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Plant Physiology 133:339-347 (2003) © 2003 American Society of Plant Biologists A Developmental Response to Pathogen Infection in Arabidopsis1Department of Ecology and Evolution, University of Chicago, 1101 East 57th Street, Chicago, Illinois 60637
We present evidence that susceptible Arabidopsis plants accelerate their reproductive development and alter their shoot architecture in response to three different pathogen species. We infected 2-week-old Arabidopsis seedlings with two bacterial pathogens, Pseudomonas syringae and Xanthomonas campestris, and an oomycete, Peronospora parasitica. Infection with each of the three pathogens reduced time to flowering and the number of aerial branches on the primary inflorescence. In the absence of competition, P. syringae and P. parasitica infection also increased basal branch development. Flowering time and branch responses were affected by the amount of pathogen present. Large amounts of pathogen caused the most dramatic changes in the number of branches on the primary inflorescence, but small amounts of P. syringae caused the fastest flowering and the production of the most basal branches. RPS2 resistance prevented large changes in development when it prevented visible disease symptoms but not at high pathogen doses and when substantial visible hypersensitive response occurred. These experiments indicate that phylogenetically disparate pathogens cause similar changes in the development of susceptible Arabidopsis. We propose that these changes in flowering time and branch architecture constitute a general developmental response to pathogen infection that may affect tolerance of and/or resistance to disease.
One way that plants can respond to pathogen infection is through an induced resistance response called R gene resistance. When a plant has an R gene that confers resistance to an infecting pathogen, the plant initiates extensive biochemical and structural defense mechanisms, including the production of phytoalexins and pathogenesis-related proteins, the strengthening of cell walls, local cell death, and systemic acquired resistance (Dangl and Jones, 2001  ). Plants that are "susceptible," i.e. do not have R gene resistance to a particular pathogen strain, exhibit many defenses similar to R gene resistance, but are slower in their expression of these responses (Yang et al., 1997; Maleck et al., 2000). Like R gene-resistant plants, susceptible plants have increased levels of salicylic acid (SA; O'Donnell et al., 2001), cell death, and defense mechanisms characteristic of systemic acquired resistance (Glazebrook, 2001). In addition, infected, susceptible plants can exhibit increased levels of jasmonic acid (JA), auxin, and ethylene (Dong, 1998; Lund et al., 1998; O'Donnell et al., 2003).
These responses of plants to pathogen infection bear some similarity to responses to abiotic stress. Both can involve cell death (Beers and McDowell, 2001
There are several other reasons to expect that plants will respond to pathogen infection with changes in the timing of reproduction. First, one study reported that Arabidopsis infected with Pseudomonas syringae DC3000 had a higher probability of bolting under 8-h light conditions (Peters, 1999
Changes in the timing of reproductive development in plants are often associated with changes in plant growth and branch architecture (Martinez-Zapater et al., 1995
In this paper, we show that pathogen infection can alter time to flowering and branch architecture in susceptible Arabidopsis plants. We investigate the generality of these changes in development by examining the effects of three distantly related pathogens: P. syringae and Xanthomonas campestris, which are biotrophic bacterial pathogens, and Peronospora parasitica, which is a biotrophic oomycete. All of these pathogens occur in natural Arabidopsis populations (Tsuji and Somerville, 1992
P. syringae Infection Alters Flowering Time and Branch Architecture in Susceptible Plants To examine the effect of P. syringae on development, we infected susceptible plants (rps2) with P. syringae DC3000 + avrRpt2 at 2 weeks old. P. syringae infection significantly accelerated flowering time, decreased the number of aerial branches (branches above the rosette), increased the number of basal branches (branches from the rosette), and decreased the height of the primary inflorescence (Tables I and II). Because plant development can vary dramatically in different growth conditions, we evaluated the effects of infection both with and without competition. When grown with competitors, susceptible plants infected with P. syringae flowered on average 5.1 d faster than mock-treated plants and, without competition, flowered 2.5 d faster. Infected plants produced almost two fewer secondary aerial branches than mock-treated plants in the presence of competition and almost three fewer in the absence of competition. Infected plants also produced, on average, 1.1 more basal branches than mock-treated plants in the absence of competition. Another indication of increased development of the basal branches is the almost 2-fold increase in the number of siliques produced by the basal branches in infected plants compared with mock-treated plants.
To investigate whether the developmental changes we observed are specific to the bacterial pathogen P. syringae, we evaluated the effects of P. parasitica Noco2 and X. campestris pv campestris 8004 on susceptible plants. Both P. parasitica and X. campestris infections accelerated flowering and decreased the number of aerial branches (Tables II and III). In the absence of competition, P. parasitica infection also significantly increased the number of siliques produced by basal branches, indicating increased basal branch development. There was no significant difference in the number of basal branches produced with and without P. parasitica infection. Fewer basal branches were produced in the P. parasitica and X. campestris experiments compared with the P. syringae experiment, which likely reflects differences in the experimental conditions used for these different pathogens. Unlike P. syringae infection, P. parasitica and X. campestris infection did not significantly alter height.
Next, we addressed whether the amount of pathogen affects the extent of developmental changes. To obtain variation in the amount of pathogen, we infected plants with four strains of P. syringae that vary in their growth in Columbia (Col). In addition to exploiting variation in the growth potential of strains, each strain was infected at three different initial doses, designated high, medium, and low. Pathogen strain and initial dose did not affect symptoms or developmental responses independent of bacterial abundance 4 d after infection. That is, differences in the initial dose were overwhelmed by the different propensities of the strains to grow, and the identity of the strain had no effect over and above its growth. We tested for effects of initial dose and pathogen strain with analyses of covariance that included Strain, Dose, Strain x Dose, and, as a surrogate for the amount of pathogen 4 d after infection, the length of the second infected leaf as a covariate. Length of the second leaf 9 d after infection correlated strongly with the amount of pathogen across pathogen dose treatments (R = -0.96) and could be measured on the same plants as the developmental traits, unlike the amount of pathogen, which requires destructive sampling. There were no effects of Dose, Strain, or Dose x Strain for any of the traits measured. As a consequence, in further analyses, strain dose treatment means are treated as independent samples in our investigation of the relationship between pathogen abundance and plant traits.
The amount of P. syringae present in the infected leaves affected the percentage of infected leaf area that was visibly damaged (
The amount of P. syringae present positively affected time to bolting (
The amount of P. syringae also affected branch architecture. The number of aerial meristems (Fig. 1C) and the number of aerial branches each decreased with greater amounts of pathogen ( Only a few plants produced basal branches in this experiment; as a consequence, no changes in the production of basal branches were evident. Because basal branching is likely to be affected by the amount of resources, we investigated the effect of initial dose of P. syringae DC3000 in plants grown in larger pots that permitted basal branching. Plants infected with a low dose of P. syringae produced more basal branches than plants infected with a high dose and also flowered more quickly (Fig. 2). There was no significant effect of dose on the number of aerial branches in this experiment.
To explore the effect of amount of pathogen for a different kind of pathogen, in conjunction with the experiment employing the different P. syringae strains, we infected plants with three doses of a compatible X. campestris strain. The effect of X. campestris dose on plant development was similar to that of P. syringae for branch architecture but not for flowering time (Fig. 1). Larger amounts of X. campestris were associated with fewer aerial branches (means contrast between high and low doses, F = 11.2, df = 1,54, P = 0.0015), a lower point of origin on the primary branch for the uppermost aerial branch (F = 10.3, df = 1,54, P = 0.002), and taller primary inflorescences (F = 4.24, df = 1,54, P = 0.044). However, larger amounts of X. campestris were associated with faster bolting (Fig. 1B) and flowering (F = 5.9, df = 1,54, P = 0.018) times. In addition, the high dose of X. campestris resulted in fewer rosette leaves than the low dose (F = 5.7, df = 1,54, P = 0.020).
To evaluate whether R gene resistance alters developmental changes with infection, we compared the responses of RPS2 and rps2 plants to P. syringae + avrRpt2 and the responses of RPP5 and rpp5 plants to P. parasitica Noco2. For RPS2, we used wild-type Col in conjunction with an rps2 mutant in the experiment described in the first section. Significant Genotype x Infection Treatment interaction terms indicate that RPS2 resistance significantly altered flowering time, numbers of aerial and basal branches, and silique production by basal branches (Table IV). When infected, RPS2 plants took longer to flower, produced more aerial branches, fewer basal branches, and fewer siliques on basal branches than infected, susceptible plants (means contrasts, all P < 0.001). In each case, RPS2 plants infected with P. syringae more closely resembled mock-treated plants than rps2 plants and were only significantly different from mock-treated resistant plants for number of aerial branches (F = 5.45, df = 1,34, P < 0.05).
For P. parasitica, we compared RPP5 lines and rpp5 lines that were created via the introgression of RPP5 from Landsburg erecta (Ler) into Col. The susceptible (rpp5) lines were homozygous for the Col RPP5 gene family, and resistant (RPP5) lines were homozygous for the Ler RPP5 gene family. In contrast to RPS2 resistance, RPP5 did not significantly alter plant responses to infection (Table IV). When infected, RPP5-resistant plants did not significantly differ from rpp5 plants in number of aerial branches, number of basal branches, or number of siliques on the basal branches (means contrasts, all P > 0.10). Although there were also no significant differences between infected and mock-treated RPP5 plants across competition treatments, in the presence of competition, RPP5 plants exhibited accelerated flowering with infection (F = 6.31, df = 1,34, P < 0.025). One factor that might explain the difference in results for RPS2 and RPP5 resistance is the amount of pathogen present in resistant plants. Although both RPS2 and RPP5 resistance significantly reduced disease symptoms (data not shown), RPS2 resistance prevented visible disease symptoms almost entirely, whereas 65% of infected RPP5 resistant plants showed some sporulation by 11 d after infection. To investigate whether the amount of pathogen present might affect the development of plants with an R gene resistance response, we infected wild-type Col plants with three different doses of P. syringae DC3000 + avrRpt2, an incompatible strain. Here, P. syringae infection led to changes in the development of resistant plants, but only when the pathogen dose was sufficiently high (Fig. 1). Resistant plants infected with a low dose of P. syringae DC3000 + pLABL18 did not differ significantly from plants given the mock treatment for any of the developmental traits. Plants given medium and high doses produced significantly fewer secondary aerial meristems and aerial branches than mock-treated plants (both P < 0.001), and the numbers for both of these traits were significantly lower for the high dose than for the low dose (means contrasts, all P < 0.01). Like for compatible interactions with similar amounts of P. syringae in this experiment, there were no significant effects of the high and medium doses on time to bolting or flowering. The responses to the different doses of incompatible pathogen parallel differences in the amount of pathogen present after 4 d and symptoms of infection. High and medium doses resulted in significantly more pathogen present 4 d after infection than the low dose (means contrasts, both P < 0.01). The medium and high doses also caused visible hypersensitive response-induced cell death, whereas the low dose resulted in symptomless leaves (Fig. 1A).
In response to compatible pathogen infection, susceptible plants undergo localized chlorosis and cell death, increases in hormones such as SA, JA, ethylene, and auxin, and changes in the expression of transcription factors associated with stress and resistance (Dong, 1998 ; Maleck et al., 2000; Glazebrook, 2001; Chen et al., 2002; O'Donnell et al., 2003). Our experiments indicate that the susceptible response to pathogen infection also extends to changes in the timing of plant development and morphology. We found that P. syringae, P. parasitica, and X. campestris infections can each cause Arabidopsis plants to flower faster and produce fewer aerial branches. In addition, P. syringae infection and P. parasitica infection can increase basal branch development under high resource conditions. These results suggest that faster flowering times and changes in branch architecture are general consequences of pathogen infection in susceptible Arabidopsis seedlings. We propose that these developmental changes are initiated by the plant, are developmentally linked, and constitute a single developmental response to pathogen infection.
The changes in plant development could be either an active response of plants to infection or the consequence of pathogens actively manipulating plant growth. Some pathogens are known to alter plant growth by inducing hormonal changes (Agrios, 1997
The overlap between responses to abiotic factors and to pathogen infection suggests that some of the same pathways could be utilized to initiate accelerated flowering. The pathways responsible for inducing faster flowering in response to abiotic stresses are unknown. However, responses to some abiotic stresses, like to pathogen infection, involve increases in SA, JA, and ethylene (Wang et al., 2002 Although the similarity of responses to different pathogens suggests that similar pathways are involved, the presence of some differences in susceptible plants' responses to the pathogens reveals that the processes differ in at least some details. In particular, similar amounts of P. syringae and X. campestris had different consequences for time to bolting and number of aerial branches (Fig. 1). In addition, the relationships between the amount of pathogen and time to bolting and between the amount of pathogen and number of rosette leaves differed between X. campestris and P. syringae. Further experiments are necessary to determine to what extent a common mechanism underlies the responses to different pathogens. Our results suggest that developmental changes with infection are dependent on the presence of sufficient amounts of pathogen and/or disease symptoms and that R gene resistance can prevent developmental changes through reduced bacterial growth. When RPS2 resistance prevented symptoms and limited pathogen growth, developmental changes were absent or small. However, when RPS2-resistant plants exhibited a visible hypersensitive response, and high amounts of pathogen were present, developmental changes like those in susceptible plants occurred. This indicates that the presence of an R gene resistance response does not directly prevent the changes in development. In susceptible plants, changes in the number of secondary aerial meristems required sufficient pathogen and/or some visible disease symptoms (Fig. 1). General stress does not appear to be responsible for the changes in development in our experiments; plant rosettes did not appear purplish before flowering (personal observation), as can be the case for nutrient-stressed plants that flower faster.
The acceleration of flowering time and changes in branch architecture are likely to be developmentally linked. Faster flowering and the production of fewer aerial branches may both be a consequence of a transition to reproduction at an earlier vegetative stage (Diggle, 1999 Although faster flowering sometimes coincided with less aerial branch production for P. syringae infection (Table I; Fig. 2), it did not always. For example, plants infected with large amounts of P. syringae produced fewer aerial branches but did not flower faster (Figs. 1 and 2). One possible explanation for this pattern is that extensive P. syringae disease symptoms slow plant growth and prevent faster flowering while still permitting a transition at a relatively early vegetative stage. In addition, we observed that very low titers of P. syringae, which caused little or no visible symptoms, resulted in faster flowering without decreases in the number of aerial meristems (Fig. 1). This suggests that faster flowering with pathogen infection may also occur by mechanisms other than a switch to reproduction after fewer cauline leaf primordia have been produced.
The smaller number of secondary aerial meristems with pathogen infection may cause the increase in basal branching under high resource conditions. After the transition to flowering, secondary meristem development is basipetal, with the uppermost secondary meristem producing the first branch (Hempel and Feldman, 1994
The developmental changes with infection might enhance a plant's ability to cope with pathogen infection in several ways. First, faster development may lead to the early development of age-related resistance in Arabidopsis (Leisner et al., 1993
Plant and Pathogen Materials
RPS2-resistant and -susceptible lines were made from wild-type Arabidopsis Col seed, provided by Jean Greenberg (University of Chicago, IL), and Col rps2-101C seed (Mindrinos et al., 1994
Experiments utilized the following Pseudomonas strains: Pseudomonas syringae pv tomato strain DC3000 (Whalen et al., 1991
Plants were grown in Promix soil in a growth room (300 µmol photons m-2 s-1) with a 12-h-light/12-h-dark cycle. Planted seeds were given a 2- to 5-d cold treatment at 4°C. Plants were not fertilized, and pots were rotated every 1 or 2 d to adjust for uneven lighting across the growth room. Due to different growth requirements for different pathogen strains, some conditions varied among experiments and are noted with the methods for each experiment.
In all experiments, the first two true leaves were infected when plants were approximately 2 weeks old. For bacterial infections, P. syringae strains were grown in King's Broth media (King et al., 1954 For P. parasitica infection, plants were infected with asexual conidiospores harvested from sporulating seedlings that had been inoculated 1 week before the experiment. Sporulating seedlings were shaken in water, the solution was spun, and the condiospores were resuspended. The concentration was adjusted to 3.5 x 105 zoospores mL-1 using a hemocytometer. Five microliters of the spore suspension was dropped onto each leaf with a pipette. The mock treatment entailed pipetting water. Because P. parasitica requires high humidity for infection, pots were placed within polyvinyl chloride frames covered with Warp's polycomb plastic sheeting. Before P. parasitica infection, pots were transferred to flats with wet sponge bottoms and, to prevent transmission of the P. parasitica to other plants, were bottom watered for a few weeks after infection.
To create homozygous resistant and susceptible lines that had the same genetic background and parental history, rps2-101C was crossed to wild-type Col, and the progeny of a single heterozygous parent were screened for homozygous RPS2 and rps2 plants using a cleaved-amplified polymorphic sequence (CAPS) marker. The selfed progeny of each selected homozygous plant were used as a line; 18 resistant and 18 susceptible lines were used.
Plants were infected with either P. syringae pv tomato DC3000 containing the avrRpt2-bearing vector pLABL18 (Whalen et al., 1991 Numbers of aerial branches, basal branches, siliques on the basal branches, and height were determined after senescence. Each trait was analyzed with an ANOVA using Statistica. Line was considered a random effect and competition treatment, infection treatment, and resistance genotype were considered fixed effects. The statistical significance of effects of pathogen versus mock treatment for susceptible plants was evaluated using means contrasts across competition treatments and within competition treatments. Because basal branches were rare in the presence of competition, ANOVAs were done for number of basal branches and number of basal siliques for the no competition treatment only. To determine the effect of RPS2 resistance, we evaluated the significance of the interaction terms Infection Treatment x Resistance Genotype and Infection Treatment x Resistance Genotype x Competition. In addition, to evaluate the nature of these interactions, means contrasts were calculated between infected, susceptible and resistant plants and between infected and uninfected resistant plants.
Near-isogenic lines were made by introgressing the Ler RPP5 gene family into Col, which is susceptible to P. parasitica Noco2 (Parker et al., 1993 The experiment entailed the same conditions, experimental design, measurements, and analyses described above for P. syringae pv tomato DC3000. Because many plants had no basal branches, there was a non-normal distribution for number of basal siliques. Thus, differences in the number of siliques on the basal branches were analyzed using line means in an ANOVA.
Plants were infected with four strains of P. syringae: P. syringae pv tomato strain DC3000, P. syringae pv maulicola strain ES4326, P. syringae strain RM18.1, and P. syringae pv phaseolicola strain NPS3121, at three initial doses, OD600= 0.03, 0.003, and 0.0003. In addition, control plants were treated with a mock treatment consisting of 10 mM MgSO4. Plants were grown at 18°C in 6-x 9-x 9-cm pots, and domes were placed over the flats for 3 d after infection. The amount of bacteria 4 d after infection was measured in separate plants from those used to measure the effect of infection on development. For each strain dose combination, one whole infected leaf was clipped from each of six plants and ground in 10 mM MgSO4. Dilutions were plated on King's Broth plates with a Whitley Automatic Spiral Plater. The number of colony-forming units per milliliter was determined by counting colonies with a ProtoCol colony counter (Synbiosis, Frederick, MD). For measurements of development, 19 plants were infected for each pathogen dose treatment or the mock treatment. Disease symptoms were measured 9 d after infection by blindly scoring the percentage of infected leaf area with visible chlorosis, water soaking, or cell death. Average log pathogen abundance 4 d after infection and the average of each plant trait were calculated for each treatment combination. These were used to calculate regression coefficients between values for the traits and pathogen abundance.
Additional Col plants were infected with an incompatible strain, P. syringae DC3000 + pLABL18 (Whalen et al., 1991 Additional plants were infected with X. campestris pv campestris strain 8004 (obtained from Jeff Dangl) at the same three doses. The amount of pathogen 4 d after infection was determined by plating dilutions of ground leaves on Luria-Bertani plates. The same analyses as for P. syringae DC3000 + avrRpt2 were performed. For analyses of the effects of X. campestris presented in Tables II and III, means contrasts were calculated between the high dose and the mock treatment. The high dose was chosen because the amount of pathogen after 4 d for this dose was closest to that of P. syringae in the first experiment. To investigate the effect of amount of compatible P. syringae on basal branching, a separate experiment was done in 12.5-x 10-x 10-cm pots at 20°C with domes on the flats for 1 d after infection. Col rps2 plants were infected with three doses of P. syringae DC3000 + pLABL18 (carrying avrRpt2) or given a mock treatment. The same analyses were done as for P. syringae DC3000 + pLABL18 in the experiment with smaller pots. Unlike in the other experiments, plants were not rotated among all positions; as a consequence, the ANOVAs included row as a blocking factor. Because there was no replication within rows, Row x Dose served as the error term.
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third party owners of all or parts of the material. Obtaining any permissions will be the responsibility of the requestor.
We thank Jean Greenberg for advice and comments on this manuscript and the V. Dropkin Foundation for the use of equipment. Received May 20, 2003; returned for revision June 13, 2003; accepted June 13, 2003.
1 This work was supported by the National Science Foundation (Dissertation Improvement Grant to T.M.K.) and by the National Institutes of Health (grant no. GM57994 to J.B.). 
2 Present address: Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman Street, Box G-W, Providence, RI 02912. * Corresponding author; e-mail Tonia_Korves{at}brown.edu; fax 401-863-2166.
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= 0.90, P < 0.0001; 
