All Mold Is Not Alike: The Importance of Intraspecific Diversity in Necrotrophic Plant Pathogens


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Published in the journal: . PLoS Pathog 6(3): e32767. doi:10.1371/journal.ppat.1000759
Category: Opinion
doi: 10.1371/journal.ppat.1000759

Summary

article has not abstract

Pathogens commonly possess naturally occurring intraspecific variation for traits associated with pathogenicity or virulence. Studies of host–pathogen interactions frequently fail to acknowledge this variation, particularly in studies of necrotrophic plant pathogens, where the molecular bases of defense are largely unknown. Necrotrophic plant pathogens, in contrast to obligate parasites of living plant cells known as biotrophs, kill plant cells before consuming them and may survive in the absence of living host cells in dormant or saprophytic states [1][4]. Necrotrophs may kill host cells using an array of toxins, although it is also proposed that these pathogens may activate plant immune responses designed to work against biotrophic pathogens, thus encouraging plant cells to kill themselves [5][9]. While many pathogen species cannot be clearly classified as either biotrophic or necrotrophic, as they shift lifestyles over the course of interactions with their hosts, commonly recognized necrotrophic plant pathogens include various species of Botrytis and Alternaria, as well as Sclerotinia sclerotiorum, Pythium irregulare, and Plectosphaerella cucurmerina [2],[10]. Of these, Botrytis cinerea, a highly generalist pathogen, and Alternaria brassicicola, a specialist pathogen of Brassica, dominate research on molecular mechanisms of plant defense against necrotrophic pathogens.

Plant immune responses against biotrophic pathogens are predominantly mediated by specific recognition of the products of pathogen “avirulence” (avr) genes directly or indirectly by the products of plant “resistance” (R) genes; localized cell death is believed to restrict the growth of obligate (biotrophic) parasites [11],[12]. Intraspecific variation in pathogen avr genes is common, as these genes are believed to confer a selective pathogen advantage in the absence of the corresponding plant R gene [13][15]. Currently, specific recognition of necrotrophic pathogens by similar mechanisms has not been documented, although similar evolutionary dynamics may shape the interplay between variable plant sensitivity to some necrotroph-produced toxins (called “host selective toxins”) and variable production of these toxins by the pathogen [15][17]. This lack of identified specific recognition has generated a prevailing view in the plant molecular defense research community that as necrotrophic pathogens are not reported to engage in specific interactions with host plants, all isolates of a particular necrotrophic pathogen species are equivalent. This opinion manifests itself in a lack of use of necrotrophic diversity in published studies, as well as a lack of reporting of identifying pathogen data, despite published evidence that necrotrophic pathogens show intraspecific variation affecting pathogenesis- or virulence-related traits [18][24]. We suggest that the limited use of pathogen diversity biases our understanding of plant–necrotroph interactions. The research community should enforce detailed reporting of identifying pathogen data for studies of plant–necrotroph interactions and encourage the use of multiple pathogen genotypes.

Lack of Diversity

The majority of studies investigating the molecular bases of plant–necrotroph interactions do not include pathogen variation. Based on a survey of published literature from the last 10 years, fewer than 12% of surveyed studies of plant defense against Botrytis cinerea, the most intensively researched plant necrotrophic pathogen as reflected by publication frequency, report experimental results for more than one pathogen isolate (see Text S1). The diversity of A. brassicicola represented in the current literature is much lower, as none of the surveyed studies reported data from multiple pathogen isolates and almost half of these studies used the same isolate, MUCL20297. While selection of a particular pathogen isolate as a model or laboratory standard may facilitate comparison among studies performed in different laboratories, data from single isolates are too often represented as informative for the whole pathogen species. If the reference isolate is atypical, misleading conclusions may be drawn regarding the biology of the plant–host interaction, and promising lines of research may be abandoned.

A Cautionary Example: Resveratrol

The controversial role of phytoalexin defense compounds in providing actual plant defense against pathogens illustrates the importance of including necrotroph variation in studies of plant defense. One phytoalexin compound implicated in plant defense is resveratrol, a stilbenoid phytoalexin produced by Vitis vinifera in response to pathogen attack [25],[26]. As the chemical precursors for resveratrol are produced by all plants, transgenic introduction of V. vinifera stilbene synthases into several crop plants provided the capacity for heterologous production of this antimicrobial compound [27]. Independent studies of transgenic tomato, barley, and tobacco evaluated resveratrol's efficacy against B. cinerea. Intriguingly, the capacity to produce resveratrol enhanced plant resistance to B. cinerea in barley and tobacco, but had no significant effect on tomato resistance to B. cinerea, despite plant accumulation of resveratrol at concentrations sufficient to inhibit B. cinerea growth [28].

While inhibition of B. cinerea growth by resveratrol might depend on the host in which it is encountered by the pathogen, the reported capacity of B. cinerea to degrade stilbenoid phytoalexins by the action of laccases suggests an alternative explanation [28],[29]. Eight surveyed B. cinerea isolates varied in their capacity to degrade resveratrol; this variation was linked to virulence on grape leaves [29]. The studies of resveratrol-producing tobacco and barley do not provide any information about the B. cinerea isolate(s) used, and the tomato study reports use of “a spore suspension of field isolates”, possibly representing a mixture of pathogen genotypes [30][32]. The observed lack of increased B. cinerea resistance in resveratrol-producing tomato plants might result from the presence of resveratrol-degrading B. cinerea isolates, while tests of transgenic tobacco and barley used isolates with reduced or no capacity to degrade resveratrol. Without documentation and archiving of B. cinerea isolates used, it is impossible to retroactively distinguish whether these conflicting results reflect pathogen isolate differences or differences in plant biochemistry and physiology.

Lack of Reporting

A lack of reported information about necrotrophic pathogen isolates is a less common, but more troubling, deficiency in the published literature. Approximately 15%–20% of surveyed publications reporting original research on plant defense against either B. cinerea or A. brassicicola did not provide any description of the pathogen isolate used. Minimally, an isolate name and explicit details of the isolate's source should be provided. In addition, references to source materials or isolation methods should include documentation of how the species identity was confirmed, as pathogens may be difficult to distinguish by morphology or collection host. Additional information, such as collection date, host, and geography, may add valuable context for other researchers, especially for species such as B. cinerea where cryptic speciation related to host use and geography have been proposed [33][36].

Steps Forward

Pathogen diversity presents serious challenges and opportunities for understanding pathogen interactions with host defenses. Conclusions drawn from studies employing single, or even multiple, isolates may not accurately represent the biology of the species as a whole. Variation in either the host or the pathogen can alter these relationships and this should be at least acknowledged in biological studies. Further, the lax acknowledgement of genotypic diversity within necrotrophic plant pathogens hinders comparison among studies through both a lack of overlap among experimental isolates used by different research groups and a lack of explicit description of the isolates used. Use of a standardized panel of pathogen isolates is impracticable given restrictions on the import and movement of plant pathogens, and might provide a false resolution to this issue, as the rate of genomic change in these pathogens, particularly in response to selection for laboratory growth, is unknown.

A promising strategy would embrace pathogen diversity to provide a more detailed picture of how plant and necrotrophic pathogen species interact, creating a valuable link between molecular- and population-level studies. This would require preliminary evaluation of diversity in a collection of isolates for a given study trait, followed by detailed characterization of a subset of isolates covering the identified range of trait variation. The paucity of studies employing this strategy likely reflects the effort required to obtain large pathogen collections and the increase in experimental resources required. Minimally, the scientific community and particularly scientific journals should require a detailed description of isolates, including isolate verification and proper referencing, as a prerequisite for publication. Cooperation among laboratories to independently confirm experimental findings should also be encouraged, as this will improve interpretation of single-isolate studies and minimize disagreements caused by pathogen variation.

Supporting Information

Attachment 1


Zdroje

1. GlazebrookJ

2005 Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43 205 227

2. OliverRP

IpchoSVS

2004 Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol Plant Pathol 5 347 352

3. van KanJAL

2006 Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11 247 253

4. WilliamsonB

TudzynskB

TudzynskiP

van KanJAL

2007 Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8 561 580

5. DickmanMB

ParkYK

OltersdorfT

LiW

ClementeT

2001 Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 98 6957 6962

6. GovrinEM

LevineA

2000 The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10 751 757

7. GovrinEM

RachmilevitchS

TiwariBS

SolomanM

LevineA

2006 An elicitor from Botrytis cinerea induces the hypersensitive response in Arabidopsis thaliana and other plants and promotes the gray mold disease. Phytopathology 96 299 307

8. KliebensteinDJ

RoweHC

2008 Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction. Plant Science 174 551 556

9. WangWM

DevotoA

TurnerJG

XiaoSY

2007 Expression of the membrane-associated resistance protein RPW8 enhances basal defense against biotrophic pathogens. Mol Plant-Microbe Interact 20 966 976

10. ThalerJS

OwenB

HigginsVJ

2004 The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135 530 538

11. DanglJL

JonesJDG

2001 Plant pathogens and integrated defence responses to infection. Nature 411 826 833

12. JonesJDG

DanglJL

2006 The plant immune system. Nature 444 323 329

13. KamounS

2007 Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10 358 365

14. SalvaudonL

GiraudT

ShykoffJA

2008 Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Curr Opin Plant Biol 11 135 143

15. StukenbrockEH

McDonaldBA

2009 Population Genetics of Fungal and Oomycete Effectors Involved in Gene-for-Gene Interactions. MolPlant-Microbe Interact 22 371 380

16. FriesenTL

FarisJD

SolomonPS

OliverRP

2008 Host-specific toxins: effectors of necrotrophic pathogenicity. Cellu Microbiol 10 1421 1428

17. LawrenceCB

MitchellTK

CravenKD

ChoY

CramerRA

2008 At death's door: Alternaria pathogenicity mechanisms. Plant Pathol J 24 101 111

18. DerckelJP

BaillieulF

ManteauS

AudranJC

HayeB

1999 Differential induction of grapevine defenses by two strains of Botrytis cinerea. Phytopathology 89 197 203

19. KliebensteinDJ

RoweHC

DenbyKJ

2005 Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant J 44 25 36

20. QuiddeT

OsbournAE

TudzynskiP

1998 Detoxification of alpha-tomatine by Botrytis cinerea. Physiol Mol Plant Pathol 52 151 165

21. SchoonbeekH

Del SorboG

De WaardMA

2001 The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Mol Plant-Microbe Interact 14 562 571

22. SellamA

Iacomi-VasilescuB

HudhommeP

SimoneauP

2007 In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathol 56 296 301

23. SiewersV

ViaudM

Jimenez-TejaD

ColladoIG

GronoverCS

2005 Functional analysis of the cytochrome P450 monooxygenase gene bcbot1 of Botrytis cinerea indicates that botrydial is a strain-specific virulence factor. Mol Plant-Microbe Interact 18 602 612

24. UngerC

KletaS

JandlG

von TiedemannA

2005 Suppression of the defence-related oxidative burst in bean leaf tissue and bean suspension cells by the necrotrophic pathogen Botrytis cinerea. J Phytopathol 153 15 26

25. JeandetP

BessisR

SbaghiM

MeunierP

1995 Production of the phytoalexin resveratrol by grapes as a response to Botrytis attack under natural conditions. J Phytopathol 143 135 139

26. KoppP

1998 Resveratrol, a phytoestrogen found in red wine. A possible explanation for the conundrum of the ‘French paradox’? Eur J Endocrinol 138 619 620

27. EssenbergM

2001 Prospects for strengthening plant defenses through phytoalexin engineering. Physiol Mol Plant Pathol 59 71 81

28. AdrianM

RajaeiH

JeandetP

VeneauJ

BessisR

1998 Resveratrol oxidation in Botrytis cinerea conidia. Phytopathology 88 472 476

29. SbaghiM

JeandetP

BessisR

LerouxP

1996 Degradation of stilbene-type phytoalexins in relation to the pathogenicity of Botrytis cinerea to grapevines. Plant Pathol 45 139 144

30. ThomzikJE

StenzelK

StockerR

SchreierPH

HainR

1997 Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans. Physiol Mol Plant Pathol 51 265 278

31. HainR

ReifHJ

KrauseE

LangebartelsR

KindlH

1993 Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361 153 156

32. LeckbandG

LörzH

1998 Transformation and expression of a stilbene synthase gene of Vitis vinifera L. in barley and wheat for increased fungal resistance. Theor Appl Genet 96 1004 1012

33. AlbertiniC

ThebaudG

FournierE

LerouxP

2002 Eburicol 14α-demethylase gene (CYP51) polymorphism and speciation in Botrytis cinerea. Mycol Res 106 1171 1178

34. CettulE

RekabD

LocciR

FirraoR

2008 Evolutionary analysis of endopolygalacturonase-encoding genes of Botrytis cinerea. Mol Plant Pathol 9 675 685

35. FournierE

GiraudT

AlbertiniC

BrygooY

2005 Partition of the Botrytis cinerea complex in France using multiple gene genealogies. Mycologia 97 1251 1267

36. GiraudT

FortiniD

LevisC

LamarqueC

LerouxP

1999 Two sibling species of the Botrytis cinerea complex, transposa and vacuma, are found in sympatry on numerous host plants. Phytopathology 89 967 973

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