susceptibility to plant disease: more than a failure of host immunity · 2016. 5. 24. · adapted...

TRPLSC-1070; No. of Pages 9

Susceptibility to plant disease: morethan a failure of host immunityDmitry Lapin and Guido Van den Ackerveken

Plant–Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, Padualaan 8, 3584 CH Utrecht,

The Netherlands

Review

Box 1. Suppression of plant immunity

Adapted pathogens have evolved effector proteins and small

molecules to suppress PAMP/MAMP-triggered immunity [98–100]

and can thereby establish effector-triggered susceptibility (ETS). A

second class of plant immune receptors, encoded by resistance

genes, has evolved to recognize these effectors or their activity.

Effector recognition activates a defense response referred to as

effector-triggered immunity (ETI). However, this second layer of

immunity can also be rendered ineffective by other effectors that

can suppress ETI, for example, by acting on downstream signaling

components [98]. The striking feature that many of these effectors

have in common is that they act within the host cell and require

specialized transport mechanisms to get there. Gram-negative

bacteria use a type III secretion system to ‘inject’ proteins into the

host cell [101,102]. Nematodes can also insert proteins directly into

plant cells by means of their stylet. By contrast, biotrophic fungi and

oomycetes secrete proteins from their hyphae or haustoria followed

by uptake or translocation over the plant cell membrane into the

host cell [32]. Research on the mode of action of effectors has

revealed intriguing ways of host manipulation, for example, by

manipulating host target proteins, mostly aimed at disabling the

plant immune system [96,97,103]. The resulting suppression is

important in the early stages of infection and remains throughout

Susceptibility to infectious diseases caused by patho-gens affects most plants in their natural habitat andleads to yield losses in agriculture. However, plantsare not helpless because their immune system can dealwith the vast majority of attackers. Nevertheless,adapted pathogens are able to circumvent or avert hostimmunity making plants susceptible to these uninvitedguests. In addition to the failure of the plant immunesystem, there are other host processes that contribute toplant disease susceptibility. In this review, we discussrecent studies that show the active role played by thehost in supporting disease, focusing mainly on bio-trophic stages of infection. Plants attract pathogens,enable their entry and accommodation, and facilitatenutrient provision.

Forced hospitality enables infectionPlants possess a dedicated immune system to fend offinfection by pathogens such as viruses, bacteria, fungi,oomycetes, and nematodes. The activation of plant defenseresponses is triggered by the recognition of invading organ-isms by immune receptors. These can be plasma mem-brane-bound receptors that monitor the extracellularenvironment or intracellular receptors that detect thepresence or activity of pathogen-derived effectors. An im-portant class of receptors recognizes molecules known aspathogen- or microbe-associated molecular patterns(PAMPs/MAMPs), which are exposed or released by abroad range of invading organisms. Well-known examplesare the pattern recognition receptors FLS2 (FLAGELLIN-SENSITIVE 2) for bacterial flagellin and the CERK1(CHITIN ELICITOR RECEPTOR KINASE 1) for fungalchitin. Recognition of PAMPs/MAMPs results in the acti-vation of the plant immune system [1]. Plants have theintrinsic capacity to detect and respond to invading patho-gens and, therefore, are resistant to the majority of poten-tial pathogens [2–4].

However, the plant immune system is rendered ineffec-tive by adapted pathogens that have evolved ways tointerfere with host defense (Box 1). The ensuing failureof the plant immune system allows further ingress ofinvading pathogens, however, not without the ‘collabora-tion’ of the host. The focus of this review is on non-immu-

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� 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2013.05.005

Corresponding author: Van den Ackerveken, G. ([email protected]).Keywords: disease susceptibility; biotrophic pathogens.

nity related plant processes that contribute to thesusceptibility of plants to pathogens at the level of: (i)pathogen attraction and attachment to the host, (ii) accom-modation of infection structures in plant cells, and (iii)nutrient production and transport from the host (Figure 1).We will mainly focus on the susceptibility of plants topathogens that have a biotrophic lifestyle, either duringinitial stages of infection (e.g., Phytophthora spp., Colleto-trichum spp.) or throughout their life cycle (e.g., the pow-dery and downy mildews) (see Glossary for terminology).

Plant signals as cues for pathogen developmentThe effect of signals from the host plant on early pathogendevelopment was convincingly illustrated in a recent anal-ysis of gene expression in germinating spores of the hemi-biotrophic fungus Colletotrichum higginsianum, whichshowed that the transcription of >1700 genes is inducedwhen the spores are on a host plant surface rather than onan artificial polystyrene surface [5]. Plant-derived mole-cules such as flavonoids, fatty acids, alcohols, and alde-hydes are known to serve as signals to attract pathogens,stimulate attachment to the plant surface, and induce

the infection process so that biotrophic pathogens can complete

their life cycle without being killed or arrested by plant defense

responses. Interestingly, some effectors stimulate susceptibility by

other means: for example, by interfering with nutrient metabolism

or transport (see text for further discussion).

Trends in Plant Science xx (2013) 1–9 1

http://dx.doi.org/10.1016/j.tplants.2013.05.005

mailto:[email protected]

A�rac�on Accommoda�on Feeding

Release of a�ractants and s�mulants

Germina�ng spore

Penetra�ng haustorium

Reorganiza�on of plant cytoskeletonand cytoplasm

Established haustorium

Flux of nutrients

Key:

Epidermal cell with cu�n and wax layers

Free pathogen spore

TRENDS in Plant Science

Figure 1. The host plant promotes susceptibility to pathogen infection at several

key steps: (i) attracting pathogens by plant-derived molecules and stimulating their

attachment and development on the host surface, (ii) accommodating pathogen

infection structures, for example, haustoria, and (iii) feeding the uninvited guests.

Glossary

Biotroph: a pathogen that lives and multiplies only on living host tissues

[104,105]. The examples of plant biotrophic pathogens are viruses, viroids,

downy and powdery mildews, rusts.

Cutin: a polymer of long-chain fatty acids and their derivatives on the plant

surface, the main component of surface cuticle [106].

Effector: microbial and pest-secreted molecules that alter host cell processes or

structures generally promoting the interaction with the host [97].

Endoreduplication: modification of the cell cycle in which nuclear DNA

undergoes replication without subsequent cell division that leads to formation

of nuclei with increased ploidy level [107]. The resulting ploidy level is

expressed as the amount of DNA compared to that of a haploid nucleus. For

example, normal diploid cell (2n) has 2C amount of DNA.

G proteins: GTP hydrolyzing proteins (GTPases) that work as molecular

switches in regulating a broad range of cell processes. Plant G proteins are

broadly classified into small G proteins (including ROPs), heterotrimeric G

proteins, and unconventional G proteins [108,109].

Hemibiotroph: a pathogen for which only a part of the life cycle is dependent

on living host tissues. For example, the oomycete pathogen Phytophthora

capsici starts the infection process in Arabidopsis thaliana as a biotrophic

pathogen but later switches to the necrotrophic stage [110,111].

Necrotroph: pathogen feeding on dead host tissues [112]. The plant

necrotrophic pathogens are exemplified by the gray mold fungus Botrytis

cinerea and oomycete parasites Pythium sp.

Strigolactones: carotenoid-derived plant hormones originally identified as

molecules from root exudates stimulating germination of seeds of parasitic

plants in the periphery of the host plant. Strigolactones are not only signals in

the rhizosphere but also play an important role as hormones in plant

development [113].

Waxes: a complex mixture of highly hydrophobic long-chain alkanes, alcohols,

and fatty acids frequently found on the surface cuticles [106].

Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x


germination and formation of penetration structuresnamed appressoria.

Flavonoids are released into the soil from the roots ofmany plant species where they can attract soil-bornepathogens. It has been shown that isoflavonoids releasedby the roots of soybean (Glycine max) and other plantsattract zoospores of Phytophthora spp., which are oomycetepathogens [6]. Flavonoids can also stimulate spore germi-nation, as shown for the fungal legume pathogen Fusariumsolani [7]. However, these compounds have not beenreported to stimulate the development of infection struc-tures in vitro.

Other compounds, for example, plant hormones, areknown to trigger pathogen development. Ethylene re-leased by ripening fruits stimulates both spore germina-tion and appressorium formation of the fungusColletotrichum gloeosporioides [8]. There are indicationsthat strigolactones also influence in vitro growth of phyto-pathogenic fungi [9], although it is not clear how theyinfluence plant infection.

Components of plant surface waxes, such as long-chainalcohols and aldehydes, play an important role in pathogenspore germination. Leaves of the maize (Zea mays)glossy11 mutant, in which very-long-chain aldehydes aredepleted from surface waxes, are poor substrates for thegermination of spores of the barley powdery mildew Blu-meria graminis f.sp. hordei. Exogenous application of theC26 aldehyde n-hexacosanal on glossy11 leaves restoredefficient spore germination, demonstrating that it servesas a cue for pathogen development [10]. Similarly, onleaves of the Medicago truncatula irg1 (inhibitor of rustgerm tube differentiation 1) mutant, spores of the fungiColletotrichum trifolii (a pathogen of Medicago) and Pha-kopsora pachyrhizi (for which Medicago is a non-host)showed reduced differentiation rates [11]. The irg1 mutanthas an altered composition of surface waxes because it is

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severely depleted in C30 primary alcohols. Transcriptomeanalysis of the irg1 mutant revealed downregulation ofECERIFERUM4, implicated in primary alcohol biosynthe-sis, and MYB96, a transcriptional regulatory gene of waxbiosynthesis. In addition, barley (Hordeum vulgare) andwheat (Triticum aestivum) wax components, such as C26and C28 n-alcohols and even-numbered C22–C30 n-alde-hydes, are known to induce germination of powdery mil-dew spores in vitro [12].

Cutin also plays a signaling role in pathogen develop-ment. M. truncatula ram2 mutant plants, which are missinga glycerol-3-phosphate acyltransferase enzyme involved incutin biosynthesis, showed increased resistance to theoomycete Phytophthora palmivora as a result of reducedappressoria formation by the pathogen. Application of theC16:0 monomer of cutin 1,16-hexadecanediol not only stim-ulated appressoria formation of P. palmivora on a polypro-pylene surface but also increased the susceptibility of theMedicago roots to oomycete infection [13]. Cutin monomers(hydroxy fatty acids) also stimulate appressorium formationand regulate the hyphal development of the obligate bio-troph Ustilago maydis [14]. We can conclude that plantcompounds can act as important attractants for pathogens,as well as triggers for the formation of penetration struc-tures, thereby contributing to disease susceptibility.

Pathogen accommodationThe accommodation of pathogens during biotrophic stagesof infection often involves specialized structures, such ashaustoria, which could be important for nutrition uptake,as shown for soybean rust (Uromyces fabae) [15], and foreffector translocation into host cells (see below). The cyto-plasm of host cells remains separated from the invadingfungal or oomycete haustoria by a host-derived extrahaus-torial membrane that is continuous with the plant cell



membrane but has a distinct set of membrane-associatedproteins [16,17]. Accommodation of the invading pathogeninside the plant cell involves large changes in host mem-brane and cytoskeleton organization to which the hostactively contributes.

Rho-like GTPases of plants (ROPs, also called RACs) arewell known for their involvement in development andinteraction with the environment [18]. In addition, thereis evidence that these proteins play a role in diseasesusceptibility. Silencing of the rice (Oryza sativa) OsRAC4and OsRAC5 genes led to reduced susceptibility to theblast fungus Magnaporthe grisea [19]. Similarly, expres-sion of a dominant negative form of ROP6 enhanced resis-tance of Arabidopsis (Arabidopsis thaliana) to powderymildew independently of salicylic acid-mediated immunity[20]. By contrast, constitutively active forms of barleyRAC3 and HvRACB, the homolog of the ArabidopsisROP6, increased susceptibility of transgenic tobacco (Ni-cotiana tabacum) plants to the powdery mildew fungusGolovinomyces cichoracearum and the bacterium Pseudo-monas syringae pv. tabaci [21]. Silencing of the barleyHvRACB in single epidermal cells showed that this ROPis indeed required for successful powdery mildew hausto-rium accommodation [22–24]. Furthermore, a regulator ofROP activity, the Arabidopsis receptor-like kinase FER-ONIA (FER) was found to be important for successfulpowdery mildew infection and for pollen tube growth[25]. Given that FER [26] as well as the barley HvRACBand Arabidopsis ROP6 [22,27] are also linked to root hairformation, this suggests that the ‘accommodation’ of fungalhaustoria, pollen tube growth, and root hair developmentshare a similar signaling pathway. Furthermore, theROP6 and ROP1 genes influence the interaction of Arabi-dopsis with the root endophyte Piriformospora indica be-cause their mutation affects plant cytoskeletonreorganization during fungal penetration and thegrowth-promoting effect by the fungus [28]. Interestingly,ROPs also play a role in the accommodation of symbioticRhizobium bacteria as shown for the Lotus japonicusROP6, which is important for infection thread formationthat precedes the accommodation of rhizobacteria [29].Also, in the interaction with arbuscular mycorrhizal fungi,a pre-penetration apparatus is assembled in epidermalroot cells of M. truncatula and of Daucus carota (carrot),a process that requires reorganization of cytoskeletonand endoplasmic reticulum components [30,31]. Reorgani-zation of host plasma membrane and aggregation oforganelles was also observed at penetration sites in Ara-bidopsis inoculated with the powdery mildew G. cichora-cearum [17], suggesting that pre-penetration complexes,involving ROPs and other proteins, are needed for accom-modation of symbiont and pathogen infection structures.

Not only do plants enable and support the accommoda-tion of pathogens but they also contribute to the transportof effector proteins (Box 1) into the host cell. Over thepast decade, many secreted oomycete and fungal proteinshave been identified that show activity inside the host cell,the so-called host-translocated or cytoplasmic effectors[32]. Pioneering electron microscopy has revealed thatthe immunogold-labeled proteins Uf-RTP1p and Us-RTP1p from the rust fungi U. fabae and Uromyces striatus,

respectively, are transported from haustoria into plantcells [33]. Two recent studies have shown that fungaleffectors localize to specific compartments at the host–pathogen interface, from where they are secreted. In Mag-naporthe oryzae-infected rice cells, this structure wasnamed the biotrophic interfacial complex [34], and similarstructures have been found in infections with the hemi-biotroph C. higginsianum, showing stage-specific foci ofeffector accumulation at discrete sites on its invasivehyphae [35]. The question remains how effectors end upin the host cell cytoplasm after being secreted to theextracellular interface between the host and the pathogen.Data collected so far point to pathogen-independent uptakeby plant cells, possibly via an endocytic route, as has beenobserved for several oomycete and fungal effectors [36–38].Inhibition of lipid raft-mediated endocytosis with filipinand nystatin has been shown to block uptake of the oomy-cete effector Avr1b into the plant cells. Given that multipleeffectors from plant pathogenic oomycetes and fungi havebeen described to bind the phosphoinositide phosphatidy-linositol-3-phosphate present in the host plasma mem-brane, it was suggested that binding initiates effectortranslocation [36,39,40]. However this could not be repro-duced by four independent laboratories [41,42], suggestingthat alternative mechanisms of translocation exist. Hostcells also enable cell-to-cell movement of effector proteins,for example, the chorismate mutase Cmu1 and PWL2 (forPrevents pathogenicity toward Weeping Lovegrass) secret-ed by U. maydis and M. oryzae, respectively, which canmove to plant cells next to the infected cells. The movementis likely to be through the plasmodesmata because Cmu1has not been observed in guard cells that lack symplasticconnections [34,43]. It is tempting to speculate that mobileeffectors could make distant tissues more accessible toinfection, thereby possibly contributing to the phenomenonof ‘induced accessibility’.

Provision of food for pathogenic guestsIn addition to accommodation, host plants also ‘offer’nutrients to their pathogenic guests. In particular, inbiotrophic interactions, the plant provides carbon andother nutrients to infecting pathogens. The photosynthe-tically active tissues of the plant produce organic carbon inthe form of sugars. Surprisingly, a reduction of plantphotosynthesis rates has been observed in tissues infectedwith biotrophic and hemibiotrophic leaf pathogens, both insusceptible and resistant plants [44]. The demand forcarbon in the infected tissue requires that there is com-pensation by carbon allocation from noninfected tissues, inparticular in nonphotosynthetically active tissues, such asin leaf epidermal cells infected by powdery mildews or rootcells parasitized by nematodes. The infected tissues be-come an important sink so that nutrients, includingsugars, are transported there. Transport of sucrose fromsource to sink tissues requires efficient unloading of thephloem into the apoplast and further transport of sugars tothe surrounding cells. The strength of the sink is largelydetermined by the level of phloem unloading which, inturn, is strongly influenced by the activity of sugar trans-porters and cell wall-bound invertases, which are highlyexpressed in sink tissues [45] (Figure 2).

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Infec�on site

Photosynthesis

SWEETs

Invertases

ADHs

DNA ploidy

Maintenance ofphotosynthesis in‘green islands’

‘Green island’

SugarsWater and minerals

Key:

Increase in ac�vityor DNA ploidy level

Infected leafHealthy systemic leaf


Figure 2. Changes in plant physiology during infection by biotrophic and

hemibiotrophic pathogens. Leaves infected with oomycete, fungal, bacterial, and

protist pathogens show elevated expression of SWEET sugar transporters and cell

wall-bound and vacuolar invertases that facilitate phloem unloading and the flux of

sugars to the infection site. ‘Green islands’ are known to surround rusts and powdery

mildew infection sites and maintain photosynthesis in the otherwise senescing host

tissues. Powdery mildew infection activates host alcohol dehydrogenases (ADHs)

that might play a role in the synthesis of specific metabolites beneficial for the fungus

and induces increased DNA ploidy levels in mesophyll cells underneath the infected

epidermal cells that could contribute to increased metabolite production. Successful

infection can also lead to systemic changes in plant physiology, for example, by

stimulating photoassimilation in uninfected leaves.



The discovery of the SWEET family of plant transmem-brane proteins was a major breakthrough because severalSWEET proteins were shown to transport glucose andsucrose across cell membranes, thus contributing to phlo-em unloading [46,47]. A subset of SWEET genes in Arabi-dopsis and rice are transcriptionally induced duringbacterial and fungal infection [46,47]. In grapevine (Vitisvinifera), the SWEET orthologs VvHT1 and VvHT5 (hexosetransporters) are also transcriptionally activated afterpowdery and downy mildew infection. Notably, analysisof VvHT5 spatial expression showed that the gene isactively transcribed in veins of diseased leaves, with thehighest abundance close to the infection site [48]. Thus, byunloading phloem, sugar transporters mediate carbontransport to bacterial, fungal, and oomycete infection sites.

The importance of these sugar transporters for diseasesusceptibility has been revealed in rice. Transcription ofthe OsSWEET11/Xa13 gene is activated by the Xantho-monas oryzae pv. oryzae (Xoo) transcription activator-like(TAL) effector PthXo1 through its specific binding to theOsSWEET11 promoter. Interestingly, recessive resistanceto Xoo mediated by xa13 alleles is based on promotermutations that make the OsSWEET11 gene nonresponsiveto the PthXo1 effector [47,49]. Apparently, the mutatedpromoter leads to lower transporter levels and consequent-ly a diminished flow of sugars to Xoo resulting in a largedecrease in susceptibility. Additional support for the im-portance of sugar transport during infection came fromstudies showing that other Xoo strains have evolved waysto activate the expression of a different rice sucrose and

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glucose transporter gene, OsSWEET14, by another TALeffector, AvrXa7 [46,47,50]. In this way, Xoo is thought tostimulate the release of sugars needed for bacterial growth.This strategy is likely to be used by other pathogens giventhat the transcriptional activation of SWEET genes wasalso observed during infection by fungi and oomycetes[47,48] (Figure 3).

Alternatively, SWEET transporters could increase sus-ceptibility of rice to Xoo by regulating host copper redistri-bution. Rice OsSWEET11 interacts both in vivo and in vitrowith the copper transporters OsCOPT1 and OsCOPT5 atthe plasma membrane. Remarkably, all three genes, OsS-WEET11, OsCOPT1, and OsCOPT5, are increased tran-script abundance during Xoo infection in rice, and areneeded for copper uptake. Their constitutive expressionled to increased copper content in rice leaf tissues, exceptin the xylem where the copper content was reduced. Infec-tion with Xoo strain PXO99 also led to the accumulation ofcopper in leaves, to which bacteria show high sensitivity.OsSWEET11, together with OsCOPTs, is suggested to limittoxic effects on the vascular pathogen Xoo by transportingcopper out of the xylem during infection [51] (Figure 3).

The increased activity of the cell wall-bound invertasesis often associated with pathogen infection and could en-hance the sink strength to provide carbon to the pathogen.In grapevine leaves, the cell wall-bound invertase geneVvcw-INV is indeed transcriptionally induced during in-fection with downy and powdery mildews [48]. Accordingly,in transgenic tomato (Solanum lycopersicum) plants inwhich the major cell wall-bound invertase isoforms hadbeen silenced, starch accumulation in leaves was reduced,suggesting that cell wall-bound invertases restrict sucroseexport [52]. Thus, cell wall-bound invertases could facili-tate efficient sugar allocation to infected tissues. In Arabi-dopsis roots, the cell wall-bound invertase gene AtcwINV1and the vacuolar invertase gene Atbfruct4 show enhancedexpression upon infection with the clubroot pathogen Plas-modiophora brassicae. Inhibition of the invertases at theinfection sites of the Arabidopsis root via the root-specificexpression of the invertase inhibitor genes AtC/VIF1 andAtC/VIF2 led to reduced gall formation by the pathogen[53], suggesting that both vacuolar and cell wall invertasescould increase disease susceptibility by enhancing the sinkstrength (Figure 3). However, the role of extracellularinvertases in disease susceptibility is likely to be morecomplex. For example, inhibition of cell wall-bound inver-tases in Arabidopsis by acarbose led to enhanced suscepti-bility to Pseudomonas syringae pv. tomato DC3000 [54],indicating that cell wall-bound invertases positively affectimmunity. In addition, effectors of Xanthomonas campes-tris pv. vesicatoria were shown to suppress cell wall-boundinvertase activity, thereby reducing sugar-mediated im-munity [55]. Therefore, it is possible that pathogens adjustplant invertase activity so that host immune responses andefficient sugar transport are balanced.

Host plants are likely to provide additional forms oforganic carbon to their microbial guests. In the nitrogen-fixing nodules on legume roots, carbon is transported to theinfected cells not only in the form of sugars but also inother organic forms, presumably tricarboxylates, from thesurrounding uninfected cells [56,57]. In barley, alcohol

Powdery mildew infec�on

Pathogenic bacteriag

Bacterial infec�on

Epidermal cells

Powdery mildew

Xylem

Phloem

Parenchyma cellsunderlying epidermis

Parenchyma cellsin vascular bundle

SucroseGlucose, fructose

SWEETs

Invertases

ADHs

COPTs

Copper

Endoreduplica�on

Key:

Parenchyma cellsin vascular bundle

wdery mPow mildew infec�ononmildew

(A) (B)


Figure 3. Model of plant susceptibility factors enabling bacterial (A) and fungal (B) pathogens to be fed by the plant, depicted in a schematic partial cross-section of a leaf.

On the schematic leaf cross-section, genes encoding for SWEET sugar transporters are transcriptionally induced after infection with fungal, oomycete, and bacterial

pathogens. In powdery and downy mildew-infected leaves, the induction of SWEET genes is associated with vascular tissues. SWEETs are suggested to unload sucrose

from the phloem into the apoplast, besides symplastic unloading via plasmodesmata. Subsequently, cell wall-bound or vacuolar invertases, activated during infection,

hydrolyze sucrose into fructose and glucose. Invertase activity, typically linked to sink tissues, promotes phloem unloading and sugar delivery to pathogens. Nuclei of

mesophyll cells underlying powdery mildew-infected epidermal cells undergo endoreduplication cycles that are suggested to enhance metabolic rates contributing to

successful pathogen development. Host alcohol dehydrogenase activity (ADH) induced during powdery mildew infection might help to reroute plant cell metabolism to

produce compounds beneficial for the pathogen. Finally, the sugar transporter OsSWEET11 together with copper transporters OsCOPT1 and OsCOPT5 might also play a

role in removing copper, which is toxic to the pathogenic bacteria Xanthomonas oryzae pv. oryzae from rice xylem sap.



dehydrogenase (ADH) activity is induced during infectionwith B. graminis f. sp. hordei. Treatment with pyrazole, aninhibitor of ADH-catalyzed alcohol oxidation, reduced thedisease symptoms and hyphal growth of the powdery mildewfungus and, accordingly, transient overexpression of thebarley HvADH1 increased the number of successfully estab-lished fungal infection sites [58]. Elevated ADH activitycould lead to the production of alternative sources of organiccarbon for pathogens. This was observed in grapevine, inwhich overexpression of VvADH2 led to the accumulation ofdiverse secondary metabolites, such as shikimates, noriso-prenoids, and terpenes [59]. Furthermore, ADH activity isinduced under hypoxic conditions in maize [60] and Arabi-dopsis [61], and ADH1 overexpression enables Arabidopsisplants to maintain root hair growth rates under oxygen-limiting conditions [62]. Increased ADH activity at powderymildew infection sites could, therefore, also contribute toprolonged survival of infected host cells (Figure 3).

Maintenance of photosynthesis in noninfected tissuescould help to supply pathogens with sufficient sugars.Healthy leaves of maize plants, infected with the smutfungus U. maydis, were found to have higher photosyn-thesis rates and senesce later than leaves of uninfectedplants [63], suggesting a systemic effect of infection. It isunknown if mobile pathogen effectors, hormones, or other

compounds are directly or indirectly responsible for sys-temic effects in noninfected host tissues. Also, ‘greenislands’, which are typical of many plant diseases andsurround infection sites [64], show prolonged photosyn-thesis, such as in senescing maize leaves infected with thehemibiotroph Colletotrichum graminicola [65], enablingprolonged feeding of the pathogen (Figure 2).

Transporters of other metabolites have also been impli-cated in pathogen feeding. For example, the poplar (Popu-lus trichocarpa) PtSultr3;5 gene encoding for a sulfatetransporter is highly expressed during rust fungus (Mel-ampsora larici-populina) infections, although its role infeeding needs to be confirmed [66]. The sulfate transportergene SST1 from L. japonicus is essential for symbioticnitrogen fixation [67]. Genome data suggest that thedowny mildew pathogen of Arabidopsis lacks the geneencoding sulfite reductase, an enzyme acting downstreamof sulfate reduction in the sulfur assimilation pathway[68]. Similarly, important enzymes involved in inorganicnitrogen metabolism in the nitrate reduction pathway aremissing in two groups of obligate biotrophic pathogens:Arabidopsis downy mildew and white rust (Albugo laiba-chii) [69] and three powdery mildew species [68,70]. Thiswould imply that the plant provides these pathogens withother forms of sulfur and nitrogen, possibly in the form of

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host-derived amino acids. However, so far, there have beenno reports regarding the involvement of plant amino acidtransporters in disease susceptibility, possibly becausetheir reduced activity can have severe pleiotropic effects.

Endoreduplication of plants cells is another strikingalteration in response to pathogen infection. Biotrophsthat feed on living host cells are suggested to abuse aregulatory mechanism of the host involved in controllingthe ploidy level of cells. Arabidopsis cells infected with thepowdery mildew fungus Golovinomyces orontii showedinduced transcription of the MYB3R4 gene that encodesa transcriptional regulator of endoreduplication. At 5 dayspost-inoculation with G. orontii, mesophyll cells underly-ing infected epidermal cells showed an increase in ploidylevel of up to 64C with a median value of 32C. Interesting-ly, myb3r4 mutants do not show a significant increase inthe ploidy level of mesophyll cells below infected epidermalcells and have reduced fungal growth [71]. Analysis ofadditional mutants showing reduced endoreduplicationlevels suggest that ploidy of mesophyll cells underlyingthe fungal feeding sites is an important susceptibilitydeterminant of powdery mildew infection [72]. Similarly,nematodes can induce endoreduplication in feeding cellsformed in host plant roots [73]. In Arabidopsis, overexpres-sion of the cell cycle inhibitor Kip-related protein 4 (KRP4)inhibits this endoreduplication and consequently delaysroot knot nematode development [74]. The increased ploidylevels of host cells infected with powdery mildew or nema-todes was shown to lead to higher relative transcript levelsof metabolic genes. This phenomenon also occurs in theabsence of infection in plant cells with higher ploidy leveland high catabolic activity, such as the endosperm andtrichomes. This suggests that endoreduplication activateshost metabolism to supply the hosted biotrophs with nutri-ents [75] (Figure 3).

Reducing crop susceptibilityUnder conditions of disease pressure, the fitness of suscep-tible crops is severely affected, resulting in yield reductionor complete crop losses. Breeding for genetic resistance isoften the best measure for crop protection because chemi-cal control can have negative environmental effects. How-ever, dominant resistance, governed by single resistance(R) genes, is often rapidly overcome by new pathogen races.Resistance mechanisms can also be genetically more com-plex, based on multiple resistance loci, as recently observedfor broad-spectrum downy mildew resistance in Arabidop-sis C24 [76]. Alternative forms of resistance can be basedon inactivating or interfering with host genes that contrib-ute to disease susceptibility. This form of resistance is oftenrecessive in nature. These alternative forms of resistance,also referred to as loss-of-susceptibility forms [77], have thepotential to provide alternative and durable sources ofdisease resistance in crops.

A well-known example of recessive resistance in cropbreeding is the use of mutations in the barley MildewResistance Locus O (MLO) gene. Plant homozygous forrecessive mlo alleles confer broad-spectrum resistance topowdery mildew fungi in barley [78,79], tomato [80], andArabidopsis [81], but even also to the bacterial pathogenXanthomonas campestris in pepper (Capsicum annuum)

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[82]. However, mlo-based resistance is most likely causedby derepression of immune responses [83], making it dif-ferent from the non-immunity related forms describedbelow. Also in rice several recessive resistance genes toXoo are known, including rice xa13, a nonpathogen-respon-sive variant of a SWEET gene that is, however, alsoassociated with abnormal pollen development and reducedseed set [49]. The application of SWEET-based loss-of-susceptibility in breeding without fitness penalties couldbe achieved by using tissue-specific silencing of SWEETs intransgenic rice [84]. A second example is the use of loss-of-susceptibility mutations in the translation initiation factoreIF4E and its homologs for resistance to viruses. In Ara-bidopsis, translation initiation factor eIF(iso)4E, a homologof eIF4E, is essential for successful infection with thetobacco etch virus. Mutants in eIF(iso)4E are resistantto the potyvirus by preventing systemic spread of the virusand, unexpectedly, not by reduced viral translation andreplication [85]. Mutations in the eIF4E group of genes arenow widely used as a source of resistance to potyviruses incrops [86–88].

How can we identify additional host susceptibilitygenes? One approach is based on exploring natural andinduced genetic variation. Mutations in the well-knownhost susceptibility factors encoding SWEETs and eIF(i-so)4E/G have been isolated in natural populations of riceand pepper (C. annuum and Capsicum chinense) conferringrecessive resistance to Xoo and potyviruses, respectively[49,50,88]. Genome-wide association mapping in naturalpopulations is expected to be an additional method ofidentifying new susceptibility genes. However, dominantrace-specific resistance genes present within the host plantspecies can obstruct this analysis, as shown in Arabidopsis,where resistance to downy mildew was strongly associatedwith R gene clusters, which are known to contain genescontrolling immunity to Hyaloperonospora arabidopsidis[89]. Recently, naturally occurring and induced mutationsin the locus Rhg4 encoding for serine hydroxymethyltrans-ferase (SHMT) were shown to confer soybean resistance tothe cyst nematode Heterodera glycines. The mutationsinterfere with the Rhg4/SHMT catalytic function in glycineand folate metabolism, suggesting that this host enzymehas a role in providing nutrients to the nematode [90].Resistance to downy mildew was obtained in Arabidopsismutants with altered amino acid metabolism. The Arabi-dopsis dmr1, rsp1, and rsp2 mutants with defectiveHOMOSERINE KINASE, ASPARTATE KINASE 2, andDIHYDRODIPICOLINATE SYNTHASE 2, respectively,show perturbations in Asp-derived amino acid synthesis,such as overaccumulation of homoserine and threonine[91–93]. Potentially, high levels of these amino acids re-duce the production of as yet unknown metabolites neededfor downy mildew infection.

Host gene expression profiling in pathogen-infectedplants is another way of discovering candidate diseasesusceptibility genes. Comparison of genes expressed inresistant and susceptible Arabidopsis accessions infectedwith H. arabidopsidis identified a malectin-like receptor-like kinase gene IMPAIRED IN OOMYCETE SUSCEPTI-BILITY 1, the mutation of which led to enhanced resis-tance to downy mildew without signs of constitutive



immune responses [94]. However, the role of the gene indisease susceptibility is unclear. Similarly, a set of Arabi-dopsis genes was identified that are specifically inducedduring infection with H. arabidopsidis in susceptibleplants and that are known to be induced under abioticstresses such as drought, salinity, and cold [95].

Host proteins that are targets of pathogen effectors couldalso be regarded as susceptibility proteins. Protein–proteininteraction studies, for example, a recent interactome studyof Arabidopsis [96], are revealing more and more effectortargets and helpers [97]. However, many of the interactingproteins are strongly linked to immunity. Ongoing andfuture studies are likely to reveal more host proteins andgenes that have a role in ‘attracting’, ‘accommodating’, and‘feeding’ plant pathogens. The identification and functionalanalysis of these genes and proteins could uncover molecu-lar processes that underlie many non-immunity relatedaspects of plant disease susceptibility and might providethe basis for novel strategies for disease resistance breeding.

AcknowledgmentsThe Leverhulme Trust (UK) is acknowledged for supporting D.L.

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