Plant disease resistance

Plant disease resistance protects plants from pathogensin two ways: by preformed mechanisms and by infection-induced responses of the immune system. Relative toa susceptible plant, disease resistance is the reductionof pathogen growth on or in the plant, while the termdisease tolerance describes plants that exhibit little dis-ease damage despite substantial pathogen levels. Diseaseoutcome is determined by the three-way interaction ofthe pathogen, the plant and the environmental conditions(an interaction known as the disease triangle).Defense-activating compounds can move cell-to-cell andsystemically through the plant vascular system. However,plants do not have circulating immune cells, so most celltypes exhibit a broad suite of antimicrobial defenses. Al-though obvious qualitative differences in disease resis-tance can be observed when multiple specimens are com-pared (allowing classification as “resistant” or “suscepti-ble” after infection by the same pathogen strain at similarinoculum levels in similar environments), a gradation ofquantitative differences in disease resistance is more typi-cally observed between plant strains or genotypes. Plantsconsistently resist certain pathogens but succumb to oth-ers; resistance is usually pathogen species- or pathogenstrain-specific.

1 Background

Plant disease resistance is crucial to the reliable produc-tion of food, and it provides significant reductions in agri-cultural use of land, water, fuel and other inputs. Plantsin both natural and cultivated populations carry inherentdisease resistance, but this has not always protected them.The late blight Irish potato famine of the 1840s wascaused by the oomycete Phytophthora infestans. Theworld’s first mass-cultivated banana cultivar Gros Michelwas lost in the 1920s to Panama disease caused by thefungus Fusarium oxysporum. The current wheat stem,leaf, and yellow stripe rust epidemics spreading from EastAfrica into the Indian subcontinent are caused by rustfungi Puccinia graminis and P. striiformis. Other epi-demics include Chestnut blight), as well as recurrent se-vere plant diseases such as Rice blast, Soybean cyst ne-matode, Citrus canker.[1]

Plant pathogens can spread rapidly over great distances,vectored by water, wind, insects, and humans. Acrosslarge regions and many crop species, it is estimated thatdiseases typically reduce plant yields by 10% every year

in more developed nations or agricultural systems, butyield loss to diseases often exceeds 20% in less developedsettings, an estimated 15% of global crop production.[1]

However, disease control is reasonably successful formost crops. Disease control is achieved by use of plantsthat have been bred for good resistance to many diseases,and by plant cultivation approaches such as crop rotation,pathogen-free seed, appropriate planting date and plantdensity, control of field moisture and pesticide use.

2 Common mechanisms

2.1 Pre-formed structures and compounds

secondary plant wall

• Plant cuticle/surface

• Plant cell walls

• Antimicrobial chemicals (for example: glucosides,saponins)

• Antimicrobial proteins

• Enzyme inhibitors

• Detoxifying enzymes that break down pathogen-derived toxins

• Receptors that perceive pathogen presence and acti-vate inducible plant defences[2]

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2 3 IMMUNE SYSTEM

2.2 Inducible post-infection plant defenses• Cell wall reinforcement (callose, lignin, suberin, cellwall proteins)

• Antimicrobial chemicals, including reactive oxygenspecies such as hydrogen peroxide or peroxynitrite,or more complex phytoalexins such as genistein orcamalexin)

• Antimicrobial proteins such as defensins, thionins,or PR-1

• Antimicrobial enzymes such as chitinases, beta-glucanases, or peroxidases

• Hypersensitive response - a rapid host cell death re-sponse associated with defence mediated by “Resis-tance genes.”[2]

• Endophyte assistance: Plant’s roots release chem-icals that attract beneficial bacteria to fight offinfections.[3]

3 Immune system

The plant immune system consists of two interconnectedtiers of receptors, one outside and one inside the cell.Both systems sense the intruder, respond to the intrusionand optionally signal to the rest of the plant and some-times to neighboring plants that the intruder is present.The two systems detect different types of pathogenmolecules and classes of plant receptor proteins.[1]

The first tier is primarily governed by pattern recognitionreceptors that are activated by recognition of evolutionar-ily conserved pathogen or microbial–associated molecu-lar patterns (PAMPs or MAMPs, here P/MAMP). Ac-tivation of PRRs leads to intracellular signaling, tran-scriptional reprogramming, and biosynthesis of a com-plex output response that limits colonization. The systemis known as PAMP-Triggered Immunity (PTI).[4][5]

The second tier (again, primarily), effector-triggered im-munity (ETI), consists of another set of receptors, thenucleotide-binding LRRs (NLRs). They operate withinthe cell, encoded by R genes. The presence of specificpathogen “effectors” activates specific NLR proteins thatlimit pathogen proliferation.[1]

Receptor responses include ion channel gating, oxidativeburst, cellular redox changes, or protein kinase cascadesthat directly activate cellular changes (such as cell wallreinforcement or antimicrobial production), or activatechanges in gene expression that then elevate other defen-sive responses.[1]

Plant immune systems show some mechanistic similar-ities with the immune systems of insects and mam-mals, but also exhibit many plant-specific characteristics.Plants can sense the presence of pathogens and the effectsof infection via different mechanisms than animals.[6]

3.1 PAMP-triggered immunity

PAMP-Triggered Immunity (PTI) is often a plant’s firstinducible response.[4][7] Immune-eliciting PAMPs in-clude bacterial flagellin or lipopolysaccharides, or fungalchitin. Much less widely conserved molecules that in-habit multiple pathogen genera are classified as MAMPsby some researchers. The defenses induced by MAMPperception are sufficient to repel most pathogens. How-ever, pathogen effector proteins are adapted to suppressbasal defenses such as PTI.[5]

3.2 Effector triggered immunity

Effector Triggered Immunity (ETI) is activated by thepresence of pathogen effectors.[4][7] The ETI immune re-sponse is reliant on R genes, and is activated by specificpathogen strains. As with PTI, many specific examplesof apparent ETI violate common PTI/ETI definitions.[8]Most plant immune systems carry a repertoire of 100-600different R genes that mediate resistance to various virus,bacteria, fungus, oomycete and nematode pathogens andinsects. Plant ETI often cause an apoptotic hypersensitiveresponse.

3.2.1 R genes and R proteins

Plants have evolved R genes (resistance genes) whoseproducts allow recognition of specific pathogen effectors,either through direct binding or by recognition of the ef-fector’s alteration of a host protein.[4] These virulencefactors drove co-evolution of plant resistant genes to com-bat the pathogens’ Avr (avirulent) genes. Many R genesencode NB-LRR proteins (nucleotide-binding/leucine-rich repeat domains, also known as NLR proteins orSTAND proteins, among other names).R gene products control a broad set of disease resistanceresponses whose induction is often sufficient to stop fur-ther pathogen growth/spread. Each plant genome con-tains a few hundred apparent R genes. Studied R genesusually confer specificity for particular pathogen strains.As first noted by Harold Flor in his mid-20th centuryformulation of the gene-for-gene relationship, the plantR gene and the pathogen Avr gene must have matchedspecificity for that R gene to confer resistance, suggestinga receptor/ligand interaction for Avr and R genes.[7] Al-ternatively, an effector can modify its host cellular target(or a molecular decoy of that target) activating an NLRassociated with the target or decoy.Plant breeders frequently rely on R genes to obtain use-ful resistance, although the durability of this resistancecan vary by pathogen, pathogen effector and R gene. Thepresence of an R gene can place significant selective pres-sure on the pathogen to alter or delete the correspondingavirulence/effector gene. Some R genes show evidence ofstability over millions of years while other R genes, espe-

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cially those that occur in small clusters of similar genes,can evolve new pathogen specificities over much shorterintervals.[9]

3.2.2 Effector biology

Effectors are central to microbes’ pathogenic or symbi-otic potential and of microscopic plant-colonizing ani-mals such as nematodes.[10][11][12] Effectors typically areproteins that are delivered mostly outside the microbeand into the host cell. Effectors manipulate cell physi-ology and development. As such, effectors offer exam-ples of co-evolution (example: a fungal protein that func-tions outside of the fungus but inside of plant cells hasevolved to take on plant-specific functions). Pathogenhost range is determined, among other things, by the pres-ence of appropriate effectors that allow colonization of aparticular host.[5] Pathogen-derived effectors are a pow-erful tool to identify host functions that are important indisease. Apparently most effectors function to manip-ulate host physiology to allow disease to occur. Well-studied bacterial plant pathogens typically express a fewdozen effectors, often delivered into the host by a TypeIII secretion apparatus.[10] Fungal, oomycete and nema-tode plant pathogens apparently express a few hundredeffectors.[11][12]

So-called “core” effectors are defined operationally bytheir wide distribution across the population of a par-ticular pathogen and their substantial contribution topathogen virulence. Genomics can be used to identifycore effectors, which can then functionally define new Ralleles, which can serve as breeding targets.[1]

3.3 RNA silencing and systemic acquiredresistance elicited by prior infections

Against viruses, plants often induce pathogen-specificgene silencing mechanisms mediated by RNA interfer-ence. This is a simple form of adaptive immunity.[13]

Plant immune systems also can respond to an initial infec-tion in one part of the plant by physiologically elevatingthe capacity for a successful defense response in otherparts. Such responses include systemic acquired resis-tance, largely mediated by salicylic acid-dependent path-ways, and induced systemic resistance, largely mediatedby jasmonic acid-dependent pathways.[14]

3.4 Species-level resistance

In a small number of cases, plant genes are effectiveagainst an entire pathogen species, even though thatspecies that is pathogenic on other genotypes of that hostspecies. Examples include barley MLO against powderymildew, wheat Lr34 against leaf rust and wheat Yr36against stripe rust. An array of mechanisms for this

type of resistance may exist depending on the partic-ular gene and plant-pathogen combination. Other rea-sons for effective plant immunity can include a lack ofcoadaptation (the pathogen and/or plant lack multiplemechanisms needed for colonization and growth withinthat host species), or a particularly effective suite of pre-formed defenses.

4 Signaling mechanisms

4.1 Perception of pathogen presence

Plant defense signaling is activated by pathogen-detectingreceptors.[5] The activated receptors frequently elicitreactive oxygen and nitric oxide production, calcium,potassium and proton ion fluxes, altered levels of salicylicacid and other hormones and activation of MAP kinasesand other specific protein kinases.[7] These events in turntypically lead to the modification of proteins that con-trol gene transcription, and the activation of defense-associated gene expression.In addition to PTI and ETI, plant defenses can be acti-vated by the sensing of damage-associated compounds(DAMP), such as portions of the plant cell wall re-leased during pathogenic infection. Many receptors forMAMPs, effectors and DAMPs have been discovered.Effectors are often detected by NLRs, while MAMPs andDAMPs are often detected by transmembrane receptor-kinases that carry LRR or LysM extracellular domains.[5]

4.2 Transcription factors and the hormoneresponse

Numerous genes and/or proteins have been identi-fied that mediate plant defense signal transduction.[15]Cytoskeleton and vesicle trafficking dynamics help to ori-ent plant defense responses toward the point of pathogenattack.

4.2.1 Mechanisms of transcription factors and hor-mones

Plant immune system activity is regulated in part by sig-naling hormones such as:[16]

• Salicylic acid

• Jasmonic acid

• Ethylene

There can be substantial cross-talk among thesepathways.[16]

4 5 PLANT BREEDING FOR DISEASE RESISTANCE

4.3 Regulation by degradation

As with many signal transduction pathways, plant geneexpression during immune responses can be regulated bydegradation. This often occurs when hormone binding tohormone receptors stimulates ubiquitin-associated degra-dation of repressor proteins that block expression of cer-tain genes. The net result is hormone-activated gene ex-pression. Examples:[17]

• Auxin: binds to receptors that then recruit and de-grade repressors of transcriptional activators thatstimulate auxin-specific gene expression.

• Jasmonic acid: similar to auxin, except withjasmonate receptors impacting jasmonate-responsesignaling mediators such as JAZ proteins.

• Gibberellic acid: Gibberellin causes receptor con-formational changes and binding and degradation ofDella proteins.

• Ethylene: Inhibitory phosphorylation of the EIN2ethylene response activator is blocked by ethylenebinding. When this phosphorylation is reduced,EIN2 protein is cleaved and a portion of the proteinmoves to the nucleus to activate ethylene-responsegene expression.

4.3.1 Ubiquitin and E3 signaling

Ubiquitination plays a central role in cell signaling thatregulates processes including protein degradation andimmunological response.[18] Although one of the mainfunctions of ubiquitin is to target proteins for destruc-tion, it is also useful in signaling pathways, hormone re-lease, apoptosis and translocation of materials throughoutthe cell. Ubiquitination is a component of several im-mune responses. Without ubiquitin’s proper functioning,the invasion of pathogens and other harmful moleculeswould increase dramatically due to weakened immunedefenses.[18]

E3 signaling The E3 Ubiquitin ligase enzyme isa main component that provides specificity in pro-tein degradation pathways, including immune signal-ing pathways.[17] The E3 enzyme components can begrouped by which domains they contain and include sev-eral types.[19] These include the Ring and U-box singlesubunit, HECT, and CRLs.[20][21] Plant signaling path-ways including immune responses are controlled by sev-eral feedback pathways, which often include negativefeedback; and they can be regulated by De-ubiquitinationenzymes, degradation of transcription factors and thedegradation of negative regulators of transcription.[17][22]

This image depicts the pathways taken during responses in plantimmunity. It highlights the role and effect ubiquitin has in regu-lating the pathway.

4.4 Mechanisms common to both plantand animal immune systems

The use of PAMP transmembrane receptors carryingleucine-rich repeat (LRR) pathogen recognition speci-ficity domains, and of cytoplasmic NB-LRR or NLRreceptors, is common to plant, insect, jawless verte-brate and mammal immune systems. The presence ofToll/Interleukin receptor (TIR) domains in plant immunereceptors and also the expression of defensins, thionins,oxidative burst and other defense responses also reveal thepresence ofmechanisms shared between plant and animalimmune systems.[4][23]

5 Plant breeding for disease resis-tance

Plant breeders emphasize selection and development ofdisease-resistant plant lines. Plant diseases can also bepartially controlled by use of pesticides and by cultiva-tion practices such as crop rotation, tillage, planting den-sity, disease-free seeds and cleaning of equipment, butplant varieties with inherent (genetically determined) dis-ease resistance are generally preferred. Breeding for dis-ease resistance began when plants were first domesti-cated. Breeding efforts continue because pathogen pop-ulations are under selection pressure for increased viru-lence, new pathogens appear, evolving cultivation prac-tices and changing climate can reduce resistance and/orstrengthen pathogens, and plant breeding for other traitscan disrupt prior resistance. A plant line with accept-able resistance against one pathogen may lack resistanceagainst others.

5.1 GM or transgenic engineered disease resistance 5

Breeding for resistance typically includes:

• Identification of plants that may be less desirable inother ways, but which carry a useful disease resis-tance trait, including wild strains that often expressenhanced resistance.

• Crossing of a desirable but disease-susceptible vari-ety to another variety that is a source of resistance.

• Growth of breeding candidates in a disease-conducive setting, possibly including pathogen in-oculation. Attention must be paid to the specificpathogen isolates, to address variability within a sin-gle pathogen species.

• Selection of disease-resistant individuals that retainother desirable traits such as yield, quality and in-cluding other disease resistance traits.

Resistance is termed durable if it continues to be effec-tive over multiple years of widespread use as pathogenpopulations evolve. "Vertical resistance" is specific tocertain races or strains of a pathogen species, is oftencontrolled by single R genes and can be less durable.Hoizontal or broad-spectrum resistance against an entirepathogen species is often only incompletely effective, butmore durable, and is often controlled by many genes thatsegregate in breeding populations.Crops such as potato, apple, banana and sugarcane areoften propagated by vegetative reproduction to preservehighly desirable plant varieties, because for these species,outcrossing seriously disrupts the preferred traits. Seealso asexual propagation. Vegetatively propagated cropsmay be among the best targets for resistance improvementby the biotechnology method of plant transformation tomanage genes that affect disease resistance.Scientific breeding for disease resistance originated withSir Rowland Biffen, who identified a single recessive genefor resistance to wheat yellow rust. Nearly every crop wasthen bred to include disease resistance (R) genes, many byintrogression from compatible wild relatives.[1]

5.1 GM or transgenic engineered diseaseresistance

The term GM (“genetically modified”) is often usedas a synonym of transgenic to refer to plants modi-fied using recombinant DNA technologies. Plants withtransgenic/GM disease resistance against insect pestshave been extremely successful as commercial prod-ucts, especially in maize and cotton, and are plantedannually on over 20 million hectares in over 20 coun-tries worldwide[24] (see also genetically modified crops).Transgenic plant disease resistance against microbialpathogens was first demonstrated in 1986. Expression of

viral coat protein gene sequences conferred virus resis-tance via small RNAs. This proved to be a widely appli-cable mechanism for inhibiting viral replication. Com-bining coat protein genes from three different viruses,scientists developed squash hybrids with field-validated,multiviral resistance. Similar levels of resistance to thisvariety of viruses had not been achieved by conventionalbreeding.A similar strategy was deployed to combat papayaringspot virus, which by 1994 threatened to destroyHawaii’s papaya industry. Field trials demonstrated ex-cellent efficacy and high fruit quality. By 1998 the firsttransgenic virus-resistant papaya was approved for sale.Disease resistance has been durable for over 15 years.Transgenic papaya accounts for ~85% of Hawaiian pro-duction. The fruit is approved for sale in the U.S., Canadaand Japan.Potato lines expressing viral replicase sequences that con-fer resistance to potato leafroll virus were sold under thetrade names NewLeaf Y and NewLeaf Plus, and werewidely accepted in commercial production in 1999-2001,until McDonald’s Corp. decided not to purchase GMpotatoes and Monsanto decided to close their Nature-Mark potato business.[25] NewLeaf Y and NewLeaf Pluspotatoes carried two GM traits, as they also expressed Bt-mediated resistance to Colorado potato beetle.No other crop with engineered disease resistance againstmicrobial pathogens had reached the market by 2013, al-though more than a dozen were in some state of develop-ment and testing.

5.1.1 PRR transfer

Research aimed at engineered resistance follows multi-ple strategies. One is to transfer useful PRRs into speciesthat lack them. Identification of functional PRRs andtheir transfer to a recipient species that lacks an orthol-ogous receptor could provide a general pathway to ad-ditional broadened PRR repertoires. For example, theArabidopsis PRR EF-Tu receptor (EFR) recognizes thebacterial translation elongation factor EF-Tu. Researchperformed at Sainsbury Laboratory demonstrated that de-ployment of EFR into either Nicotiana benthamianaorSolanum lycopersicum (tomato), which cannot recognizeEF-Tu, conferred resistance to a wide range of bacte-rial pathogens. EFR expression in tomato was espe-cially effective against the widespread and devastatingsoil bacterium Ralstonia solanacearum.[26] Conversely,the tomato PRR Verticillium 1 (Ve1) gene can be trans-ferred from tomato to Arabidopsis, where it confers resis-tance to race 1 Verticillium isolates.[1]

5.1.2 Stacking

The second strategy attempts to deploy multiple NLRgenes simultaneously, a breeding strategy known as

6 5 PLANT BREEDING FOR DISEASE RESISTANCE

stacking. Cultivars generated by either DNA-assistedmolecular breeding or gene transfer will likely displaymore durable resistance, because pathogens would haveto mutate multiple effector genes. DNA sequencing al-lows researchers to functionally “mine” NLR genes frommultiple species/strains.[1]

The avrBs2 effector gene from Xanthomona perforans isthe causal agent of bacterial spot disease of pepper andtomato. The first “effector-rationalized” search for a po-tentially durable R gene followed the finding that avrBs2is found in most disease-causing Xanthomonas speciesand is required for pathogen fitness. The Bs2 NLR genefrom the wild pepper, Capsicum chacoense, was movedinto tomato, where it inhibited pathogen growth. Fieldtrials demonstrated robust resistance without bactericidalchemicals. However, rare strains of Xanthomonas over-came Bs2-mediated resistance in pepper by acquisition ofavrBs2 mutations that avoid recognition but retain viru-lence. Stacking R genes that each recognize a differentcore effector could delay or prevent adaptation.[1]

More than 50 loci in wheat strains confer disease re-sistance against wheat stem, leaf and yellow stripe rustpathogens. The Stem rust 35 (Sr35) NLR gene, clonedfrom a diploid relative of cultivated wheat, Triticummonococcum, provides resistance to wheat rust isolateUg99. Similarly, Sr33, from the wheat relative Aegilopstauschii, encodes a wheat ortholog to barley Mla pow-dery mildew–resistance genes. Both genes are unusualin wheat and its relatives. Combined with the Sr2 genethat acts additively with at least Sr33, they could providedurable disease resistance to Ug99 and its derivatives.[1]

5.1.3 Executor genes

Another class of plant disease resistance genes opensa “trap door” that quickly kills invaded cells, stoppingpathogen proliferation. Xanthomonas and Ralstoniatranscription activator–like (TAL) effectors are DNA-binding proteins that activate host gene expression to en-hance pathogen virulence. Both the rice and pepper lin-eages independently evolved TAL-effector binding sitesthat instead act as an executioner that induces hypersen-sitive host cell death when up-regulated. Xa27 from riceand Bs3 and Bs4c from pepper, are such “executor” (or“executioner”) genes that encode non-homologous plantproteins of unknown function. Executor genes are ex-pressed only in the presence of a specific TAL effector.[1]

Engineered executor genes were demonstrated by suc-cessfully redesigning the pepper Bs3 promoter to con-tain two additional binding sites for TAL effectors fromdisparate pathogen strains. Subsequently, an engineeredexecutor gene was deployed in rice by adding five TALeffector binding sites to the Xa27 promoter. Thesynthetic Xa27 construct conferred resistance againstXanthomonas bacterial blight and bacterial leaf streakspecies.[1]

5.1.4 Host susceptibility alleles

Most plant pathogens reprogram host gene expressionpatterns to directly benefit the pathogen. Reprogrammedgenes required for pathogen survival and proliferationcan be thought of as “disease-susceptibility genes.” Re-cessive resistance genes are disease-susceptibility can-didates. For example, a mutation disabled an Ara-bidopsis gene encoding pectate lyase (involved in cellwall degradation), conferring resistance to the powderymildew pathogen Golovinomyces cichoracearum. Simi-larly, the Barley MLO gene and spontaneously mutatedpea and tomato MLO orthologs also confer powderymildew resistance.[1]

Lr34 is a gene that provides partial resistance to leafand yellow rusts and powdery mildew in wheat. Lr34encodes an adenosine triphosphate (ATP)–binding cas-sette (ABC) transporter. The dominant allele that pro-vides disease resistance was recently found in cultivatedwheat (not in wild strains) and, likeMLO provides broad-spectrum resistance in barley.[1]

Natural alleles of host translation elongation initiationfactors eif4e and eif4g are also recessive viral-resistancegenes. Some have been deployed to control potyvirusesin barley, rice, tomato, pepper, pea, lettuce and melon.The discovery prompted a successful mutant screen forchemically induced eif4e alleles in tomato.[1]

Natural promoter variation can lead to the evolution ofrecessive disease-resistance alleles. For example, the re-cessive resistance gene xa13 in rice is an allele ofOs-8N3.Os-8N3 is transcriptionally activated byXanthomonasoryzae pv. oryzae strains that express the TAL effectorPthXo1. The xa13 gene has a mutated effector-bindingelement in its promoter that eliminates PthXo1 bindingand renders these lines resistant to strains that rely onPthXo1. This finding also demonstrated that Os-8N3 isrequired for susceptibility.[1]

Xa13/Os-8N3 is required for pollen development, show-ing that such mutant alleles can be problematic should thedisease-susceptibility phenotype alter function in otherprocesses. However, mutations in the Os11N3 (OsS-WEET14) TAL effector–binding element were made byfusing TAL effectors to nucleases (TALENs). Genome-edited rice plants with altered Os11N3 binding sites re-mained resistant to Xanthomonas oryzae pv. oryzae, butstill provided normal development function.[1]

5.1.5 Gene silencing

RNA silencing-based resistance is a powerful tool for en-gineering resistant crops. The advantage of RNAi as anovel gene therapy against fungal, viral and bacterial in-fection in plants lies in the fact that it regulates gene ex-pression via messenger RNA degradation, translation re-pression and chromatin remodelling through small non-coding RNAs. Mechanistically, the silencing processes

7

are guided by processing products of the double-strandedRNA (dsRNA) trigger, which are known as small inter-fering RNAs and microRNAs.[27]

6 Host range

See also: Plant pathology

Among the thousands of species of plant pathogenic mi-croorganisms, only a small minority have the capacity toinfect a broad range of plant species. Most pathogens in-stead exhibit a high degree of host-specificity. Non-hostplant species are often said to express non-host resistance.The term host resistance is used when a pathogen speciescan be pathogenic on the host species but certain strainsof that plant species resist certain strains of the pathogenspecies. The causes of host resistance and non-host resis-tance can overlap. Pathogen host range can change quitesuddenly if, for example, the pathogen’s capacity to syn-thesize a host-specific toxin or effector is gained by geneshuffling/mutation, or by horizontal gene transfer.

7 Epidemics and population biol-ogy

Native populations are often characterized by substantialgenotype diversity and dispersed populations (growth ina mixture with many other plant species). They also haveundergone of plant-pathogen coevolution. Hence as longas novel pathogens are not introduced/do not evolve, suchpopulations generally exhibit only a low incidence of se-vere disease epidemics.[28]

Monocrop agricultural systems provide an ideal envi-ronment for pathogen evolution, because they offer ahigh density of target specimens with similar/identicalgenotypes.[28]

The rise in mobility stemming from modern transporta-tion systems provides pathogens with access to more po-tential targets.[28]

Climate change can alter the viable geographic range ofpathogen species and cause some diseases to become aproblem in areas where the disease was previously lessimportant.[28]

These factors make modern agriculture more prone todisease epidemics. Common solutions include constantbreeding for disease resistance, use of pesticides, use ofborder inspections and plant import restrictions, main-tenance of significant genetic diversity within the cropgene pool (see crop diversity), and constant surveillanceto accelerate initiation of appropriate responses. Somepathogen species havemuch greater capacity to overcomeplant disease resistance than others, often because of theirability to evolve rapidly and to disperse broadly.[28]

8 See also• Disease resistance in fruit and vegetables

• Gene-for-gene relationship

• Plant defense against herbivory

• Plant pathology

• Plant use of endophytic fungi in defense

• Systemic acquired resistance

• Sainsbury Laboratory

9 References

9.1 Notes[1] Dangl, J. L.; Horvath, D. M.; Staskawicz, B. J.

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[2] Lutz, Diana (2012). Key part of plants’ rapid responsesystem revealed. Washington University in St. Louis.

[3] Bryant, Tracy (2008). When under attack, plants can sig-nal microbial friends for help. University of Delaware.

[4] Jones, J. D.; Dangl, J.L. (2006). “Theplant immune system”. Nature 444 (7117):323–329. Bibcode:2006Natur.444..323J.doi:10.1038/nature05286. PMID 17108957.

[5] Dodds, P. N.; Rathjen, J. P. (2010). “Plant immu-nity: Towards an integrated view of plant–pathogeninteractions”. Nature Reviews Genetics 11 (8): 539.doi:10.1038/nrg2812.

[6] Boyd, Jade (2012). A bit touchy: Plants’ insect defensesactivated by touch. Rice University.

[7] Numberger, T.; Brunner, F., Kemmerling, B., and Pi-ater, L.; Kemmerling, B; Piater, L (2004). “Innateimmunity in plants and animals: striking similaritiesand obvious differences”. Immunological Reviews 198:249–266. doi:10.1111/j.0105-2896.2004.0119.x. PMID15199967.

[8] Thomma, B.; Nurnberger, T.; Joosten, M. (2011). “OfPAMPs and Effectors: The Blurred PTI-ETI Dichotomy”.The Plant Cell 23 (4): 15. doi:10.1105/tpc.110.082602.PMC 3051239. PMID 21278123.

[9] Friedman, A. R.; Baker, B. J. (2007). “The evolution ofresistance genes inmulti-protein plant resistance systems”.Current Opinion in Genetics & Development 17 (6): 493–9. doi:10.1016/j.gde.2007.08.014. PMID 17942300.

[10] Lindeberg, M; Cunnac, S; Collmer, A (2012). “Pseu-domonas syringae type III effector repertoires: Lastwords in endless arguments”. Trends in Microbiology 20(4): 199–208. doi:10.1016/j.tim.2012.01.003. PMID22341410.

8 10 EXTERNAL LINKS

[11] Rafiqi, M; Ellis, J. G.; Ludowici, V. A.; Hardham, A. R.;Dodds, P. N. (2012). “Challenges and progress towardsunderstanding the role of effectors in plant-fungal inter-actions”. Current Opinion in Plant Biology 15 (4): 477–82.doi:10.1016/j.pbi.2012.05.003. PMID 22658704.

[12] Hewezi, T; Baum, T. J. (2013). “Manipulation ofplant cells by cyst and root-knot nematode effectors”.Molecular Plant-Microbe Interactions 26 (1): 9–16.doi:10.1094/MPMI-05-12-0106-FI. PMID 22809272.

[13] Ding, S. W.; Voinnet, O. (2007). “Antiviral Immu-nity Directed by Small RNAs”. Cell 130 (3): 413–426.doi:10.1016/j.cell.2007.07.039. PMC 2703654. PMID17693253.

[14] Spoel, Steven H.; Dong, Xinnian (2012). “How do plantsachieve immunity? Defence without specialized immunecells”. Nature Reviews Immunology 12 (2): 89–100.doi:10.1038/nri3141. PMID 22273771.

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[19] Craig, A.; Ewan, R.; Mesmar, J.; Gudipati, V.; Sadanan-dom, A. (10 March 2009). “E3 ubiquitin ligases and plantinnate immunity”. Journal of Experimental Botany 60 (4):1123–1132. doi:10.1093/jxb/erp059. PMID 19276192.

[20] Moon, J. (1 December 2004). “The Ubiquitin-Proteasome Pathway and Plant Development”.The Plant Cell Online 16 (12): 3181–3195.doi:10.1105/tpc.104.161220.

[21] Trujillo, Marco; Shirasu, Ken (1 August 2010). “Ubiqui-tination in plant immunity”. Current Opinion in Plant Bi-ology 13 (4): 402–408. doi:10.1016/j.pbi.2010.04.002.PMID 20471305.

[22] Shirsekar, Gautam; Dai, Liangying; Hu, Yajun; Wang,Xuejun; Zeng, Lirong; Wang, Guo-Liang; Hu, Yajun;Wang, Xuejun; Zeng, Lirong; Wang, Guo-Liang (2010).“Role of Ubiquitination in Plant Innate Immunity andPathogenVirulence”. Journal of Plant Biology 53 (1): 10–18. doi:10.1007/s12374-009-9087-x.

[23] Ting, J. P.; Willingham, S. B.; Bergstralh, D. T.(2008). “NLRs at the intersection of cell death and im-munity”. Nature Reviews Immunology 8 (5): 372–9.doi:10.1038/nri2296. PMID 18362948.

[24] Tabashnik, Bruce E.; Brevault, Thierry; Carriere, Yves(2013). “Insect resistance to Bt crops: lessons from thefirst billion acres”. Nature Biotechnology 31: 510–521.doi:10.1038/nbt.2597.

[25] Kaniewski, Wojciech K.; Thomas, Peter E. (2004). “ThePotato Story”. AgBioForum 7 (1&2): 41–46.

[26] Lacombe et al., 2010 Interfamily transfer of a plantpattern-recognition receptor confers broad-spectrum bac-terial resistance, Nature Biotech 28, 365–369

[27] Karthikeyan, A.; Deivamani, M.; Shobhana, V. G.;Sudha, M.; Anandhan, T. (2013). “RNA interference:Evolutions and applications in plant disease manage-ment”. Archives of Phytopathology and Plant Protection46 (12): 1430. doi:10.1080/03235408.2013.769315.

[28] McDonald, B. A.; Linde, C (2002). “Pathogen popula-tion genetics, evolutionary potential, and durable resis-tance”. Annual Review of Phytopathology 40: 349–79.doi:10.1146/annurev.phyto.40.120501.101443. PMID12147764.

9.2 Further reading

• Lucas, J.A., “Plant Defence.” Chapter 9 in PlantPathology and Plant Pathogens, 3rd ed. 1998 Black-well Science. ISBN 0-632-03046-1

• Hammond-Kosack, K. and Jones, J.D.G. “Re-sponses to plant pathogens.” In: Buchanan, Gruis-sem and Jones, eds. Biochemistry and Molecu-lar Biology of Plants. 2000 Amer.Soc.Plant Biol.,Rockville, MD. ISBN 0-943088-39-9

• Dodds, P.; Rathjen, J. (2010). “Plant immunity:towards an integrated view of plant–pathogen in-teractions”. Nature Reviews Genetics 11: 539.doi:10.1038/nrg2812.

• Schumann, G. Plant Diseases: Their Biology andSocial Impact. 1991 APS Press, St. Paul, MN ISBN0890541167

10 External links• http://www.apsnet.org/

9

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