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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

Hessian fly larval responses to inhibition of wheat ODC activity with Difluoromethylornithine (DFMO). a) Length of biotype L larvae (measured 7 DAH) feeding on susceptible Newton wheat plants that were pretreated with 1, 3 and 5 mM concentrations of DFMO to block wheat ODC activity. Data are represented as mean larval length ± SE for the respective number of larvae (given above each bar) measured for each treatment. Treatments showing statistically significant (p < 0.05) differences between DFMO-treated and untreated plants (0 mM DFMO) are indicated with ‘*’. b) Representative photomicrographs of biotype L Hessian fly larvae from each of the treatments. c) Mean percentage ± SE for the respective number (given above each bar) of insects for each treatment in larval (solid filled bars) or pupal stages (striped bars) on treated susceptible Newton wheat plants 18 DAH. Treatments showing statistically significant (p < 0.05) differences from the control (0 mM DFMO) are indicated with ‘*’.
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Fig7: Hessian fly larval responses to inhibition of wheat ODC activity with Difluoromethylornithine (DFMO). a) Length of biotype L larvae (measured 7 DAH) feeding on susceptible Newton wheat plants that were pretreated with 1, 3 and 5 mM concentrations of DFMO to block wheat ODC activity. Data are represented as mean larval length ± SE for the respective number of larvae (given above each bar) measured for each treatment. Treatments showing statistically significant (p < 0.05) differences between DFMO-treated and untreated plants (0 mM DFMO) are indicated with ‘*’. b) Representative photomicrographs of biotype L Hessian fly larvae from each of the treatments. c) Mean percentage ± SE for the respective number (given above each bar) of insects for each treatment in larval (solid filled bars) or pupal stages (striped bars) on treated susceptible Newton wheat plants 18 DAH. Treatments showing statistically significant (p < 0.05) differences from the control (0 mM DFMO) are indicated with ‘*’.

Mentions: To study the effects of limiting wheat polyamine production on virulent Hessian fly larval growth, we used DFMO to inhibit ODC enzymatic activity of the susceptible host plants. The larvae were prevented from coming into direct contact with the applied DFMO because the blade of the first leaf was painted with the inhibitor and allowed to dry before adult flies were released onto the plant. The eggs were oviposited on the second leaf blade ensuring lack of direct contact with the DFMO. Since peak abundance of most polyamines as well as the transcripts encoding the enzymes were observed between 4 and 8 DAH, larval length measurements were taken 7 DAH. The larvae growing on plants treated with 3 or 5 mM DFMO were significantly smaller (p < 0.0001) compared to larvae on untreated plants (Figure 7a-b). No significant difference (p = 0.4667) was seen in the size of larvae growing on plants treated with 1 mM DFMO. In addition, at concentrations of 3 and 5 mM DFMO the percentage of insects that had reached pupation 18 DAH was significantly lower (Figure 7c) indicating delayed larval development. Larvae inhabiting plants treated with 1 mM DFMO did not exhibit significant differences in pupation rate as compared to the control (Figure 7c).Figure 7


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)

Hessian fly larval responses to inhibition of wheat ODC activity with Difluoromethylornithine (DFMO). a) Length of biotype L larvae (measured 7 DAH) feeding on susceptible Newton wheat plants that were pretreated with 1, 3 and 5 mM concentrations of DFMO to block wheat ODC activity. Data are represented as mean larval length ± SE for the respective number of larvae (given above each bar) measured for each treatment. Treatments showing statistically significant (p < 0.05) differences between DFMO-treated and untreated plants (0 mM DFMO) are indicated with ‘*’. b) Representative photomicrographs of biotype L Hessian fly larvae from each of the treatments. c) Mean percentage ± SE for the respective number (given above each bar) of insects for each treatment in larval (solid filled bars) or pupal stages (striped bars) on treated susceptible Newton wheat plants 18 DAH. Treatments showing statistically significant (p < 0.05) differences from the control (0 mM DFMO) are indicated with ‘*’.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig7: Hessian fly larval responses to inhibition of wheat ODC activity with Difluoromethylornithine (DFMO). a) Length of biotype L larvae (measured 7 DAH) feeding on susceptible Newton wheat plants that were pretreated with 1, 3 and 5 mM concentrations of DFMO to block wheat ODC activity. Data are represented as mean larval length ± SE for the respective number of larvae (given above each bar) measured for each treatment. Treatments showing statistically significant (p < 0.05) differences between DFMO-treated and untreated plants (0 mM DFMO) are indicated with ‘*’. b) Representative photomicrographs of biotype L Hessian fly larvae from each of the treatments. c) Mean percentage ± SE for the respective number (given above each bar) of insects for each treatment in larval (solid filled bars) or pupal stages (striped bars) on treated susceptible Newton wheat plants 18 DAH. Treatments showing statistically significant (p < 0.05) differences from the control (0 mM DFMO) are indicated with ‘*’.
Mentions: To study the effects of limiting wheat polyamine production on virulent Hessian fly larval growth, we used DFMO to inhibit ODC enzymatic activity of the susceptible host plants. The larvae were prevented from coming into direct contact with the applied DFMO because the blade of the first leaf was painted with the inhibitor and allowed to dry before adult flies were released onto the plant. The eggs were oviposited on the second leaf blade ensuring lack of direct contact with the DFMO. Since peak abundance of most polyamines as well as the transcripts encoding the enzymes were observed between 4 and 8 DAH, larval length measurements were taken 7 DAH. The larvae growing on plants treated with 3 or 5 mM DFMO were significantly smaller (p < 0.0001) compared to larvae on untreated plants (Figure 7a-b). No significant difference (p = 0.4667) was seen in the size of larvae growing on plants treated with 1 mM DFMO. In addition, at concentrations of 3 and 5 mM DFMO the percentage of insects that had reached pupation 18 DAH was significantly lower (Figure 7c) indicating delayed larval development. Larvae inhabiting plants treated with 1 mM DFMO did not exhibit significant differences in pupation rate as compared to the control (Figure 7c).Figure 7

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