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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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Canonical discriminate analysis of treatment and leaf position as classification variables.Concentrations of 12 elements analyzed were considered as independent variables, while experimental set and time points were considered as replicates. A) Leaves were separated according to relative position in the plant between leaves #1–3 (circles) which are older, directly-inoculated and leaves ≥ #4 (inverted triangles) that represent new growth after inoculation. B) Leaves at the same position were compared according to presence or absence of X. fastidiosa. Circle = position #4; inverted triangle = position #5; square = position #6; diamond = position #7; triangle = position #8. Phenotypic correlations for Can1 are driven significantly (p<0.05) by Ca (r = −0.98), Mg (r = −0.89), Na (r = 0.85), K (r = 0.74), and Mn (r = −0.59) and for Can2 by Cu (r = 0.57) and S (r = −0.52). B, Fe, Mo, P, and Zn have no significant effect on discrimination among classes. Red symbols indicate leaves infected with X. fastidiosa and green symbols indicate non-infected leaves. The length of the axes is proportional to the accounted for percentage of the total multivariance.
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pone-0062945-g002: Canonical discriminate analysis of treatment and leaf position as classification variables.Concentrations of 12 elements analyzed were considered as independent variables, while experimental set and time points were considered as replicates. A) Leaves were separated according to relative position in the plant between leaves #1–3 (circles) which are older, directly-inoculated and leaves ≥ #4 (inverted triangles) that represent new growth after inoculation. B) Leaves at the same position were compared according to presence or absence of X. fastidiosa. Circle = position #4; inverted triangle = position #5; square = position #6; diamond = position #7; triangle = position #8. Phenotypic correlations for Can1 are driven significantly (p<0.05) by Ca (r = −0.98), Mg (r = −0.89), Na (r = 0.85), K (r = 0.74), and Mn (r = −0.59) and for Can2 by Cu (r = 0.57) and S (r = −0.52). B, Fe, Mo, P, and Zn have no significant effect on discrimination among classes. Red symbols indicate leaves infected with X. fastidiosa and green symbols indicate non-infected leaves. The length of the axes is proportional to the accounted for percentage of the total multivariance.

Mentions: Initially, multivariate statistical analysis was conducted to establish the joint effect of all variables considered. Sampled leaves were classified by treatment according to the following: i) “infected”, including all leaves from bacterium-inoculated plants that were positive for X. fastidiosa by qPCR; and ii) “non-infected”, including all leaves from buffer-inoculated plants and leaves from bacterium-inoculated plants that were negative for X. fastidiosa by qPCR. This classification was used throughout the analysis, as having detectable levels of X. fastidiosa was considered the best indication of the infection status of a particular leaf at a specific time. Canonical discriminant analysis (CDA) was performed considering treatment and leaf position as classification variables, while time and experimental set were considered as replication variables. The concentrations of the 12 elements (B, Ca, Cu, Fe, K, Mg, Mo, Mn, Na, P, S, and Zn) were considered as independent variables (Fig. 2A). Leaves were grouped according to their position in the plant: leaves from positions #1–3 (older leaves, needle-inoculated) or leaves from positions ≥ #4 (new growth after inoculation). Graphing centroid means for canonical variate 2 (Can2, 12% of the variation) against canonical variate 1 (Can1, 75% of the variation) demonstrates that leaves in positions #1–3 were fundamentally different from the ones in positions ≥ #4. Leaves with position ≥ #4 clustered together according to treatment (Fig. 2A, green and red inverted triangles) along Can2. This indicates that a treatment effect could be dissected among leaves ≥ #4 that were colonized by X. fastidiosa during the course of the experiment; therefore, these leaves were used for further analyses.


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)

Canonical discriminate analysis of treatment and leaf position as classification variables.Concentrations of 12 elements analyzed were considered as independent variables, while experimental set and time points were considered as replicates. A) Leaves were separated according to relative position in the plant between leaves #1–3 (circles) which are older, directly-inoculated and leaves ≥ #4 (inverted triangles) that represent new growth after inoculation. B) Leaves at the same position were compared according to presence or absence of X. fastidiosa. Circle = position #4; inverted triangle = position #5; square = position #6; diamond = position #7; triangle = position #8. Phenotypic correlations for Can1 are driven significantly (p<0.05) by Ca (r = −0.98), Mg (r = −0.89), Na (r = 0.85), K (r = 0.74), and Mn (r = −0.59) and for Can2 by Cu (r = 0.57) and S (r = −0.52). B, Fe, Mo, P, and Zn have no significant effect on discrimination among classes. Red symbols indicate leaves infected with X. fastidiosa and green symbols indicate non-infected leaves. The length of the axes is proportional to the accounted for percentage of the total multivariance.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3646994&req=5

pone-0062945-g002: Canonical discriminate analysis of treatment and leaf position as classification variables.Concentrations of 12 elements analyzed were considered as independent variables, while experimental set and time points were considered as replicates. A) Leaves were separated according to relative position in the plant between leaves #1–3 (circles) which are older, directly-inoculated and leaves ≥ #4 (inverted triangles) that represent new growth after inoculation. B) Leaves at the same position were compared according to presence or absence of X. fastidiosa. Circle = position #4; inverted triangle = position #5; square = position #6; diamond = position #7; triangle = position #8. Phenotypic correlations for Can1 are driven significantly (p<0.05) by Ca (r = −0.98), Mg (r = −0.89), Na (r = 0.85), K (r = 0.74), and Mn (r = −0.59) and for Can2 by Cu (r = 0.57) and S (r = −0.52). B, Fe, Mo, P, and Zn have no significant effect on discrimination among classes. Red symbols indicate leaves infected with X. fastidiosa and green symbols indicate non-infected leaves. The length of the axes is proportional to the accounted for percentage of the total multivariance.
Mentions: Initially, multivariate statistical analysis was conducted to establish the joint effect of all variables considered. Sampled leaves were classified by treatment according to the following: i) “infected”, including all leaves from bacterium-inoculated plants that were positive for X. fastidiosa by qPCR; and ii) “non-infected”, including all leaves from buffer-inoculated plants and leaves from bacterium-inoculated plants that were negative for X. fastidiosa by qPCR. This classification was used throughout the analysis, as having detectable levels of X. fastidiosa was considered the best indication of the infection status of a particular leaf at a specific time. Canonical discriminant analysis (CDA) was performed considering treatment and leaf position as classification variables, while time and experimental set were considered as replication variables. The concentrations of the 12 elements (B, Ca, Cu, Fe, K, Mg, Mo, Mn, Na, P, S, and Zn) were considered as independent variables (Fig. 2A). Leaves were grouped according to their position in the plant: leaves from positions #1–3 (older leaves, needle-inoculated) or leaves from positions ≥ #4 (new growth after inoculation). Graphing centroid means for canonical variate 2 (Can2, 12% of the variation) against canonical variate 1 (Can1, 75% of the variation) demonstrates that leaves in positions #1–3 were fundamentally different from the ones in positions ≥ #4. Leaves with position ≥ #4 clustered together according to treatment (Fig. 2A, green and red inverted triangles) along Can2. This indicates that a treatment effect could be dissected among leaves ≥ #4 that were colonized by X. fastidiosa during the course of the experiment; therefore, these leaves were used for further analyses.

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