intrinsic light scattering in bR) will help establish
the exact nature of the field interaction. The main
conclusion is that the experiment is clearly in the
weak field limit and the laser field is not strongly
perturbing the underlying thermally populated
modes, but rather inducing their interference in
also compared with and without phase control
(Fig. 6C), keeping spectral amplitudes constant
(Fig. 6D; spectral profiles were confirmed using
a tunable monochromator with 0.2-nm spec-
tral resolution). The data show a clear phase
dependence indicative of coherent control.
Pure amplitude modulation alters the temporal
profile of the pulse (fig. S5); therefore, removing
the phase modulation affects the isomerization
yield by only 5 to 7%. The phase sensitivity of
the control efficiency further illustrates the co-
herent nature of the state preparation.
anti-optimal pulses and the observed degree of the
isomerization yield control are consistent with the
known fast electronic dephasing of bR (10, 38).
The largest field amplitudes are confined to ap-
proximately 300-fs widths to yield 20% control. In
the case of transform-limited pulses, all the vibra-
tional levels within the excitation bandwidth are
excited in phase and there is a fast decoherence in
the initial electronic polarization (38). However,
with the phase-selective restricted bandwidths in
the shaped pulses, there is an opportunity to ma-
er coherence times than the electronic polarization.
The resultant constructive and destructive interfer-
ence effects involving vibrational modes displaced
controlling isomerization. Experimental obser-
vations presented here show that the wave proper-
to the point that they can even be manipulated.
References and Notes
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36. The saturation energy is related to the absorption cross
section s as Es0 1/strans(for a negligibly small
contribution of the excited-state emission), and s is
related to the extinction coefficient e as s 0 [log(10)/
NA]e 0 3.86 ? 10j21e, where NAis Avogadro’s number.
37. The fraction of excited molecules can be estimated as a
ratio between the number of absorbed photons np0
Eexc? pd20/4 and the number of retinal molecules Nm0
C ? V in an excited volume V0; l0? pd20/4, where the
concentration is C 0 2.303A0/strans, A0is OD at 565 nm
(0.9), l00 0.04 cm is the path length in the cell used,
and d00 0.015 cm is the beam diameter in the sample.
This gives a fraction of excited molecules of 0.0236 (that
is, 1 out of 42.3 molecules will be excited during the
excitation pulse at a given fluence). The fraction of
double-excited molecules can be estimated from the
Poisson distribution f(k) 0 ejl(l)k/k!, where l 0 0.0236,
and k is the number of occurrences (k 0 1 for the
single excitation, k 0 2 for the double excitation, etc.).
Thus, the fraction of double-excited molecules
f(2)/f(1) 0 l/2; that is, 1.18%.
38. V. F. Kamalov, T. M. Masciangioli, M. A. El-Sayed, J. Phys.
Chem. 100, 2762 (1996).
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40. This work was supported by the National Sciences and
Engineering Research Council of Canada. The authors
thank J.T.M. Kennis, Vrije Universiteit Amsterdam, for
helpful discussions of preliminary results.
Supporting Online Material
Materials and Methods
Figs. S1 to S5
1 June 2006; accepted 10 August 2006
Phytophthora Genome Sequences
Uncover Evolutionary Origins and
Mechanisms of Pathogenesis
Brett M. Tyler,1* Sucheta Tripathy,1Xuemin Zhang,1Paramvir Dehal,2,3Rays H. Y. Jiang,1,4
Andrea Aerts,2,3Felipe D. Arredondo,1Laura Baxter,5Douda Bensasson,2,3,6Jim L. Beynon,5
Jarrod Chapman,2,3,7Cynthia M. B. Damasceno,8Anne E. Dorrance,9Daolong Dou,1
Allan W. Dickerman,1Inna L. Dubchak,2,3Matteo Garbelotto,10Mark Gijzen,11
Stuart G. Gordon,9Francine Govers,4Niklaus J. Grunwald,12Wayne Huang,2,14
Kelly L. Ivors,10,15Richard W. Jones,16Sophien Kamoun,9Konstantinos Krampis,1
Kurt H. Lamour,17Mi-Kyung Lee,18W. Hayes McDonald,19Mo ´nica Medina,20
Harold J. G. Meijer,4Eric K. Nordberg,1Donald J. Maclean,21Manuel D. Ospina-Giraldo,22
Paul F. Morris,23Vipaporn Phuntumart,23Nicholas H. Putnam,2,3Sam Rash,2,13
Jocelyn K. C. Rose,24Yasuko Sakihama,25Asaf A. Salamov,2,3Alon Savidor,17
Chantel F. Scheuring,18Brian M. Smith,1Bruno W. S. Sobral,1Astrid Terry,2,13
Trudy A. Torto-Alalibo,1Joe Win,9Zhanyou Xu,18Hongbin Zhang,18Igor V. Grigoriev,2,3
Daniel S. Rokhsar,2,7Jeffrey L. Boore2,3,26,27
Draft genome sequences have been determined for the soybean pathogen Phytophthora sojae and
the sudden oak death pathogen Phytophthora ramorum. Oo ¨mycetes such as these Phytophthora
species share the kingdom Stramenopila with photosynthetic algae such as diatoms, and the
presence of many Phytophthora genes of probable phototroph origin supports a photosynthetic
ancestry for the stramenopiles. Comparison of the two species’ genomes reveals a rapid expansion
and diversification of many protein families associated with plant infection such as hydrolases, ABC
transporters, protein toxins, proteinase inhibitors, and, in particular, a superfamily of 700 proteins
with similarity to known oo ¨mycete avirulence genes.
of potato caused by Phytophthora infestans re-
sulted in the Irish potato famine in the 19th cen-
hytophthora plant pathogens attack a
wide range of agriculturally and orna-
mentally important plants (1). Late blight
tury, and P. sojae costs the soybean industry
millions of dollars each year. In California and
Oregon, a newly emerged Phytophthora species,
P. ramorum, is responsible for a disease called
sudden oak death (2) that affects not only the live
www.sciencemag.orgSCIENCEVOL 3131 SEPTEMBER 2006
oaks that are the keystone species of the eco-
system but also a large variety of woody shrubs
that inhabit the oak ecosystems, such as bay
laurel and viburnum (2). Many other members of
the oPmycete phylum are plant or animal patho-
gens, and some pose biosecurity threats such
as the maize downy mildews Peronosclerospora
philippinesis and Sclerophthora rayssiae. Ex-
tensive classical and molecular genetic tools and
genomics resources have been developed for
P. sojae and P. infestans (3, 4).
(5, 6), which also includes golden-brown algae,
diatoms, and brown algae such as kelp (Fig. 1A).
The algal stramenopiles are secondarily photo-
synthetic, having engulfed a red alga and
adopted its plastid approximately 1,300 million
years ago (6). However, nonphotosynthetic
stramenopiles, such as the oPmycetes, do not
even have the vestigial plastids found in api-
complexan and euglenoid parasites that origi-
nate from phototrophs. Therefore, an important
evolutionary question is whether the kingdom
Stramenopila was founded by a photosynthetic
or nonphotosynthetic organism and, more
generally, whether a much larger group of sec-
ondarily photosynthetic organisms, called the
chromalveolates (6), was founded by a single pho-
We report here the draft genome sequences
of P. sojae and P. ramorum. The sequences, a
nine-fold coverage of the 95 Mb P. sojae ge-
nome and a seven-fold coverage of the 65 Mb
P. ramorum genome, were produced using a
whole-genome shotgun approach (7). We con-
structed a physical map of P. sojae to aid the
sequence assembly by using restriction enzyme
fingerprinting of bacterial artificial chromosome
(BAC) clones from two libraries (7). We iden-
genomeofP. sojae and 15,743 in the genome of
P. ramorum, supported in part by expressed se-
quence tags (ESTs) from P. sojae and proteomic
surveys in P. ramorum (7). Of these, 9768 pairs
of gene models could be identified as putative
orthologs (7). There are 1755 gene models in
P. sojae and 624 in P. ramorum encoding unique
proteins that do not have a homolog in the other
genome at a significance threshold of 10–8. The
overall higher number of predicted genes in
P. sojae results from a greater size of many gene
families within the species.
There is extensive colinearity of orthologs
between the two genomes. One colinear block,
illustrated in Fig. 2, spans 1.8 Mb of P. sojae
sequence and 0.8 Mb of P. ramorum sequence
and contains 425 P. sojae and 265 P. ramorum
genes, respectively, of which 170 are orthologous
(7). The longest colinear block spans an estimated
4.8 Mb in P. sojae and 2.9 Mb in P. ramorum
and contains 1129 P. sojae and 793 P. ramorum
gene models, respectively, of which 463 are
orthologous. The long-range colinearity be-
tween the two genomes is preserved despite
the presence of many local rearrangements and
many nonorthologous genes. Local disruptions
of the gene colinearity are particularly com-
mon in the vicinity of genes associated with
plant infection such as P. sojae Avr1b-1 (8)
The genome sequences of P. sojae and P.
ramorum imply several metabolic idiosyncra-
sies. For example, the CYP51 group of cyto-
chrome P450 enzymes are considered necessary
for sterol biosynthesis (9). Consistent with Phy-
tophthora being sterol auxotrophs, none of these
genes could be identified in either Phytophthora
genome, although most other sterol biosynthetic
genes could be recognized. More unexpectedly,
neither genome appears to contain any gene for
phospholipase C (PLC), an enzyme present in
all eukaryotes sequenced so far (10), nor are
PLC sequences present in a collection of 75,757
ESTs from Phytophthora infestans (11). In con-
trast, the diatom Thalassiosira pseudonana has
three PLC genes. No other highly conserved
genes were identified as missing from both the
P. sojae and P. ramorum genomes.
Because P. ramorum has recently appeared
in California and Europe, an important priority
is the development of genetic markers for pop-
ulation genetics and strain tracking of the
pathogen. Through sequencing the P. ramorum
genome, we identified È13,643 single nucleo-
tide polymorphisms (SNPs) (7) and numerous
simple sequence repeats useful for this purpose.
The P. sojae genome sequence contains only
499 SNPs, probably because P. sojae is homo-
thallic (inbreeding), whereas P. ramorum is
To address whether the kingdom Stramenopila
might have been founded by a photosynthetic
ancestor (6), we searched for Phytophthora
genes that had especially strong similarities to
genes of photosynthetic organisms (7). We iden-
tified 855 genes with a putative heritage from a
red alga or cyanobacterium (fig. S2), of which
30 are detailed in table S4. Some of the most
striking examples of the putative acquisition of
genes from a photosynthetic ancestor are pro-
vided by genes encoding biosynthetic enzymes
targeted to the chloroplasts of photosynthetic
organisms and to the mitochondria of nonphoto-
synthetic organisms. Table S4 includes 12 genes
whose protein product has a predicted mitochon-
drial location in Phytophthora and a predicted
plastid location in plants and/or algae. One ex-
ample, the gene for 2-isopropylmalate synthase
(functioning in leucine biosynthesis), is shown in
Fig. 1B. Although a few details of this tree appear
to be anomalous, owing perhaps to the ancient
separation of these lineages and sparse taxon
sampling, there are clearly two major phyloge-
netic groups of this gene: one acquired in fungi
by transfer from an a-proteobacterium, presum-
ably the endosymbiont that gave rise to mitochon-
dria, and the other acquired in algae, plants, and
stramenopiles from a cyanobacterium, presum-
ably the endosymbiont that originally gave rise
to plastids. It is further interesting that this gene
in the diatom Thalassiosira pseudonana groups
with those of green plants rather than red algae,
perhaps indicating a separate ancestry, as has
been suggested for some other chromalveolates
(12, 13), although this could alternatively be an
artifact due to incomplete sampling of lineages
or of the genes within them. Figure 1C shows a
more unusual example, from the sixth step of
purine biosynthesis. The two Phytophthora spe-
cies, together with the diatom Thalassiosira
pseudonana and the green alga Chlamydomonas
reinhardtii, are unique among eukaryotes be-
cause they have a prokaryotic, organelle-targeted
(NCAIR) mutase homolog closely resembling
that of cyanobacteria (14), in addition to a
conventional eukaryotic, cytoplasmic-targeted
carboxylase (Fig. 1C). The presence of numer-
ous genes of putative phototroph origin in the
Phytophthora genomes lends support to the hy-
pothesis that the stramenopile ancestor was
photosynthetic, which is consistent with the
Genes involved in the interactions of P. sojae
and P. ramorum with their hosts are of central
interest. Motile Phytophthora zoospores exhibit
1Virginia Bioinformatics Institute, Virginia Polytechnic Insti-
tute and State University, Blacksburg, VA 24061, USA.
2Department of Energy Joint Genome Institute, Walnut
Creek, CA 94598, USA.3Genomics Division, Ernest Orlando
Lawrence Berkeley National Laboratory, Berkeley, CA 94720,
USA.4Laboratory of Phytopathology, Wageningen University,
NL-6709 PD Wageningen, Netherlands.
search International,Wellesbourne,Warwick CV35 9EF, United
Kingdom.6Department of Biological Sciences, Imperial Col-
lege, London SL5 7PY, United Kingdom.7Center for Integra-
tive Genomics, University of California, Berkeley, CA 94720,
Ithaca, NY 14853, USA.9Department of Plant Pathology, Ohio
Agricultural Research and Development Center,The Ohio State
University, Wooster, OH 44691, USA.10Department of Envi-
ronmental Science, Policy, and Management, Ecosystem Sci-
ences Division, University of California, Berkeley, CA 94720,
USA.11Agriculture and Agri-Food Canada, London, ON, Canada,
Agricultural Research Service, Corvallis, OR 97330, USA.
13Biosciences Directorate,14Computation Directorate, Lawrence
Livermore National Laboratory, Livermore, CA 94550, USA.
15North Carolina State University Mountain Horticultural Crops
Research and Extension Center, Fletcher, NC 28732, USA.
16Vegetable Laboratory, Henry Wallace Beltsville Agriculture
Research Center, USDA Agricultural Research Service, Beltsville,
MD 20705, USA.
Pathology, University of Tennessee, Knoxville, TN 37996, USA.
18Department of Soil and Crop Sciences,Texas A&M University,
College Station, TX 77843, USA.19Chemical Sciences Division,
Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA.
20School of Natural Sciences, University of California, Merced,
CA 95344, USA.21Department of Biochemistry & Molecular
Biology, University of Queensland, St. Lucia, Queensland
4072, Australia.22Department of Biology, Wilkes University,
Wilkes-Barre, PA 18766, USA.
Sciences, Bowling Green State University, Bowling Green, OH
43402, USA.24Department of Plant Biology, Cornell University,
Ithaca, NY 14853, USA.25Laboratory of Ecological Chemistry,
Hokkaido University, Sapporo 060-8589, Japan.26Department
of Integrative Biology, University of California, Berkeley, CA
94720, USA.27Genome Project Solutions, Hercules, CA 94547,
8Department of Plant Pathology, Cornell University,
12Horticultural Crops Research Laboratory, USDA
17Department of Entomology and Plant
23Department of Biological
*To whom correspondence should be addressed. E-mail:
1 SEPTEMBER 2006 VOL 313SCIENCEwww.sciencemag.org
chemotaxis toward signals from host tissue such
as isoflavones (15). In other eukaryotes, chemo-
taxis reception is mediated by G protein–coupled
receptors (GPCRs) (16). P. sojae and P. ramorum
each have 24 GPCRs, four of which show a
top match to the Dictyostelium cyclic adeno-
sine monophosphate chemotaxis receptor. An-
other 12 GPCRs have a C-terminal intracellular
phosphatidylinositol-4-phosphate 5-kinase do-
main similar to the RpkA gene of Dictyostelium
(17); this domain would enable signaling to
bypass the heterotrimeric G proteins, perhaps
explaining why the Phytophthora genomes con-
tain only single genes for G-a and G-b sub-
Fig. 1. Identification of genes potentially origi-
nating from a photosynthetic endosymbiont. (A)
Schematic phylogenetic tree of the eukaryotes.The
tree is adapted from that of Baldauf et al. (5) that
is based on a concatenation of six highly conserved
proteins. Filled green circles on the right indicate
photosynthetic species, open green circles indicate
species with vestigial plastids of photosynthetic origin.
The dotted arrows indicate hypothetical events in
which an ancient red algal endosymbiont might have
been acquired by an ancestor of the chromalveolates
(left arrow) or of the stramenopiles alone (right
arrow).(B and C) Phylogenetic trees produced using
maximum parsimony (with the branch and bound
algorithm) of amino acid sequences with the
computer program PAUP 4.0b10 (32). Inferred
amino acid sequences were aligned using ClustalW,
and these were manually trimmed at each end to
a position of confident alignment. (B) and (C)
show strict consensus trees for two and three
equally parsimonious trees, respectively. In both
cases, numerals indicate bootstrap support values,
and any with less than 80% have been collapsed.
Branch lengths are proportional to sequence
change using the accelerated transformation
mode for character state reconstruction. Trees
were rooted by specifying Methanocaldococcus
jannaschii and the NCAIR mutase/cpmA cluster of
genes as outgroups for (B) and (C), respectively.
Taxonomic affinities of the organisms listed are as
in (A), with the following additions: green plants,
Helicosporidium sp.; cyanobacteria, Nostoc sp.,
Trichodesmium erythraeum, and Synechocystis sp.;
other eubacteria, Pseudomonas aeruginosa, Bacillus
halodurans, and Clostridium acetylbutylicum; archae-
bacteria, Thermoplasma volcanium, M. jannaschii,
and Methanopyrus kandleri. In (C), NCAIRm, AIRc,
and cpmA denote, respectively, N-phosphoribosyl-
carboxy-aminoimidazole (NCAIR) mutase,
carboxylase, and the circadian modifer gene cpmA
that is a memberof the NCAIR mutase family (14).
www.sciencemag.orgSCIENCEVOL 3131 SEPTEMBER 2006
Because P. sojae and P. ramorum have very
different host ranges, it is expected that some
of their genes involved in host interactions
will have rapidly diverged between the two
species as a result of strong selection for
effective pathogenesis. Because Phytophthora
species are cellular pathogens, secreted proteins
are prime candidates for mediators of host
interactions (18). The predicted secretomes (7)
of the two species (1464 and 1188 proteins,
respectively) are evolving significantly more
rapidly than the overall proteome. For example,
17% and 11% of the secreted P. sojae and P.
ramorum proteins, respectively, are unique at
the 30% identify level, whereas only 9% and
4%, respectively, of the overall proteomes are
unique. The relatively rapid diversification of the
secretomes is also evident in the number of
multigene families encoding these proteins: 77%
of the proteins belong to families of two or more
members, and 30% belong to families of 10 or
Both P. sojae and P. ramorum derive their
nutrition biotrophically from living plant tissue
during the initial hours of infection, but they
switch to necrotrophic growth once the infec-
tion has been established, deriving their nutri-
tion from killed plant tissue. As hemibiotrophs,
the two species are expected to produce gene
products that enable them to evade or suppress
the plant_s defense responses during early bio-
trophic infection and to produce gene products
that kill and destroy plant tissue during later
necrotrophic growth. Table 1 summarizes a wide
variety of hydrolytic enzymes encoded by the
genomes of the two species in comparison
with the genome of the diatom Thalassiosira
pseudonana, an autotroph. These destructive en-
zymes potentially could be associated with the
necrotrophic phase. The two Phytophthora ge-
nomes encode large numbers of secreted prote-
ases in contrast to the diatom and also encode
the pectinases and cutinases required for hydro-
lyzing plant cell wall and cuticular material.
The number of proteinase inhibitor genes re-
quired to protect the pathogens from plant pro-
teases is also expanded in the Phytophthora
Gene families encoding proteins previously
demonstrated to be toxic to plants show striking
diversification; fewer than 25% of the genes
remain identifiably orthologous between the two
Fig. 2. Long-range gene colinearity
betweenthegenomesofP. sojae and P.
ramorum. In (A) and (B), black and red
lines link orthologs of like and reversed
orientation, respectively. In (A), colored
bars indicate orthologs located in
different P. sojae sequence scaffolds.
Gray bars indicate genes without
orthologs. Filled red circles indicate
scaffolds linked by a single end-
sequenced BAC, and open red circles
indicate scaffolds linked by end-
sequenced BAC contigs. The boxed
area in (A) is enlarged in (B).
Fig. 3. Sequence diver-
gence of two potential
families of pathogenici-
ty genes. (A) NPP1 or
Nep1-like (NLP) protein
sequences. A total of 89
sequences were used to
construct this phylogram,
including 40 P. ramorum
and 29 P. sojae se-
quences. The remaining
sequences were retrieved
from GenBank.Protein se-
quences were edited to
remove signal peptides
and other domains and
were aligned using Clus-
talW, and the unrooted
phylogram was made us-
ing the neighbor-joining
method (MEGA 3.1). The
scale bar represents 10%
weighted sequence diver-
gence. Species of origin
are abbreviated as fol-
lows: An, Aspergillus
nidulans; Bh, Bacillus
halodurans; Ec, Erwinia
caratovora; Fo, Fusarium
oxysporum; Gz, Giberella
zeae; Mg, Magnaporthe
grisea; Nc, Neurospora
crassa; Pa, Pythium
Pm, Pythium monosper-
mum; Pp, Phytophthora parasitica; Ps, Phytophthora sojae; Pr, Phytophthora ramorum; Sc, Streptomyces
coelicolor; Vd,Verticillium dahlia; Vp,Vibrio pommerensis. (B) Similarity of P. sojae Avh genes to P. ramorum.
Purple indicates Avh genes, and crimson indicates a set of randomly chosen P. sojae genes having a functional
annotation. The red arrow indicates the class that contains the Avr1b-1 gene itself.
1 SEPTEMBER 2006 VOL 313SCIENCE www.sciencemag.org
species, and in several cases there are no iden-
tifiable orthologs (Table 1). There are also sub-
stantial differences in sizes of the gene families.
The NPP1 family (19, 20) is more expanded and
diversified in P. ramorum, whereas the PcF
(18, 21) and crn (22) toxin families are more
expanded in P. sojae. Figure 3A illustrates the
explosive diversification of the NPP1 toxin fam-
ily in the genus Phytophthora. This toxin fam-
ily is interesting because several fungal plant
pathogens also contain NPP1 toxin genes (19, 20),
but they contain only two to four genes, where-
as the Phytophthora species contain 29 or 40
The largest and most diverse family of
infection-associated genes identified in the
P. sojae and P. ramorum genomes is a super-
family with È350 genes in each genome (7) that
are similar to four oPmycete genes identified as
Bavirulence[ or Beffector[ genes, namely Avr1b-1
of P. sojae (8), Avr3a of P. infestans (23), and
Atr1 (24) and Atr13 (25) of Hyaloperonospora
parasitica. We have termed these Avh (aviru-
lence homolog) genes. Avirulence genes were
historically identified by their genetic interac-
tion with plant disease resistance genes that
encode defense receptors (26). In bacterial plant
pathogens, some avirulence proteins function to
promote infection by suppressing the plant de-
fense response—hence their renaming as
Beffector[ proteins (26). Many of these bacte-
rial effector proteins are injected into host cells
by the type III secretion machinery (26), which
explains the intracellular location of many
resistance gene–encoded plant defense recep-
tors. Intriguingly, the plant defense receptors
that interact with the four cloned oPmycete
avirulence proteins also have a predicted in-
tracellular location (8, 23–25, 27). However,
the mechanisms by which the oPmycete proteins
may enter the plant cell are unknown. The four
oPmycete avirulence proteins share only very
modest sequence similarity, but they do share
two motifs, named RXLR and dEER, near the N
terminus (24, 28) which are also shared by all of
the 700 Avh gene products. Comparison of the
700 Avh sequences reveals a nonrandom distri-
bution of amino acid residues surrounding each
motif (7), which could potentially contribute to
the their functions. Similarity of the RXLR motif
to a motif used by the malaria parasite to
transport proteins across the membrane of the
parasitiphorous vacuole into the cytoplasm of
human erythrocytes (29, 30) suggests that the
RXLR motif may function to transport oPmycete
effector proteins into the plant cytoplasm. Figure
3B shows that the Avh gene family has under-
gone extensive diversification in comparison with
a random set of P. sojae and P. ramorum genes.
The diversification of the Avh family, driven
presumably by selection pressure from the host
defense machinery, underlines the potential
importance of this superfamily for infection by
these pathogens. Further characterization of these
genomes will be published elsewhere (31).
References and Notes
1. D. C. Erwin, O. K. Ribiero, Phytophthora Diseases
Worldwide (APS Press, St. Paul, MN, 1996).
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Phytopathol. 43, 309 (2005).
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Proc. Natl. Acad. Sci. U.S.A. 99, 15507 (2002).
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material on Science Online.
8. W. Shan, M. Cao, D. Leung, B. M. Tyler, Mol. Plant
Microbe Interact. 17, 394 (2004).
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11. T. A. Randall et al., Mol. Plant Microbe Interact. 18, 229
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Mol. Biol. Evol. 23, 663 (2006).
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F. Govers, Trends Microbiol., in press, doi: 10.1016/
18. S. Kamoun, Annu. Rev. Phytopathol. 44, 41 (2006).
Table 1. Potential infection-related genes in the P. sojae and P. ramorum genome sequences.
Numbers of genes
P. sojaeP. ramorum Orthologs* Diatom
Protease inhibitors, all
Six Cys family
Eight Cys family
Secondary metabolite biosynthesis
Nonribosomal peptide synthetases
Avh (RXLR) family
0 35083 (21)††
*Genes orthologous between P. sojae and P. ramorum were estimated based on bidirectional best BLAST hits and/or
using similarity trees created by ClustalW.
†n.d., not determined
¬Crinkling and necrosis-inducing protein family (22).
#Multi-drug resistance transporters. **Multi-drug resistance–associated transporters.
the estimations of orthology are uncertain due to the rapid divergence of this family. The number in parentheses refers to orthologs
that are syntenic and hence most likely to be correct.
‡Necrosis and ethylene-inducing protein family
¶Pleiotropic drug resistance trans-
††For the Avh family,
www.sciencemag.org SCIENCEVOL 3131 SEPTEMBER 2006
19. G. Fellbrich et al., Plant J. 32, 375 (2002). Download full-text
20. D. Qutob, S. Kamoun, M. Gijzen, Plant J. 32, 361 (2002).
21. G. Orsomando et al., J. Biol. Chem. 276, 21578
22. T. A. Torto et al., Genome Res. 13, 1675 (2003).
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24. A. P. Rehmany et al., Plant Cell 17, 1839 (2005).
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Opin. Microbiol. 7, 11 (2004).
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Mol. Plant Microbe Interact. 18, 1035 (2005).
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J. L. Beynon, Trends Microbiol. 14, 8 (2006).
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Science 306, 1930 (2004).
30. N. L. Hiller et al., Science 306, 1934 (2004).
31. A series of papers describing detailed analyses of the
P. sojae and P. ramorum genome sequences will be
published in a special issue of Molecular Plant-Microbe
Interactions in December 2006.
32. D. Swofford, PAUP*: Phylogenetic Analysis Using Parsi-
mony* (and other methods), 4.0b7 beta version (Sinauer
Associates Sunderland, MA, 2002).
33. We thank M. Arnaud, G. Cai, S. Constanzo, M. DiLeo,
S. Doyle, C. Paeper, L. Waller, and L. Zhou for their
contributions to the annotation of the P. sojae and
P. ramorum sequences; C. Volker and M. Chibucos for
manuscript preparation; and J. Mullins for preparation of
illustrations. This work was supported by grants to B.M.T.
from the National Research Initiative of the USDA
Cooperative State Research, Education, and Extension
Service, grant numbers 00-52100-9684, 2001-35319-
14251, and 2002-35600-12747; from the U.S. National
Science Foundation, grant numbers MCB-0242131 and
EF-0130263; and by funds from the U.S. Department of
Energy Joint Genome Institute and the Virginia Bio-
informatics Institute. Much of this work was performed
under the auspices of the U.S. Department of Energy’s
Office of Science, Biological, and Environmental Research
Program and by University of California, Lawrence
Livermore National Laboratory under contract no.
W-7405-Eng-48; Lawrence Berkeley National Laboratory
under contract no. DE-AC02-05CH11231; and Los Alamos
National Laboratory under contract no. W-7405-ENG-36.
R.H.Y.J. was supported by Aspasia grant no. 015.000.057
from the Netherlands Science Foundation and fellowship
NGI 050-72-404 from Netherlands Genomics Initiative.
The P. sojae and P. ramorum whole-genome shotgun
projects have been deposited at DDBJ/EMBL/GenBank
under the project accessions AAQY00000000 and
AAQX00000000, respectively. The versions described in
this paper are the first versions, AAQY01000000 and
Supporting Online Material
Materials and Methods
Figs. S1 to S3
Tables S1 to S5
17 April 2006; accepted 18 July 2006
Anomalous Spiral Motion of Steps
Near Dislocations on Silicon Surfaces
J. B. Hannon,1* V. B. Shenoy,2K. W. Schwarz1
We have used low-energy electron microscopy to measure step motion on Si(111) and Si(001) near
dislocations during growth and sublimation. Steps on Si(111) exhibit the classic rotating Archimedean
different manner.The anomalous behavior can be understood in detail by considering how the local step
velocity is affected by the nonuniform strain field arising from the dislocation.We show how the dynamic
step-flow pattern is related to the dislocation slip system.
detail for more than 50 years. Although most
investigations have focused on bulk proper-
ties, dislocations also influence surface pro-
cesses. Perhaps the most striking example is
the realization by Frank (1) that dislocations
mediate crystal growth underconditions of low
supersaturation and provide the surface steps
required to capture deposited atoms. On a low-
spontaneously nucleate before such growth can
More recently, there has been interest in
exploiting the strain field of bulk dislocations
to tailor surface properties. For example, pe-
riodic arrays of dislocations have been used to
film. The strain pattern can be used to pref-
islocations strongly influence both the
mechanical and electrical properties of
solids, and have been investigated in
erentially nucleate Ge quantum dots at specific
locations on a surface (2, 3). Here, we describe
how the dislocation strain fields influence step
motion during growth. By imaging the Si(001)
surface in real-time at 1100-C, during growth
and sublimation, we show that step motion
near the dislocation core is inconsistent with
classic models that predict rotating spiral step
profiles (4). We find instead that the step ve-
locity can be interpreted directly in terms of
the surface strain field generated by a bulk
Images of a step on Si(111) emerging from
a screw dislocation (Fig. 1A) were obtained
using low-energy electron microscopy (LEEM)
(5) during sublimation at elevated temperatures
(T , 1100-C). Si atoms evaporated from the
terrace are replenished by atoms detaching
from steps, causing the steps to retract. Burton,
Cabrera, and Frank (BCF) (4) developed a
simple theory of step motion near a dislocation
1IBM Research Division, T. J. Watson Research Center,
Yorktown Heights, NY 10598, USA.2Division of Engineer-
ing, Brown University, Providence, RI 02912, USA.
*To whom correspondence should be addressed. E-mail:
Fig. 1. (A to C) Step motion near a
dislocation core on Si(111) during
sublimation. (A) 40 eV LEEM image
of a step emerging from a disloca-
tion core measured at time t1. The
step curvature decreases monotoni-
cally away from the core (indicated
by an arrow). (B) Position of the step
at 5-s intervals as it winds (counter-
clockwise) about the core during
sublimation.The curve corresponding
to (A) is shown in bold. (C) Measured
step profiles, each rotated by an
angle (t j t1)/t0, where t00 36 s is
the period of the step motion and t
is the time the profile was measured.
The solid curve shows the prediction
of the BCF model with rc0 93 nm.
(D) Spiral onset from growth and
sublimation of a surface step emerg-
ing from a dislocation. The step separates two surface phases: A on the lower side of the step and B on the
upper side. If the step direction is reversed, so is the direction of motion.
1 SEPTEMBER 2006 VOL 313SCIENCE www.sciencemag.org