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Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens.

Reem NT, Pogorelko G, Lionetti V, Chambers L, Held MA, Bellincampi D, Zabotina OA - Front Plant Sci (2016)

Bottom Line: Transgenic Arabidopsis plants expressing AnFAE showed a significant reduction of monomeric ferulic acid, decreased amounts of wall-associated extensins, and increased susceptibility to Botrytis cinerea, compared with wild type.Transgenic Brachypodium showed reductions in monomeric and dimeric ferulic acids and increased susceptibility to Bipolaris sorokiniana.These results demonstrate a role, in both monocot and dicot plants, of polysaccharide feruloylation in plant CWI, which contributes to plant resistance to necrotrophic pathogens.

View Article: PubMed Central - PubMed

Affiliation: Roy J. Carver Department of Biochemistry, Biophysiscs and Molecular Biology, Iowa State University, Ames, IA USA.

ABSTRACT
The complexity of cell wall composition and structure determines the strength, flexibility, and function of the primary cell wall in plants. However, the contribution of the various components to cell wall integrity (CWI) and function remains unclear. Modifications of cell wall composition can induce plant responses known as CWI control. In this study, we used transgenic expression of the fungal feruloyl esterase AnFAE to examine the effect of post-synthetic modification of Arabidopsis and Brachypodium cell walls. Transgenic Arabidopsis plants expressing AnFAE showed a significant reduction of monomeric ferulic acid, decreased amounts of wall-associated extensins, and increased susceptibility to Botrytis cinerea, compared with wild type. Transgenic Brachypodium showed reductions in monomeric and dimeric ferulic acids and increased susceptibility to Bipolaris sorokiniana. Upon infection, transgenic Arabidopsis and Brachypodium plants also showed increased expression of several defense-related genes compared with wild type. These results demonstrate a role, in both monocot and dicot plants, of polysaccharide feruloylation in plant CWI, which contributes to plant resistance to necrotrophic pathogens.

No MeSH data available.


Related in: MedlinePlus

Hydroxyproline content in cell walls of wild-type and two AnFAEArabidopsis lines. (A) Total hydroxyproline content incell walls as determined by absorbance at 560 nm. (B)Hydroxyproline content in the HF-insoluble cell wall fraction (μg Hyp/mgHF-Insoluble). (C) Percent of HF-soluble protein per mg cell wall(mg/mg CW) (D) Hydroxyproline content in HF-soluble protein(μg Hyp/mg CW). Asterisks indicate statistical significance(Student’s t-test, p < 0.05,n = 3).
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Figure 5: Hydroxyproline content in cell walls of wild-type and two AnFAEArabidopsis lines. (A) Total hydroxyproline content incell walls as determined by absorbance at 560 nm. (B)Hydroxyproline content in the HF-insoluble cell wall fraction (μg Hyp/mgHF-Insoluble). (C) Percent of HF-soluble protein per mg cell wall(mg/mg CW) (D) Hydroxyproline content in HF-soluble protein(μg Hyp/mg CW). Asterisks indicate statistical significance(Student’s t-test, p < 0.05,n = 3).

Mentions: Previous work indicated that in dicots, FA may be involved in cross-linking pectinswith extensins (Qi et al., 1995). Extensinsare also induced during defense responses of Arabidopsis plants(Lamport et al., 2011). To investigatewhether Arabidopsis plants expressing AnFAE havealtered amounts of extensin in their cell walls, HF was used to deglycosylate cellwalls. The HF-soluble fraction represents the pool of wall-associated extensins,while the HF-insoluble fraction represents the pool of crosslinked extensins (Mort and Lamport, 1977). The amount ofhydroxyproline was quantified as an indicator of extensin contents. We found that thetotal extensin content was unchanged in transgenic and wild-type cell walls(Figure 5A). The amount ofcrosslinked extensin was slightly elevated in walls from AnFAEtransgenic plants (Figure 5B).However, the proportion of HF-soluble protein per mg cell wall was significantlyreduced in cell walls from AnFAE transgenic plants (Figure5C). In the HF-soluble fraction,AnFAE cell wall samples contained lower amounts of hydroxyproline(Figure 5D). This indicates thatreduction of cell wall feruloylation affects extensin self-cross-linking.


Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens.

Reem NT, Pogorelko G, Lionetti V, Chambers L, Held MA, Bellincampi D, Zabotina OA - Front Plant Sci (2016)

Hydroxyproline content in cell walls of wild-type and two AnFAEArabidopsis lines. (A) Total hydroxyproline content incell walls as determined by absorbance at 560 nm. (B)Hydroxyproline content in the HF-insoluble cell wall fraction (μg Hyp/mgHF-Insoluble). (C) Percent of HF-soluble protein per mg cell wall(mg/mg CW) (D) Hydroxyproline content in HF-soluble protein(μg Hyp/mg CW). Asterisks indicate statistical significance(Student’s t-test, p < 0.05,n = 3).
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4862258&req=5

Figure 5: Hydroxyproline content in cell walls of wild-type and two AnFAEArabidopsis lines. (A) Total hydroxyproline content incell walls as determined by absorbance at 560 nm. (B)Hydroxyproline content in the HF-insoluble cell wall fraction (μg Hyp/mgHF-Insoluble). (C) Percent of HF-soluble protein per mg cell wall(mg/mg CW) (D) Hydroxyproline content in HF-soluble protein(μg Hyp/mg CW). Asterisks indicate statistical significance(Student’s t-test, p < 0.05,n = 3).
Mentions: Previous work indicated that in dicots, FA may be involved in cross-linking pectinswith extensins (Qi et al., 1995). Extensinsare also induced during defense responses of Arabidopsis plants(Lamport et al., 2011). To investigatewhether Arabidopsis plants expressing AnFAE havealtered amounts of extensin in their cell walls, HF was used to deglycosylate cellwalls. The HF-soluble fraction represents the pool of wall-associated extensins,while the HF-insoluble fraction represents the pool of crosslinked extensins (Mort and Lamport, 1977). The amount ofhydroxyproline was quantified as an indicator of extensin contents. We found that thetotal extensin content was unchanged in transgenic and wild-type cell walls(Figure 5A). The amount ofcrosslinked extensin was slightly elevated in walls from AnFAEtransgenic plants (Figure 5B).However, the proportion of HF-soluble protein per mg cell wall was significantlyreduced in cell walls from AnFAE transgenic plants (Figure5C). In the HF-soluble fraction,AnFAE cell wall samples contained lower amounts of hydroxyproline(Figure 5D). This indicates thatreduction of cell wall feruloylation affects extensin self-cross-linking.

Bottom Line: Transgenic Arabidopsis plants expressing AnFAE showed a significant reduction of monomeric ferulic acid, decreased amounts of wall-associated extensins, and increased susceptibility to Botrytis cinerea, compared with wild type.Transgenic Brachypodium showed reductions in monomeric and dimeric ferulic acids and increased susceptibility to Bipolaris sorokiniana.These results demonstrate a role, in both monocot and dicot plants, of polysaccharide feruloylation in plant CWI, which contributes to plant resistance to necrotrophic pathogens.

View Article: PubMed Central - PubMed

Affiliation: Roy J. Carver Department of Biochemistry, Biophysiscs and Molecular Biology, Iowa State University, Ames, IA USA.

ABSTRACT
The complexity of cell wall composition and structure determines the strength, flexibility, and function of the primary cell wall in plants. However, the contribution of the various components to cell wall integrity (CWI) and function remains unclear. Modifications of cell wall composition can induce plant responses known as CWI control. In this study, we used transgenic expression of the fungal feruloyl esterase AnFAE to examine the effect of post-synthetic modification of Arabidopsis and Brachypodium cell walls. Transgenic Arabidopsis plants expressing AnFAE showed a significant reduction of monomeric ferulic acid, decreased amounts of wall-associated extensins, and increased susceptibility to Botrytis cinerea, compared with wild type. Transgenic Brachypodium showed reductions in monomeric and dimeric ferulic acids and increased susceptibility to Bipolaris sorokiniana. Upon infection, transgenic Arabidopsis and Brachypodium plants also showed increased expression of several defense-related genes compared with wild type. These results demonstrate a role, in both monocot and dicot plants, of polysaccharide feruloylation in plant CWI, which contributes to plant resistance to necrotrophic pathogens.

No MeSH data available.


Related in: MedlinePlus