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The bacterial pathogen Xylella fastidiosa affects the leaf ionome of plant hosts during infection.

De La Fuente L, Parker JK, Oliver JE, Granger S, Brannen PM, van Santen E, Cobine PA - PLoS ONE (2013)

Bottom Line: The elemental composition of leaves was used as an indicator of the physiological changes in the host at a specific time and relative position during plant development.Bacterial infection was found to cause significant increases in concentrations of calcium prior to the appearance of symptoms and decreases in concentrations of phosphorous after symptoms appeared.This descriptive ionomics approach characterizes the existence of a mineral element-based response to X. fastidiosa using a model system suitable for further manipulation to uncover additional details of the role of mineral elements during plant-pathogen interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, United States of America. lzd0005@auburn.edu

ABSTRACT
Xylella fastidiosa is a plant pathogenic bacterium that lives inside the host xylem vessels, where it forms biofilm believed to be responsible for disrupting the passage of water and nutrients. Here, Nicotiana tabacum was infected with X. fastidiosa, and the spatial and temporal changes in the whole-leaf ionome (i.e. the mineral and trace element composition) were measured as the host plant transitioned from healthy to diseased physiological status. The elemental composition of leaves was used as an indicator of the physiological changes in the host at a specific time and relative position during plant development. Bacterial infection was found to cause significant increases in concentrations of calcium prior to the appearance of symptoms and decreases in concentrations of phosphorous after symptoms appeared. Field-collected leaves from multiple varieties of grape, blueberry, and pecan plants grown in different locations over a four-year period in the Southeastern US showed the same alterations in Ca and P. This descriptive ionomics approach characterizes the existence of a mineral element-based response to X. fastidiosa using a model system suitable for further manipulation to uncover additional details of the role of mineral elements during plant-pathogen interactions. This is the first report on the dynamics of changes in the ionome of the host plant throughout the process of infection by a pathogen.

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Infection of Nicotiana tabacum ‘Petite Havana SR1’ with Xylella fastidiosa.A) Progression of symptom development in tobacco plants infected with X. fastidiosa Temecula. The percentage of symptomatic leaves showing marginal leaf scorch at a specific leaf position on the plant (increasing numbers from bottom to top of the plant) and at a specific time are represented in the graph. Sampling times numbered 1 through 5 in the graph correspond to 0, 22, 27, 38, 48, and 59 days post inoculation, respectively. Five tobacco plants were analyzed at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment. B) Population of X. fastidiosa Temecula in petioles of infected tobacco plants. Bacterial populations were quantified by specific qPCR using sections of petioles as source material. Five tobacco plants were analyzed per sampling time at several days post-infection (dpi). Data represented in the graph correspond to means and standard errors of bacterial populations of all leaves at positions ≥#4 at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment.
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pone-0062945-g001: Infection of Nicotiana tabacum ‘Petite Havana SR1’ with Xylella fastidiosa.A) Progression of symptom development in tobacco plants infected with X. fastidiosa Temecula. The percentage of symptomatic leaves showing marginal leaf scorch at a specific leaf position on the plant (increasing numbers from bottom to top of the plant) and at a specific time are represented in the graph. Sampling times numbered 1 through 5 in the graph correspond to 0, 22, 27, 38, 48, and 59 days post inoculation, respectively. Five tobacco plants were analyzed at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment. B) Population of X. fastidiosa Temecula in petioles of infected tobacco plants. Bacterial populations were quantified by specific qPCR using sections of petioles as source material. Five tobacco plants were analyzed per sampling time at several days post-infection (dpi). Data represented in the graph correspond to means and standard errors of bacterial populations of all leaves at positions ≥#4 at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment.

Mentions: To facilitate ionomic studies in plants infected with X. fastidiosa, a previously described model system, Nicotiana tabacum ‘Petite Havana SR1’ (tobacco), was used [31]. Relative position on the tobacco plants and visual symptom appearance (marginal leaf scorch) were recorded for each leaf. Symptoms were detected in leaves at position #4 and above approximately 41–48 days post inoculation (dpi) (Fig. 1), a typical latency period previously observed [1], [31], [37]. Symptoms in leaves from the bottom three positions (#1–3) were detected earlier, but, due to significant contributions from natural senescence and the fact that these leaves were directly needle-inoculated, these symptoms were not considered diagnostic of successful infection. Once symptoms were detected in any of the leaves at positions #4 and above, they rapidly (ca. 8–12 days) spread to the rest of the leaves acropetally, as is typical for X. fastidiosa infections [31], [38]. Populations of the bacterium in leaves #4 and above increased rapidly from 25–30 dpi, indicating movement of the bacterium inside xylem vessels, and reached a plateau (ca. log 3.4 CFU/mg tissue) after approximately 50 dpi (Fig. 1).


The bacterial pathogen Xylella fastidiosa affects the leaf ionome of plant hosts during infection.

De La Fuente L, Parker JK, Oliver JE, Granger S, Brannen PM, van Santen E, Cobine PA - PLoS ONE (2013)

Infection of Nicotiana tabacum ‘Petite Havana SR1’ with Xylella fastidiosa.A) Progression of symptom development in tobacco plants infected with X. fastidiosa Temecula. The percentage of symptomatic leaves showing marginal leaf scorch at a specific leaf position on the plant (increasing numbers from bottom to top of the plant) and at a specific time are represented in the graph. Sampling times numbered 1 through 5 in the graph correspond to 0, 22, 27, 38, 48, and 59 days post inoculation, respectively. Five tobacco plants were analyzed at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment. B) Population of X. fastidiosa Temecula in petioles of infected tobacco plants. Bacterial populations were quantified by specific qPCR using sections of petioles as source material. Five tobacco plants were analyzed per sampling time at several days post-infection (dpi). Data represented in the graph correspond to means and standard errors of bacterial populations of all leaves at positions ≥#4 at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3646994&req=5

pone-0062945-g001: Infection of Nicotiana tabacum ‘Petite Havana SR1’ with Xylella fastidiosa.A) Progression of symptom development in tobacco plants infected with X. fastidiosa Temecula. The percentage of symptomatic leaves showing marginal leaf scorch at a specific leaf position on the plant (increasing numbers from bottom to top of the plant) and at a specific time are represented in the graph. Sampling times numbered 1 through 5 in the graph correspond to 0, 22, 27, 38, 48, and 59 days post inoculation, respectively. Five tobacco plants were analyzed at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment. B) Population of X. fastidiosa Temecula in petioles of infected tobacco plants. Bacterial populations were quantified by specific qPCR using sections of petioles as source material. Five tobacco plants were analyzed per sampling time at several days post-infection (dpi). Data represented in the graph correspond to means and standard errors of bacterial populations of all leaves at positions ≥#4 at each sampling time. The experiment was repeated three times and data in the graph corresponds to one representative experiment.
Mentions: To facilitate ionomic studies in plants infected with X. fastidiosa, a previously described model system, Nicotiana tabacum ‘Petite Havana SR1’ (tobacco), was used [31]. Relative position on the tobacco plants and visual symptom appearance (marginal leaf scorch) were recorded for each leaf. Symptoms were detected in leaves at position #4 and above approximately 41–48 days post inoculation (dpi) (Fig. 1), a typical latency period previously observed [1], [31], [37]. Symptoms in leaves from the bottom three positions (#1–3) were detected earlier, but, due to significant contributions from natural senescence and the fact that these leaves were directly needle-inoculated, these symptoms were not considered diagnostic of successful infection. Once symptoms were detected in any of the leaves at positions #4 and above, they rapidly (ca. 8–12 days) spread to the rest of the leaves acropetally, as is typical for X. fastidiosa infections [31], [38]. Populations of the bacterium in leaves #4 and above increased rapidly from 25–30 dpi, indicating movement of the bacterium inside xylem vessels, and reached a plateau (ca. log 3.4 CFU/mg tissue) after approximately 50 dpi (Fig. 1).

Bottom Line: The elemental composition of leaves was used as an indicator of the physiological changes in the host at a specific time and relative position during plant development.Bacterial infection was found to cause significant increases in concentrations of calcium prior to the appearance of symptoms and decreases in concentrations of phosphorous after symptoms appeared.This descriptive ionomics approach characterizes the existence of a mineral element-based response to X. fastidiosa using a model system suitable for further manipulation to uncover additional details of the role of mineral elements during plant-pathogen interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, United States of America. lzd0005@auburn.edu

ABSTRACT
Xylella fastidiosa is a plant pathogenic bacterium that lives inside the host xylem vessels, where it forms biofilm believed to be responsible for disrupting the passage of water and nutrients. Here, Nicotiana tabacum was infected with X. fastidiosa, and the spatial and temporal changes in the whole-leaf ionome (i.e. the mineral and trace element composition) were measured as the host plant transitioned from healthy to diseased physiological status. The elemental composition of leaves was used as an indicator of the physiological changes in the host at a specific time and relative position during plant development. Bacterial infection was found to cause significant increases in concentrations of calcium prior to the appearance of symptoms and decreases in concentrations of phosphorous after symptoms appeared. Field-collected leaves from multiple varieties of grape, blueberry, and pecan plants grown in different locations over a four-year period in the Southeastern US showed the same alterations in Ca and P. This descriptive ionomics approach characterizes the existence of a mineral element-based response to X. fastidiosa using a model system suitable for further manipulation to uncover additional details of the role of mineral elements during plant-pathogen interactions. This is the first report on the dynamics of changes in the ionome of the host plant throughout the process of infection by a pathogen.

Show MeSH
Related in: MedlinePlus