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Hessian fly larval feeding triggers enhanced polyamine levels in susceptible but not resistant wheat.
BMC Plant Biol. 2015 Jan 16; 15:3.BP

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.

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Authors+Show Affiliations

Subramanyam S
Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA. shubha@purdue.edu.
Sardesai N
Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA. nsardesai@dow.com. Present address: Dow AgroSciences LLC, Indianapolis, IN, 46268, USA. nsardesai@dow.com.
Minocha SC
Department of Biological Sciences, University of New Hampshire, Durham, NH, 03824, USA. Subhash.Minocha@unh.edu.
Zheng C
Department of Statistics, Purdue University, West Lafayette, IN, 47907, USA. zhengcheng@gmail.com. Present address: Novartis Pharmaceuticals Corporation, East Hanover, NJ, 07936, USA. zhengcheng@gmail.com.
Shukle RH
Department of Entomology, Purdue University, West Lafayette, IN, 47907, USA. shukle@purdue.edu. USDA-ARS Crop Production and Pest Control Research Unit, West Lafayette, IN, 47907, USA. shukle@purdue.edu.
Williams CE
Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA. christie.williams@ars.usda.gov. USDA-ARS Crop Production and Pest Control Research Unit, West Lafayette, IN, 47907, USA. christie.williams@ars.usda.gov.

MeSH

Adenosylmethionine DecarboxylaseAmino AcidsAnimalsBiosynthetic PathwaysDipteraEflornithineGene Expression Regulation, PlantGenes, PlantHerbivoryLarvaModels, BiologicalOrnithineOrnithine DecarboxylasePhylogenyPlant DiseasesPolyaminesRNA, MessengerTriticumVirulence

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

25592131

Citation

Subramanyam, Subhashree, et al. "Hessian Fly Larval Feeding Triggers Enhanced Polyamine Levels in Susceptible but Not Resistant Wheat." BMC Plant Biology, vol. 15, 2015, p. 3.
Subramanyam S, Sardesai N, Minocha SC, et al. Hessian fly larval feeding triggers enhanced polyamine levels in susceptible but not resistant wheat. BMC Plant Biol. 2015;15:3.
Subramanyam, S., Sardesai, N., Minocha, S. C., Zheng, C., Shukle, R. H., & Williams, C. E. (2015). Hessian fly larval feeding triggers enhanced polyamine levels in susceptible but not resistant wheat. BMC Plant Biology, 15, 3. https://doi.org/10.1186/s12870-014-0396-y
Subramanyam S, et al. Hessian Fly Larval Feeding Triggers Enhanced Polyamine Levels in Susceptible but Not Resistant Wheat. BMC Plant Biol. 2015 Jan 16;15:3. PubMed PMID: 25592131.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Hessian fly larval feeding triggers enhanced polyamine levels in susceptible but not resistant wheat. AU - Subramanyam,Subhashree, AU - Sardesai,Nagesh, AU - Minocha,Subhash C, AU - Zheng,Cheng, AU - Shukle,Richard H, AU - Williams,Christie E, Y1 - 2015/01/16/ PY - 2014/09/18/received PY - 2014/12/22/accepted PY - 2015/1/17/entrez PY - 2015/1/17/pubmed PY - 2016/3/29/medline SP - 3 EP - 3 JF - BMC plant biology JO - BMC Plant Biol VL - 15 N2 - 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. SN - 1471-2229 UR - https://www.unboundmedicine.com/medline/citation/25592131/Hessian_fly_larval_feeding_triggers_enhanced_polyamine_levels_in_susceptible_but_not_resistant_wheat_ DB - PRIME DP - Unbound Medicine ER -