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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 Hessian fly larval transcripts for polyamine biosynthesis. Transcript levels of a)Mdes-odc, b)Mdes-samdc, c)Mdes-spds, and d)Mdes-spms were quantified by RT-qPCR. Values are the log fold-change ± SE for avirulent and virulent Hessian fly larvae that have fed on host plants compared to neonate larvae (collected on the day of egg hatch; baseline of 0) that had not fed on plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
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Fig6: Abundance of Hessian fly larval transcripts for polyamine biosynthesis. Transcript levels of a)Mdes-odc, b)Mdes-samdc, c)Mdes-spds, and d)Mdes-spms were quantified by RT-qPCR. Values are the log fold-change ± SE for avirulent and virulent Hessian fly larvae that have fed on host plants compared to neonate larvae (collected on the day of egg hatch; baseline of 0) that had not fed on plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.

Mentions: As polyamine levels of susceptible wheat increased, so did polyamine levels in the virulent Hessian fly larvae. To ascertain whether increased larval polyamine levels were caused by activation of polyamine pathway genes in the larvae or whether larval polyamines were plant-derived we carried out RT-qPCR studies to look at expression of Mdes-odc, Mdes-samdc, Mdes-spds and Mdes-spms genes in the virulent and avirulent Hessian fly larvae. Expression levels were compared to those in neonate larvae that had never fed on a wheat plant. ODC is considered the rate-determining enzyme in polyamine biosynthesis; however, transcripts for Mdes-odc were significantly less abundant in virulent larvae than in the neonate larvae (Figure 6a). In contrast, transcripts for the other three genes increased greatly (Figure 6b-d) in abundance 2–4 DAH (once the virulent larvae had established feeding sites), indicating an increased capacity, especially for spermidine production, through non-Mdes-odc entry points. The abundance of Mdes-samdc, Mdes-spds and Mdes-spms transcripts gradually decreased by 8 DAH in virulent larvae (Figure 6b-d). In the avirulent Hessian fly larvae, transcripts for all four genes under study were significantly lower at all stages of development as compared to the neonate larvae (Figure 6a-d).Figure 6


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 Hessian fly larval transcripts for polyamine biosynthesis. Transcript levels of a)Mdes-odc, b)Mdes-samdc, c)Mdes-spds, and d)Mdes-spms were quantified by RT-qPCR. Values are the log fold-change ± SE for avirulent and virulent Hessian fly larvae that have fed on host plants compared to neonate larvae (collected on the day of egg hatch; baseline of 0) that had not fed on 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

Fig6: Abundance of Hessian fly larval transcripts for polyamine biosynthesis. Transcript levels of a)Mdes-odc, b)Mdes-samdc, c)Mdes-spds, and d)Mdes-spms were quantified by RT-qPCR. Values are the log fold-change ± SE for avirulent and virulent Hessian fly larvae that have fed on host plants compared to neonate larvae (collected on the day of egg hatch; baseline of 0) that had not fed on plants. Statistically significant (p < 0.05) differences are indicated by ‘*’ with linear fold-change values.
Mentions: As polyamine levels of susceptible wheat increased, so did polyamine levels in the virulent Hessian fly larvae. To ascertain whether increased larval polyamine levels were caused by activation of polyamine pathway genes in the larvae or whether larval polyamines were plant-derived we carried out RT-qPCR studies to look at expression of Mdes-odc, Mdes-samdc, Mdes-spds and Mdes-spms genes in the virulent and avirulent Hessian fly larvae. Expression levels were compared to those in neonate larvae that had never fed on a wheat plant. ODC is considered the rate-determining enzyme in polyamine biosynthesis; however, transcripts for Mdes-odc were significantly less abundant in virulent larvae than in the neonate larvae (Figure 6a). In contrast, transcripts for the other three genes increased greatly (Figure 6b-d) in abundance 2–4 DAH (once the virulent larvae had established feeding sites), indicating an increased capacity, especially for spermidine production, through non-Mdes-odc entry points. The abundance of Mdes-samdc, Mdes-spds and Mdes-spms transcripts gradually decreased by 8 DAH in virulent larvae (Figure 6b-d). In the avirulent Hessian fly larvae, transcripts for all four genes under study were significantly lower at all stages of development as compared to the neonate larvae (Figure 6a-d).Figure 6

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