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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 polyamine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-odc, b)Hfr-spds, c)Ta-sams, and d)Hfr-samdc in crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to uninfested control (baseline of 0) plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
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Fig3: Abundance of polyamine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-odc, b)Hfr-spds, c)Ta-sams, and d)Hfr-samdc in crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to uninfested control (baseline of 0) plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.

Mentions: The biosynthesis of putrescine, spermidine and spermine from amino acids involves several enzymatic steps. To determine which of the genes in the polyamine biosynthesis pathway are activated by Hessian fly infestation we carried out RT-qPCR expression studies (Figure 3). In susceptible Newton wheat infested with biotype L, transcripts encoding ornithine decarboxylase (Ta-odc), s-adenosylmethionine synthetase (Ta-sams) and s-adenosylmethionine decarboxylase (Hfr-samdc) were significantly responsive over time from 2 through 8 DAH compared to the uninfested controls. While arginine decarboxylase (Ta-adc) did not show an increase in transcript abundance (data not shown), spermidine synthase (Hfr-spds) showed a small but significant increase only at later times (Figure 3b). In contrast, in the resistant H9-Iris wheat line only transcripts for Ta-odc accumulated to significantly higher levels than the uninfested control following attack by the avirulent larvae (Figure 3a). Transcript levels of polyamine oxidase (Ta-pao), involved in the catabolism of polyamines did not show any change in either susceptible or resistant wheat (data not shown). Transcriptional profiling studies carried out in other wheat genotypes infested with either a different Hessian fly biotype or harboring a different R gene (vH9 on H9-Iris wheat, Additional file 1; vH13 on H13-wheat, Additional file 2) yielded very similar patterns of expression with significant accumulation of polyamine pathway transcripts during compatible interactions.Figure 3


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 polyamine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-odc, b)Hfr-spds, c)Ta-sams, and d)Hfr-samdc in crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to uninfested control (baseline of 0) 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

Fig3: Abundance of polyamine biosynthesis pathway transcripts inH9-Irisand Newton wheat infested with biotype L Hessian fly larvae. Transcript levels of a)Ta-odc, b)Hfr-spds, c)Ta-sams, and d)Hfr-samdc in crown tissue (leaf 2) quantified by RT-qPCR. Values are the log fold-change ± SE of infested compared to uninfested control (baseline of 0) plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
Mentions: The biosynthesis of putrescine, spermidine and spermine from amino acids involves several enzymatic steps. To determine which of the genes in the polyamine biosynthesis pathway are activated by Hessian fly infestation we carried out RT-qPCR expression studies (Figure 3). In susceptible Newton wheat infested with biotype L, transcripts encoding ornithine decarboxylase (Ta-odc), s-adenosylmethionine synthetase (Ta-sams) and s-adenosylmethionine decarboxylase (Hfr-samdc) were significantly responsive over time from 2 through 8 DAH compared to the uninfested controls. While arginine decarboxylase (Ta-adc) did not show an increase in transcript abundance (data not shown), spermidine synthase (Hfr-spds) showed a small but significant increase only at later times (Figure 3b). In contrast, in the resistant H9-Iris wheat line only transcripts for Ta-odc accumulated to significantly higher levels than the uninfested control following attack by the avirulent larvae (Figure 3a). Transcript levels of polyamine oxidase (Ta-pao), involved in the catabolism of polyamines did not show any change in either susceptible or resistant wheat (data not shown). Transcriptional profiling studies carried out in other wheat genotypes infested with either a different Hessian fly biotype or harboring a different R gene (vH9 on H9-Iris wheat, Additional file 1; vH13 on H13-wheat, Additional file 2) yielded very similar patterns of expression with significant accumulation of polyamine pathway transcripts during compatible interactions.Figure 3

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