annurev-phyto-072910-095255

PY50CH17-Stuart ARI 4 July 2012 14:17

Gall Midges (Hessian Flies)as Plant PathogensJeff J. Stuart,1 Ming-Shun Chen,2 Richard Shukle,3

and Marion O. Harris4

1Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089;email: [email protected] and Department of Entomology, Kansas State University, Manhattan,Kansas 66506; email: [email protected] and Department of Entomology, Purdue University, West Lafayette,Indiana 47909-2089; email: [email protected] of Entomology, North Dakota State University, Fargo, North Dakota 58105;email: [email protected]

Annu. Rev. Phytopathol. 2012. 50:339–57

First published online as a Review in Advance onMay 29, 2012

The Annual Review of Phytopathology is online atphyto.annualreviews.org

This article’s 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, avirulencegene, effector proteins, nutritive tissue

Abstract

Gall midges constitute an important group of plant-parasitic insects.The Hessian fly (HF; Mayetiola destructor), the most investigated gallmidge, was the first insect hypothesized to have a gene-for-gene inter-action with its host plant, wheat (Triticum spp.). Recent investigationssupport that hypothesis. The minute larval mandibles appear to act ina manner that is analogous to nematode stylets and the haustoria offilamentous plant pathogens. Putative effector proteins are encodedby hundreds of genes and expressed in the HF larval salivary gland.Cultivar-specific resistance (R) genes mediate a highly localized plantreaction that prevents the survival of avirulent HF larvae. Fine-scalemapping of HF avirulence (Avr) genes provides further evidenceof effector-triggered immunity (ETI) against HF in wheat. Takentogether, 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 hasin the study of insect-induced plant gall formation.

339

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


INTRODUCTION

In 1970, Hatchett & Gallun reported that thegenetic interaction between wheat (Triticumspp.) and Hessian fly (HF; Mayetiola destruc-tor) fit the gene-for-gene model (57). This dis-covery firmly connected an insect to a conceptthat was of major interest in plant pathology.During the ensuing years, plant pathologistshave made remarkable progress in understand-ing how plant immunity and pathogen effec-tors underlie gene-for-gene interactions (12,62), but only a few reports tied the emerg-ing paradigm to plant defense against insects(64). The most important of these includedthe discovery that the cloned Mi resistance (R)gene confers resistance to potato aphids andwhiteflies (86, 99), and the discovery that an-other cecidomyiid, the Asian rice gall midge(Orseolia oryzae), has a gene-for-gene interac-tion with rice (9, 13). The paucity of data hasbeen attributed to the lack of good experimentalsystems (56); most plant-parasitic insects havesimply not been amenable to classical geneticanalysis. However, genomic technologies arechanging this situation, permitting one to askwhether some insects are another form of plantpathogen, albeit with unique attributes (18, 59).

This question brings us back to the HF, aninsect that is both an important pest and in-creasingly amenable to genetic and genomicanalyses. This review is centered on the hypoth-esis that gall midges use an effector-based strat-egy that is remarkably similar to the one used byplant-pathogenic organisms and the discoveriesthat support that hypothesis (Figure 1). Ourgoals are to review those aspects of the wheat-HF interaction that are relevant to plant pathol-ogy and to present the capacity of the HF as anexperimental model. The review is organized topresent detailed pictures of both the compat-ible and incompatible wheat-HF interactionsas well as what is known regarding the effec-tors, the R genes, and the avirulence (Avr) genesthat underlie these interactions. We are con-vinced that the wheat-HF interaction has muchto offer both plant pathologists and entomolo-gists as a model for investigations of plant-insect

E

R

E

Modulation ofhost development

Resistance

Salivary gland

HF larva

Plant cell

Mandible

Cell wall

Chloroplast

Cytoplasm Nucleus

E

Figure 1Diagram illustrating the hypothesized wheat–Hessian fly (HF) interaction, modeled afterTorto-Alalibo et al. (115). The first-instar HF larvadelivers effector proteins (E) produced in its salivarygland through highly modified mandibles into orjust below the cell walls of expanding leaf sheathepidermal cells. Direct or indirect interactions withresistance proteins (R) elicit resistance responsesthat kill the larva. In the absence of cognateresistance proteins, the effectors defeat host defenseand induce plant galling.

interactions and insect-induced plant gall for-mation. Because the HF is a gall midge, a rel-atively large, understudied, and economicallyimportant group of insects (43, 44), we beginwith a brief description of the biology of the gallmidge family (Cecidomyiidae), giving emphasisto the evolution of the gall-forming habit.

GALL MIDGE BIOLOGY

The gall midges (Diptera: Cecidomyiidae) be-long to the lower Diptera (the Nematocera),which includes other midges, black flies, gnats,and mosquitoes (97). They likely arose dur-ing the Cretaceous period and are probably

340 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


most closely related to mycetophilids and fun-gus gnats (14). More than 5,700 cecidomyiidspecies have been described (35, 44), and newspecies are regularly discovered (67, 68, 111).The phylogenetic relationships among speciesare still being determined (36, 119), and im-portant host relationships are still being clari-fied (37, 116, 126). For those that are interestedin their study, Raymond Gagne’s books are es-sential (43, 44). They present a comprehensiveaccount of general gall midge biology; the his-tory of cecidomyiid study; useful keys; and a de-scription of gall midge collection, rearing, andspecimen preparation.

According to Roskam (97), the Cecidomyi-idae is composed of four subfamilies. Threeof these, the Catotrichinae, Lestreminnae, andPorricondylinae, are relatively ancient groupswith a combined total of approximately 1,300species that typically live on saprophytic fungi(35). Some of these species reproduce via anunusual form of cyclic parthenogenesis thatinvolves both chromosome elimination andpaedogenesis (immature asexual reproduction).The cytology associated with these phenom-ena was once intensely investigated (66). M.J.D.White was a major participant in these investi-gations, and he summarized his findings and thediscoveries of others in a chapter covering theevolution of aberrant genetic systems (118). Fora more recent and comprehensive treatment ofthese investigations, dating back to 1908, thereader is referred to Matuszewski’s 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 feedby extracting liquids (81). Gagne uses the termgall midge to refer to the plant-galling speciesand cecidomyiid to refer to any member of thefamily (43). We use the same terminology here.The majority of the species in the Cecidomyi-inae (∼4,000 species) are gall midges (43).These evolved in an explosive adaptive radia-tion on flowering plants (87). Compared withother gall-forming insect taxa, the gall midgeshave colonized the widest variety of plants: 89plant families in North America alone (43, 87).

As a group, gall midges produce plant galls onthe buds, stems, leaves, flowers, and fruit ofdicotyledons, monocotyledons, gymnosperms,ferns, and mushrooms (44). Most species areadapted to only one type of plant tissue on asingle plant species or a closely related group ofspecies, and certain plants are host to multiple,monophyletic, gall midge species (63). As withmost parasites, gall midge life cycles are highlysynchronized with those of their hosts (43).From the standpoint of plant pathology, it isinteresting to note that the gall-forming habitclearly evolved from mycetophagy (81, 97, 98).In addition, extant species in three gall midgetribes live symbiotically with fungi in ambrosiagalls (125), in which a gall midge inoculates theplant with a fungus and feeds on fungal myceliawhile the fungus undermines plant defenses, in-duces the gall, and extracts nutrients (96). Thus,two evolutionary routes between mycetophagyand gall-forming herbivory were possible (97):(a) a direct route and (b) a transitional routein which ambrosia galls were intermediate.Phylogenetic, anatomical, and ecologicalanalyses suggest that both routes occurredmultiple times (16, 81, 97, 98). It remainsan open question whether horizontal genetransfer played a role in any of the transitions.

In many respects, the biology of gallmidges overtly resembles that of manyplant pathogens; they have biotrophic orhemibiotrophic lifestyles, the feeding (in-fection) site is localized, and the gall midgeinduces both plant susceptibility and qualitativeresistance. Gall midges are also able to repro-duce quickly; adult females emerge with a fullcohort of mature eggs and typically have lessthan one day to deposit those eggs before theydie (56). Although adults are short lived, gallmidges have another nonfeeding life stage, thelast larval instar, which, like a spore, can surviveextended periods of harsh environmental con-ditions. Nonfeeding larvae have been observedto remain in diapause for years, with 12 yearsbeing the record for Sitodiplosis mosellana (8).

Unlike plant-parasitic microorganisms, gallmidges have a central nervous system and sen-sory organs that are essential for mating, active

www.annualreviews.org • The Hessian Fly Gall Midge 341

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


dispersal, and plant selection. The wingedadult is free-living and entirely devoted tosexual reproduction. Adult males are attractedto a volatile sex pheromone produced by virginadult females (52). Males mate many times, butfemales mate only once (56). Host selection isthe responsibility of the mated adult female,who typically has less than a day to find hostsusing a relatively sophisticated behavior, whichinvolves discrimination of the plant’s chemical,visual, and physical cues (65). Host selection iscritical to reproductive fitness (55).

HESSIAN FLY BIOLOGY

The HF is one of the most economicallyimportant gall midges. It belongs to a genuscontaining 29 species whose larvae live ongrasses (45). Its biology resembles that of themajority of cecidomyiids, but because it attackswheat seedlings, and up to 50 larvae can surviveon the same seedling (gall), it is the mostamenable to propagation in the laboratory(56). HFs are easily reared and maintainedat 17 to 24◦C in either the greenhouse orgrowth chamber. The life cycle is completedin approximately 28 days and consists of theegg, three larval instars, the pupa, and the adult(Figure 2). The pheromone that adult femalesuse to attract mates has been identified (5).Females distribute their eggs (∼200) on the up-per surfaces of young wheat leaves (Figure 2a).Only the first and second larval instars feed.After hatching, the first-instar larvae crawl tothe base of the seedling, where they attemptto establish a feeding site (Figure 2b). Asdescribed in greater detail below, first-instarlarval modulation of plant development iscritical to larval survival. Second-instar larvaeare sessile and imbibe the liquids presented tothem by the reprogrammed plant (the gall).Third-instar larvae and pupae develop withina puparium, which consists of the cuticle of thesecond-instar larva (Figure 2c,e). This cuticleeventually hardens, sclerotizes, and becomesdark brown. Because of its appearance, thisstage is commonly referred to as the flax seed.

HF adults eclose from the puparia and live foronly one to four days (56). The HF is not asso-ciated with a fungus, but it does harbor severalspecies of bacteria that are transferred via theanus of the modified adult female gut intoeach of her eggs upon oviposition (6). The rolethese bacteria play in HF survival is uncertain.As third instars, HFs can enter a cold-induceddiapause and can be conveniently maintainedin diapause at 4◦C for up to a year. After threemonths in the cold, room temperature breaksdiapause, and adults emerge in 10–14 days.Females typically produce offspring of onlyone sex (11). Therefore, by isolating families ofindividual females on caged pots, one can easilyobtain 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 in-jury anywhere wheat is grown in the UnitedStates (27, 71, 90, 106, 117). The insect is of-ten a greater problem in the southern UnitedStates because there are typically more genera-tions per year in the south (six to eight) than inthe north, and there is no planting time whenHF is dormant (20, 23, 40). HF damage ex-ceeded $4 million per year from 1984 to 1989 inSouth Carolina (25). Yield loss in Georgia from1988 to 1989 was $20 million (21), and lossesof 21 bushels per infested acre occurred in 1985in Alabama (40). The deployment of cultivar-specific R genes has been the most successfulHF control strategy (23, 27, 56). Historically,however, virulent genotypes (biotypes) in HFpopulations overcome the resistance conferredby single R genes in six to eight years (27, 42,82, 90). Because wheat acreage is expected toincrease, tillage conservation is expanding, andthe frequency of virulence in HF populationsis increasing, future economic losses from HFare predicted to be as high as any time in therecent past (33, 40). Therefore, there is a needfor virulence diagnostics, stacked R genes, andthe development of genetically engineered re-sistance to protect wheat from HF attack.

342 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


a c d e

11 223 4

34

5

b

1 mm1 mm1 mm1 mm

1 mm1 mm

1 mm1 mm

1 mm

Figure 2Critical stages in the Hessian fly (HF) life cycle. (a) HF female depositing eggs (arrowhead ) in the grooves onthe upper surface of a wheat leaf. (b) Multiple first-instar HF larvae (arrowhead ) attempting to develop afeeding 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 ofinternodes between the � second, � third, and � fourth leaves. The plant is permanently stunted, andthere will be no further growth from its apical meristem. (d ) HF-infested, resistant, wheat seedling 15 daysafter infestation. Note the light green color, the presence of internodes, and the presence of a � fifth leafinitial. Dead first-instar larvae, which are typically present behind the leaves at the base of the seedling, arenot visible in this photograph. (e) The first 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 ge-nomic organization and chromosome behavioris unusual, involving both chromosome im-printing and chromosome elimination (11).HF chromosomes are classified as eitherE (eliminated) or S (somatic), according toconvention (118). The E chromosomes vary innumber and are strictly germ-line-limited andstrictly maternally inherited. They are essential

only to the development of the male and femalegonads (7). As in other dipteran species, thesomatic (S) chromosome number is small, andlike most gall midges, the HF S chromosomesconsist of two autosomes (A1 and A2) andtwo X chromosomes (X1 and X2) (108, 118).The S chromosomes are diploid in the germline and form chiasmata during oogenesis,but fail to recombine during spermatogen-esis. Ova contain a haploid complement of


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


N

A1

vH5vH24

vH13

vH9

vH6vHdic

X1

X2A2

BAC contigs

Figure 3Hessian fly larval salivary gland polytene chromosomes illustrating the abilityto use fluorescence in situ hybridization to resolve the relative positions ofbacterial artificial chromosome (BAC) contigs. Green and red fluorescenceindicates the positions of 17 different BAC contigs on the autosomes (A1 andA2). None of the BACs in this preparation hybridized to the X chromosomes(X1 and X2). The locations of the centromeres (arrowheads) and the nucleolarorganizer (N) are indicated. The positions of six Avr genes (vH5, vH6, vH9,vH13, vH24, and vHdic) that have been genetically and physically mapped onthe chromosomes are shown.

S chromosomes and between 24 and 32 Echromosomes (A1A2X1X2E). Sperm carryonly the maternally derived S chromosomes(A1A2X1X2). Ova and sperm combine toform zygotes that have a full complement of Echromosomes and a diploid number of S chro-mosomes (A1A2X1X2E/A1A2X1X2). The Echromosomes are always eliminated from thepresumptive somatic cells during early embryo-genesis. If only the E chromosomes are elimi-nated, the embryo develops as a female with 2n= 8 S chromosomes (A1A2X1X2/A1A2X1X2)in the soma. However, if the paternally derivedX1 and X2 chromosomes are also eliminated,the embryo develops as a male with 2n =6 S chromosomes (A1A2X1X2/A1A2OO) inthe soma. Maternal genotype conditions theretention or elimination of the paternallyderived X chromosomes and, in so doing, thesex of the offspring (11). Thus, females usuallyproduce either all-female or all-male broods.

Because the HF interaction with wheat in-volves only somatic tissues, HF genomics hasfocused almost exclusively on the S chromo-somes. The S genome size is relatively small(∼158 Mb) (61), and importantly, the S chro-mosomes are polytene in the HF larval sali-vary glands (Figure 3). Thus, although exper-imental matings do permit the development ofgenetic maps, the polytene chromosomes alsopermit physical mapping at a relatively highresolution (10). Therefore, HF bacterial arti-ficial chromosome (BAC) contigs were devel-oped uisng high-resolution DNA fingerprintsof end-sequenced BACs, and the largest contigswere then physically positioned on the chromo-somes using fluorescence in situ hybridization(1). This placed approximately 60% of the HFgenome on the chromosomes as end-sequencedBAC contigs. In turn, the physical map servedas a reference that was subsequently used to as-sign whole genome shotgun sequencing data tochromosomes (93). These data have been sub-mitted to GenBank (Accession PRJNA45867),and a HF genome browser supports the data(19).

THE WHEAT–HESSIANFLY INTERACTION

Interactions between plants and their parasiticfungi, oomycetes, and nematodes suggest thatplant immunity has required each group of par-asites to converge on a similar effector-basedmechanism of attack (62, 115). The mechanicsof HF attack, the presence of transcripts encod-ing putative effector proteins in the HF salivarygland, and the gene-for-gene manner in whichwheat R genes provide HF resistance suggestthat insect plant parasites use the same strategy(Figure 1).

The physical interaction between wheat andHF begins when a neonate larva (460 μmlong) emerges from an egg that was depositedon the upper surface of a young wheat leaf(Figure 2a). The larva then uses the parallelvenation of the leaf to guide its migration(1 cm h−1) down the leaf blade and enterthe shelter that bundled leaf sheaths provide.

344 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


hh

m

bb

ggh

m

tt1 1 μm1 μm

Figure 4Mesal view of the first-instar mandible showing thehole (h) at the base of the grove (g) in the blade (b)of the mandible and the minute teeth (t) positionedbehind the blade along the mandible’s dorsal edge.The position of the mouth (m) of the insect isindicated. Scanning electron micrograph kindlyprovided by J.H. Hatchett.

Within 1 to 2 cm of the base of the leaf, thelarva attacks the still-expanding sheath epider-mal cells of the abaxial surface of the adja-cent, younger leaf (53, 54) (Figure 2b). Sixdecades ago, Painter concluded that the first-instar larva is incapable of physically rupturingplant cells (58), and recent investigations sup-port that conclusion. First-instar HF larvae usepaired, microscopic mandibles to penetrate intothe cell wall (53, 54, 58) (Figure 4). The tip ofthe mandible resembles the end of a hypoder-mic needle; it is grooved on the internal lateralsurface, and this groove extends from the tipof the mandible internally into the basal hole.Salivary fluid is presumably delivered throughthe hole so that it travels down the groove andinto the small punctures that have been ob-served in the cell walls of infested plants (53).The mandible blades extend into, or perhapsthrough, the epidermal cell wall but do not ap-pear long enough to pierce the plasma mem-brane. They therefore appear to act in a mannerthat is analogous to a short stylet, or haustorium(115), that injects effectors into, or just below,

the cell wall without physically disturbing theplasma membrane (54) (Figure 1). The cellu-lar responses that follow this attack have beenexamined in both compatible and incompatibleinteractions.

The Compatible Interaction

To benefit its own growth, the successful larvaalters the developmental pathways of wheatcells, severely compromising the growth of theplant (2, 3, 53, 54, 130) (Table 1). The epi-dermal and mesophyll sheath cells near thefeeding site become the nutritive feeding cells(54) that characterize all gall midge–inducedgalls (95). These have an enriched cytoplasm,an altered nucleus, and a thin cell wall thateventually breaks down to provide a liquiddiet to the larva (54). Cell division and cellelongation cease, and chloroplasts accumu-late (24). Outwardly, HF-infested susceptiblewheat seedlings appear dark green and stunted(Figure 2c,e). Although the seedling may com-pensate by tillering (4), the shoot apical meris-tem eventually dies. Plants that are attackedduring stem elongation have similar symptoms,tend to lodge, and produce heads with lessseed weight and fewer seeds (91). Like othergall midges (114), the HF avoids inducing theproduction of plant volatiles that might attractparasitoids and predators (112, 113).

These symptoms are associated with alteredpatterns of plant gene transcription (Table 1).Most upregulated genes of known function areinvolved in nutrient metabolism and transport(72). Some of these genes encode stress pro-teins (heat-shock proteins and components ofthe ubiquitin pathway), which may reflect thestate of stress exerted by HF attack. Othersencode transcription factors, which may beused to modulate plant development. Themost interesting change is the coordinatedupregulation of genes involved in primarymetabolic pathways (130). These changes mayreflect an elevated consumption of carbohy-drates and an elevated synthesis of amino acids.This possibility is consistent with both theobservation that the carbon-to-nitrogen ratio is


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


Table 1 Phenotypic responses of wheat and Hessian fly during compatible and incompatibleinteractions

Compatible interaction Incompatible interactionLarval growth completed in 10–12 days Larvae die within 5 days of attack

No larval growthGut shows signs of toxin exposure

Seedling apical shoot meristem deathShorter plants, fewer heads, fewer seeds

Seedling survival

Increased cell permeability at attack sitesCreation of nutritive cellsCell wall breakdown

Localized cell deathAccumulation of reactive oxygen speciesAdjacent living cells are fortifiedTransient increase in permeabilityEpicuticular waxes accumulate

Membrane permeability increasesa

Stress-related proteins increasea

C/N ratio shift favors N (52% change)a

Nutrient metabolism and transport increasesa

Toxin production increasesa

Class III peroxidases increasea

Phenylpropanoid metabolism increasesa

Cell wall and lipid metabolism increasesa

Basal defense responses suppresseda

Cell wall metabolism decreasesa

Phenylpropanoid metabolism suppresseda

Histones and structural proteins decreasea

Nutrient metabolism and transport suppresseda

Fatty acid degradation suppresseda

Phospholipid metabolism suppresseda

Stress-related proteins decreasea

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

dramatically decreased at the feeding site (100,130), and the requirements of an insect thatlives on a food source that is normally nitrogenpoor. Other upregulated genes may act to makenutrients more accessible for the growing larva(72). These include genes encoding a varietyof nutrient transporters. Interestingly, thewheat gene Hfr-2, which encodes a cytolytictoxin-like protein with multiple agglutinindomains and a membrane-binding domain, isalso upregulated (88). It is possible that thisprotein inserts into cell membranes and makesthem more permeable.

Not surprisingly, many plant defense genesare downregulated (Table 1). These in-clude genes encoding protease inhibitors,lectins, enzymes involved in secondary metabo-lite synthesis (O-methyltransferases and chal-cone synthases), enzymes involved in cellwall metabolism (xyloglucan endotransgly-cosylases and cellulose synthases) (72), li-pases and lipid transfer proteins (100), andclass III peroxidases (72). Consistent withan inhibition of plant growth and a low-ered demand for structural proteins, genes

encoding various histones and a histone acetyl-transferase are also strongly downregulated(72).

In the HF, both the mandibles and the sali-vary glands display morphological changes thatare correlated with changes in wheat morphol-ogy (58, 107) (Table 1). Only four days afterinfestation by just a single larva, susceptiblewheat seedlings are irreversibly compromised(2, 3, 22, 103): Plant seedlings are stunted, plantdefense genes are suppressed (72), metabolicpathways in the plant are reprogrammed (130),nutrient tissue forms (54), and the cell wallsnear the feeding site become thin and perme-able (53, 69, 120). During this period, the larvaremains a first instar, its mandibles are sharp,and the basal cells of the salivary gland are fullydeveloped. After the plant has been irreversiblytransformed into a permeable nutrient sink(120), the larva molts into a second instar, itsmandibles are blunt, and the basal salivary glandcells begin to decay (58, 107). Thus, the first-instar larval stage is critical to gall formation andinsect survival, and the first-instar larval salivarygland is the most obvious source of the factors

346 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


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

Putative Effector Proteins

Within the first-instar salivary gland, morethan 50% of all transcripts encode proteinscontaining a secretion signal (26, 76). Less than5% of these encode proteins with sequencesimilarity to known proteins; these includeproteases (73, 131) and protease inhibitors (80),which are also expressed in the larval gut (129),and lipase-like proteins (104). The remainingsignal peptide–encoding transcripts encode pu-tative effector proteins called secreted salivarygland proteins (SSGPs) (28). SSGPs lack se-quence similarity to any other known proteins(31). Hundreds of SSGP-encoding transcriptshave been classified into families and super-families on the basis of sequence similarities(31). The majority of these encode small (50-to 250-residue) proteins. Genomic analyses ofa few SSGP families found that most of therelated transcripts are nonallelic; that familymembers are often clustered within smallchromosomal segments; and that within thesesegments, the genes appear to be experiencingstrong positive selection and functional adapta-tion (29, 30). Remarkably, among genes withingene families, the noncoding genic regionshave far more sequence similarity (75%–95%)than the regions encoding the mature proteins(30%–60%). Such strong positive selection isusually associated with genes that function ininterspecies molecular recognition, e.g., thegenes encoding immunoglobulins (110), plantR genes (84), and plant pathogen effectors (85).The possibility that SSGPs are effectors isfurther supported by the observation that geneswith a similar pattern of sequence conservationwere discovered in the salivary gland tran-scriptome of another gall-forming gall midge,the Asian rice gall midge (O. oryzae), but theywere absent in the salivary transcriptomes ofa wheat-seed-feeding cecidomyiid, the wheatblossom midge (Sitodiplosis mosellana) (30).

The dependence of the HF on induced nu-tritive tissue, the abundance and small size of

SSGP-encoding transcripts, their presence inthe first-instar salivary gland, and their unusualpattern of conservation leave little doubt that atleast some of these genes encode effector pro-teins that modulate plant development. Nev-ertheless, the role that individual SSGPs playin this process remains to be determined. Thusfar, efforts to identify the corresponding pro-teins with peptide-based antibodies have notbeen successful (31). Possible reasons for thisare that little or no protein may be produced,that only some of the transcripts are translated,or that the SSGPs are secreted into host tissuesimmediately after translation. We also antic-ipate that functional redundancies exist withinSSGP families, as they do in oomycete effectors(15), and that these will complicate the devel-opment of assays capable of testing how SSGPsfunction in compatible interactions. With re-gard to incompatible interactions, as describedbelow, genetic evidence clearly points to cer-tain SSGPs as the elicitors of effector-triggeredimmunity (ETI) (Figure 1).

The Incompatible Interaction

Precisely how resistant wheat plants preventthe creation of nutritive cells and cause HFlarval death is not known. However, thereaction is clearly induced and highly localized,and it resembles the subcellular responsesthat mediate plant responses to fungal at-tack (53) (Table 1). Outwardly, the planttypically displays little evidence of HF attack(Figure 2d ). Immediately at the site of attack, asmall number of epidermal cells die (50, 53), andreactive oxygen species (ROS) accumulate (74).Adjacent epidermal and mesophyll cells survivethe attack and exhibit swollen mitochondria,reinforced cell walls, and an elaboration of theGolgi complex–endoplasmic reticulum withmany small vesicles docking at the plasmamembrane (53). A granular material accumu-lates in the paramural space between the plasmamembrane and the outer cell wall, and withinpockets embedded in the outer cell wall. Thesegranular materials may be toxins (47, 109);larvae attempting to feed on resistant plants


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


exhibit the disrupted midgut microvilli thatcharacterize insect exposure to gut toxins (105).

Changes in plant gene expression cor-respond with these histological changes(Table 1). Upregulated genes in responseto HF include those that encode moleculesknown to have insect toxicity (26, 32, 38,70), including those encoding wheat proteaseinhibitors (72, 121), lectins (47, 72, 109), andenzymes that produce phenylpropanoids (72).Genes involved in cell wall metabolism arealso upregulated, including the genes encodingvarious xyloglucan endotransglycosylases,β-expansins, pectinesterases, glucanases, cellu-lose synthases, and dirigent-like proteins (72).Class III peroxidase genes are also upregulated(74) and may be responsible for generatingROS in response to HF just as they do inresponse to certain pathogens (17). In additionto a potential role in ROS generation, class IIIperoxidases could play other roles, such as cellwall cross-linking and signaling. Additionalupregulated genes encode lipid transfer pro-teins (60, 100) and a variety of lipases, whichare associated with the rapid mobilizationof membrane lipids at the attacked tissue(Y.C. Zhu, X. Liu, H. Wang, C. Khajuria,J.C. Reese, R.J. Whitworth, R. Welti, andM.-S. Chen, unpublished research). Analysisof lipid metabolism-related pathways indicatesthat the mobilized lipids may be convertedinto components of cuticle wax (69). Rapidmobilization of membrane lipids and othermolecules and subsequent conversion of theseinto components for cell wall strengtheningmay constitute a layer of defense that preventslarval mouthparts from placing effectors in theapoplast (53).

Hessian Fly R Genes in Wheat

Underlying the incompatible interaction are33 different HF R genes in wheat. These havebeen named H1-H3, h4, H5-H32, and Hdic(75, 101). All of these, except h4, are dominantor semidominant genes that have been eitherdiscovered in wheat or brought into wheatgermplasm via wide crosses (91). All genes havebeen shown either to recombine or to differ

with respect to their resistance to one or moreHF genotypes (biotypes). Thus far, only oneHF R gene (Hdic) has been cloned (X. Liu &M.-S. Chen, unpublished research). It containsboth the nucleotide binding (NB) and leucine-rich repeat (LRR) motifs that characterize themajority of the genes that confer resistance toplant pathogens (62). However, mapping dataalso indicate that other HF R genes encodeNB-LRR proteins: H3, H5, H6, H9, H10, H11,H12, H14, H15, H16, H17, H19, H28, and H29are all clustered in the distal gene-rich region ofwheat chromosome A1S, which contains Hdicand other NB-LRR genes (75, 77). AdditionalHF R genes are clustered with defense responsegenes in wheat: H13, H23, and another putativeHF resistance gene (HWGRC4) cluster with awheat curl mite R gene (Cmc4) on chromosome6DS (78), and H24, H26, and H32 are clusteredon chromosome 3DL (123, 124). Althoughpyramiding HF R genes was suggested asa deployment strategy years ago (48), mostreleases have involved only single genes (91).Only six (H12, H13, H18, H24, H25, and H26)have significant efficacy in the southern UnitedStates (23). The remainder either have losteffectiveness since they were deployed or nevershowed promise (91). Thus, there is a needfor the discovery of additional HF R genes aswell as novel control methods that preserve thegenes’ efficacy in HF populations.

Hessian Fly Avirulence Genes

The existence of HF R genes in wheat andputative effector-encoding genes in the HFsupports the hypothesis that the same ETIthat underlies gene-for-gene interactionsbetween plants and plant pathogens (62) alsounderlies wheat-HF incompatible interactions(Figure 1). To test that hypothesis further,genetic analyses have been performed todetermine if avirulence can be attributedto effector-encoding Avr genes. Hatchett &Gallun (57) began these investigations, showingthat virulence (the ability of HF larvae to sur-vive on and stunt wheat seedlings) to the R geneH3 and virulence to the coordinated R gene pairH7H8 are conditioned by independent, simply

348 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


inherited, recessive genetic factors. Withina few years, Gallun’s group had obtainedevidence of the first X-linked HF Avr gene andextended the gene-for-gene association to fourR genes in wheat (H3, H5, H6, and H7H8) (46).With the discovery that virulence to H9 andvirulence to H13 were clearly X-linked, theconvention of placing a small v (for recessivevirulence to) in front of the R gene name wasadopted in naming HF Avr genes (vH9 andvH13) (41, 127). The adoption of polymerasechain reaction (PCR)-based methods in theseinvestigations permitted greater resolutionin testing the gene-for-gene hypothesis (10,79, 94), and the current ability to resolve Avrgene positions on the FPC-based physical mapleaves little question regarding the hypothesis’sveracity (Figure 3). To date, six HF Avr genes(vH5, vH6, vH9, vH13, vH24, and vHdic) havebeen mapped within chromosome segmentsspanning less than 600 kb (10; J.J. Stuart,unpublished data). The resolution of the genesthat are near telomeres (vH9, vH13, and vH24),where recombination rates are greatest, is evenbetter ( J.J. Stuart, unpublished data).

WHEAT–HESSIAN FLYCOEVOLUTION

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

particularly the related grasses in the tribe Trit-iceae. Its genus (Mayetiola) contains 29 specieswhose larvae live on the stems of grasses (45).The HF’s center of origin overlaps with thecenter of origin of wheat (8, 34), and althoughwheat is its preferred host (56), the host range ofthe HF includes grasses in more than 17 genera,including many prairie grasses (Elymus canaden-sis, Pascopyrum intermedium, Thinopyrum inter-medium, and Agropyron cristatum) (8, 56). Manyof the more effective HF R genes (e.g., H26)have been found in grasses other than breadwheat (91, 125). This suggests that the HF andits allies have exerted significant selection pres-sure on grasses in the tribe Triticeae and thatH gene–mediated resistance has, in turn, beenan important source of selection pressure forHF adaptation (56). Supporting this idea arestudies showing that the highest frequenciesof virulence are found in HF populations inthe Fertile Crescent, near its shared center oforigin with wheat (39); here, there are onlytwo known H genes, H25 and H26, for whichvirulence has not been found.

One phenomenon that probably reduces Rgene selection pressure on the HF is resistanceobviation (51). To describe obviation, we useH13 as an example here (Table 2), but thephenomenon is probably common to all HF Rgenes ( J.J. Stuart, unpublished observations).When only H13-avirulent larvae attack an

Table 2 Gene-for-gene interactions involving Hessian fly strains and near-isogenic susceptibleand resistant wheat lines

Wheat isogenic line (122)

Hessian flystrain Newton (susceptible) Molly (H13-resistant)H13-Avirulent Compatible interaction

Hessian fly: larval survivalWheat: seedling mortality/seed loss

Incompatible interactionHessian fly: 100% larval mortalityWheat: normal or better reproduction

H13-Virulent Compatible interactionHessian fly: similar survival but 12% lossin reproduction

Wheat: seedling mortality/seed loss

Compatible interactionHessian fly: some larval survival but noloss in reproduction

Wheat: seedling mortality/seed lossAvirulent +virulent coattack

Compatible interactionHessian fly: both types of larvae surviveWheat: seedling mortality/seed loss

Resistance obviationHessian fly: both types of larvae surviveWheat: seedling mortality/seed loss


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


H13-protected plant, they trigger defenseresponses and die (53). However, when H13-virulent and H13-avirulent larvae co-attack,both types of larvae feed, survive, and de-velop into reproductive adults (51). Threenotable deductions can be drawn from theseobservations: (a) H13-avirulent larvae surviveby feeding on the nutritive tissue induced byH13-virulent larvae; (b) H13 resistance is highlylocalized (54) and susceptibility is systemic (3,130); and (c) H13 obviation provides refugia forH13-avirulent genotypes in areas where H13 isbeing used for HF control. These refugia areexpected to slow the evolution of H13-virulence(49).

Fitness costs also influence the rate at whichplants and their parasites adapt (92). Thesmaller the cost, the greater potential there isfor rapid evolution. It appears that wheat paysno cost for resistance (4). Using isogenic wheatlines carrying either H6, H9, or H13 R genes(122), there was no fitness cost for either Hgene expression or the downstream-inducedresistance responses triggered by avirulentlarvae (Table 2). In fact, for the H13 line,attacked plants produced even more seed thannonattacked controls. However, HF virulencedoes appear to have a cost (128). When rearedon susceptible plants, HFs virulent to multipleR genes developed into significantly smalleradults than avirulent strains. This size differen-tial translated into a 12% (for the strain virulentto 9 H genes) or 32% (for the strain virulent to

11 H genes) reduction in the female’s ability toproduce eggs, and an 11% or 18% reductionin the male’s potential to inseminate females.Thus, there may be a reproductive fitnesscost of 1% to 3% for the loss of each Avrgene. Taken together with the diversity ofputative effector-encoding genes in the HF,this observation suggests that selection favorsgenetic diversification for effector function tocompensate for Avr gene loss (15).

CONCLUSIONS

The HF shares many features with biotrophicor hemibiotropic plant pathogens. In fact, itis remarkable how many HF plant-parasiticmechanisms closely resemble those of nema-todes, fungi, and oomycetes (Figure 1). Theseinclude the manner in which the HF feeds onits host, its ability to modulate gene expres-sion, and the presence and structure of hun-dreds of putative effector-encoding genes in itsgenome. However, the most convincing argu-ment in favor of our hypothesis comes from theplant’s own perception of the disease-causingagent: Wheat responds to HF attack as if itwere a plant pathogen, using cultivar-specificNB-LRR R genes to guard against cognateAvr-gene-encoded effectors. There is now littledoubt that Hatchett & Gallun (57) were cor-rect when they proposed over four decades agothat gene-for-gene interactions exist betweenHF and wheat.

SUMMARY POINTS

1. Hessian fly interactions with wheat share important features with many plant pathogenand nematode interactions with plants, including a hemibiotrophic lifestyle, a sessilefeeding stage, a narrow host range, minute mouthparts, an effector-based mechanism ofattack, and ETI in the plant.

2. High-resolution genetic mapping utilizing the sequenced HF genome and an FPC-basedphysical map of the HF polytene chromosomes has permitted insect Avr gene mappingand discovery.

3. Hundreds of putative HF effector proteins exist in the HF genome. These show unmis-takable signs of diversifying selection.

350 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


4. Wheat responds to HF attack with a qualitative resistance that is conferred by majorresistance (H) genes. More than 32 H genes have been identified. The cloned Hdic genehas NBS-LRR motifs. Resistance mediated by these genes is highly effective, typicallykilling 100% of attacking larvae. Attacked resistant plants grow normally and reproduceas well as or better than unattacked resistant plants.

5. The histology of HF resistance resembles plant resistance to fungi. It involves a localizedhypersensitive reaction, the release of an oxygen burst, the fortification of the cell wall,and an upregulation of toxin-encoding genes.

6. Coevolutionary interactions between the Hessian fly and grasses are not constrained bymajor fitness costs, there being no fitness cost for H-gene-mediated resistance and arelatively small fitness cost for Hessian fly adaptation to plant resistance.

FUTURE ISSUES

1. The roles that the Avr-gene-encoded effectors and other putative effectors play in bothcompatible and incompatible interactions have not been characterized. Where are theseproteins localized in plant cells, how are they transported, and what are their cellulartargets in the compatible interaction? Do Avr-gene-encoded proteins interact directlyor indirectly with H-gene products? Are the abundance and diversity of effector proteinsassociated 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 fly larvae fromfeeding and eventually cause death? Do all HF R genes in wheat use the same resistancemechanisms and pathways? Do HF R genes mediate plant resistance to organisms otherthan the Hessian fly?

3. Knowledge regarding the molecular mechanisms associated with HF resistance in wheatis forthcoming. How can this information be translated into durable plant resistance?

4. Comparative genomics provides an opportunity to understand the evolution of effectorproteins. What effector proteins and motifs are conserved among Mayetiola gall midgespecies? 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 gallmidges? Did gall midges obtain their effectors via horizontal gene transfer?

5. Pheromone traps can be combined with PCR-based diagnostics for virulence and avir-ulence now that HF Avr genes and mutations can be identified. These combined tech-nologies will permit an analysis of the evolution of virulence in field populations exposedto monocultures of HF R genes. Will they permit the development of methodologiesthat prolong R gene efficacy?

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


ACKNOWLEDGMENTS

We dedicate this article to Jim Hatchett and the late Bob Gallun, whose pioneering work estab-lished the Hessian fly as a genetic model for plant-insect interactions. Funding for this work hasbeen provided from USDA NRI grants 2004-03099 and 2009-35302-05262, and USDA NIFAgrant 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 Hessianfly genome anchored to polytene chromosomes. BMC Genomics 10:293

2. Anderson KG, Harris MO. 2006. Does R gene resistance to Hessian fly allow wheat seedlings to escapelarval-induced growth deficits? J. Econ. Entomol. 99:1842–53

3. Anderson KG, Harris MO. 2008. Leaf growth signals the onset of effective plant resistance againstHessian fly larvae. Entomol. Exp. Appl. 128:184–95

4. Anderson KM, Kang Q, Reber J, Harris MO. 2011. No fitness cost for wheat’s H-gene mediated resis-tance to Hessian fly (Diptera: Cecidomyiidae). J. Econ. Entomol. 104:1393–405

5. Andersson MN, Haftmann J, Stuart JJ, Cambron SE, Harris MO, et al. 2009. Identification of sexpheromone components of the Hessian fly, Mayetiola destructor. J. Chem. Ecol. 35:81–95

6. Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ, et al. 2011. Hessian fly–associatedbacteria: 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. 24:257–86

8. Barnes HF. 1956. Gall Midges of Cereal Crops. London: Crosby Lockwood9. 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. 263:328–3410. 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 ofHessian fly chromosome A2. Genetics 167:343–55

11. Benatti T, Valicente FH, Aggarwal R, Zhao C, Walling JG, et al. 2010. A neo-sex chromosome thatdrives postzygotic sex determination in the Hessian fly (Mayetiola destructor). Genetics 184:769–77

12. Bent AF, Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply ofquestions. Annu. Rev. Phytopathol. 45:399–46

13. Bentur JS, Pasalu IC, Sarma NP, Prasada Rao U, Mishra B. 2003. Gall Midge Resistance in Rice: CurrentStatus in India and Future Strategies. Hyderabad, India: Dir. Rice Research

14. Bertone MA, Courtney GW, Wiegmann BM. 2008. Phylogenetics and temporal diversification of theearliest true flies (Insecta: Diptera) based on multiple nuclear genes. Syst. Entomol. 33:668–87

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. 11:373–79

16. Bisset J, Borkent A. 1988. Ambrosia galls: the significance of fungal nutrition in the evolution of the Ce-cidomyiidae (Diptera). In Coevolution of Fungi with Plants and Animals, ed. KA Pirozynski, DL Hawsworth,pp. 203–25. London: Academic

17. Bolwell GP, Bindschedler LV, Blee KA, Butt V, Davies DR, et al. 2002. The apoplastic oxidative burstin response to biotic stress in plants: a three-component system. J. Exp. Bot. 53:1367–76

18. Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA. 2010. A functional genomics approachidentifies 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 StateUniv. http://www.agripestbase.org.

20. Buntin GD. 1999. Hessian fly (Diptera: Cecidomyiidae) injury and loss of winter wheat grain yield andquality. J. Econ. Entomol. 92:1190–97

21. Buntin GD, Ott SL, Johnson JW. 1992. Integration of plant resistance, insecticides, and planting date formanagement of the Hessian fly (Diptera: Cecidomyiidae) in winter wheat. J. Econ. Entomol. 85:530–38

352 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.

http://www.agripestbase.org


22. Byers RA, Gallun RL. 1972. Ability of the Hessian fly to stunt winter wheat. 1. Effect of larval feedingon elongation of leaves. J. Econ. Entomol. 65:955–58

23. Cambron SE, Buntin GD, Weisz R, Holland JD, Flanders KL, et al. 2010. Virulence in Hessian fly(Diptera: Cecidomyiidae) field collections from the southeastern United States to 21 resistance genes inwheat. J. Econ. Entomol. 103:2229–35

24. Cartwright WB, Caldwell RM, Compton LE. 1959. Responses of resistant and susceptible wheats toHessian fly attack. Agron. J. 51:529–31

25. Chapin JW. 2009. Hessian fly: a pest of wheat, triticale, barley and rye. Clemson Ext. Bull. http://www.clemson.edu/extension/rowcrops/small_grains/pdfs/hessian_fly.pdf

26. Chen M-S. 2008. Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15:101–1427. Chen M-S, Echegaray E, Whitworth RJ, Wang H, Sloderbeck PE, et al. 2009. Virulence analysis of

Hessian fly populations from Texas, Oklahoma, and Kansas. J. Econ. Entomol. 102:774–8028. Chen M-S, Fellers JP, Stuart JJ, Reese JC, Liu XM. 2004. A group of related cDNAs encoding secreted

proteins from Hessian fly [Mayetiola destructor (Say)] salivary glands. Insect Mol. Biol. 13:101–829. 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 fly, Mayetiola destructor. J. Insect Sci. 6:1230. 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. 10:29631. Chen M-S, Zhao H-X, Zhu YC, Scheffler B, Liu X, et al. 2008. Analysis of transcripts and proteins

expressed in the salivary glands of Hessian fly (Mayetiola destructor) larvae. J. Insect Physiol. 54:1–1632. 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. 30:347–4833. Del Conte SCC, Bosque-Perez NA, Schotzko DJ, Guy SO. 2005. Impact of tillage practices on Hessian

fly–susceptible and resistant spring wheat cultivars. J. Econ. Entomol. 98:805–1334. Devos KM. 2010. Grass genome organization and evolution. Curr. Opin. Plant Biol. 13:139–4535. Dorchin N. 2008. Gall midges (Diptera: Cecidomyiidae). In Encyclopedia of Entomology, ed. JL Capinera,

pp. 1576–80. Dordrecht, The Netherlands: Springer Verlag36. 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 plant-galler relationships. Mol. Phylogenet. Evol. 30:503–15

37. Dorchin N, Scott ER, Clarkin CE, Luongo MP, Jordan S, Abrahamson WG. 2009. Behavioural, eco-logical and genetic evidence confirm the occurrence of host-associated differentiation in goldenrodgall-midges. J. Evol. Biol. 22:729–39

38. Dunaevsky YE, Elpidina EN, Vinokurov KS, Belozersky MA. 2005. Protease inhibitors in improvementof plant resistance to pathogens and insects. Mol. Biol. 39:702–8

39. El Bouhssini M, Chen M, Lhaloui S, Zharmukhamedova G, Rihawi F. 2009. Virulence of Hessian fly(Diptera: Cecidomyiidae) in the Fertile Crescent. J. Appl. Entomol. 133:381–85

40. Flanders KL, Buntin GD, Mask PL. 2008. Biology and management of Hessian fly 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 againstwheat resistance gene H9 in the Hessian fly (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 89:428–34

42. Foster JE, Ohm HW, Patterson FL, Taylor PL. 1991. Effectiveness of deploying single gene resistancesin wheat for controlling damage by the Hessian fly (Diptera: Cecidomyiidae). Environ. Entomol. 20:964–69

43. Gagne RJ. 1989. The Plant-Feeding Gall Midges of North America. Ithaca, NY: Cornell Univ. Press.340 pp.

44. Gagne RJ. 1994. The Gall Midges of the Neotropical Region. Ithaca, NY: Comstock Publ. Assoc. 352 pp.45. Gagne 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 fly epidemics. Ann. N. Y. Acad. Sci. 287:222–29


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.

http://www.clemson.edu/extension/rowcrops/small_grains/pdfs/hessian_fly.pdf

http://www.clemson.edu/extension/rowcrops/small_grains/pdfs/hessian_fly.pdf

http://www.ars.usda.gov/SP2UserFiles/Place/12754100/Gagne_2010_World_Catalog_Cecidomyiidae.pdf

http://www.ars.usda.gov/SP2UserFiles/Place/12754100/Gagne_2010_World_Catalog_Cecidomyiidae.pdf


47. Giovanini MP, Saltzmann KD, Putoff D, Gonzalo M, Ohm HW, Williams CE. 2006. A novel wheatgene encoding a putative chitin-binding lectin is associated with resistance against Hessian fly. Mol. PlantPathol. 8:69–82

48. Gould F. 1986. Simulation models for predicting durability of insect-resistant germplasm: Hessian fly(Diptera: Cecidomyiidae)–resistant winter wheat. Environ. Entomol. 15:11–23

49. Gould F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology.Annu. Rev. Entomol. 43:701–26

50. Grover PB Jr. 1995. Hypersensitive response of wheat to the Hessian fly. Entomol. Exp. Appl. 74:283–9451. Grover PB Jr, Shukle RH, Foster JE. 1989. Interactions of Hessian fly (Diptera: Cecidomyiidae) biotypes

on resistant wheat. Environ. Entomol. 18:687–9052. Harris MO, Foster SP. 1999. Gall midges. In Pheromones of Non-Lepidopteran Insects Associated with

Agricultural Plants, ed. J Hardie, AK Minks, pp. 27–49. Oxford, UK: CABI53. Harris MO, Freeman TP, Anderson KG, Moore JA, Payne SA, et al. 2010. H gene–mediated resistance

to Hessian fly exhibits features of penetration resistance to fungi. Phytopathology 100:279–8954. Harris MO, Freeman TP, Rohfritsch O, Anderson KG, Payne SA, Moore JA. 2006. Virulent Hessian

fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat.Ann. Entomol. Soc. Am. 99:305–16

55. Harris MO, Sandanayake M, Griffin W. 2001. Oviposition preferences of the Hessian fly and theirconsequences for the survival and reproductive potential of offspring. Ecol. Entomol. 26:1–14

56. Harris MO, Stuart JJ, Mohan M, Nair S, Lamb RJ, Rohfritsch O. 2003. Grasses and gall midges: plantdefense and insect adaptation. Annu. Rev. Entomol. 48:549–77

57. Hatchett JH, Gallun RL. 1970. Genetics of the ability of the Hessian fly, Mayetiola destructor, to surviveon wheats having different genes for resistance. Ann. Entomol. Soc. Am. 63:1400–7

58. Hatchett JH, Kreitner GL, Elzinga RJ. 1990. Larval mouthparts and feeding mechanism of the Hessianfly (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 83:1137–47

59. Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S. 2009. Emerging concepts in effectorbiology of plant-associated organisms. Mol. Plant-Microbe Interact. 22:115–22

60. Jang CS, Johnson JW, Seo YW. 2005. Differential expression of TaLTP3 and TaCOMT1 induced byHessian fly larval infestation in a wheat line possessing H21 resistance gene. Plant Sci. 168:1319–26

61. Johnston JS, Ross LD, Bean L, Hughes DP, Kathirithamby J. 2004. Tiny genomes and endoreduplica-tion in Strepsiptera. Insect Mol. Biol. 13:581–85

62. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–2963. Joy JB, Crespi BJ. 2007. Adaptive radiation of gall-inducing insects within a single host-plant species.

Evolution 61:784–9564. Kaloshian I. 2004. Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem.

Ecol. 30:2419–3865. Kanno H, Harris MO. 2000. Both chemical and physical features of grass leaves influence host selection

by the Hessian fly. J. Chem. Ecol. 26:2335–5466. Kloc M. 2008. Basic science B.D. (before Drosophila): cytology at the University of Warsaw (Poland).

Int. J. Dev. Biol. 52:115–1967. Kolesik P, Adair RJ, Eick G. 2005. Nine new species of Dasineura (Diptera: Cecidomyiidae) from flowers

of Australian Acacia (Mimosaceae). Syst. Entomol. 30:454–7968. 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 andPapua New Guinea. Aust. J. Entomol. 48:310–16

69. Kosma DK, Nemacheck JA, Jenks MA, Williams CE. 2010. Changes in properties of wheat leaf cuticleduring interactions with Hessian fly. Plant J. 63:31–43

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 fly (Diptera: Cecidomyiidae)resistance in Texas. J. Econ. Entomol. 83:1135–39

72. Liu X, Bai J, Huang L, Zhu L, Liu X, et al. 2007. Gene expression of different wheat genotypes duringattack by virulent and avirulent Hessian fly (Mayetiola destructor) larvae. J. Chem. Ecol. 33:2171–94

354 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


73. Liu X, Fellers JP, Zhu YC, Mutti NS, El-Bouhssini M, Chen MS. 2006. Cloning and characterization ofcDNAs encoding carboxypeptidase-like proteins from the gut of Hessian fly [Mayetiola destructor (Say)]larvae. Insect Biochem. Mol. Biol. 36:665–73

74. Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyam S, et al. 2010. Reactive oxygen species areinvolved in plant defense against a gall midge. Plant Physiol. 152:985–99

75. Liu XM, Brown-Guedira GL, Hatchett JH, Owuoche JO, Chen M-S. 2005. Genetic characterizationand molecular mapping of a Hessian fly-resistance gene transferred from T. turgidum ssp. dicoccum tocommon wheat. Theor. Appl. Genet. 111:1308–15

76. Liu XM, Fellers JP, Wilde GE, Stuart JJ, Chen MS. 2004. Characterization of two genes expressed inthe salivary glands of the Hessian fly [Mayetiola destructor (Say)]. J. Insect Biochem. Mol. Biol. 34:229–37

77. Liu XM, Fritz AK, Reese JC, Wilde GE, Gill BS, Chen MS. 2005. H9, H10, and H11 compose a clusterof Hessian fly resistance genes in the distal gene-rich region of wheat chromosome 1AS. Theor. Appl.Genet. 110:1473–80

78. Liu XM, Gill BS, Chen M-S. 2005. Hessian fly resistance gene H13 is mapped to a distal cluster ofresistance genes in chromosome 6DS of wheat. Theor. Appl. Genet. 111:243–49

79. Lobo NF, Behura SK, Aggarwal R, Chen M-S, Hill CA, et al. 2006. Genomic analysis of a 1 Mb regionnear the telomere of Hessian fly 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 proteaseinhibitor–like cDNAs from the Hessian fly Mayetiola destructor (Say). Insect Mol. Biol. 15:485–96

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

fly resistance gene (H30) transferred from the wild grass Aegilops triuncialis to hexaploid wheat. Theor.Appl. Genet. 106:1248–55

83. Matuszewski B. 1982. Animal Cytogenetics. Insecta 3. Diptera I: Cecidomyiidae. Berlin, Germany: JohnGebruder Burtraeger. 140 pp.

84. Michelmore RW, Meyers BC. 1998. Clusters of resistance genes in plants evolve by divergent selectionand a birth-and-death process. Genome Res. 8:1113–30

85. Morgan W, Kamoun S. 2007. RXLR effectors of plant pathogenic oomycetes. Curr. Opin. Microbiol.10:332–38

86. Nombela G, Williamson VM, Muniz M. 2003. The root-knot nematode resistance gene Mi-1.2 of tomatois responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant-Microbe Interact. 16:645–49

87. Price PW. 2005. Adaptive radiation of gall-inducing insects. Basic Appl. Ecol. 6:413–2188. 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 fly larval feeding. Mol. Plant Pathol. 6:411–2389. Raman A, Schaefer CW, Withers TM, eds. 2005. Biology, Ecology, and Evolution of Gall-Inducing Arthropods.

Enfield, NH: Sci. Publ. Inc.90. Ratcliffe RH, Cambron SE, Flanders KL, Bosque-Perez NA, Clement SL, Ohm HW. 2000. Biotype

composition of Hessian fly (Diptera: Cecidomyiidae) populations from the southeastern, midwestern,and northwestern United States and virulence to resistance genes in wheat. J. Econ. Entomol. 93:1319–28

91. Ratcliffe RH, Hatchett JH. 1997. Biology and genetics of the Hessian fly and resistance in wheat. In NewDevelopments in Entomology, ed. K Bondari, pp. 47–56. Trivandurm, India: Res. Signpost Sci. Inf. Guild

92. Rausher MD. 2001. Co-evolution and plant resistance to natural enemies. Nature 411:857–6493. Richards S. 2011. Hessian fly genome project. Baylor, TX: Hum. Genome Seq. Cent., Baylor Sch. Med.

http://www.hgsc.bcm.tmc.edu/project-species-i-Hessian_fly.hgsc94. Rider JSD, Sun W, Ratcliffe RH, Stuart JJ. 2002. Chromosome landing near avirulence gene vH13 in

the Hessian fly. Genome 45:812–2295. Rohfritsch O. 1992. Patterns in gall development. See Reference 102, pp. 60–8696. Rohfritsch O. 2008. Plants, gall midges, and fungi: a three-component system. Entomol. Exp. Appl.

128:208–1697. Roskam HC. 2005. Phylogeny of gall midges (Cecidomyiidae). See Reference 89, pp. 307–1998. Roskam JC. 1992. Evolution of the gall-inducing guild. See Reference 102, pp. 34–49


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.

http://www.hgsc.bcm.tmc.edu/project-species-i-Hessian_fly.hgsc


99. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematoderesistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA95:9750–54

100. Saltzmann KD, Giovanini M, Ohm H, Williams CE. 2009. Transcript profiles of two wheat lipid transferprotein-encoding genes are altered during attack by Hessian fly larvae. Plant Physiol. Biochem. 48:54–61

101. Sardesai N, Nemacheck JA, Subramanyam S, Williams CE. 2005. Identification and mapping of H32, anew wheat gene conferring resistance to Hessian fly. Theor. Appl. Genet. 111:1167–73

102. Shorthouse JD, Rohfritsch O, eds. 1992. Biology of Insect-Induced Galls. New York: Oxford Univ. Press103. Shukle RH, Grover PB, Mocelin G. 1992. Response of susceptible and resistant wheat associated with

Hessian fly (Diptera: Cecidomyiidae) infestation. Environ. Entomol. 21:845–53104. 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 fly,Mayetiola destructor (Say). J. Insect Physiol. 55:105–12

105. Shukle RH, Subramanyam S, Saltzmann KA, Williams CE. 2010. Ultrastructural changes in the midgutsof Hessian fly larvae feeding on resistant wheat. J. Insect Physiol. 56:754–60

106. Smiley RW, Gourlle JA, Whittaker RG, Easley SA, Kidwell KK. 2004. Economic impact of Hessian fly(Diptera: Cecidomyiidae) on spring wheat in Oregon and additive yield losses with Fusarium crown rotand lesion nematode. J. Econ. Entomol. 97:304–408

107. Stuart JJ, Hatchett JH. 1987. Morphogenesis and cytology of the salivary gland of the Hessian fly,Mayetiola destructor (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 80:475–82

108. Stuart JJ, Hatchett JH. 1988. Cytogenetics of the Hessian fly, Mayetiola destructor (Say): II. Inheritanceand behavior of somatic and germ-line-limited chromosomes. J. Hered. 79:190–99

109. Subramanyam S, Sardesai N, Puthoff D, Meyer J, Nemacheck J, et al. 2006. Expression of two wheatdefense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci. 170:90–103

110. Tanaka R, Nei M. 1989. Positive Darwinian selection observed at the variable-region genes of im-munoglobulins. Mol. Biol. Evol. 6:447–59

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. 101:301–6

112. Tooker JF, De Moraes CM. 2007. Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does notinduce plant indirect defences. Ecol. Entomol. 32:153–61

113. Tooker JF, Moraes CM. 2010. Feeding by Hessian fly [Mayetiola destructor (Say)] larvae on wheat increaseslevels of fatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling.J. Plant Growth Regul. 30:158–65

114. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM. 2008. Gall insects can avoid and alter indirectplant defenses. New Phytol. 178:657–71

115. Torto-Alalibo TA, Collmer CW, Lindeberg M, Bird D, Collmer A, Tyler BM. 2009. Common andcontrasting themes in host cell–targeted effectors from bacterial, fungal, oomycete and nematode plantsymbionts 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. 40:597–607

117. Watson S. 2005. Hessian fly problems have been increasing in recent years in the Central Plains. WheatFarmer Row Crop Farmer 9:4–5

118. White MJD. 1973. Animal Cytology and Evolution. London: Cambridge Univ. Press. 468 pp.119. Widenfalk O, Gyllenstrand N, Sylven 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. 27:519–28

120. Williams CE, Nemacheck JA, Shukle JT, Subramanyam S, Saltzmann KD, Shukle RH. 2011. Inducedepidermal permeability modulates resistance and susceptibility of wheat seedlings to herbivory by Hessianfly larvae. J. Exp. Bot. 62:4521–31

121. Wu J-X, Liu X-M, Zhang S-Z, Zhu Y-C, Whitworth RJ, Chen MS. 2008. Differential responses ofwheat inhibitor-like genes to Hessian fly, Mayetiola destructor, attacks during compatible and incompatibleinteractions. J. Chem. Ecol. 34:1005–12

356 Stuart et al.

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.


122. Xu SS, Chu CG, Harris MO, Williams CE. 2011. Comparative analysis of genetic background in eightnear-isogenic wheat lines with different H genes conferring resistance to Hessian fly. Genome 54:81–89

123. Yu GT, Cai X, Harris MO, Gu YQ, Luo M-C, Xu SS. 2009. Saturation and comparative mapping of thegenomic region harboring Hessian fly resistance gene H26 in wheat. Theor. Appl. Genet. 118:1589–99

124. Yu GT, Williams CE, Harris MO, Cai X, Mergoum M, Xu SS. 2010. Development and validation ofmolecular markers closely linked to H32 for resistance to Hessian fly in wheat. Crop Sci. 50:1325

125. Yukawa J, Rohfritsch O. 2005. Biology and ecology of gall-inducing Cecidomyiidae (Diptera). SeeReference 89, pp. 273–304

126. Yukawa J, Uechi N, Horikiri M, Tuda M. 2003. Description of the soybean pod gall midge, Asphondyliayushimai sp. n. (Diptera: Cecidomyiidae), a major pest of soybean and findings of host alternation.Bull. Entomol. Res. 93:73–86

127. Zantoko L, Shukle RH. 1997. Genetics of virulence in the Hessian fly to resistance gene H13 in wheat.J. Hered. 88:120–23

128. Zhang H, Anderson KM, Stuart JJ, Cambron S, and Harris MO. 2011. A reproductive fitness costassociated with Hessian fly (Diptera: Cecidomyiidae) virulence to gene-for-gene resistance. J. Econ.Entomol. 104:1055–64

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. 56:1198–206

130. Zhu L, Liu X, Liu X, Jeannotte R, Reese JC, et al. 2008. Hessian fly (Mayetiola destructor) attack causesa dramatic shift in carbon and nitrogen metabolism in wheat. Mol. Plant-Microbe Interact. 21:70–78

131. Zhu YC, Liu X, Maddur AA, Oppert B, Chen MS. 2005. Cloning and characterization of chymotrypsin-and trypsin-like cDNAs from the gut of the Hessian fly [Mayetiola destructor (Say)]. Insect Biochem. Mol.Biol. 35:23–32


Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.

PY50-FrontMatter ARI 9 July 2012 19:8

Annual Review ofPhytopathology

Volume 50, 2012Contents

An Ideal JobKurt J. Leonard � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Arthur Kelman: Tribute and RemembranceLuis Sequeira � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �15

Stagonospora nodorum: From Pathology to Genomicsand Host ResistanceRichard P. Oliver, Timothy L. Friesen, Justin D. Faris, and Peter S. Solomon � � � � � � � � � �23

Apple Replant Disease: Role of Microbial Ecologyin Cause and ControlMark Mazzola and Luisa M. Manici � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �45

Pathogenomics of the Ralstonia solanacearum Species ComplexStephane Genin and Timothy P. Denny � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �67

The Genomics of Obligate (and Nonobligate) BiotrophsPietro D. Spanu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �91

Genome-Enabled Perspectives on the Composition, Evolution, andExpression of Virulence Determinants in Bacterial Plant PathogensMagdalen Lindeberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 111

Suppressive Composts: Microbial Ecology Links Between AbioticEnvironments and Healthy PlantsYitzhak Hadar and Kalliope K. Papadopoulou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 133

Plant Defense Compounds: Systems Approaches to Metabolic AnalysisDaniel J. Kliebenstein � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 155

Role of Nematode Peptides and Other Small Moleculesin Plant ParasitismMelissa G. Mitchum, Xiaohong Wang, Jianying Wang, and Eric L. Davis � � � � � � � � � � � � 175

New Grower-Friendly Methods for Plant Pathogen MonitoringSolke H. De Boer and Marıa M. Lopez � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 197

Somatic Hybridization in the UredinalesRobert F. Park and Colin R. Wellings � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 219

v

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.

PY50-FrontMatter ARI 9 July 2012 19:8

Interrelationships of Food Safety and Plant Pathology: The Life Cycleof Human Pathogens on PlantsJeri D. Barak and Brenda K. Schroeder � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 241

Plant Immunity to NecrotrophsTesfaye Mengiste � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Mechanisms and Evolution of Virulence in OomycetesRays H.Y. Jiang and Brett M. Tyler � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 295

Variation and Selection of Quantitative Traits in Plant PathogensChristian Lannou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 319

Gall Midges (Hessian Flies) as Plant PathogensJeff J. Stuart, Ming-Shun Chen, Richard Shukle, and Marion O. Harris � � � � � � � � � � � � � � 339

Phytophthora Beyond AgricultureEverett M. Hansen, Paul W. Reeser, and Wendy Sutton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 359

Landscape Epidemiology of Emerging Infectious Diseasesin Natural and Human-Altered EcosystemsRoss K. Meentemeyer, Sarah E. Haas, and Tomas Vaclavık � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 379

Diversity and Natural Functions of Antibiotics Produced by Beneficialand Plant Pathogenic BacteriaJos M. Raaijmakers and Mark Mazzola � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 403

The Role of Secretion Systems and Small Molecules in Soft-RotEnterobacteriaceae PathogenicityAmy Charkowski, Carlos Blanco, Guy Condemine, Dominique Expert, Thierry Franza,

Christopher Hayes, Nicole Hugouvieux-Cotte-Pattat, Emilia Lopez Solanilla,David Low, Lucy Moleleki, Minna Pirhonen, Andrew Pitman, Nicole Perna,Sylvie Reverchon, Pablo Rodrıguez Palenzuela, Michael San Francisco, Ian Toth,Shinji Tsuyumu, Jacquie van der Waals, Jan van der Wolf,Frederique Van Gijsegem, Ching-Hong Yang, and Iris Yedidia � � � � � � � � � � � � � � � � � � � � � � 425

Receptor Kinase Signaling Pathways in Plant-Microbe InteractionsMeritxell Antolın-Llovera, Martina K. Ried, Andreas Binder,

and Martin Parniske � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 451

Fire Blight: Applied Genomic Insights of thePathogen and HostMickael Malnoy, Stefan Martens, John L. Norelli, Marie-Anne Barny,

George W. Sundin, Theo H.M. Smits, and Brion Duffy � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 475

Errata

An online log of corrections to Annual Review of Phytopathology articles may be found athttp://phyto.annualreviews.org/

vi Contents

Ann

u. R

ev. P

hyto

path

ol. 2

012.

50:3

39-3

57. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by D

'You

ville

Col

lege

on

02/2

6/13

. For

per

sona

l use

onl

y.

annurev-phyto-072910-095255

Documents

Transcript of annurev-phyto-072910-095255