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Gall Midges (Hessian Flies) as Plant Pathogens


Jeff J. Stuart,1 Ming-Shun Chen,2 Richard Shukle,3 and Marion O. Harris4
1 Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089; email: stuartjj@purdue.edu 2 USDA-ARS and Department of Entomology, Kansas State University, Manhattan, Kansas 66506; email: mchen@ksu.edu 3 USDA-ARS and Department of Entomology, Purdue University, West Lafayette, Indiana 47909-2089; email: shukle@purdue.edu 4 Department of Entomology, North Dakota State University, Fargo, North Dakota 58105; email: marion.harris@ndsu.edu

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Annu. Rev. Phytopathol. 2012. 50:33957 First published online as a Review in Advance on May 29, 2012 The Annual Review of Phytopathology is online at phyto.annualreviews.org This articles doi: 10.1146/annurev-phyto-072910-095255 Copyright c 2012 by Annual Reviews. All rights reserved 0066-4286/12/0908-0339$20.00

Keywords
Cecidomyiidae, gene-for-gene interaction, resistance gene, avirulence gene, effector proteins, nutritive tissue

Abstract
Gall midges constitute an important group of plant-parasitic insects. The Hessian y (HF; Mayetiola destructor), the most investigated gall midge, was the rst 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 lamentous plant pathogens. Putative effector proteins are encoded by hundreds of genes and expressed in the HF larval salivary gland. Cultivar-specic 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.

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INTRODUCTION
In 1970, Hatchett & Gallun reported that the genetic interaction between wheat (Triticum spp.) and Hessian y (HF; Mayetiola destructor) t the gene-for-gene model (57). This discovery rmly connected an insect to a concept that was of major interest in plant pathology. During the ensuing years, plant pathologists have made remarkable progress in understanding how plant immunity and pathogen effectors underlie gene-for-gene interactions (12, 62), but only a few reports tied the emerging paradigm to plant defense against insects (64). The most important of these included the discovery that the cloned Mi resistance (R) gene confers resistance to potato aphids and whiteies (86, 99), and the discovery that another cecidomyiid, the Asian rice gall midge (Orseolia oryzae), has a gene-for-gene interaction with rice (9, 13). The paucity of data has been attributed to the lack of good experimental systems (56); most plant-parasitic insects have simply not been amenable to classical genetic analysis. However, genomic technologies are changing this situation, permitting one to ask whether some insects are another form of plant pathogen, albeit with unique attributes (18, 59). This question brings us back to the HF, an insect that is both an important pest and increasingly amenable to genetic and genomic analyses. This review is centered on the hypothesis that gall midges use an effector-based strategy that is remarkably similar to the one used by plant-pathogenic organisms and the discoveries that support that hypothesis (Figure 1). Our goals are to review those aspects of the wheatHF interaction that are relevant to plant pathology and to present the capacity of the HF as an experimental model. The review is organized to present detailed pictures of both the compatible and incompatible wheat-HF interactions as well as what is known regarding the effectors, the R genes, and the avirulence (Avr) genes that underlie these interactions. We are convinced that the wheat-HF interaction has much to offer both plant pathologists and entomologists as a model for investigations of plant-insect

HF larva Salivary gland

Mandible Plant cell Cell wall

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Re

t sis

an

ce

E Modulation of host development

Chloroplast Cytoplasm

Nucleus

Figure 1 Diagram illustrating the hypothesized wheat Hessian y (HF) interaction, modeled after Torto-Alalibo et al. (115). The rst-instar HF larva delivers effector proteins (E) produced in its salivary gland through highly modied mandibles into or just below the cell walls of expanding leaf sheath epidermal cells. Direct or indirect interactions with resistance proteins (R) elicit resistance responses that kill the larva. In the absence of cognate resistance proteins, the effectors defeat host defense and induce plant galling.

interactions and insect-induced plant gall formation. Because the HF is a gall midge, a relatively large, understudied, and economically important group of insects (43, 44), we begin with a brief description of the biology of the gall midge family (Cecidomyiidae), giving emphasis to the evolution of the gall-forming habit.

GALL MIDGE BIOLOGY


The gall midges (Diptera: Cecidomyiidae) belong to the lower Diptera (the Nematocera), which includes other midges, black ies, gnats, and mosquitoes (97). They likely arose during the Cretaceous period and are probably

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most closely related to mycetophilids and fungus gnats (14). More than 5,700 cecidomyiid species have been described (35, 44), and new species are regularly discovered (67, 68, 111). The phylogenetic relationships among species are still being determined (36, 119), and important host relationships are still being claried (37, 116, 126). For those that are interested in their study, Raymond Gagn es books are essential (43, 44). They present a comprehensive account of general gall midge biology; the history of cecidomyiid study; useful keys; and a description of gall midge collection, rearing, and specimen preparation. According to Roskam (97), the Cecidomyiidae is composed of four subfamilies. Three of these, the Catotrichinae, Lestreminnae, and Porricondylinae, are relatively ancient groups with a combined total of approximately 1,300 species that typically live on saprophytic fungi (35). Some of these species reproduce via an unusual form of cyclic parthenogenesis that involves both chromosome elimination and paedogenesis (immature asexual reproduction). The cytology associated with these phenomena was once intensely investigated (66). M.J.D. White was a major participant in these investigations, and he summarized his ndings and the discoveries of others in a chapter covering the evolution of aberrant genetic systems (118). For a more recent and comprehensive treatment of these investigations, dating back to 1908, the reader is referred to Matuszewskis review (83). The fourth subfamily, the Cecidomyiinae, contains the HF, mycetophages, predators, and all of the other plant-gall-making species. Regardless of the food source, all species feed by extracting liquids (81). Gagn e uses the term gall midge to refer to the plant-galling species and cecidomyiid to refer to any member of the family (43). We use the same terminology here. The majority of the species in the Cecidomyiinae (4,000 species) are gall midges (43). These evolved in an explosive adaptive radiation on owering plants (87). Compared with other gall-forming insect taxa, the gall midges have colonized the widest variety of plants: 89 plant families in North America alone (43, 87).

As a group, gall midges produce plant galls on the buds, stems, leaves, owers, and fruit of dicotyledons, monocotyledons, gymnosperms, ferns, and mushrooms (44). Most species are adapted to only one type of plant tissue on a single plant species or a closely related group of species, and certain plants are host to multiple, monophyletic, gall midge species (63). As with most parasites, gall midge life cycles are highly synchronized with those of their hosts (43). From the standpoint of plant pathology, it is interesting to note that the gall-forming habit clearly evolved from mycetophagy (81, 97, 98). In addition, extant species in three gall midge tribes live symbiotically with fungi in ambrosia galls (125), in which a gall midge inoculates the plant with a fungus and feeds on fungal mycelia while the fungus undermines plant defenses, induces the gall, and extracts nutrients (96). Thus, two evolutionary routes between mycetophagy and gall-forming herbivory were possible (97): (a) a direct route and (b) a transitional route in which ambrosia galls were intermediate. Phylogenetic, anatomical, and ecological analyses suggest that both routes occurred multiple times (16, 81, 97, 98). It remains an open question whether horizontal gene transfer played a role in any of the transitions. In many respects, the biology of gall midges overtly resembles that of many plant pathogens; they have biotrophic or hemibiotrophic lifestyles, the feeding (infection) site is localized, and the gall midge induces both plant susceptibility and qualitative resistance. Gall midges are also able to reproduce quickly; adult females emerge with a full cohort of mature eggs and typically have less than one day to deposit those eggs before they die (56). Although adults are short lived, gall midges have another nonfeeding life stage, the last larval instar, which, like a spore, can survive extended periods of harsh environmental conditions. Nonfeeding larvae have been observed to remain in diapause for years, with 12 years being the record for Sitodiplosis mosellana (8). Unlike plant-parasitic microorganisms, gall midges have a central nervous system and sensory organs that are essential for mating, active
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dispersal, and plant selection. The winged adult is free-living and entirely devoted to sexual reproduction. Adult males are attracted to a volatile sex pheromone produced by virgin adult females (52). Males mate many times, but females mate only once (56). Host selection is the responsibility of the mated adult female, who typically has less than a day to nd hosts using a relatively sophisticated behavior, which involves discrimination of the plants chemical, visual, and physical cues (65). Host selection is critical to reproductive tness (55).
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HESSIAN FLY BIOLOGY


The HF is one of the most economically important gall midges. It belongs to a genus containing 29 species whose larvae live on grasses (45). Its biology resembles that of the majority of cecidomyiids, but because it attacks wheat seedlings, and up to 50 larvae can survive on the same seedling (gall), it is the most amenable to propagation in the laboratory (56). HFs are easily reared and maintained at 17 to 24 C in either the greenhouse or growth chamber. The life cycle is completed in approximately 28 days and consists of the egg, three larval instars, the pupa, and the adult (Figure 2). The pheromone that adult females use to attract mates has been identied (5). Females distribute their eggs (200) on the upper surfaces of young wheat leaves (Figure 2a). Only the rst and second larval instars feed. After hatching, the rst-instar larvae crawl to the base of the seedling, where they attempt to establish a feeding site (Figure 2b). As described in greater detail below, rst-instar larval modulation of plant development is critical to larval survival. Second-instar larvae are sessile and imbibe the liquids presented to them by the reprogrammed plant (the gall). Third-instar larvae and pupae develop within a puparium, which consists of the cuticle of the second-instar larva (Figure 2c,e). This cuticle eventually hardens, sclerotizes, and becomes dark brown. Because of its appearance, this stage is commonly referred to as the ax seed.

HF adults eclose from the puparia and live for only one to four days (56). The HF is not associated with a fungus, but it does harbor several species of bacteria that are transferred via the anus of the modied adult female gut into each of her eggs upon oviposition (6). The role these bacteria play in HF survival is uncertain. As third instars, HFs can enter a cold-induced diapause and can be conveniently maintained in diapause at 4 C for up to a year. After three months in the cold, room temperature breaks diapause, and adults emerge in 1014 days. Females typically produce offspring of only one sex (11). Therefore, by isolating families of individual females on caged pots, one can easily obtain virgin females for experimental matings.

Pest Status
The HF is present in North Africa, Europe, Western Asia, Central Asia, North America, and New Zealand. It can cause economic injury anywhere wheat is grown in the United States (27, 71, 90, 106, 117). The insect is often a greater problem in the southern United States because there are typically more generations per year in the south (six to eight) than in the north, and there is no planting time when HF is dormant (20, 23, 40). HF damage exceeded $4 million per year from 1984 to 1989 in South Carolina (25). Yield loss in Georgia from 1988 to 1989 was $20 million (21), and losses of 21 bushels per infested acre occurred in 1985 in Alabama (40). The deployment of cultivarspecic R genes has been the most successful HF control strategy (23, 27, 56). Historically, however, virulent genotypes (biotypes) in HF populations overcome the resistance conferred by single R genes in six to eight years (27, 42, 82, 90). Because wheat acreage is expected to increase, tillage conservation is expanding, and the frequency of virulence in HF populations is increasing, future economic losses from HF are predicted to be as high as any time in the recent past (33, 40). Therefore, there is a need for virulence diagnostics, stacked R genes, and the development of genetically engineered resistance to protect wheat from HF attack.

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1 mm

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b
1 3 4 2 1 2

1 mm

1 mm

Figure 2 Critical stages in the Hessian y (HF) life cycle. (a) HF female depositing eggs (arrowhead ) in the grooves on the upper surface of a wheat leaf. (b) Multiple rst-instar HF larvae (arrowhead ) attempting to develop a feeding site near the meristem at the crown of a wheat seedling one day after hatching. (c) HF-infested, susceptible, wheat seedling 15 days after infestation. Two early, nonfeeding third-instar larvae (arrowheads) are visible behind the leaves near the base of the seedling. Note the dark green color and the absence of internodes between the second, third, and fourth leaves. The plant is permanently stunted, and there will be no further growth from its apical meristem. (d ) HF-infested, resistant, wheat seedling 15 days after infestation. Note the light green color, the presence of internodes, and the presence of a fth leaf initial. Dead rst-instar larvae, which are typically present behind the leaves at the base of the seedling, are not visible in this photograph. (e) The rst leaf of the plant shown in panel c is pulled back to reveal healthy, nonfeeding late second-instar larvae (arrowheads).

Genome Organization
Like that of all other cecidomyiids, HF genomic organization and chromosome behavior is unusual, involving both chromosome imprinting and chromosome elimination (11). HF chromosomes are classied as either E (eliminated) or S (somatic), according to convention (118). The E chromosomes vary in number and are strictly germ-line-limited and strictly maternally inherited. They are essential

only to the development of the male and female gonads (7). As in other dipteran species, the somatic (S) chromosome number is small, and like most gall midges, the HF S chromosomes consist of two autosomes (A1 and A2) and two X chromosomes (X1 and X2) (108, 118). The S chromosomes are diploid in the germ line and form chiasmata during oogenesis, but fail to recombine during spermatogenesis. Ova contain a haploid complement of

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BAC contigs vH9

vH13

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vH5

vH24

vHdic vH6

A1 X1 A2
Figure 3 Hessian y larval salivary gland polytene chromosomes illustrating the ability to use uorescence in situ hybridization to resolve the relative positions of bacterial articial chromosome (BAC) contigs. Green and red uorescence indicates the positions of 17 different BAC contigs on the autosomes (A1 and A2). None of the BACs in this preparation hybridized to the X chromosomes (X1 and X2). The locations of the centromeres (arrowheads) and the nucleolar organizer (N) are indicated. The positions of six Avr genes (vH5, vH6, vH9, vH13, vH24, and vHdic) that have been genetically and physically mapped on the chromosomes are shown.

X2

Because the HF interaction with wheat involves only somatic tissues, HF genomics has focused almost exclusively on the S chromosomes. The S genome size is relatively small (158 Mb) (61), and importantly, the S chromosomes are polytene in the HF larval salivary glands (Figure 3). Thus, although experimental matings do permit the development of genetic maps, the polytene chromosomes also permit physical mapping at a relatively high resolution (10). Therefore, HF bacterial articial chromosome (BAC) contigs were developed uisng high-resolution DNA ngerprints of end-sequenced BACs, and the largest contigs were then physically positioned on the chromosomes using uorescence in situ hybridization (1). This placed approximately 60% of the HF genome on the chromosomes as end-sequenced BAC contigs. In turn, the physical map served as a reference that was subsequently used to assign whole genome shotgun sequencing data to chromosomes (93). These data have been submitted to GenBank (Accession PRJNA45867), and a HF genome browser supports the data (19).

S chromosomes and between 24 and 32 E chromosomes (A1A2X1X2E). Sperm carry only the maternally derived S chromosomes (A1A2X1X2). Ova and sperm combine to form zygotes that have a full complement of E chromosomes and a diploid number of S chromosomes (A1A2X1X2E/A1A2X1X2). The E chromosomes are always eliminated from the presumptive somatic cells during early embryogenesis. If only the E chromosomes are eliminated, the embryo develops as a female with 2n = 8 S chromosomes (A1A2X1X2/A1A2X1X2) in the soma. However, if the paternally derived X1 and X2 chromosomes are also eliminated, the embryo develops as a male with 2n = 6 S chromosomes (A1A2X1X2/A1A2OO) in the soma. Maternal genotype conditions the retention or elimination of the paternally derived X chromosomes and, in so doing, the sex of the offspring (11). Thus, females usually produce either all-female or all-male broods.
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THE WHEATHESSIAN FLY INTERACTION


Interactions between plants and their parasitic fungi, oomycetes, and nematodes suggest that plant immunity has required each group of parasites to converge on a similar effector-based mechanism of attack (62, 115). The mechanics of HF attack, the presence of transcripts encoding putative effector proteins in the HF salivary gland, and the gene-for-gene manner in which wheat R genes provide HF resistance suggest that insect plant parasites use the same strategy (Figure 1). The physical interaction between wheat and HF begins when a neonate larva (460 m long) emerges from an egg that was deposited on the upper surface of a young wheat leaf (Figure 2a). The larva then uses the parallel venation of the leaf to guide its migration (1 cm h1 ) down the leaf blade and enter the shelter that bundled leaf sheaths provide.

the cell wall without physically disturbing the plasma membrane (54) (Figure 1). The cellular responses that follow this attack have been examined in both compatible and incompatible interactions.
g b

The Compatible Interaction


To benet its own growth, the successful larva alters the developmental pathways of wheat cells, severely compromising the growth of the plant (2, 3, 53, 54, 130) (Table 1). The epidermal and mesophyll sheath cells near the feeding site become the nutritive feeding cells (54) that characterize all gall midgeinduced galls (95). These have an enriched cytoplasm, an altered nucleus, and a thin cell wall that eventually breaks down to provide a liquid diet to the larva (54). Cell division and cell elongation cease, and chloroplasts accumulate (24). Outwardly, HF-infested susceptible wheat seedlings appear dark green and stunted (Figure 2c,e). Although the seedling may compensate by tillering (4), the shoot apical meristem eventually dies. Plants that are attacked during stem elongation have similar symptoms, tend to lodge, and produce heads with less seed weight and fewer seeds (91). Like other gall midges (114), the HF avoids inducing the production of plant volatiles that might attract parasitoids and predators (112, 113). These symptoms are associated with altered patterns of plant gene transcription (Table 1). Most upregulated genes of known function are involved in nutrient metabolism and transport (72). Some of these genes encode stress proteins (heat-shock proteins and components of the ubiquitin pathway), which may reect the state of stress exerted by HF attack. Others encode transcription factors, which may be used to modulate plant development. The most interesting change is the coordinated upregulation of genes involved in primary metabolic pathways (130). These changes may reect an elevated consumption of carbohydrates and an elevated synthesis of amino acids. This possibility is consistent with both the observation that the carbon-to-nitrogen ratio is
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1 m

Figure 4 Mesal view of the rst-instar mandible showing the hole (h) at the base of the grove (g) in the blade (b) of the mandible and the minute teeth (t) positioned behind the blade along the mandibles dorsal edge. The position of the mouth (m) of the insect is indicated. Scanning electron micrograph kindly provided by J.H. Hatchett.

Within 1 to 2 cm of the base of the leaf, the larva attacks the still-expanding sheath epidermal cells of the abaxial surface of the adjacent, younger leaf (53, 54) (Figure 2b). Six decades ago, Painter concluded that the rstinstar larva is incapable of physically rupturing plant cells (58), and recent investigations support that conclusion. First-instar HF larvae use paired, microscopic mandibles to penetrate into the cell wall (53, 54, 58) (Figure 4). The tip of the mandible resembles the end of a hypodermic needle; it is grooved on the internal lateral surface, and this groove extends from the tip of the mandible internally into the basal hole. Salivary uid is presumably delivered through the hole so that it travels down the groove and into the small punctures that have been observed in the cell walls of infested plants (53). The mandible blades extend into, or perhaps through, the epidermal cell wall but do not appear long enough to pierce the plasma membrane. They therefore appear to act in a manner that is analogous to a short stylet, or haustorium (115), that injects effectors into, or just below,

Table 1 Phenotypic responses of wheat and Hessian y during compatible and incompatible interactions Compatible interaction Larval growth completed in 1012 days Incompatible interaction Larvae die within 5 days of attack No larval growth Gut shows signs of toxin exposure Seedling survival Localized cell death Accumulation of reactive oxygen species Adjacent living cells are fortied Transient increase in permeability Epicuticular waxes accumulate Toxin production increasesa Class III peroxidases increasea Phenylpropanoid metabolism increasesa Cell wall and lipid metabolism increasesa Nutrient metabolism and transport suppresseda Fatty acid degradation suppresseda Phospholipid metabolism suppresseda Stress-related proteins decreasea

Seedling apical shoot meristem death Shorter plants, fewer heads, fewer seeds Increased cell permeability at attack sites Creation of nutritive cells Cell wall breakdown

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Membrane permeability increasesa Stress-related proteins increasea C/N ratio shift favors N (52% change)a Nutrient metabolism and transport increasesa Basal defense responses suppresseda Cell wall metabolism decreasesa Phenylpropanoid metabolism suppresseda Histones and structural proteins decreasea
a

Responses based on gene expression data (47, 72, 109, 121).

dramatically decreased at the feeding site (100, 130), and the requirements of an insect that lives on a food source that is normally nitrogen poor. Other upregulated genes may act to make nutrients more accessible for the growing larva (72). These include genes encoding a variety of nutrient transporters. Interestingly, the wheat gene Hfr-2, which encodes a cytolytic toxin-like protein with multiple agglutinin domains and a membrane-binding domain, is also upregulated (88). It is possible that this protein inserts into cell membranes and makes them more permeable. Not surprisingly, many plant defense genes are downregulated (Table 1). These include genes encoding protease inhibitors, lectins, enzymes involved in secondary metabolite synthesis (O-methyltransferases and chalcone synthases), enzymes involved in cell wall metabolism (xyloglucan endotransglycosylases and cellulose synthases) (72), lipases and lipid transfer proteins (100), and class III peroxidases (72). Consistent with an inhibition of plant growth and a lowered demand for structural proteins, genes
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encoding various histones and a histone acetyltransferase are also strongly downregulated (72). In the HF, both the mandibles and the salivary glands display morphological changes that are correlated with changes in wheat morphology (58, 107) (Table 1). Only four days after infestation by just a single larva, susceptible wheat seedlings are irreversibly compromised (2, 3, 22, 103): Plant seedlings are stunted, plant defense genes are suppressed (72), metabolic pathways in the plant are reprogrammed (130), nutrient tissue forms (54), and the cell walls near the feeding site become thin and permeable (53, 69, 120). During this period, the larva remains a rst instar, its mandibles are sharp, and the basal cells of the salivary gland are fully developed. After the plant has been irreversibly transformed into a permeable nutrient sink (120), the larva molts into a second instar, its mandibles are blunt, and the basal salivary gland cells begin to decay (58, 107). Thus, the rstinstar larval stage is critical to gall formation and insect survival, and the rst-instar larval salivary gland is the most obvious source of the factors

the insect uses to modulate plant development (Figure 1).

Putative Effector Proteins


Within the rst-instar salivary gland, more than 50% of all transcripts encode proteins containing a secretion signal (26, 76). Less than 5% of these encode proteins with sequence similarity to known proteins; these include proteases (73, 131) and protease inhibitors (80), which are also expressed in the larval gut (129), and lipase-like proteins (104). The remaining signal peptideencoding transcripts encode putative effector proteins called secreted salivary gland proteins (SSGPs) (28). SSGPs lack sequence similarity to any other known proteins (31). Hundreds of SSGP-encoding transcripts have been classied into families and superfamilies on the basis of sequence similarities (31). The majority of these encode small (50to 250-residue) proteins. Genomic analyses of a few SSGP families found that most of the related transcripts are nonallelic; that family members are often clustered within small chromosomal segments; and that within these segments, the genes appear to be experiencing strong positive selection and functional adaptation (29, 30). Remarkably, among genes within gene families, the noncoding genic regions have far more sequence similarity (75%95%) than the regions encoding the mature proteins (30%60%). Such strong positive selection is usually associated with genes that function in interspecies molecular recognition, e.g., the genes encoding immunoglobulins (110), plant R genes (84), and plant pathogen effectors (85). The possibility that SSGPs are effectors is further supported by the observation that genes with a similar pattern of sequence conservation were discovered in the salivary gland transcriptome of another gall-forming gall midge, the Asian rice gall midge (O. oryzae), but they were absent in the salivary transcriptomes of a wheat-seed-feeding cecidomyiid, the wheat blossom midge (Sitodiplosis mosellana) (30). The dependence of the HF on induced nutritive tissue, the abundance and small size of

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SSGP-encoding transcripts, their presence in the rst-instar salivary gland, and their unusual pattern of conservation leave little doubt that at least some of these genes encode effector proteins that modulate plant development. Nevertheless, the role that individual SSGPs play in this process remains to be determined. Thus far, efforts to identify the corresponding proteins with peptide-based antibodies have not been successful (31). Possible reasons for this are that little or no protein may be produced, that only some of the transcripts are translated, or that the SSGPs are secreted into host tissues immediately after translation. We also anticipate that functional redundancies exist within SSGP families, as they do in oomycete effectors (15), and that these will complicate the development of assays capable of testing how SSGPs function in compatible interactions. With regard to incompatible interactions, as described below, genetic evidence clearly points to certain SSGPs as the elicitors of effector-triggered immunity (ETI) (Figure 1).

The Incompatible Interaction


Precisely how resistant wheat plants prevent the creation of nutritive cells and cause HF larval death is not known. However, the reaction is clearly induced and highly localized, and it resembles the subcellular responses that mediate plant responses to fungal attack (53) (Table 1). Outwardly, the plant typically displays little evidence of HF attack (Figure 2d ). Immediately at the site of attack, a small number of epidermal cells die (50, 53), and reactive oxygen species (ROS) accumulate (74). Adjacent epidermal and mesophyll cells survive the attack and exhibit swollen mitochondria, reinforced cell walls, and an elaboration of the Golgi complexendoplasmic reticulum with many small vesicles docking at the plasma membrane (53). A granular material accumulates in the paramural space between the plasma membrane and the outer cell wall, and within pockets embedded in the outer cell wall. These granular materials may be toxins (47, 109); larvae attempting to feed on resistant plants
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exhibit the disrupted midgut microvilli that characterize insect exposure to gut toxins (105). Changes in plant gene expression correspond with these histological changes (Table 1). Upregulated genes in response to HF include those that encode molecules known to have insect toxicity (26, 32, 38, 70), including those encoding wheat protease inhibitors (72, 121), lectins (47, 72, 109), and enzymes that produce phenylpropanoids (72). Genes involved in cell wall metabolism are also upregulated, including the genes encoding various xyloglucan endotransglycosylases, -expansins, pectinesterases, glucanases, cellulose synthases, and dirigent-like proteins (72). Class III peroxidase genes are also upregulated (74) and may be responsible for generating ROS in response to HF just as they do in response to certain pathogens (17). In addition to a potential role in ROS generation, class III peroxidases could play other roles, such as cell wall cross-linking and signaling. Additional upregulated genes encode lipid transfer proteins (60, 100) and a variety of lipases, which are associated with the rapid mobilization of membrane lipids at the attacked tissue (Y.C. Zhu, X. Liu, H. Wang, C. Khajuria, J.C. Reese, R.J. Whitworth, R. Welti, and M.-S. Chen, unpublished research). Analysis of lipid metabolism-related pathways indicates that the mobilized lipids may be converted into components of cuticle wax (69). Rapid mobilization of membrane lipids and other molecules and subsequent conversion of these into components for cell wall strengthening may constitute a layer of defense that prevents larval mouthparts from placing effectors in the apoplast (53).

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with respect to their resistance to one or more HF genotypes (biotypes). Thus far, only one HF R gene (Hdic) has been cloned (X. Liu & M.-S. Chen, unpublished research). It contains both the nucleotide binding (NB) and leucinerich repeat (LRR) motifs that characterize the majority of the genes that confer resistance to plant pathogens (62). However, mapping data also indicate that other HF R genes encode NB-LRR proteins: H3, H5, H6, H9, H10, H11, H12, H14, H15, H16, H17, H19, H28, and H29 are all clustered in the distal gene-rich region of wheat chromosome A1S, which contains Hdic and other NB-LRR genes (75, 77). Additional HF R genes are clustered with defense response genes in wheat: H13, H23, and another putative HF resistance gene (HWGRC4 ) cluster with a wheat curl mite R gene (Cmc4) on chromosome 6DS (78), and H24, H26, and H32 are clustered on chromosome 3DL (123, 124). Although pyramiding HF R genes was suggested as a deployment strategy years ago (48), most releases have involved only single genes (91). Only six (H12, H13, H18, H24, H25, and H26) have signicant efcacy in the southern United States (23). The remainder either have lost effectiveness since they were deployed or never showed promise (91). Thus, there is a need for the discovery of additional HF R genes as well as novel control methods that preserve the genes efcacy in HF populations.

Hessian Fly Avirulence Genes


The existence of HF R genes in wheat and putative effector-encoding genes in the HF supports the hypothesis that the same ETI that underlies gene-for-gene interactions between plants and plant pathogens (62) also underlies wheat-HF incompatible interactions (Figure 1). To test that hypothesis further, genetic analyses have been performed to determine if avirulence can be attributed to effector-encoding Avr genes. Hatchett & Gallun (57) began these investigations, showing that virulence (the ability of HF larvae to survive on and stunt wheat seedlings) to the R gene H3 and virulence to the coordinated R gene pair H7H8 are conditioned by independent, simply

Hessian Fly R Genes in Wheat


Underlying the incompatible interaction are 33 different HF R genes in wheat. These have been named H1-H3, h4, H5-H32, and Hdic (75, 101). All of these, except h4, are dominant or semidominant genes that have been either discovered in wheat or brought into wheat germplasm via wide crosses (91). All genes have been shown either to recombine or to differ
348 Stuart et al.

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inherited, recessive genetic factors. Within a few years, Galluns group had obtained evidence of the rst X-linked HF Avr gene and extended the gene-for-gene association to four R genes in wheat (H3, H5, H6, and H7H8) (46). With the discovery that virulence to H9 and virulence to H13 were clearly X-linked, the convention of placing a small v (for recessive virulence to) in front of the R gene name was adopted in naming HF Avr genes (vH9 and vH13) (41, 127). The adoption of polymerase chain reaction (PCR)-based methods in these investigations permitted greater resolution in testing the gene-for-gene hypothesis (10, 79, 94), and the current ability to resolve Avr gene positions on the FPC-based physical map leaves little question regarding the hypothesiss veracity (Figure 3). To date, six HF Avr genes (vH5, vH6, vH9, vH13, vH24, and vHdic) have been mapped within chromosome segments spanning less than 600 kb (10; J.J. Stuart, unpublished data). The resolution of the genes that are near telomeres (vH9, vH13, and vH24), where recombination rates are greatest, is even better ( J.J. Stuart, unpublished data).

WHEATHESSIAN FLY COEVOLUTION


The HF appears to be the descendant of an ancient enemy of grasses (family Poaceae), and

particularly the related grasses in the tribe Triticeae. Its genus (Mayetiola) contains 29 species whose larvae live on the stems of grasses (45). The HFs center of origin overlaps with the center of origin of wheat (8, 34), and although wheat is its preferred host (56), the host range of the HF includes grasses in more than 17 genera, including many prairie grasses (Elymus canadensis, Pascopyrum intermedium, Thinopyrum intermedium, and Agropyron cristatum) (8, 56). Many of the more effective HF R genes (e.g., H26) have been found in grasses other than bread wheat (91, 125). This suggests that the HF and its allies have exerted signicant selection pressure on grasses in the tribe Triticeae and that H genemediated resistance has, in turn, been an important source of selection pressure for HF adaptation (56). Supporting this idea are studies showing that the highest frequencies of virulence are found in HF populations in the Fertile Crescent, near its shared center of origin with wheat (39); here, there are only two known H genes, H25 and H26, for which virulence has not been found. One phenomenon that probably reduces R gene selection pressure on the HF is resistance obviation (51). To describe obviation, we use H13 as an example here (Table 2), but the phenomenon is probably common to all HF R genes ( J.J. Stuart, unpublished observations). When only H13-avirulent larvae attack an

Table 2 Gene-for-gene interactions involving Hessian y strains and near-isogenic susceptible and resistant wheat lines Wheat isogenic line (122) Hessian y strain H13-Avirulent Newton (susceptible) Compatible interaction Hessian y: larval survival Wheat: seedling mortality/seed loss Compatible interaction Hessian y: similar survival but 12% loss in reproduction Wheat: seedling mortality/seed loss Compatible interaction Hessian y: both types of larvae survive Wheat: seedling mortality/seed loss Molly (H13-resistant) Incompatible interaction Hessian y: 100% larval mortality Wheat: normal or better reproduction Compatible interaction Hessian y: some larval survival but no loss in reproduction Wheat: seedling mortality/seed loss Resistance obviation Hessian y: both types of larvae survive Wheat: seedling mortality/seed loss
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H13-Virulent

Avirulent + virulent coattack

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H13-protected plant, they trigger defense responses and die (53). However, when H13virulent and H13-avirulent larvae co-attack, both types of larvae feed, survive, and develop into reproductive adults (51). Three notable deductions can be drawn from these observations: (a) H13-avirulent larvae survive by feeding on the nutritive tissue induced by H13-virulent larvae; (b) H13 resistance is highly localized (54) and susceptibility is systemic (3, 130); and (c) H13 obviation provides refugia for H13-avirulent genotypes in areas where H13 is being used for HF control. These refugia are expected to slow the evolution of H13-virulence (49). Fitness costs also inuence the rate at which plants and their parasites adapt (92). The smaller the cost, the greater potential there is for rapid evolution. It appears that wheat pays no cost for resistance (4). Using isogenic wheat lines carrying either H6, H9, or H13 R genes (122), there was no tness cost for either H gene expression or the downstream-induced resistance responses triggered by avirulent larvae (Table 2). In fact, for the H13 line, attacked plants produced even more seed than nonattacked controls. However, HF virulence does appear to have a cost (128). When reared on susceptible plants, HFs virulent to multiple R genes developed into signicantly smaller adults than avirulent strains. This size differential translated into a 12% (for the strain virulent to 9 H genes) or 32% (for the strain virulent to

11 H genes) reduction in the females ability to produce eggs, and an 11% or 18% reduction in the males potential to inseminate females. Thus, there may be a reproductive tness cost of 1% to 3% for the loss of each Avr gene. Taken together with the diversity of putative effector-encoding genes in the HF, this observation suggests that selection favors genetic diversication for effector function to compensate for Avr gene loss (15).

CONCLUSIONS
The HF shares many features with biotrophic or hemibiotropic plant pathogens. In fact, it is remarkable how many HF plant-parasitic mechanisms closely resemble those of nematodes, fungi, and oomycetes (Figure 1). These include the manner in which the HF feeds on its host, its ability to modulate gene expression, and the presence and structure of hundreds of putative effector-encoding genes in its genome. However, the most convincing argument in favor of our hypothesis comes from the plants own perception of the disease-causing agent: Wheat responds to HF attack as if it were a plant pathogen, using cultivar-specic NB-LRR R genes to guard against cognate Avr-gene-encoded effectors. There is now little doubt that Hatchett & Gallun (57) were correct when they proposed over four decades ago that gene-for-gene interactions exist between HF and wheat.

SUMMARY POINTS 1. Hessian y interactions with wheat share important features with many plant pathogen and nematode interactions with plants, including a hemibiotrophic lifestyle, a sessile feeding stage, a narrow host range, minute mouthparts, an effector-based mechanism of attack, and ETI in the plant. 2. High-resolution genetic mapping utilizing the sequenced HF genome and an FPC-based physical map of the HF polytene chromosomes has permitted insect Avr gene mapping and discovery. 3. Hundreds of putative HF effector proteins exist in the HF genome. These show unmistakable signs of diversifying selection.

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4. Wheat responds to HF attack with a qualitative resistance that is conferred by major resistance (H) genes. More than 32 H genes have been identied. The cloned Hdic gene has NBS-LRR motifs. Resistance mediated by these genes is highly effective, typically killing 100% of attacking larvae. Attacked resistant plants grow normally and reproduce as well as or better than unattacked resistant plants. 5. The histology of HF resistance resembles plant resistance to fungi. It involves a localized hypersensitive reaction, the release of an oxygen burst, the fortication of the cell wall, and an upregulation of toxin-encoding genes. 6. Coevolutionary interactions between the Hessian y and grasses are not constrained by major tness costs, there being no tness cost for H-gene-mediated resistance and a relatively small tness cost for Hessian y adaptation to plant resistance.

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FUTURE ISSUES 1. The roles that the Avr-gene-encoded effectors and other putative effectors play in both compatible and incompatible interactions have not been characterized. Where are these proteins localized in plant cells, how are they transported, and what are their cellular targets in the compatible interaction? Do Avr-gene-encoded proteins interact directly or indirectly with H-gene products? Are the abundance and diversity of effector proteins associated with functional redundancy? 2. The resistance response to HF feeding in wheat is still relatively poorly understood. What is the sequence of downstream plant responses that prevent Hessian y larvae from feeding and eventually cause death? Do all HF R genes in wheat use the same resistance mechanisms and pathways? Do HF R genes mediate plant resistance to organisms other than the Hessian y? 3. Knowledge regarding the molecular mechanisms associated with HF resistance in wheat is forthcoming. How can this information be translated into durable plant resistance? 4. Comparative genomics provides an opportunity to understand the evolution of effector proteins. What effector proteins and motifs are conserved among Mayetiola gall midge species? Which, if any, of the effectors are effective in cells of different grass species? What are the evolutionary relationships among effectors in more distantly related gall midges? Did gall midges obtain their effectors via horizontal gene transfer? 5. Pheromone traps can be combined with PCR-based diagnostics for virulence and avirulence now that HF Avr genes and mutations can be identied. These combined technologies will permit an analysis of the evolution of virulence in eld populations exposed to monocultures of HF R genes. Will they permit the development of methodologies that prolong R gene efcacy?

DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial holdings that might be perceived as affecting the objectivity of this review.
www.annualreviews.org The Hessian Fly Gall Midge 351

ACKNOWLEDGMENTS
We dedicate this article to Jim Hatchett and the late Bob Gallun, whose pioneering work established the Hessian y as a genetic model for plant-insect interactions. Funding for this work has been provided from USDA NRI grants 2004-03099 and 2009-35302-05262, and USDA NIFA grant 2010-03741. LITERATURE CITED
1. Aggarwal R, Benatti T, Gill N, Zhao C, Chen M-S, et al. 2009. A BAC-based physical map of the Hessian y genome anchored to polytene chromosomes. BMC Genomics 10:293 2. Anderson KG, Harris MO. 2006. Does R gene resistance to Hessian y allow wheat seedlings to escape larval-induced growth decits? J. Econ. Entomol. 99:184253 3. Anderson KG, Harris MO. 2008. Leaf growth signals the onset of effective plant resistance against Hessian y larvae. Entomol. Exp. Appl. 128:18495 4. Anderson KM, Kang Q, Reber J, Harris MO. 2011. No tness cost for wheats H-gene mediated resistance to Hessian y (Diptera: Cecidomyiidae). J. Econ. Entomol. 104:1393405 5. Andersson MN, Haftmann J, Stuart JJ, Cambron SE, Harris MO, et al. 2009. Identication of sex pheromone components of the Hessian y, Mayetiola destructor. J. Chem. Ecol. 35:8195 6. Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ, et al. 2011. Hessian yassociated bacteria: transmission, essentiality, and composition. PLoS ONE 6:e23170 7. Bantock CR. 1970. Experiments on chromosome elimination in the gall midge, Mayetiola destructor. J. Embryol. Exp. Morphol. 24:25786 8. Barnes HF. 1956. Gall Midges of Cereal Crops. London: Crosby Lockwood 9. Behura SK, Nair S, Sahu SC, Mohan M. 2000. An AFLP marker that differentiates biotypes of the Asian rice gall midge (Orseolia oryzae) is sex-linked and also linked to virulence. Mol. Gen. Genet. 263:32834 10. Behura SK, Valicente FH, Rider SD Jr, Shun-Chen M, Jackson S, Stuart JJ. 2004. A physically anchored genetic map and linkage to avirulence reveals recombination suppression over the proximal region of Hessian y chromosome A2. Genetics 167:34355 11. Benatti T, Valicente FH, Aggarwal R, Zhao C, Walling JG, et al. 2010. A neo-sex chromosome that drives postzygotic sex determination in the Hessian y (Mayetiola destructor). Genetics 184:76977 12. Bent AF, Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:39946 13. Bentur JS, Pasalu IC, Sarma NP, Prasada Rao U, Mishra B. 2003. Gall Midge Resistance in Rice: Current Status in India and Future Strategies. Hyderabad, India: Dir. Rice Research 14. Bertone MA, Courtney GW, Wiegmann BM. 2008. Phylogenetics and temporal diversication of the earliest true ies (Insecta: Diptera) based on multiple nuclear genes. Syst. Entomol. 33:66887 15. Birch PR, Boevink PC, Gilroy EM, Hein I, Pritchard L, Whisson SC. 2008. Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr. Opin. Plant Biol. 11:37379 16. Bisset J, Borkent A. 1988. Ambrosia galls: the signicance of fungal nutrition in the evolution of the Cecidomyiidae (Diptera). In Coevolution of Fungi with Plants and Animals, ed. KA Pirozynski, DL Hawsworth, pp. 20325. London: Academic 17. Bolwell GP, Bindschedler LV, Blee KA, Butt V, Davies DR, et al. 2002. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53:136776 18. Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA. 2010. A functional genomics approach identies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet. 6:e1001216 19. Brown SJ, Caragea D. 2011. Agricultural Pest Genomics Resource Database. Manhattan, KS: Kansas State Univ. http://www.agripestbase.org. 20. Buntin GD. 1999. Hessian y (Diptera: Cecidomyiidae) injury and loss of winter wheat grain yield and quality. J. Econ. Entomol. 92:119097 21. Buntin GD, Ott SL, Johnson JW. 1992. Integration of plant resistance, insecticides, and planting date for management of the Hessian y (Diptera: Cecidomyiidae) in winter wheat. J. Econ. Entomol. 85:53038
352 Stuart et al.

Annu. Rev. Phytopathol. 2012.50:339-357. Downloaded from www.annualreviews.org by D'Youville College on 02/26/13. For personal use only.

22. Byers RA, Gallun RL. 1972. Ability of the Hessian y to stunt winter wheat. 1. Effect of larval feeding on elongation of leaves. J. Econ. Entomol. 65:95558 23. Cambron SE, Buntin GD, Weisz R, Holland JD, Flanders KL, et al. 2010. Virulence in Hessian y (Diptera: Cecidomyiidae) eld collections from the southeastern United States to 21 resistance genes in wheat. J. Econ. Entomol. 103:222935 24. Cartwright WB, Caldwell RM, Compton LE. 1959. Responses of resistant and susceptible wheats to Hessian y attack. Agron. J. 51:52931 25. Chapin JW. 2009. Hessian y: a pest of wheat, triticale, barley and rye. Clemson Ext. Bull. http://www. clemson.edu/extension/rowcrops/small_grains/pdfs/hessian_y.pdf 26. Chen M-S. 2008. Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15:10114 27. Chen M-S, Echegaray E, Whitworth RJ, Wang H, Sloderbeck PE, et al. 2009. Virulence analysis of Hessian y populations from Texas, Oklahoma, and Kansas. J. Econ. Entomol. 102:77480 28. Chen M-S, Fellers JP, Stuart JJ, Reese JC, Liu XM. 2004. A group of related cDNAs encoding secreted proteins from Hessian y [Mayetiola destructor (Say)] salivary glands. Insect Mol. Biol. 13:1018 29. Chen M-S, Fellers JP, Zhu YC, Stuart JJ, Hulbert S, et al. 2006. A super-family of genes coding for secreted salivary gland proteins from the Hessian y, Mayetiola destructor. J. Insect Sci. 6:12 30. Chen M-S, Liu X, Yang Z, Zhao H, Shukle RH, et al. 2010. Unusual conservation among genes encoding small secreted salivary gland proteins from a gall midge. BMC Evol. Biol. 10:296 31. Chen M-S, Zhao H-X, Zhu YC, Schefer B, Liu X, et al. 2008. Analysis of transcripts and proteins expressed in the salivary glands of Hessian y (Mayetiola destructor) larvae. J. Insect Physiol. 54:116 32. de Leo F, Volpicella M, Licciulli F, Liuni S, Gallerani R, Ceci LR. 2002. PLANT-PIs: a database for plant protease inhibitors and their genes. Nucleic Acid Res. 30:34748 33. Del Conte SCC, Bosque-P erez NA, Schotzko DJ, Guy SO. 2005. Impact of tillage practices on Hessian ysusceptible and resistant spring wheat cultivars. J. Econ. Entomol. 98:80513 34. Devos KM. 2010. Grass genome organization and evolution. Curr. Opin. Plant Biol. 13:13945 35. Dorchin N. 2008. Gall midges (Diptera: Cecidomyiidae). In Encyclopedia of Entomology, ed. JL Capinera, pp. 157680. Dordrecht, The Netherlands: Springer Verlag 36. Dorchin N, Freidberg A, Mokady O. 2004. Phylogeny of the Baldratiina (Diptera: Cecidomyiidae) inferred from morphological, ecological and molecular data sources, and evolutionary patterns in plantgaller relationships. Mol. Phylogenet. Evol. 30:50315 37. Dorchin N, Scott ER, Clarkin CE, Luongo MP, Jordan S, Abrahamson WG. 2009. Behavioural, ecological and genetic evidence conrm the occurrence of host-associated differentiation in goldenrod gall-midges. J. Evol. Biol. 22:72939 38. Dunaevsky YE, Elpidina EN, Vinokurov KS, Belozersky MA. 2005. Protease inhibitors in improvement of plant resistance to pathogens and insects. Mol. Biol. 39:7028 39. El Bouhssini M, Chen M, Lhaloui S, Zharmukhamedova G, Rihawi F. 2009. Virulence of Hessian y (Diptera: Cecidomyiidae) in the Fertile Crescent. J. Appl. Entomol. 133:38185 40. Flanders KL, Buntin GD, Mask PL. 2008. Biology and management of Hessian y in wheat. Ala. Coop. Ext. Serv. Bull. ANR-1069. 4 pp. 41. Formusoh ES, Hatchett JH, Black WC, Stuart JJ. 1996. Sex-linked inheritance of virulence against wheat resistance gene H9 in the Hessian y (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 89:42834 42. Foster JE, Ohm HW, Patterson FL, Taylor PL. 1991. Effectiveness of deploying single gene resistances in wheat for controlling damage by the Hessian y (Diptera: Cecidomyiidae). Environ. Entomol. 20:964 69 43. Gagn e RJ. 1989. The Plant-Feeding Gall Midges of North America. Ithaca, NY: Cornell Univ. Press. 340 pp. e RJ. 1994. The Gall Midges of the Neotropical Region. Ithaca, NY: Comstock Publ. Assoc. 352 pp. 44. Gagn 45. Gagn e RJ. 2010. Update for a Catalog of the Cecidomyiidae (Diptera) of the World. Washington, DC: Entomol. Soc. Wash. 544 pp. http://www.ars.usda.gov/SP2UserFiles/Place/12754100/ Gagne_2010_World_Catalog_Cecidomyiidae.pdf 46. Gallun RL. 1977. Genetic basis of Hessian y epidemics. Ann. N. Y. Acad. Sci. 287:22229
www.annualreviews.org The Hessian Fly Gall Midge 353

Annu. Rev. Phytopathol. 2012.50:339-357. Downloaded from www.annualreviews.org by D'Youville College on 02/26/13. For personal use only.

47. Giovanini MP, Saltzmann KD, Putoff D, Gonzalo M, Ohm HW, Williams CE. 2006. A novel wheat gene encoding a putative chitin-binding lectin is associated with resistance against Hessian y. Mol. Plant Pathol. 8:6982 48. Gould F. 1986. Simulation models for predicting durability of insect-resistant germplasm: Hessian y (Diptera: Cecidomyiidae)resistant winter wheat. Environ. Entomol. 15:1123 49. Gould F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43:70126 50. Grover PB Jr. 1995. Hypersensitive response of wheat to the Hessian y. Entomol. Exp. Appl. 74:28394 51. Grover PB Jr, Shukle RH, Foster JE. 1989. Interactions of Hessian y (Diptera: Cecidomyiidae) biotypes on resistant wheat. Environ. Entomol. 18:68790 52. Harris MO, Foster SP. 1999. Gall midges. In Pheromones of Non-Lepidopteran Insects Associated with Agricultural Plants, ed. J Hardie, AK Minks, pp. 2749. Oxford, UK: CABI 53. Harris MO, Freeman TP, Anderson KG, Moore JA, Payne SA, et al. 2010. H genemediated resistance to Hessian y exhibits features of penetration resistance to fungi. Phytopathology 100:27989 54. Harris MO, Freeman TP, Rohfritsch O, Anderson KG, Payne SA, Moore JA. 2006. Virulent Hessian y (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Ann. Entomol. Soc. Am. 99:30516 55. Harris MO, Sandanayake M, Grifn W. 2001. Oviposition preferences of the Hessian y and their consequences for the survival and reproductive potential of offspring. Ecol. Entomol. 26:114 56. Harris MO, Stuart JJ, Mohan M, Nair S, Lamb RJ, Rohfritsch O. 2003. Grasses and gall midges: plant defense and insect adaptation. Annu. Rev. Entomol. 48:54977 57. Hatchett JH, Gallun RL. 1970. Genetics of the ability of the Hessian y, Mayetiola destructor, to survive on wheats having different genes for resistance. Ann. Entomol. Soc. Am. 63:14007 58. Hatchett JH, Kreitner GL, Elzinga RJ. 1990. Larval mouthparts and feeding mechanism of the Hessian y (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 83:113747 59. Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S. 2009. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant-Microbe Interact. 22:11522 60. Jang CS, Johnson JW, Seo YW. 2005. Differential expression of TaLTP3 and TaCOMT1 induced by Hessian y larval infestation in a wheat line possessing H21 resistance gene. Plant Sci. 168:131926 61. Johnston JS, Ross LD, Bean L, Hughes DP, Kathirithamby J. 2004. Tiny genomes and endoreduplication in Strepsiptera. Insect Mol. Biol. 13:58185 62. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:32329 63. Joy JB, Crespi BJ. 2007. Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61:78495 64. Kaloshian I. 2004. Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30:241938 65. Kanno H, Harris MO. 2000. Both chemical and physical features of grass leaves inuence host selection by the Hessian y. J. Chem. Ecol. 26:233554 66. Kloc M. 2008. Basic science B.D. (before Drosophila): cytology at the University of Warsaw (Poland). Int. J. Dev. Biol. 52:11519 67. Kolesik P, Adair RJ, Eick G. 2005. Nine new species of Dasineura (Diptera: Cecidomyiidae) from owers of Australian Acacia (Mimosaceae). Syst. Entomol. 30:45479 68. Kolesik P, Rice AD, Bellis GA, Wirthensohn MG. 2009. Procontarinia pustulata, a new gall midge species (Diptera: Cecidomyiidae) feeding on mango, Mangifera indica (Anarcadiaceae), in northern Australia and Papua New Guinea. Aust. J. Entomol. 48:31016 69. Kosma DK, Nemacheck JA, Jenks MA, Williams CE. 2010. Changes in properties of wheat leaf cuticle during interactions with Hessian y. Plant J. 63:3143 70. Lawrence PK, Koundal KR. 2002. Plant protease inhibitors in control of phytophagous insects. Electron. J. Biotechnol. 5:1 71. Lidell MC, Schuster MF. 1990. Effectiveness of wheat genes for Hessian y (Diptera: Cecidomyiidae) resistance in Texas. J. Econ. Entomol. 83:113539 72. Liu X, Bai J, Huang L, Zhu L, Liu X, et al. 2007. Gene expression of different wheat genotypes during attack by virulent and avirulent Hessian y (Mayetiola destructor) larvae. J. Chem. Ecol. 33:217194
354 Stuart et al.

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73. Liu X, Fellers JP, Zhu YC, Mutti NS, El-Bouhssini M, Chen MS. 2006. Cloning and characterization of cDNAs encoding carboxypeptidase-like proteins from the gut of Hessian y [Mayetiola destructor (Say)] larvae. Insect Biochem. Mol. Biol. 36:66573 74. Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyam S, et al. 2010. Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol. 152:98599 75. Liu XM, Brown-Guedira GL, Hatchett JH, Owuoche JO, Chen M-S. 2005. Genetic characterization and molecular mapping of a Hessian y-resistance gene transferred from T. turgidum ssp. dicoccum to common wheat. Theor. Appl. Genet. 111:130815 76. Liu XM, Fellers JP, Wilde GE, Stuart JJ, Chen MS. 2004. Characterization of two genes expressed in the salivary glands of the Hessian y [Mayetiola destructor (Say)]. J. Insect Biochem. Mol. Biol. 34:22937 77. Liu XM, Fritz AK, Reese JC, Wilde GE, Gill BS, Chen MS. 2005. H9, H10, and H11 compose a cluster of Hessian y resistance genes in the distal gene-rich region of wheat chromosome 1AS. Theor. Appl. Genet. 110:147380 78. Liu XM, Gill BS, Chen M-S. 2005. Hessian y resistance gene H13 is mapped to a distal cluster of resistance genes in chromosome 6DS of wheat. Theor. Appl. Genet. 111:24349 79. Lobo NF, Behura SK, Aggarwal R, Chen M-S, Hill CA, et al. 2006. Genomic analysis of a 1 Mb region near the telomere of Hessian y chromosome X2 and avirulence gene vH13. BMC Genomics 7:7 80. Maddur AA, Liu XM, Zhu YC, Fellers FP, Oppert B, et al. 2006. Cloning and characterization of protease inhibitorlike cDNAs from the Hessian y Mayetiola destructor (Say). Insect Mol. Biol. 15:48596 81. Mamaev BM. 1975. Evolution of Gall Forming Insects: Gall Midges. Wetherby, UK: Br. Libr. 317 pp. 82. Martin-Sanchez JA, Gomez-Colmenarejo M, Del Moral J, Sin E, Montes MJ, et al. 2003. A new Hessian y resistance gene (H30) transferred from the wild grass Aegilops triuncialis to hexaploid wheat. Theor. Appl. Genet. 106:124855 83. Matuszewski B. 1982. Animal Cytogenetics. Insecta 3. Diptera I: Cecidomyiidae. Berlin, Germany: John Gebruder Burtraeger. 140 pp. 84. Michelmore RW, Meyers BC. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8:111330 85. Morgan W, Kamoun S. 2007. RXLR effectors of plant pathogenic oomycetes. Curr. Opin. Microbiol. 10:33238 86. Nombela G, Williamson VM, Muniz M. 2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitey Bemisia tabaci. Mol. Plant-Microbe Interact. 16:64549 87. Price PW. 2005. Adaptive radiation of gall-inducing insects. Basic Appl. Ecol. 6:41321 88. Puthoff DP, Sardesai N, Subramanyam S, Nemacheck JA, Williams CE. 2005. Hfr-2, a wheat cytolytic toxin-like gene, is up-regulated by virulent Hessian y larval feeding. Mol. Plant Pathol. 6:41123 89. Raman A, Schaefer CW, Withers TM, eds. 2005. Biology, Ecology, and Evolution of Gall-Inducing Arthropods. Eneld, NH: Sci. Publ. Inc. 90. Ratcliffe RH, Cambron SE, Flanders KL, Bosque-Perez NA, Clement SL, Ohm HW. 2000. Biotype composition of Hessian y (Diptera: Cecidomyiidae) populations from the southeastern, midwestern, and northwestern United States and virulence to resistance genes in wheat. J. Econ. Entomol. 93:131928 91. Ratcliffe RH, Hatchett JH. 1997. Biology and genetics of the Hessian y and resistance in wheat. In New Developments in Entomology, ed. K Bondari, pp. 4756. Trivandurm, India: Res. Signpost Sci. Inf. Guild 92. Rausher MD. 2001. Co-evolution and plant resistance to natural enemies. Nature 411:85764 93. Richards S. 2011. Hessian y genome project. Baylor, TX: Hum. Genome Seq. Cent., Baylor Sch. Med. http://www.hgsc.bcm.tmc.edu/project-species-i-Hessian_y.hgsc 94. Rider JSD, Sun W, Ratcliffe RH, Stuart JJ. 2002. Chromosome landing near avirulence gene vH13 in the Hessian y. Genome 45:81222 95. Rohfritsch O. 1992. Patterns in gall development. See Reference 102, pp. 6086 96. Rohfritsch O. 2008. Plants, gall midges, and fungi: a three-component system. Entomol. Exp. Appl. 128:20816 97. Roskam HC. 2005. Phylogeny of gall midges (Cecidomyiidae). See Reference 89, pp. 30719 98. Roskam JC. 1992. Evolution of the gall-inducing guild. See Reference 102, pp. 3449
www.annualreviews.org The Hessian Fly Gall Midge 355

Annu. Rev. Phytopathol. 2012.50:339-357. Downloaded from www.annualreviews.org by D'Youville College on 02/26/13. For personal use only.

99. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA 95:975054 100. Saltzmann KD, Giovanini M, Ohm H, Williams CE. 2009. Transcript proles of two wheat lipid transfer protein-encoding genes are altered during attack by Hessian y larvae. Plant Physiol. Biochem. 48:5461 101. Sardesai N, Nemacheck JA, Subramanyam S, Williams CE. 2005. Identication and mapping of H32, a new wheat gene conferring resistance to Hessian y. Theor. Appl. Genet. 111:116773 102. Shorthouse JD, Rohfritsch O, eds. 1992. Biology of Insect-Induced Galls. New York: Oxford Univ. Press 103. Shukle RH, Grover PB, Mocelin G. 1992. Response of susceptible and resistant wheat associated with Hessian y (Diptera: Cecidomyiidae) infestation. Environ. Entomol. 21:84553 104. Shukle RH, Mittapalli O, Morton PK, Chen MS. 2009. Characterization and expression analysis of a gene encoding a secreted lipase-like protein expressed in the salivary glands of the larval Hessian y, Mayetiola destructor (Say). J. Insect Physiol. 55:10512 105. Shukle RH, Subramanyam S, Saltzmann KA, Williams CE. 2010. Ultrastructural changes in the midguts of Hessian y larvae feeding on resistant wheat. J. Insect Physiol. 56:75460 106. Smiley RW, Gourlle JA, Whittaker RG, Easley SA, Kidwell KK. 2004. Economic impact of Hessian y (Diptera: Cecidomyiidae) on spring wheat in Oregon and additive yield losses with Fusarium crown rot and lesion nematode. J. Econ. Entomol. 97:304408 107. Stuart JJ, Hatchett JH. 1987. Morphogenesis and cytology of the salivary gland of the Hessian y, Mayetiola destructor (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 80:47582 108. Stuart JJ, Hatchett JH. 1988. Cytogenetics of the Hessian y, Mayetiola destructor (Say): II. Inheritance and behavior of somatic and germ-line-limited chromosomes. J. Hered. 79:19099 109. Subramanyam S, Sardesai N, Puthoff D, Meyer J, Nemacheck J, et al. 2006. Expression of two wheat defense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci. 170:90103 110. Tanaka R, Nei M. 1989. Positive Darwinian selection observed at the variable-region genes of immunoglobulins. Mol. Biol. Evol. 6:44759 111. Tokuda M, Yukawa J, Suasa-Ard W. 2008. Dimocarpomyia, a new oriental genus of the tribe Asphondyliini (Diptera: Cecidomyiidae) inducing leaf galls on longan (Sapindaceae). Ann. Entomol. Soc. Am. 101:3016 112. Tooker JF, De Moraes CM. 2007. Feeding by Hessian y [Mayetiola destructor (Say)] larvae does not induce plant indirect defences. Ecol. Entomol. 32:15361 113. Tooker JF, Moraes CM. 2010. Feeding by Hessian y [Mayetiola destructor (Say)] larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling. J. Plant Growth Regul. 30:15865 114. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM. 2008. Gall insects can avoid and alter indirect plant defenses. New Phytol. 178:65771 115. Torto-Alalibo TA, Collmer CW, Lindeberg M, Bird D, Collmer A, Tyler BM. 2009. Common and contrasting themes in host celltargeted effectors from bacterial, fungal, oomycete and nematode plant symbionts described using the gene ontology. BMC Microbiol. 9:S3 116. Uechi N, Yukawa J, Usuba S. 2005. Discovery of an additional winter host of the soybean pod gall midge, Asphondylia yushimai (Diptera: Cecidomyiidae). Appl. Entomol. Zool. 40:597607 117. Watson S. 2005. Hessian y problems have been increasing in recent years in the Central Plains. Wheat Farmer Row Crop Farmer 9:45 118. White MJD. 1973. Animal Cytology and Evolution. London: Cambridge Univ. Press. 468 pp. 119. Widenfalk O, Gyllenstrand N, Sylv en E, Solbreck C. 2002. Identity and phylogenetic status of two sibling gall midge species (Diptera: Cecidomyiidae: Contarinia) on the perennial herb Vincetoxicum hirundinaria. Syst. Entomol. 27:51928 120. Williams CE, Nemacheck JA, Shukle JT, Subramanyam S, Saltzmann KD, Shukle RH. 2011. Induced epidermal permeability modulates resistance and susceptibility of wheat seedlings to herbivory by Hessian y larvae. J. Exp. Bot. 62:452131 121. Wu J-X, Liu X-M, Zhang S-Z, Zhu Y-C, Whitworth RJ, Chen MS. 2008. Differential responses of wheat inhibitor-like genes to Hessian y, Mayetiola destructor, attacks during compatible and incompatible interactions. J. Chem. Ecol. 34:100512
356 Stuart et al.

Annu. Rev. Phytopathol. 2012.50:339-357. Downloaded from www.annualreviews.org by D'Youville College on 02/26/13. For personal use only.

Annu. Rev. Phytopathol. 2012.50:339-357. Downloaded from www.annualreviews.org by D'Youville College on 02/26/13. For personal use only.

122. Xu SS, Chu CG, Harris MO, Williams CE. 2011. Comparative analysis of genetic background in eight near-isogenic wheat lines with different H genes conferring resistance to Hessian y. Genome 54:8189 123. Yu GT, Cai X, Harris MO, Gu YQ, Luo M-C, Xu SS. 2009. Saturation and comparative mapping of the genomic region harboring Hessian y resistance gene H26 in wheat. Theor. Appl. Genet. 118:158999 124. Yu GT, Williams CE, Harris MO, Cai X, Mergoum M, Xu SS. 2010. Development and validation of molecular markers closely linked to H32 for resistance to Hessian y in wheat. Crop Sci. 50:1325 125. Yukawa J, Rohfritsch O. 2005. Biology and ecology of gall-inducing Cecidomyiidae (Diptera). See Reference 89, pp. 273304 126. Yukawa J, Uechi N, Horikiri M, Tuda M. 2003. Description of the soybean pod gall midge, Asphondylia yushimai sp. n. (Diptera: Cecidomyiidae), a major pest of soybean and ndings of host alternation. Bull. Entomol. Res. 93:7386 127. Zantoko L, Shukle RH. 1997. Genetics of virulence in the Hessian y to resistance gene H13 in wheat. J. Hered. 88:12023 128. Zhang H, Anderson KM, Stuart JJ, Cambron S, and Harris MO. 2011. A reproductive tness cost associated with Hessian y (Diptera: Cecidomyiidae) virulence to gene-for-gene resistance. J. Econ. Entomol. 104:105564 129. Zhang SZ, Shukle R, Mittapalli O, Zhu YC, Reese JC, et al. 2010. The gut transcriptome of a gall midge, Mayetiola destructor. J. Insect Physiol. 56:1198206 130. Zhu L, Liu X, Liu X, Jeannotte R, Reese JC, et al. 2008. Hessian y (Mayetiola destructor) attack causes a dramatic shift in carbon and nitrogen metabolism in wheat. Mol. Plant-Microbe Interact. 21:7078 131. Zhu YC, Liu X, Maddur AA, Oppert B, Chen MS. 2005. Cloning and characterization of chymotrypsinand trypsin-like cDNAs from the gut of the Hessian y [Mayetiola destructor (Say)]. Insect Biochem. Mol. Biol. 35:2332

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An Ideal Job Kurt J. Leonard p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Arthur Kelman: Tribute and Remembrance Luis Sequeira p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 15 Stagonospora nodorum: From Pathology to Genomics and Host Resistance Richard P. Oliver, Timothy L. Friesen, Justin D. Faris, and Peter S. Solomon p p p p p p p p p p 23 Apple Replant Disease: Role of Microbial Ecology in Cause and Control Mark Mazzola and Luisa M. Manici p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 45 Pathogenomics of the Ralstonia solanacearum Species Complex St ephane Genin and Timothy P. Denny p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 67 The Genomics of Obligate (and Nonobligate) Biotrophs Pietro D. Spanu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 91 Genome-Enabled Perspectives on the Composition, Evolution, and Expression of Virulence Determinants in Bacterial Plant Pathogens Magdalen Lindeberg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111 Suppressive Composts: Microbial Ecology Links Between Abiotic Environments and Healthy Plants Yitzhak Hadar and Kalliope K. Papadopoulou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 133 Plant Defense Compounds: Systems Approaches to Metabolic Analysis Daniel J. Kliebenstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 155 Role of Nematode Peptides and Other Small Molecules in Plant Parasitism Melissa G. Mitchum, Xiaohong Wang, Jianying Wang, and Eric L. Davis p p p p p p p p p p p p 175 New Grower-Friendly Methods for Plant Pathogen Monitoring Solke H. De Boer and Mar a M. L opez p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 197 Somatic Hybridization in the Uredinales Robert F. Park and Colin R. Wellings p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 219

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Interrelationships of Food Safety and Plant Pathology: The Life Cycle of Human Pathogens on Plants Jeri D. Barak and Brenda K. Schroeder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 241 Plant Immunity to Necrotrophs Tesfaye Mengiste p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267 Mechanisms and Evolution of Virulence in Oomycetes Rays H.Y. Jiang and Brett M. Tyler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 295 Variation and Selection of Quantitative Traits in Plant Pathogens Christian Lannou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 319
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Gall Midges (Hessian Flies) as Plant Pathogens Jeff J. Stuart, Ming-Shun Chen, Richard Shukle, and Marion O. Harris p p p p p p p p p p p p p p 339 Phytophthora Beyond Agriculture Everett M. Hansen, Paul W. Reeser, and Wendy Sutton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 359 Landscape Epidemiology of Emerging Infectious Diseases in Natural and Human-Altered Ecosystems Ross K. Meentemeyer, Sarah E. Haas, and Tom as V aclav k p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 379 Diversity and Natural Functions of Antibiotics Produced by Benecial and Plant Pathogenic Bacteria Jos M. Raaijmakers and Mark Mazzola p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 403 The Role of Secretion Systems and Small Molecules in Soft-Rot Enterobacteriaceae Pathogenicity Amy Charkowski, Carlos Blanco, Guy Condemine, Dominique Expert, Thierry Franza, Christopher Hayes, Nicole Hugouvieux-Cotte-Pattat, Emilia L opez Solanilla, David Low, Lucy Moleleki, Minna Pirhonen, Andrew Pitman, Nicole Perna, Sylvie Reverchon, Pablo Rodr guez Palenzuela, Michael San Francisco, Ian Toth, Shinji Tsuyumu, Jacquie van der Waals, Jan van der Wolf, Fr ed erique Van Gijsegem, Ching-Hong Yang, and Iris Yedidia p p p p p p p p p p p p p p p p p p p p p p 425 Receptor Kinase Signaling Pathways in Plant-Microbe Interactions Meritxell Antol n-Llovera, Martina K. Ried, Andreas Binder, and Martin Parniske p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 451 Fire Blight: Applied Genomic Insights of the Pathogen and Host Mickael Malnoy, Stefan Martens, John L. Norelli, Marie-Anne Barny, George W. Sundin, Theo H.M. Smits, and Brion Duffy p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 475 Errata An online log of corrections to Annual Review of Phytopathology articles may be found at http://phyto.annualreviews.org/
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