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Hessian fly larval feeding triggers enhanced polyamine levels in susceptible but not resistant wheat.

Subramanyam S, Sardesai N, Minocha SC, Zheng C, Shukle RH, Williams CE - BMC Plant Biol. (2015)

Bottom Line: A concurrent increase in polyamine levels occurred in the virulent larvae despite a decrease in abundance of Mdes-odc (ornithine decarboxylase) transcript encoding a key enzyme in insect putrescine biosynthesis.In contrast, resistant wheat and avirulent Hessian fly larvae did not exhibit significant changes in transcript abundance of genes involved in polyamine biosynthesis or in free polyamine levels.The major findings from this study are: (i) although polyamines contribute to defense in some plant-pathogen interactions, their production is induced in susceptible wheat during interactions with Hessian fly larvae without contributing to defense, and (ii) due to low abundance of transcripts encoding the rate-limiting ornithine decarboxylase enzyme in the larval polyamine pathway the source of polyamines found in virulent larvae is plausibly wheat-derived.

View Article: PubMed Central - PubMed

Affiliation: Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA. shubha@purdue.edu.

ABSTRACT

Background: Hessian fly (Mayetiola destructor), a member of the gall midge family, is one of the most destructive pests of wheat (Triticum aestivum) worldwide. Probing of wheat plants by the larvae results in either an incompatible (avirulent larvae, resistant plant) or a compatible (virulent larvae, susceptible plant) interaction. Virulent larvae induce the formation of a nutritive tissue, resembling the inside surface of a gall, in susceptible wheat. These nutritive cells are a rich source of proteins and sugars that sustain the developing virulent Hessian fly larvae. In addition, on susceptible wheat, larvae trigger a significant increase in levels of amino acids including proline and glutamic acid, which are precursors for the biosynthesis of ornithine and arginine that in turn enter the pathway for polyamine biosynthesis.

Results: Following Hessian fly larval attack, transcript abundance in susceptible wheat increased for several genes involved in polyamine biosynthesis, leading to higher levels of the free polyamines, putrescine, spermidine and spermine. A concurrent increase in polyamine levels occurred in the virulent larvae despite a decrease in abundance of Mdes-odc (ornithine decarboxylase) transcript encoding a key enzyme in insect putrescine biosynthesis. In contrast, resistant wheat and avirulent Hessian fly larvae did not exhibit significant changes in transcript abundance of genes involved in polyamine biosynthesis or in free polyamine levels.

Conclusions: The major findings from this study are: (i) although polyamines contribute to defense in some plant-pathogen interactions, their production is induced in susceptible wheat during interactions with Hessian fly larvae without contributing to defense, and (ii) due to low abundance of transcripts encoding the rate-limiting ornithine decarboxylase enzyme in the larval polyamine pathway the source of polyamines found in virulent larvae is plausibly wheat-derived. The activation of the host polyamine biosynthesis pathway during compatible wheat-Hessian fly interactions is consistent with a model wherein the virulent larvae usurp the polyamine biosynthesis machinery of the susceptible plant to acquire nutrients required for their own growth and development.

No MeSH data available.


Related in: MedlinePlus

Specific activity of wheat Hfr-SAMDC (s-adenosyl methionine decarboxylase) inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Hfr-SAMDC enzymatic activity was measured in wheat crown tissue (leaf 2). Data are presented as mean ± SE. Statistically significant (p < 0.05) differences between infested and uninfested control are indicated by ‘*’ with fold-change values.
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Fig5: Specific activity of wheat Hfr-SAMDC (s-adenosyl methionine decarboxylase) inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Hfr-SAMDC enzymatic activity was measured in wheat crown tissue (leaf 2). Data are presented as mean ± SE. Statistically significant (p < 0.05) differences between infested and uninfested control are indicated by ‘*’ with fold-change values.

Mentions: Increase in Hfr-samdc transcript abundance (Figure 3d) resulted in higher Hfr-SAMDC enzyme activity in the susceptible wheat line after Hessian fly attack. Significantly higher levels of Hfr-SAMDC activity were detected in the infested susceptible plants than in uninfested controls at 6 (5.6-fold, p = 0.0032) and 8 (3.5-fold, p = 0.0256) DAH (Figure 5). Although Hfr-SAMDC transcripts were significantly higher at 4 DAH in susceptible wheat (2.2-fold, p < 0.001, Figure 3), significant increases in Hfr-SAMDC enzyme activity were not detected until later. At no time did Hfr-SAMDC activity significantly differ (p > 0.4) between the resistant and their uninfested control plants (Figure 5).Figure 5


Hessian fly larval feeding triggers enhanced polyamine levels in susceptible but not resistant wheat.

Subramanyam S, Sardesai N, Minocha SC, Zheng C, Shukle RH, Williams CE - BMC Plant Biol. (2015)

Specific activity of wheat Hfr-SAMDC (s-adenosyl methionine decarboxylase) inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Hfr-SAMDC enzymatic activity was measured in wheat crown tissue (leaf 2). Data are presented as mean ± SE. Statistically significant (p < 0.05) differences between infested and uninfested control are indicated by ‘*’ with fold-change values.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4308891&req=5

Fig5: Specific activity of wheat Hfr-SAMDC (s-adenosyl methionine decarboxylase) inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Hfr-SAMDC enzymatic activity was measured in wheat crown tissue (leaf 2). Data are presented as mean ± SE. Statistically significant (p < 0.05) differences between infested and uninfested control are indicated by ‘*’ with fold-change values.
Mentions: Increase in Hfr-samdc transcript abundance (Figure 3d) resulted in higher Hfr-SAMDC enzyme activity in the susceptible wheat line after Hessian fly attack. Significantly higher levels of Hfr-SAMDC activity were detected in the infested susceptible plants than in uninfested controls at 6 (5.6-fold, p = 0.0032) and 8 (3.5-fold, p = 0.0256) DAH (Figure 5). Although Hfr-SAMDC transcripts were significantly higher at 4 DAH in susceptible wheat (2.2-fold, p < 0.001, Figure 3), significant increases in Hfr-SAMDC enzyme activity were not detected until later. At no time did Hfr-SAMDC activity significantly differ (p > 0.4) between the resistant and their uninfested control plants (Figure 5).Figure 5

Bottom Line: A concurrent increase in polyamine levels occurred in the virulent larvae despite a decrease in abundance of Mdes-odc (ornithine decarboxylase) transcript encoding a key enzyme in insect putrescine biosynthesis.In contrast, resistant wheat and avirulent Hessian fly larvae did not exhibit significant changes in transcript abundance of genes involved in polyamine biosynthesis or in free polyamine levels.The major findings from this study are: (i) although polyamines contribute to defense in some plant-pathogen interactions, their production is induced in susceptible wheat during interactions with Hessian fly larvae without contributing to defense, and (ii) due to low abundance of transcripts encoding the rate-limiting ornithine decarboxylase enzyme in the larval polyamine pathway the source of polyamines found in virulent larvae is plausibly wheat-derived.

View Article: PubMed Central - PubMed

Affiliation: Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA. shubha@purdue.edu.

ABSTRACT

Background: Hessian fly (Mayetiola destructor), a member of the gall midge family, is one of the most destructive pests of wheat (Triticum aestivum) worldwide. Probing of wheat plants by the larvae results in either an incompatible (avirulent larvae, resistant plant) or a compatible (virulent larvae, susceptible plant) interaction. Virulent larvae induce the formation of a nutritive tissue, resembling the inside surface of a gall, in susceptible wheat. These nutritive cells are a rich source of proteins and sugars that sustain the developing virulent Hessian fly larvae. In addition, on susceptible wheat, larvae trigger a significant increase in levels of amino acids including proline and glutamic acid, which are precursors for the biosynthesis of ornithine and arginine that in turn enter the pathway for polyamine biosynthesis.

Results: Following Hessian fly larval attack, transcript abundance in susceptible wheat increased for several genes involved in polyamine biosynthesis, leading to higher levels of the free polyamines, putrescine, spermidine and spermine. A concurrent increase in polyamine levels occurred in the virulent larvae despite a decrease in abundance of Mdes-odc (ornithine decarboxylase) transcript encoding a key enzyme in insect putrescine biosynthesis. In contrast, resistant wheat and avirulent Hessian fly larvae did not exhibit significant changes in transcript abundance of genes involved in polyamine biosynthesis or in free polyamine levels.

Conclusions: The major findings from this study are: (i) although polyamines contribute to defense in some plant-pathogen interactions, their production is induced in susceptible wheat during interactions with Hessian fly larvae without contributing to defense, and (ii) due to low abundance of transcripts encoding the rate-limiting ornithine decarboxylase enzyme in the larval polyamine pathway the source of polyamines found in virulent larvae is plausibly wheat-derived. The activation of the host polyamine biosynthesis pathway during compatible wheat-Hessian fly interactions is consistent with a model wherein the virulent larvae usurp the polyamine biosynthesis machinery of the susceptible plant to acquire nutrients required for their own growth and development.

No MeSH data available.


Related in: MedlinePlus