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Appl Environ Microbiol, July 1998, p. 2341-2345, Vol. 64, No. 7
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Root Colonization by Agrobacterium
tumefaciens Is Reduced in cel, attB,
attD, and attR Mutants
Ann G.
Matthysse* and
Susan
McMahan
Department of Biology, University of North
Carolina, Chapel Hill, North Carolina 27599-3280
Received 26 June 1997/Accepted 11 April 1998
 |
ABSTRACT |
Root colonization by Agrobacterium tumefaciens was
measured by using tomato and Arabidopsis thaliana roots
dipped in a bacterial suspension and planted in soil. Wild-type
bacteria showed extensive growth on tomato roots; the number of
bacteria increased from 103 bacteria/cm of root length at
the time of inoculation to more than 107 bacteria/cm after
10 days. The numbers of cellulose-minus and nonattaching
attB, attD, and attR mutant
bacteria were less than 1/10,000th the number of wild-type bacteria
recovered from tomato roots. On roots of A. thaliana
ecotype Landsberg erecta, the numbers of wild-type bacteria
increased from about 30 to 8,000 bacteria/cm of root length after 8 days. The numbers of cellulose-minus and nonattaching mutant bacteria
were 1/100th to 1/10th the number of wild-type bacteria recovered after
8 days. The attachment of A. tumefaciens to cut A. thaliana roots incubated in 0.4% sucrose and observed with a
light microscope was also reduced with cel and
att mutants. These results suggest that cellulose synthesis and attachment genes play a role in the ability of the bacteria to
colonize roots, as well as in bacterial pathogenesis.
| |
INTRODUCTION |
Infections of wound sites on
dicotyledonous plants by the soil bacterium Agrobacterium
tumefaciens result in the formation of crown gall tumors. An early
step in tumor formation is the attachment of the bacteria to the plant
cell surface. This attachment is required for bacterial virulence. All
nonattaching mutants currently described are reduced in virulence
(6, 17, 30).
In previous studies of the surface interactions between bacteria and
plant cells leading to tumor formation, we identified two regions of
the bacterial chromosome containing genes involved in tight binding of
the bacteria to host cells (17, 20). The bacterium binds to
host cells in a two-step process (19). The first step
results in loose binding to the plant cell surface. At this stage the
bacteria can be removed by shear forces, such as water washing or
vortexing of tissue culture cells. Mutants in this step are avirulent.
A series of genes required for this step have been located on the
bacterial chromosome and are referred to as att genes
(17). The genes attA1 to attH encode
proteins with homology to ABC transporter systems in several bacteria, including the pot genes of Escherichia coli
(21). These genes appear to be required for signaling
between the bacteria and the plant host (18). Other
att genes (including attR) appear to be required
for the synthesis of surface molecules which may play a role in the
actual attachment of the bacteria to the plant cell surface
(25).
The second step in bacterial attachment is the synthesis of cellulose
fibrils by the bacteria. This step results in tight binding of the
bacteria; they can no longer be removed from the plant cells by shear
forces (16). The genes required for bacterial cellulose
synthesis (cel genes) are located on the bacterial
chromosome near, but not contiguous with, the att genes
(26). Cellulose-minus bacterial mutants show reduced
virulence (between 10 and 1,000 times more bacteria are required to
induce a tumor [22]).
The study described here was undertaken to explore the possible role of
these genes in the interaction of the bacteria with intact roots.
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MATERIALS AND METHODS |
Bacterial strains and growth.
Wild-type virulent A. tumefaciens C58 and mutants derived from it were grown in Luria
broth at 25°C. The cellulose-minus mutants C58::1 and
C58::A60 have been described previously (20), as have the attachment-minus mutants C58::N004,
C58::B123, and C58::A205 (21). The
locations of the transposon insertions in these mutants are shown in
Fig. 1. Spontaneous rifampin-resistant
mutants of each of these strains were selected and used for root
colonization experiments. The growth characteristics of the parent and
mutant strains in liquid media (Luria broth or minimal medium) were not significantly different.
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FIG. 1.
Positions of transposon insertions in mutants used in
this study. The cel and att regions of the
bacterial chromosome are shown. Both of these regions have been
sequenced (20, 21). An enlargement of the left end of the
att region is shown below the diagram of the larger clone.
Triangles indicate the sites of transposon insertion in mutants used in
this study. The small arrows with the triangles indicate the
orientation of the promoterless  -galactosidase gene contained in
Tn3HoHo1. The locations and directions of open reading
frames (ORFs) are indicated by the larger arrows. The genes which have
the highest homology to the open reading frames are indicated below the
arrows (20, 21). Restriction sites are indicated as follows:
E, EcoRI; C, ClaI; P, PstI; B,
BamHI; X, XbaI; H, HindIII; S,
SacI.
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Growth and inoculation of plants.
Seeds of tomato
(Lycopersicon esculentum cv. Marglobe) were surface
sterilized in 0.16% sodium hypochlorite and germinated on 1% water
agar in petri dishes. Seeds of Arabidopsis thaliana ecotype
Landsberg erecta were surface sterilized in 1.6% sodium hypochlorite, stored at 4°C for 3 days, and planted in petri dishes containing MS salts, Gamborg's B5 vitamin mixture, and 2% sucrose in
0.8% Phytagar (all obtained from GIBCO Laboratories, Grand Island,
N.Y.).
When the tomato roots were 1 to 2 cm long and the
A. thaliana roots were 0.25 to 0.5 cm long, the roots were dipped for
1
min into a suspension containing 10
5 bacteria per ml of
0.1 M sodium phosphate buffer (pH 7.0)-0.1%
peptone (washing buffer
[
14]). The intact plants were then placed
in soil in
Conetainers (Stuewe and Sons, Inc., Corvallis, Oreg.)
(tomato) or in
1.5-ml Eppendorf tubes which had a hole pierced
in the tip (
A. thaliana). The soil was a Gilead loamy sand which
had been
pasteurized by heating it in a microwave oven in sealed
bags and stored
for more than 4 weeks before use according to
the procedure of Ferriss
(
7,
13). The bottom of each container
was sealed with
Parafilm, and the plant and the top of the container
were covered with
Parafilm. The plants were grown without additional
water at 22 to
24°C with 14 h of light per day for up to 10 days,
at which time
they were too large to remain covered in their containers.
After 10 days the tomato roots were between 8 and 13 cm long.
The
A. thaliana roots were between 2 and 3 cm long when they were
harvested after 8 days.
Sampling of roots.
At different times after inoculation the
plants and soil were removed from the containers, the soil was
carefully separated from the roots, and the roots were gently shaken.
Each whole plant was placed in 5 ml (tomato) or 2 ml (A. thaliana) of washing buffer in a vial. The vial was sealed and
inverted 10 times. The washing buffer was removed, and the procedure
was repeated. The number of viable bacteria per milliliter of washing
buffer was determined by viable cell counts using Luria agar containing
50 µg of rifampin per ml. The viable cell counts in the first two
washes were combined to give the number of bacteria loosely bound to
the roots. Each plant was then placed in 5 or 2 ml of washing buffer
and sonicated with a Branson ultrasonic cleaner (model B220) for
60 s (tomato) or 30 s (A. thaliana). The viable
cell counts for the bacteria released into the washing buffer were
determined, and the resulting data are reported below as the number of
tightly bound bacteria. The plants were then removed from the buffer,
placed on Luria agar plates containing rifampin, and covered with soft
(0.7%) agar. The root lengths were measured. The plates were incubated until colonies were apparent. The number of colonies per centimeter of
root length was determined with a dissecting microscope, and the
resulting data are reported below as the number of irreversibly bound
bacteria. The results are expressed as CFU per centimeter of root
length rather than CFU per gram of root weight since the drying
necessary to obtain reproducible root weights interfered with the
recovery of viable bacteria which were bound to the roots. The number
of CFU per centimeter of root length was calculated and was transformed
to a log10 CFU/centimeter value (14) before the
means and standard deviations were calculated. Experiments were
repeated four times with a minimum of four plants per time interval.
Microscopic observation of bacterial attachment to cut A. thaliana roots.
Microscopic observation of bacterial
attachment to cut roots of A. thaliana was carried out as
described previously (23). Briefly, cut roots floating in 2 ml of 0.4% sucrose-1 mM CaCl2 were inoculated with
approximately 108 bacteria. The roots were incubated at
room temperature, and bacterial attachment was scored after 24, 48, and
72 h with a microscope (Zeiss photoscope 2) equipped with Nomarski
optics.
| |
RESULTS |
Bacterial binding to cut A. thaliana roots.
Wild-type strain C58 bacteria bound to cut roots of A. thaliana within 24 h. Large numbers of bacteria were visibly
bound to the epidermis, root hairs, and cut end of each root segment (Fig. 2). These surfaces appeared to be
uniformly covered with bacteria; no preferential sites of attachment
were observed. Fewer bacteria were seen on the root cap, although
numerous bacteria were observed attached to the border cells behind the
root cap. Bacterial aggregates were observed on the root hairs and
epidermis (data not shown). Very few cellulose-minus mutant bacteria
were observed at any location on the surfaces of roots after 24 h
of incubation. No bacterial aggregates were seen. Similarly, very few
attB, attD, or attR mutant bacteria
were seen at any location on the root surface. These results suggest
that the cel, attB, attD, and
attR genes may be involved in bacterial attachment to intact
surfaces of roots, as well as to cut plant surfaces and to tissue
culture cells.
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FIG. 2.
Attachment of bacteria to A. thaliana root
hairs. Wild-type and mutant A. tumefaciens strains were
incubated with roots of A. thaliana in 0.4% sucrose for 2 days. (A) Wild-type strain C58. Note the numerous bacteria attached to
the root hairs. (B) Cellulose-minus strain C58::1. (C)
Attachment-minus mutant C58::A205. The attachment of the
cel and att mutants was much reduced compared
with the attachment of the wild type. Similar results were observed for
bacteria attached to the root epidermis. Bar = 5 µm.
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Bacterial colonization of tomato roots.
Wild-type strain C58
bacteria were able to colonize the roots of tomato plants grown in
soil. After an initial lag during the first 2 days following
inoculation, there was an increase in the number of bacteria recovered
in all three categories (loosely bound, tightly bound, and irreversibly
bound). After 9 days there had been a 10,000-fold increase in the
number of loosely and tightly bound bacteria per centimeter of root
length and a 1,000-fold increase in the number of irreversibly bound
bacteria (Table 1). After roots were
placed in petri dishes and covered with soft agar, bacterial colonies
were uniformly distributed throughout the length of the root, except
that few colonies were observed at the root tip.
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TABLE 1.
Numbers of wild-type strain C58 bacteria associated with
tomato roots after incubation in soil for up to 10 days
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|
When
cel and
att mutant bacteria were inoculated
onto roots, they failed to show much growth compared to the wild-type
parent
(Fig.
3). The numbers of loosely
bound cellulose-minus mutant
cells, as well as the numbers of tightly
and irreversibly bound
cellulose-minus mutant cells were reduced
compared with the wild
type (Table
2,
C58::1 data; similar data were obtained for
C58::A60).
All three nonattaching mutants examined showed
reduced attachment
to tomato roots (Fig.
3B). Again, decreases were
observed in all
three categories of attachment, loosely bound, tightly
bound,
and irreversibly bound (data not shown). Thus, wild-type
A. tumefaciens is capable of colonizing tomato roots, and
colonization was reduced
in
cel and
att mutants.
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FIG. 3.
Numbers of bacteria recovered from tomato roots. (A)
Log10 total number of bacteria per centimeter of root
length recovered from tomato roots inoculated with wild-type strain C58
( ) and cellulose-minus mutants C58::1 ( ) and
C58::A60 ( ). (B) Log10 total number of
bacteria per centimeter of root length recovered from tomato roots
inoculated with wild-type strain C58 () and attachment-minus mutants
C58::A205 (), C58::N004 (), and
C58::B123 (×). Note that cellulose-minus and
attachment-minus bacteria had reduced abilities to colonize roots.
These reductions were due to reductions in loosely bound, tightly
bound, and irreversibly bound bacteria. The numbers shown are the means
from a minimum of four separate experiments. The standard deviation of
all points was less than 0.9.
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TABLE 2.
Numbers of cellulose-minus C58::1 bacteria
associated with tomato roots after incubation in soil for up to
10 days
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|
Bacterial colonization of A. thaliana roots.
The
colonization of A. thaliana roots by wild-type bacteria,
expressed as the number of bacteria per centimeter of root length, was
less than the colonization of tomato roots. This may reflect the
smaller diameter of the A. thaliana roots. The numbers of bacteria per centimeter of root length increased about 100-fold for
loosely bound, tightly bound, and irreversibly bound bacteria (Fig.
4). In contrast to the data obtained for
tomato roots, all of the mutants except C58::N004 showed some
initial growth on A. thaliana roots. However, after 8 days
the growth of the mutants lagged behind the growth of the wild-type
strain. Colonization of cellulose-minus and attachment-minus mutants
was reduced for all three binding categories (loosely, tightly, and
irreversibly bound) (data not shown). Thus, colonization of A. thaliana roots by A. tumefaciens was reduced in
att and cel mutants compared with the wild type.
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FIG. 4.
Numbers of bacteria recovered from A. thaliana roots. (A) Log10 total number of bacteria per
centimeter of root length recovered from A. thaliana roots
inoculated with wild-type strain C58 () and cellulose-minus mutants
C58::1 () and C58::A60 (). (B)
Log10 total number of bacteria per centimeter of root
length recovered from A. thaliana roots inoculated with
wild-type strain C58 () and attachment-minus mutants
C58::A205 () and C58::N004 (). Note that
cellulose-minus and attachment-minus bacteria had reduced abilities to
colonize the roots after the first day. The reductions in the total
numbers of bacteria were due to reductions in loosely bound, tightly
bound, and irreversibly bound bacteria. The numbers shown are the means
from a minimum of four separate experiments. The standard deviation of
all points was less than 0.5.
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| |
DISCUSSION |
Wild-type A. tumefaciens C58 colonized tomato roots in
numbers comparable to the numbers observed for colonization of tomato roots by the biocontrol strains Agrobacterium rhizogenes K84
and J73 (15), for colonization of pea roots by A. tumefaciens A723 (8), and for colonization of many root
systems by pseudomonads (3, 4, 11, 29). All regions of the
root except the root tip were found to be colonized. Under the
microscope bacteria were observed adhering to all regions of the root,
including the border cells of the root cap. Adherence of agrobacteria
to root cap cells has been described previously by Hawes and Pueppke
(9). In the present colonization studies root cap cells were
removed from the root by the washing steps, and the bacteria adhering to them were included in the data for the loosely bound bacteria.
Both tomato and A. thaliana are susceptible to crown gall
tumor formation by A. tumefaciens. However, the bacterial
colonization of A. thaliana roots was less than the
bacterial colonization of tomato roots when data were expressed as
number of bacteria per centimeter of root length. A. thaliana roots are much smaller than tomato roots and weigh
between 40 and 100 times less per centimeter of root length than tomato
roots. If this weight ratio is used to correct the numbers of bacteria
found on A. thaliana roots, then the levels of bacterial
colonization were roughly comparable for the two plants.
Mutations in genes involved in the synthesis of surface polysaccharides
(cel and attR) and in genes involved in signaling between the plant and bacteria (attB and attD)
reduced the ability of the bacteria to attach to and colonize intact
roots. These genes are known to play a role in the pathogenic
interaction of the bacteria with wound sites. Thus, it appears that the
initial stages of pathogenesis and root colonization may depend on many of the same genes and processes.
The results reported here add to the number and type of genes known to
be involved in root colonization. Previously identified genes include
genes required for the synthesis of bacterial agglutinins of
pseudomonads (2), flagellar, motility, and chemotaxis genes of rhizobia, agrobacteria, and pseudomonads (1, 5, 10, 24,
28), chvA and chvB of A. tumefaciens (8), the pilus genes of pseudomonads
(31), genes required for biosynthesis of amino acids and
thiamine (27, 28), genes required for synthesis of the
lipopolysaccharide O-antigens of pseudomonads (28), and genes affecting siderophore synthesis in pseudomonads (12).
| |
ACKNOWLEDGMENTS |
This research was supported by grant 94-37303 from the U.S.
Department of Agriculture Competitive Grants Program and by grant MCB-9405844 from NSF.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biology, University of North Carolina, Chapel Hill, NC 27599-3280. Phone: (919) 962-6941. Fax: (919) 962-1625. E-mail:
matthysse{at}unc.edu.
| |
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Appl Environ Microbiol, July 1998, p. 2341-2345, Vol. 64, No. 7
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
