Gall-forming arthropods are highly specialized herbivores that, in combination with their hosts, produce extended phenotypes with unique morphologies [1]. Many are economically important, and others have improved our understanding of ecology and adaptive radiation [2]. However, the mechanisms that these arthropods use to induce plant galls are poorly understood. We sequenced the genome of the Hessian fly (Mayetiola destructor; Diptera: Cecidomyiidae), a plant parasitic gall midge and a pest of wheat (Triticum spp.), with the aim of identifying genic modifications that contribute to its plant-parasitic lifestyle. Among several adaptive modifications, we discovered an expansive reservoir of potential effector proteins. Nearly 5% of the 20,163 predicted gene models matched putative effector gene transcripts present in the M. destructor larval salivary gland. Another 466 putative effectors were discovered among the genes that have no sequence similarities in other organisms. The largest known arthropod gene family (family SSGP-71) was also discovered within the effector reservoir. SSGP-71 proteins lack sequence homologies to other proteins, but their structures resemble both ubiquitin E3 ligases in plants and E3-ligase-mimicking effectors in plant pathogenic bacteria. SSGP-71 proteins and wheat Skp proteins interact in vivo. Mutations in different SSGP-71 genes avoid the effector-triggered immunity that is directed by the wheat resistance genes H6 and H9. Results point to effectors as the agents responsible for arthropod-induced plant gall formation.
Gall midges constitute an important group of plant-parasitic insects. The Hessian fly (HF; Mayetiola destructor), the most investigated gall midge, was the first insect hypothesized to have a gene-for-gene interaction with its host plant, wheat (Triticum spp.). Recent investigations support that hypothesis. The minute larval mandibles appear to act in a manner that is analogous to nematode stylets and the haustoria of filamentous plant pathogens. Putative effector proteins are encoded by hundreds of genes and expressed in the HF larval salivary gland. Cultivar-specific resistance (R) genes mediate a highly localized plant reaction that prevents the survival of avirulent HF larvae. Fine-scale mapping of HF avirulence (Avr) genes provides further evidence of effector-triggered immunity (ETI) against HF in wheat. Taken together, these discoveries suggest that the HF, and other gall midges, may be considered biotrophic, or hemibiotrophic, plant pathogens, and they demonstrate the potential that the wheat-HF interaction has in the study of insect-induced plant gall formation.
Herbivorous insect species are constantly challenged with reactive oxygen species (ROS) generated from endogenous and exogenous sources. ROS produced within insects because of stress and prooxidant allelochemicals produced by host plants in response to herbivory require a complex mode of antioxidant defense during insect/plant interactions. Some insect herbivores have a midgutbased defense against the suite of ROS encountered. Because the Hessian fly (Mayetiola destructor) is the major insect pest of wheat worldwide, and an emerging model for all gall midges, we investigated its antioxidant responses during interaction with its host plant. Quantitative data for two phospholipid glutathione peroxidases (MdesPHGPX-1 and MdesPHGPX-2), two catalases (MdesCAT-1 and MdesCAT-2), and two superoxide dismutases (MdesSOD-1 and MdesSOD-2) revealed high levels of all of the mRNAs in the midgut of larvae on susceptible wheat (compatible interaction). During development of the Hessian fly on susceptible wheat, a differential expression pattern was observed for all six genes. Analysis of larvae on resistant wheat (incompatible interaction) compared with larvae on susceptible wheat showed increased levels of mRNAs in larvae on resistant wheat for all of the antioxidant genes except MdesSOD-1 and MdesSOD-2. We postulate that the increased mRNA levels of MdesPHGPX-1, MdesPH-GPX-2, MdesCAT-1, and MdesCAT-2 reflect responses to ROS encountered by larvae while feeding on resistant wheat seedlings and/or ROS generated endogenously in larvae because of stress/ starvation. These results provide an opportunity to understand the cooperative antioxidant defense responses in the Hessian fly/ wheat interaction and may be applicable to other insect/plant interactions.Hessian fly ͉ insect/plant interaction ͉ reactive oxygen species ͉ wheat
BackgroundIn most protein-coding genes, greater sequence variation is observed in noncoding regions (introns and untranslated regions) than in coding regions due to selective constraints. During characterization of genes and transcripts encoding small secreted salivary gland proteins (SSSGPs) from the Hessian fly, we found exactly the opposite pattern of conservation in several families of genes: the non-coding regions were highly conserved, but the coding regions were highly variable.ResultsSeven genes from the SSSGP-1 family are clustered as one inverted and six tandem repeats within a 15 kb region of the genome. Except for SSSGP-1A2, a gene that encodes a protein identical to that encoded by SSSGP-1A1, the other six genes consist of a highly diversified, mature protein-coding region as well as highly conserved regions including the promoter, 5'- and 3'-UTRs, a signal peptide coding region, and an intron. This unusual pattern of highly diversified coding regions coupled with highly conserved regions in the rest of the gene was also observed in several other groups of SSSGP-encoding genes or cDNAs. The unusual conservation pattern was also found in some of the SSSGP cDNAs from the Asian rice gall midge, but not from the orange wheat blossom midge. Strong positive selection was one of the forces driving for diversification whereas concerted homogenization was likely a mechanism for sequence conservation.ConclusionRapid diversification in mature SSSGPs suggests that the genes are under selection pressure for functional adaptation. The conservation in the noncoding regions of these genes including introns also suggested potential mechanisms for sequence homogenization that are not yet fully understood. This report should be useful for future studies on genetic mechanisms involved in evolution and functional adaptation of parasite genes.
Salivary secretions of neonate Hessian fly larvae initiate a two-way exchange of molecules with their wheat host. Changes in properties of the leaf surface allow larval effectors to enter the plant where they trigger plant processes leading to resistance and delivery of defence molecules, or susceptibility and delivery of nutrients. To increase understanding of the host plant's response, the timing and characteristics of the induced epidermal permeability were investigated. Resistant plant permeability was transient and limited in area, persisting just long enough to deliver defence molecules before gene expression and permeability reverted to pre-infestation levels. The abundance of transcripts for GDSL-motif lipase/hydrolase, thought to contribute to cuticle reorganization and increased permeability, followed the same temporal profile as permeability in resistant plants. In contrast, susceptible plants continued to increase in permeability over time until the entire crown of the plant became a nutrient sink. Permeability increased with higher infestation levels in susceptible but not in resistant plants. The ramifications of induced plant permeability on Hessian fly populations are discussed.
Genetic similarities between plant interactions with microbial pathogens and wheat interactions with Hessian fly larvae prompted us to investigate defense and counterdefense mechanisms. Plant oxidative burst, a rapid increase in the levels of active oxygen species (AOS) within the initial 24 h of an interaction with pathogens, commonly is associated with defenses that are triggered by gene-for-gene recognition events similar to those involving wheat and Hessian fly larvae. RNAs encoded by Hessian fly superoxide dismutase (SOD) and catalase (CAT) genes, involved in detoxification of AOS, increased in first-instar larvae during both compatible and incompatible interactions. However, mRNA levels of a wheat NADPH oxidase (NOX) gene that generates superoxide (O2-) did not increase. In addition, inhibiting wheat NOX enzyme with diphenyleneiodonium did not result in increased survival of avirulent larvae. However, nitro blue tetrazolium staining indicated that basal levels of O2- are present in both uninfested and infested wheat tissue. mRNA encoded by wheat genes involved in detoxification of the cellular environment, SOD, CAT, and glutathione-S-transferase did not increase in abundance. Histochemical staining with 3,3-diaminobenzidine revealed no increases in wheat hydrogen peroxide (H2O2) during infestation that were correlated with the changes in larval SOD and CAT mRNA. However, treatment with 2',7'-dichlorofluorescin demonstrated the presence of basal levels of H2O2 in the elongation zone of both infested and uninfested plants. The accumulation of a wheat flavanone 3-hydroxylase mRNA did show some parallels with larval gene mRNA profiles. These results suggested that larvae encounter stresses imposed by mechanisms other than an oxidative burst in wheat seedlings.
BackgroundHessian 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.ResultsFollowing 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0396-y) contains supplementary material, which is available to authorized users.
Feeding behavior of Sitobion avenae F. (Homoptera: Aphididae) on oats (Avena sativa cv. ‘Clintland 64’) was electronically monitored, and waveforms corresponding to salivation, ingestion, and sieve element penetration described. During 90 min plant access, aphids ingested from phloem for 0–43 min (mean: 8.1 min) and non‐phloem for 0–60 min (mean: 19 min). Only 65% of the aphids tested made phloem contact within 90 min, contacting phloem after 18–85 min (mean: 32 min). No significant difference was observed in the feeding behavior of aphids carrying barley yellow dwarf virus (BYDV) from that of non‐viruliferous aphids. Penetration of a sieve element was a prerequisite for BYDV transmission but did not insure transmission. Penetration of one sieve element resulted in a 65% chance of transmission independent of the duration of phloem contact. The chance of transmission increased with increasing number of sieve element penetrations. Inoculation of oat seedlings with single, viruliferous aphids for 90 min is estimated to cause 54% of the plants to be infected. Also, it is estimated that no transmission can occur with plant access periods shorter than 17 min. Zusammenfassung Sitobion avenae auf Hafer: Probeverhalten und Übertragung des Barley Yellow Dwarf Virus Das Probeverhalten von Sitobion avenae F. (Homoptera: Aphididae) auf Hafer (Sorte ‘Clint‐land 64’) wurden elektronisch verfolgt. Drei Wellenformen (S = Speichelfluss, X = das Eindringen in ein Siebelement, I = Nahrungsaufname) wurden registriert. In histologischen Untersuchungen wurden diese Wellenformen mit der Position der Stechborsten korreliert. Wenn X‐Wellen oder eine X‐I‐Folge registriert wurden, war die Stechborste immer im Phloëm; bei S‐Wellen oder bei einer S‐I‐Folge, war die Stechborste nie im Phloëm. Die Blattläuse wurden auf gesunden, fünf Tage alten Pflanzen während 90 Min beobachtet. 65% der Blattläuse erreichten nach 18–85 Min (Durchschnitt 32 Min) das Phloëm. Innerhalb 90 Min nahmen die Blattläuse während 0–43 Min (Durchschnitt 8.1 Min) Saft aus dem Phloem und während 0–60 Min (Durchschnitt 19 Min) Saft aus dem Mesophyll auf. Keine signifikanten Unterschiede im Probeverhalten wurden bei Blattläusen mit und ohne Barley Yellow Dwarf Virus (BYDV) festgestellt. Blattläuse, die innerhalb 24 Stunden BYDV übermitteln können, wurden für Übertragungsversuche verwendet. Das Probeverhalten dieser Blattläuser wurde manipuliert, und die Leistungsfähigkeit der Übertragung mit einer immunologischen Technik (ELISA) untersucht. Um BYDV zu übertragen mussten die Blattläuse mit einem Siebelement in Kontakt kommen. Nach der Stechborstenpenetration in ein Siebelement wurden 65% der Pflanzen mit BYDV infiziert. Der Prozentsatz infizierter Pflanzen und der Virustiter in den infizierten Pflanzen waren mit der Dauer der Siebelementpenetration (Anzahl von X‐Wellen) nicht proportional. Wenn die Blattläuse mit zwei oder drei Siebelementen in Kontakt kamen, wurde der Prozentsatz infizierter Pflanzen signifikant erhöht, während der Virustiter nich verändert wurde. In...
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