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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

Abundance of ornithine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-p5cs, b)Ta-glr, and c)Ta-aor from crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to the uninfested control plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
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Fig4: Abundance of ornithine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-p5cs, b)Ta-glr, and c)Ta-aor from crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to the uninfested control plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.

Mentions: Expression (RT-qPCR) studies revealed increased abundance of transcripts encoding enzymes catalyzing the conversion of the precursor amino acids proline and glutamic acid to ornithine (Figure 4). Transcripts for genes encoding pyrroline-5-carboxylate synthetase (Ta-p5cs), glutamate reductase (Ta-glr) and acetylornithinase (Ta-aor) were most responsive in the susceptible Newton wheat (Figure 4), whereas transcripts of pyrroline-5-carboxylate reductase (Ta-p5cr), arginase (Ta-arg), and ornithine aminotransferase (Ta-oat), showed a minimal transient response (Additional file 3). A similar expression profile was observed in other wheat genotypes infested with different fly biotypes also resulting in compatible interactions (Additional files 4 and 5). However, unlike the H9-wheat, the H13-wheat transcript abundance increased for Ta-oat and decreased for Ta-glr.Figure 4


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)

Abundance of ornithine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-p5cs, b)Ta-glr, and c)Ta-aor from crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to the uninfested control plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Abundance of ornithine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-p5cs, b)Ta-glr, and c)Ta-aor from crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to the uninfested control plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
Mentions: Expression (RT-qPCR) studies revealed increased abundance of transcripts encoding enzymes catalyzing the conversion of the precursor amino acids proline and glutamic acid to ornithine (Figure 4). Transcripts for genes encoding pyrroline-5-carboxylate synthetase (Ta-p5cs), glutamate reductase (Ta-glr) and acetylornithinase (Ta-aor) were most responsive in the susceptible Newton wheat (Figure 4), whereas transcripts of pyrroline-5-carboxylate reductase (Ta-p5cr), arginase (Ta-arg), and ornithine aminotransferase (Ta-oat), showed a minimal transient response (Additional file 3). A similar expression profile was observed in other wheat genotypes infested with different fly biotypes also resulting in compatible interactions (Additional files 4 and 5). However, unlike the H9-wheat, the H13-wheat transcript abundance increased for Ta-oat and decreased for Ta-glr.Figure 4

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