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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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Changes in element concentrations by leaf position over time.Element concentrations in tobacco leaves inoculated with buffer (green circle, control plants) or X. fastidiosa cell suspension (red circle, infected treatment) were followed over time considering relative leaf position in the plant (1 = most basal leaf, 10 = most apical leaf). Data correspond to leaves in positions ≥#4. For the first column (initial), leaves were collected between 25–27 days post infection (dpi); for the second column (intermediate), samples were collected 39–47 dpi; and for the third column (final), samples were obtained 56–59 dpi. From top to bottom, rows of graphs correspond to concentrations of Ca and P expressed in mg per g of plant tissue. Values represent means and standard errors (n = 5) from one out of three experimental sets conducted. *Indicates significant difference (p<0.05) between treatments at a specific leaf position according to one-way ANOVA or Kruskal-Wallis.
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pone-0062945-g004: Changes in element concentrations by leaf position over time.Element concentrations in tobacco leaves inoculated with buffer (green circle, control plants) or X. fastidiosa cell suspension (red circle, infected treatment) were followed over time considering relative leaf position in the plant (1 = most basal leaf, 10 = most apical leaf). Data correspond to leaves in positions ≥#4. For the first column (initial), leaves were collected between 25–27 days post infection (dpi); for the second column (intermediate), samples were collected 39–47 dpi; and for the third column (final), samples were obtained 56–59 dpi. From top to bottom, rows of graphs correspond to concentrations of Ca and P expressed in mg per g of plant tissue. Values represent means and standard errors (n = 5) from one out of three experimental sets conducted. *Indicates significant difference (p<0.05) between treatments at a specific leaf position according to one-way ANOVA or Kruskal-Wallis.

Mentions: X. fastidiosa moves acropetally inside the xylem vessels of the host plant aided by the xylem flow. Leaf position had a significant effect on the concentration of Ca (p<0.0001), Cu, K, Mg, Mn, Mo, Na, and Zn (p<0.03), but had no effect on the concentration of B, Fe, P and S (p>0.05). To assess the influence of relative leaf position during disease development, mean element concentrations were considered for each leaf position. This analysis suggests that differences between treatments are accentuated as time progresses (Fig. 4). Comparisons of leaves in identical leaf positions from plants inoculated with buffer versus those inoculated with the bacterium show that the increase in Ca concentration in infected plants becomes evident in the upper leaves at approximately 39 dpi (“intermediate” column in Fig. 4). This timeframe coincides with exponential growth of X. fastidiosa in the plant and precedes visualization of symptoms (Fig. 1). By 59 dpi, differences in Ca were distributed across all leaves (“final” column in Fig. 4). As an example, at leaf position #9 for the experiment represented in Figure 4, infected leaves had ∼47% (30.8 to 20.9 mg/g tissue, p = 0.11) more Ca than the buffer-inoculated control. Deficiencies in P concentrations in infected leaves were evident towards the end of the experiments when leaves were symptomatic (56 dpi, “final” column Fig. 4). For the experiment represented in Figure 4, leaves at position #9 showed a decrease of ∼46% (3.3 to 6.1 mg/g tissue, p = 0.02) in concentration of P compared to control plants.


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)

Changes in element concentrations by leaf position over time.Element concentrations in tobacco leaves inoculated with buffer (green circle, control plants) or X. fastidiosa cell suspension (red circle, infected treatment) were followed over time considering relative leaf position in the plant (1 = most basal leaf, 10 = most apical leaf). Data correspond to leaves in positions ≥#4. For the first column (initial), leaves were collected between 25–27 days post infection (dpi); for the second column (intermediate), samples were collected 39–47 dpi; and for the third column (final), samples were obtained 56–59 dpi. From top to bottom, rows of graphs correspond to concentrations of Ca and P expressed in mg per g of plant tissue. Values represent means and standard errors (n = 5) from one out of three experimental sets conducted. *Indicates significant difference (p<0.05) between treatments at a specific leaf position according to one-way ANOVA or Kruskal-Wallis.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3646994&req=5

pone-0062945-g004: Changes in element concentrations by leaf position over time.Element concentrations in tobacco leaves inoculated with buffer (green circle, control plants) or X. fastidiosa cell suspension (red circle, infected treatment) were followed over time considering relative leaf position in the plant (1 = most basal leaf, 10 = most apical leaf). Data correspond to leaves in positions ≥#4. For the first column (initial), leaves were collected between 25–27 days post infection (dpi); for the second column (intermediate), samples were collected 39–47 dpi; and for the third column (final), samples were obtained 56–59 dpi. From top to bottom, rows of graphs correspond to concentrations of Ca and P expressed in mg per g of plant tissue. Values represent means and standard errors (n = 5) from one out of three experimental sets conducted. *Indicates significant difference (p<0.05) between treatments at a specific leaf position according to one-way ANOVA or Kruskal-Wallis.
Mentions: X. fastidiosa moves acropetally inside the xylem vessels of the host plant aided by the xylem flow. Leaf position had a significant effect on the concentration of Ca (p<0.0001), Cu, K, Mg, Mn, Mo, Na, and Zn (p<0.03), but had no effect on the concentration of B, Fe, P and S (p>0.05). To assess the influence of relative leaf position during disease development, mean element concentrations were considered for each leaf position. This analysis suggests that differences between treatments are accentuated as time progresses (Fig. 4). Comparisons of leaves in identical leaf positions from plants inoculated with buffer versus those inoculated with the bacterium show that the increase in Ca concentration in infected plants becomes evident in the upper leaves at approximately 39 dpi (“intermediate” column in Fig. 4). This timeframe coincides with exponential growth of X. fastidiosa in the plant and precedes visualization of symptoms (Fig. 1). By 59 dpi, differences in Ca were distributed across all leaves (“final” column in Fig. 4). As an example, at leaf position #9 for the experiment represented in Figure 4, infected leaves had ∼47% (30.8 to 20.9 mg/g tissue, p = 0.11) more Ca than the buffer-inoculated control. Deficiencies in P concentrations in infected leaves were evident towards the end of the experiments when leaves were symptomatic (56 dpi, “final” column Fig. 4). For the experiment represented in Figure 4, leaves at position #9 showed a decrease of ∼46% (3.3 to 6.1 mg/g tissue, p = 0.02) in concentration of P compared to control plants.

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