation of RIN4 — and what the Avr on the position, orientation or uniform iment is to test whether the speed of lig cht, , is
proteins do. It is known that some fungal and velocity of the laboratory in which they are a universal constant — is there a limiting
bacterial Avr proteins function in susceptible measured — a property generally known as speed for matter, c , that is different from them
plants as ‘virulence factors’, thought to be Lorentz invariance. Relativity has been test- speed of light? For instance, my colleagues
2required for maximum virulence of the ed, implicitly and explicitly, in countless and I have sought a difference in the values
11 3pathogen experiments; as yet, no failure of the theory. Mackey et al. have revealed that of these numbers by comparing the behav-
199 201Avr proteins can do this by increasing the has been observed. But most explicit tests iour of two atomic nuclei, Hg and Hg. In
have been confined to laboratories on Earth.activity of a plant defence inhibitor. an applied magnetic field, the magnetic-
This study should give a boost to those In Physical Review Letters , a theoretical moment vector of a nucleus precesses about
1studying the molecular interactions between analysis by Bluhm et al. shows that experi- the field direction at a particular frequency
plants and microbes. It is likely that the directments in space — some already planned for (this process is also the basis of magnetic
199interaction shown for the rice and rice-blast resonance imaging). The the International Space Station — could Hg nucleus is
6fungus proteins is the exception, not the rule; offer better sensitivity, as well as extending spherical and so its orientation in space (usu-
the range of tests that could be performed.mechanisms like that described by Mackeety ally defined relative to distant, ‘fixed’ stars)
3al. may be more common. Many labs are Some of the most exacting tests of relativi-does not affect the precession frequency. But
201ty have involved atomic clocks. These ‘tick’ bythe now hunting for virulence-related targets of Hg nucleus is egg-shaped — its lack of
Avr proteins, akin to RIN4, in other model electrons moving between energy levels spherical symmetry means that the angle
emitting a photon with a certain frequency.gene-for-gene systems. It will be interesting between its velocity vector and its magnetic
to see whether different pathogens use the The tests compare the tick rates of two differ-moment becomes important; and if c is notm
same targets. For instance, if the P. parasitica ent atomic clocks as a function of their orien-identically equal toc , a shift in the precession
201 199Avr proteins (which have not yet been identi- tation and velocity through space. The idea is frequency of Hg compared to that of Hg
fied) also interact with RIN4, that might that, if the two clocks are based on different appears. In this Earth-bound experiment,
explain why plants that are susceptible to types of energy-level transitions, any failure no difference between c and c was detected,m
P. syringae are also susceptible to P. para- of Lorentz invariance would show up as a implying that if such a difference exists, then
22sitica. Another question is whether different relative shift in the two frequencies of the 11c /c*10 — a rather astoundinglym
Avr proteins from the same pathogen are clocks, because the physical ‘constants’ gov- accurate limit.
recognized by the same plant protein, as are erning the ticks of the clocks would not actu- This experiment is prototypical of many
AvrB and AvrRpm1. I anticipate that most ally be constant, but would change with the of the experiments described by Bluhm et
1pathogens have a set of Avr proteins that clocks’ orientation and velocity. al. , and we can question whether there
work together to afford full virulence. In Earth-based experiments, the orienta- would be an advantage to performing it in
Finally, as mentioned above, some Avr tion and velocity of the clocks are deter- space. Among the advantages that Bluhm et
proteins — such as those from the tomato mined by the Earth’s rotation and revolution al. specifically address is the ability to
8pathogen Cladosporium fulvum — are about the Sun, and by the motion of the Solarchange the orientation and velocity of
System relative to the Universe as a whole. space-borne clocks to arbitrary directions;detected by LRR motifs on the outside of
plant cells, rather than inside. Might a simi- Typically, the differential clock frequencies orientation changes could also be made
are measured as a function of time. Given themore rapidly than the once-per-day changelar guard mechanism protect against
pathogens like these, too? Support for this Earth coordinates of the clocks, together withfor an Earth-based experiment (which
idea comes from the finding that the hyper- the time and date, the time-dependent orien- would avoid problems due to slow drift in
sensitive response of tomato to one C. fulvum tation of the clock can be determined. Then, the clock frequencies). In fact, in the specific
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