ANRV283-PY44-21 ARI 13 June 2006 13:56

Climate Change Effects on
Plant Disease: Genomes
to Ecosystems
Annu. Rev. Phytopathol. 2006.44:489-509. Downloaded from arjournals.annualreviews.org

K. A. Garrett, S. P. Dendy, E. E. Frank,
M. N. Rouse, and S. E. Travers
Department of Plant Pathology, Kansas State University, Manhattan, Kansas 66506;
by 190.40.126.128 on 10/08/07. For personal use only.

email: kgarrett@ksu.edu; sdendy@ksu.edu; efrank@ksu.edu; mrouse@ksu.edu;
travers@ksu.edu

Annu. Rev. Phytopathol. Key Words
2006. 44:489–509
climate variability, disease ecology, ecological genomics,
First published online as a
Review in Advance on epidemiology, global warming
May 23, 2006
Abstract
The Annual Review of
Phytopathology is online at Research in the effects of climate change on plant disease contin-
phyto.annualreviews.org ues to be limited, but some striking progress has been made. At the
doi: 10.1146/ genomic level, advances in technologies for the high-throughput
annurev.phyto.44.070505.143420 analysis of gene expression have made it possible to begin discrim-
Copyright 
c 2006 by inating responses to different biotic and abiotic stressors and po-
Annual Reviews. All rights tential trade-offs in responses. At the scale of the individual plant,
reserved
enough experiments have been performed to begin synthesizing the
0066-4286/06/0908- effects of climate variables on infection rates, though pathosystem-
0489$20.00
specific characteristics make synthesis challenging. Models of plant
disease have now been developed to incorporate more sophisticated
climate predictions. At the population level, the adaptive potential
of plant and pathogen populations may prove to be one of the most
important predictors of the magnitude of climate change effects.
Ecosystem ecologists are now addressing the role of plant disease in
ecosystem processes and the challenge of scaling up from individual
infection probabilities to epidemics and broader impacts.

489

ANRV283-PY44-21 ARI 13 June 2006 13:56

INTRODUCTION sion in the development of genomics tools and
their application (reviewed in 56). And, with
Eight years ago, Coakley et al. (38) reviewed
the turn of the millennium, groups such as
IPCC: the implications of climate change for plant
Intergovernmental the UN have reevaluated progress toward so-
disease management in the Annual Review of
Panel on Climate cietal goals through the formulation of Mil-
Phytopathology series. They pointed out sev-
Change lennium Development Goals and the Millen-
eral challenges for evaluating the likely ef-
nium Ecosystem Assessment, while the U.S.
fects of climate change. Most experiments
National Research Council has formulated a
considering climate change effects include
list of Grand Challenges for the environmen-
only one or two of the changing climatic
tal sciences, which includes climate change as
factors, experiments tend to be performed
well as infectious disease (96).
under conditions very different from those
in the field, and experiments are generally
Annu. Rev. Phytopathol. 2006.44:489-509. Downloaded from arjournals.annualreviews.org

short-term. But there were already enough re- CLIMATE CHANGE
sults in hand to indicate that climate change
The Intergovernmental Panel on Climate
could “alter stages and rates of develop-
Change (IPCC), which was jointly established
ment of the pathogen, modify host resis-
by the World Meteorological Organization
tance, and result in changes in the physiol-
by 190.40.126.128 on 10/08/07. For personal use only.

(WMO) and the United Nations Environ-
ogy of host-pathogen interactions.” Coakley
ment Program (UNEP) in 1988, has respon-
et al. (38) concluded that the effects of climate
sibility for assessing information relevant to
change on plant disease management may
climate change and summarizing this infor-
be less important than changes in land-use
mation for policy makers and the public. It
patterns, transgenic technologies, and avail-
has published major assessment reports most
ability of chemical pesticides. Another gen-
recently in 1995 and 2001 (69). A new as-
eral conclusion was that the effects of climate
sessment is scheduled for publication in 2007,
change will tend to be different for different
and updated predictions are available in other
pathosystems in different locations, so that
publications (e.g., 142). Since the 1995 report,
generalization is a challenge. Here we con-
there have been a number of advances, includ-
sider multiple scales of host-pathogen inter-
ing improvements in the Atmosphere-Ocean
action (Figure 1) and review factors that con-
General Circulation Models (AOGCM) used
tribute to determining how and when climate
to predict climate change. Other improve-
change could have important effects on plant
ments include better regionalization tech-
disease.
niques, a better understanding of the physical
Since the review by Coakley et al. (38),
processes underlying the models, and better
what has changed? Consensus has contin-
availability of paleoclimate data for evaluating
ued building among climatologists that global
long-term temperature change and historic
warming is occurring and linked to human
climate data for evaluating preindustrial
activity (62). Scientists have also continued
atmospheric concentrations of greenhouse
to evaluate the effects of climate change on
gases.
disease risk across systems (63). More stud-
Climate change predictions are based on
ies of the “fingerprint” of global warming
scenarios that describe greenhouse gas emis-
have appeared as interest in the effect grows
sions from potential resource use patterns,
and as trends become more distinct (66, 85,
technological innovations, and demographics.
108, 120, 140). More climate change simula-
The results from modeling experiments based
tion experiments have been put in place (28).
on these emissions scenarios give a range of
Ecologists working outside agricultural sys-
predictions, depending on the assumptions
tems have turned more attention to the ecol-
quantified by each scenario. Sources of un-
ogy of disease (58). There has been an explo-
certainty in predictions include inability to

490 Garrett et al.

Rev. 145). cluded in 2001 that there was no compelling plete understanding of climate processes. Downloaded from arjournals. (47.org Genome processes Physiology dynamics Downregulation of Stomatal Higher fecundity of Increased Needle blight moving Soybean rust HR and other closure and Colletotrichum CO2 increased north as precipitation pathogen climate change effects Examples of potential genes in tallgrass leaf growth gloeosporioides fungal pathogen patterns change (148) immigration prairie grass in inhibition under increased load in prairie potentially via by 190. Likewise. For personal use only.org • Climate Change Effects on Plant Disease 491 . extratropical storms have changed. more frequent extreme high temper. Arrows indicate propagation of effects from smaller to larger processes. Pathogen role in processes that Proteomic cific diversity. (32) Heating of in Europe due to In preparation) montane prairie temperature had mixed change (16) Peanut gene Plant effects (121) expression structural response to changes in drought and response to Aspergillus (81) CO2 (117) Gene Multifactor Better models of Good models of Long-term large-.annualreviews. In evidence that characteristics of tropical and addition to the predicted increases in tem. For tempera. e. increased Additional predictive variability comes intensity of precipitation events is predicted in into play for modeling of regional climates some regions.g. Integrated expression in studies of adaptation rates interspecific scale records of multi- plants and climate interactions like pathogen and host disciplinary pathogens in change competition and distributions international Research needs response to Better data and facilitation networks for effects models related to climatic data collection factors dispersal.126.annualreviews. more re- perature for much of the world. but feedbacks will also link across scales. peratures are predicted. Phytopathol. 2006. ANRV283-PY44-21 ARI 13 June 2006 13:56 Environment Microclimate Local climate Regional limate Microclimate Global climate Local climate Region l cli te Subconti ental Pathogen Genome Cellular Physiology Intrapopulation processes dynamics Host-pathogen Host-pathogen Community Regional interactions interactions and ecosystem ecosystem Biosphere dynamics dynamics Host plant Cellular Intrapopulation Annu.44:489-509. changes in cent analyses have concluded that there have extremes are also predicted. fully predict human resource use and incom. (69). movement of pathogens (26).128 on 10/08/07. and of propagules and responses heritability of traits vectors Figure 1 Examples of potential climate change effects and research needs across biological scales. All the forms of uncertainty about global www.40. cinnamomi hurricane precipitation drought. Although the IPCC (69) con. predicted expansion change (Travers et al. response to during CO2 (29) (91) P. current Models of regional and synthesis levels of intraspe. which could influence the global atures and less frequent extreme low tem. been changes in storm patterns in recent years ture. long-term incorporate disease and/or strength of selection ecological metabolomic under different processes Data and models studies of host climate change regarding dispersal and pathogen scenarios.

These changes will certainly af- leaf surface wetness and leaf surface wet. diameter have been observed under elevated cipitation are predicted to increase on aver. Asia. abiotic stress the Philippines was estimated to decline 10% such as heat and drought may contribute to for each 1◦ C increase in the minimum tem- plant susceptibility to pathogens or it may in. the structure of leaf surfaces.org In northern mid-latitudes.40. damage from ozone are also reported un- precipitation is predicted to increase in both der elevated CO2 (139).128 on 10/08/07. 2006. and so make infection by fo. perature during the dry season (110). Phytopathol. ANRV283-PY44-21 ARI 13 June 2006 13:56 processes are still a factor. and stems and branches with greater eas. warming. with additional Elevated CO2 levels tend to result in uncertainty due to lack of data from some changed plant structure. but increasing temperature. leaf folding. Changes physiological responses including changes in in plant architecture may affect microclimate RNA metabolism and protein synthesis. pathogens benefit from denser plant growth Annu. en- and thus risks of infection (27). As a striking example of the how abiotic stress factors interact to affect potential effect on the yield of crop plants in plants will be key to understanding climate response to elevated temperature. Decreased snow cover and land-ice ex. CO2 (117). cate the effects of elevated CO2 . warming Plant Responses in General: At the may relieve plant stress. particularly in remote re. Downloaded from arjournals. difficult to predict. fect susceptibility to pathogens. higher total leaf area per produce rapid climatic variation over small ar. though the ness duration. precipitation is predicted to (27).44:489-509. tered precipitation. Supplementary material on in a California annual grassland. increased leaf thickness. elevated CO2 ap- peared to suppress the positive effects of the other factors (131). plant. and reduced precipitation are region specific. At multiple scales. regions. Rev. plant vidual plants and plant communities may oc. responses may be similar to those induced by cur in the absence of pathogens. dicted for southern Africa. duce general defense pathways which increase Elevated ozone concentrations can change resistance. For personal use only. While water vapor. in multifactor treatments. and and the resulting more humid microclimate tropical Africa. . When The direct effects of climate change on indi. isoenzymes. But interactions with summer. In general. and Australia. with symptoms including wilt- bring about changes in plants that will affect ing. leaf burn. and their interactions with pathogens. But. Central America. In general. other changing climatic variables may compli- by 190. and tions. wide range of changes may make interactions liar pathogens more likely (65). Since many foliar summer and winter in high-latitude regions. Meteorological stations in some plant organs may increase in size: Increased regions are sparse. higher gions with complex topography that may numbers of leaves. elevated CO2 each increased net primary pro- tent are expected to follow from the trend in ductivity when applied as single factors. whereas during hotter Level of the Individual parts of the year it may increase stress. leaf area. altering the 492 Garrett et al. and pre. Antarctica. but may also water stress. and plant growth hor- increased plant density will tend to increase mones (34). addition of nitrogen. in- age.126. high-temperature stress is exacerbated. evaporation. In southern and eastern plant architecture to increase infection rates. of course. and abscission. Decreases in winter rainfall are pre. PLANT RESPONSES TO The effects of elevated temperature on CLIMATE CHANGE plants will tend to vary greatly throughout the year. For example. During colder parts of the year. precipitation is predicted to increase in all else being equal. al- IPCC websites supplies finer scale predic. there is the potential for these changes in increase in winter. zymes. rice yield in change effects on plants (92).annualreviews. Enhanced photosynthesis. predictions about increased or decreased creased water use efficiency.

Temperature may have important reper- J. ANRV283-PY44-21 ARI 13 June 2006 13:56 physical topography as well as the chemical patterns in tallgrass prairie. For example. which acts vances in microarray technologies to the point to protect plant cells from dehydration). pyrroline-5-carboxylate synthetase (with a they also are important as an illustration of ad- role in biosynthesis of proline. Travers et al. al. the fact that foliar pathogens will tend to have soluble proteins. Up-regulated genes included Host Resistance those involved in cellular metabolism. found that.H. suggesting a defensive cost associ- stress.126. (34). et al. all influencing the ability of pogon gerardii. resistance is ap- pression responses to environmental changes parently reduced under drought conditions in natural plant populations. as well hydrophilic. Down-regulated genes in. such as stomatal closure and the inhibi. plant resistance to infection is complicated by tional regulation.E. between precipitation events decreased tran- Gene expression studies of plant responses scription of genes related to photosynthesis Annu. Way et al. gerardii to which rainout exclu- to enhance attacks on plants by necrotrophic sion shelters were applied to impose the differ- fungi. and where highly variable natural field systems can fatty acid alpha-oxidase (involved in repair. gene pathogens to attach to leaf surfaces and in. root-rot fungi. expression was studied in the natural popu- fect (74). Increased intervals (123). Pennypacker et al. Bai. M. This experiment focused on the tall- such as leaf wettability and the ability of leaves grass prairie dominant plant species Andro- to retain solutes. But plant pathologists have studied the well as cellulases. Rev. sults are of interest in and of themselves for nase (associated with osmoregulation). Phytopathol. Smith. For some host- It is now possible to measure gene ex. under both short. as (65). heat.. 2006. J. including the struc. and bark beetles ent precipitation patterns.E. Bray (24) summarized expression responses to drought stress across gene classes. (144) regulated under the treatment with increased by 190. though it may generally be chal- simulated changes in predicted precipitation lenging to discriminate between temperature www.44:489-509. toms under drought stress. changes in leaf architec. Leach.and long-term intervals. where one pre- composition of surfaces. Verticillium albo-atrum exhibited fewer symp- ture. signal transduction. was significantly down- ple of expression responses. Hulbert. (111) found that alfalfa plants inoculated with tion of leaf growth. Whereas these re- cluded those coding for aldehyde dehydroge. ability to toxic ions). Downloaded from arjournals. ated with climate change. delta understanding the tallgrass prairie ecosystem. diction is for increased intervals between rain ture of epicuticular wax (74). pathogen systems.annualreviews. lower infection success under dry conditions cluded those involved in cell wall synthesis.D.annualreviews. Travers. Ozone exposure has been proposed lation of A. These changes in events even if total precipitation is not re- leaf structure may alter leaf surface properties duced. plant. 34). tive reaction.org • Climate Change Effects on Plant Disease 493 . cussions on the effectiveness of resistance manuscript submitted) studied the effects of genes. and carbon fixation and increased transcrip- lowing a more mechanistic understanding of tion of a variety of heat shock proteins and responses and comparison between responses kinases. and transcrip. As an exam. For personal use only. interactions between pathogen and drought These results can be linked to well-known stress at the scale of pathogen populations for processes occurring at a larger scale within a some time. however. cellular Detecting the effects of drought stress on transport. HIR1. Using maize microarrays. S. and germin-like proteins.128 on 10/08/07. and change in root:shoot ratio (32. to climate change simulations.org to drought stress have expanded rapidly.40. A gene associated with a hypersensi- to drought and other stressors. For example. be sampled and statistically significant differ- ing stress-induced damage in membranes and ences in gene expression observed in response regulating fluidity of membrane and perme. (S. genes significantly up-regulated in.

of exposure to these temperatures. (81) examined tered climate. which confers resistance to Xan. For example. Browder & drought. Level of the Population ature (79a). pathogen pressure due to climate change (or Other systems such as sunflower-broomrape other factors). there is the potential to determine the molecular Plant Responses in General: At the basis of the differences in response to temper.org sion once an adequate water supply is restored. In this system. perhaps es- CO2. If cli- by 190. M. rate of migration of plants from one region to port that high levels of CO2 may prevent in. sponses to climate change (41. Downloaded from arjournals. fragment plant populations. so that popula- if it is found in many pathosystems. responses to climate change has focused on tential to influence the effectiveness of host plant species range shifts (10.126. Even if there is genetic vari- into studies of plant responses will help ation present in a population for traits that to unravel the effects of multiple stressors could support adaptation to a location with al- (92). For personal use only. But the letotrichum gloeosporioides increased on both re. may be tions of plant species will be subject to rapid one of the most important effects of elevated changes in their genetic structure. T. The tions will tend not to have sufficient time to potential for accelerated pathogen evolution. The detected variation in gene expression Puccinia recondita system. W. blight resistance genes are less effective with increasing temperature. ANRV283-PY44-21 ARI 13 June 2006 13:56 effects on host resistance genes versus ef. Cruz & J. and Aspergillus/drought treatments. C. correlations between traits that gene expression in a drought-tolerant and do not support selection for the new climate Aspergillus-resistant peanut line. Webb. the slow resistance (114. pecially for plant species with long genera- Integration of gene expression analyses tion times (72). Thrall & Burdon (137) have found important ity. .128 on 10/08/07. 115). virulence among natural populations. A. another. In rice.40. (46) have shown similar temperature sensitiv. ent populations of the same species may differ 494 Garrett et al. may make adap- On the other hand. Ona.44:489-509. Newton More data about the population genetics & Young (101) have suggested that resistance of defense genes in natural plant populations mechanisms in barley may be disrupted fol. the shift in selection gene (Xa7). ment can be studied at the genomic level to ular pairings tended to produce low infection increase understanding of processes at larger rates at specific temperatures and time periods scales. pathogen. differ- causes significant disease under drought con. fects on pathogen virulence. As Aspergillus may limit adaptive evolution (50). tial for adaptation under potential changes in Annu. and environ- ently to different temperature ranges. Partic. current state of research in plant adaptation sistant and susceptible varieties of Stylosanthes to climate change suggests that plant popula- scabra in a controlled environment (29).annualreviews. ditions. tion between host. Webb et al. tation the more important factor in plant re- fecundity of the anthracanose pathogen Col. variation in both host resistance and pathogen ˜ K. Although much research on plant community Elevated CO2 and ozone also have the po. mate change increases or decreases environ- tion) found that one bacterial blight resistance mental conduciveness. Rev. Garrett. 2006. M. 88). (106) re. E. Phytopathol. pressure on the host populations could result thomonas oryzae pv. oryzae. for the wheat. Also. adapt to altered climates (50). J. Bai. manuscript in prepara. at twice ambient CO2 . Pangga et al. Vera I. Leach. will be important for determining the poten- lowing drought stress as cells undergo expan. Mew. Luo et al. host-pathogen gene among treatments indicates that the interac- pairs related to resistance responded differ. Eversmeyer (25) reported that. In an unusually extensive study. is more effective in shifts in the diversity of resistance genes at high temperatures whereas other bacterial present. peanuts were examined under control. 42). (K. combined with land use patterns that duced resistance as plants grow more rapidly.

Bale et al. They concluded that if they must be adapted to a more variable temperature was the dominant climate factor environment? in terms of direct effects through effects on www. 2006. 132.40. movement. another problem is whether in situ (119). the introduction of multiple Annu. along with evaluation of phenotypic plasticity increases the ability of the pathogen to over- in response to predicted changes in climate.org • Climate Change Effects on Plant Disease 495 . as species may lose climatic requirements for overwintering or their ability to recover from other perturba- oversummering of the pathogen or vector. 122. Where seed from vari- survival. scribed in other sections of this chapter? Will In a review of the effect of climate change less emphasis on local adaptation be possible. and 15◦ –35◦ C for stem rust settings. whether ble to produce varieties that are as productive insect-vectored or not. rather the Temperature requirements for infection dif- concern is whether farmers will be able to fer among pathogen species.128 on 10/08/07. As a result of CHANGE climate change. 136). More studies on trait vari- thora infestans. 10◦ –30◦ C 54. and reproduction. 98– ulations of wild crop relatives will be out- 100) and other effects of change on insects competed by other species better adapted (112) may have important effects on pathogen to the new climate.annualreviews. higher winter temperatures of climatic extremes within a background of cli- −6◦ C versus −10◦ C increase survivorship of mate changes (60. greatly tially valuable populations may be generated. For pathogens subject to an Allee ef- In agricultural systems.44:489-509. Downloaded from arjournals. processes of adap- example.126. For personal use only. introduction of the glassy-winged tation will change the selection pressures on sharp shooter has led to increased patterns these populations and. ANRV283-PY44-21 ARI 13 June 2006 13:56 in both their genetic structure and the extent PATHOGEN AND VECTOR to which climate change will push the species RESPONSES TO CLIMATE to its physiological limits (49). and For example. 134). through mechanisms de- facilitation may be shifted (e.annualreviews. while new and poten- of infection of grape plants in winter. allowing sexual reproduction. (11) make many as conditions change rapidly? Will it be possi- points relevant to plant pathogens. 31. 73. the abundance of particular The range of many pathogens is limited by species may change rapidly.org ation related to climate change are needed. For cases where timing of infection current crop breeding programs. winter. Novel plant com- overwintering rust fungi (Puccinia graminis) munities may result (141). on insect herbivory. 72. Rev. through fragmented landscapes. Interactions be- much genetic diversity may be lost in subse- tween pathogens may also shift with climate quent selection to the changing climate. identify and acquire crop genotypes that are wheat rust fungi differ in their require- adapted to their changing climates (8. production at low population levels. conservation of traditional land races can be Similarly. 93–95. tions such as diseases. For able land races is saved.g. 2). comparable by different pathogen species is important for concerns would include the following: Can determining the outcome of interactions be- climate change result in shorter useful lives tween pathogens. mating types. the form of competition or for resistance genes. 45. release by 190. In traditional agricultural for leaf rust. insect herbivores. In the case of Phytoph- pathogens (107). In change. For example. ments from 2◦ –15◦ C for stripe rust.. with the increased and increase subsequent disease on Festuca potential for new patterns of host-sharing by and Lolium (113). or destabilizing density-dependent re- plant population structure are different. the introduction of new vec- meaningfully maintained when local condi- tor species and changes in vector overwinter- tions change too rapidly and whether pop- ing and oversummering (52. Phytopathol. questions about fect. altering infection rates (3). There is no direct concern about whether from overwintering restrictions may have plant populations can successfully migrate a much stronger effect than expected (55).

48). in interactions among microbial species (e..org movement with changing climate. Wheat stripe rust is spreading in South Africa in association with changes Climate Change Effects on in rainfall patterns and native grass infec. populations that precipitation effects had not been stud. Aggressiveness. 23). ence disease (6. Bergot et al. Recent technological advances such as to increased temperatures that would allow metagenomic analyses (118) will increase our for overwintering of this oomycete in new ar. Pathogen range shifts that appear to be and other environments. 103) and providing new oppor. associated with climate change are now be- ing reported. plant growth.44:489-509. to make use of extended seasons in temperate Other factors such as acid rain may also influ. which in turn facilitated plant tems (146a). it is difficult to predict the effect of cli- ment may act synergistically with temperature mate change on the disease-suppressive qual- changes (4. understanding of microbial dynamics in soil eas. might need to undergo extensive adaptation ied sufficiently to draw a general conclusion. Increased pathogen ranges production per time interval. . But if some parts of pathogen life cy- evidence of direct effects of CO2 or UVB and cles are photoperiod sensitive.126. Soil nitrate concen- larger scales. with the potential to plant growth. But new phasized that elevated CO2 . observed (67). 2006. Because of the great variation tunities for pathogen hybridization (22. though plant commu- of pathogen and vector distributions. Such approaches can be applied N acquisition. Increased transportation and human move. 40). which facilitated plant uptake revolutionize our understanding of pathogen of N and dominance of fungi in the microbial communities and their movement. 7. Researchers have em- Annu. These studies suggest that micro- In many cases. so it is not surprising Soil microbial communities are likely to shift that few studies have addressed changes in with climate change. temperature increases are bial communities may generally experience predicted to lead to the geographic expansion decreased available N. Virulence. nity composition and soil type will generally ing pathogens into contact with more poten. ANRV283-PY44-21 ARI 13 June 2006 13:56 overwintering and the potentially important sure to reservoir host species that increase combination of photoperiod and temperature. In a microcosm by 190. Downloaded from arjournals. areas.40. characteristics such as heritability of traits 496 Garrett et al. For personal use only. diagnostic arrays trations are reduced under elevated CO2 in are being developed to identify large num. along with other may also have the effect of including expo. Phytopathol. have large effects on the type of responses tial hosts (10. CO2 increased plant species in agricultural and natural sys. the number of generations of pathogen re- cipitation (148). 12). needle blight Fecundity of Pathogens caused by Dothistroma septosporum is moving Pathogen evolution rates are determined by north with increasing temperatures and pre. Similarly. prevalence of disease in other adjacent taxa They further concluded that there was little (116). (16) agricultural systems where farmers are try- predicted the geographic range expansion of ing actively to increase disease suppressive- Phytophthora cinnamomi in Europe in response ness. Rev. or tion (19). grassland microcosms (13). In North America. In one of the most detailed ities of soils.annualreviews. increasing temper- to monitor changes in pathogen populations ature by 2◦ C in a tallgrass prairie increased over time and space. Microbial Interactions neous environment. (64). bring. both in natural systems and in analyses of a plant pathogen. temperature and diagnostic techniques will make it easier to nitrogen deposition are important factors in study large numbers of pathogen species over driving soil communities. bers of virus species simultaneously across experiment by Hu et al. Pathogen movement is difficult to study at large scales even in a relatively homoge. For example. community.128 on 10/08/07.g.

Decreases in precipitation.40. longevity and photosynthetic rate. ple. von Tiedemann & Firsching (139) found by 190. as examples. But most pathogens will have the ad. For rust fungi. derstood. Rev. for exam. this interac- fects of CO2 on plant disease.44:489-509. that benefits from elevated CO2 counterbal- vor overwintering of sexual propagules (113). like prairie. For 15 nario. grassland ecosystems could thus be increased ity to move readily through wind dispersal. challenging. led to increased rust incidence in their study. bility. For exam- populations reproduce sexually or asexually. (78) suggest may not be straightforward to study and pre- that particular strains of cholera are selected dict (123). Longer sea. perhaps due to increased leaf change. 9 exhibited an increase in disease severity. of elevated CO2 on plants with the effects on summering rates will also contribute. in some cases. so that disease will allow more time for pathogen evolu. may potentially be unable to migrate or elevated CO2 increased the pathogen load adapt as rapidly as environmental conditions of C3 grasses. including wetta- duced sensitivity to fluctuations. and the root rot pathogen Monospo. Downloaded from arjournals. 2006.annualreviews. be considered a phenotypic trait subject to (74) suggested that the effects of ozone on evolution and pathogens may evolve to re. in many cases. This suggests that predicting ef- temperature over a range of temperatures fects for unstudied pathosystems will be quite (135).org • Climate Change Effects on Plant Disease 497 . Plant pathologists have studied the rela- Gene Expression and Plant tionship between precipitation and disease for Physiology decades. (89. they found an increase in disease sever. they reported that production for many pathogens. caused by pathogens that infect through stom- tion. von Tiedemann & Firsching (139) also observed that rust-infected plants exhibited HOST-PATHOGEN symptoms of ozone damage several weeks ear- INTERACTION RESPONSES lier and with higher severity than uninfected TO CLIMATE CHANGE plants. 91) found that plants. ANRV283-PY44-21 ARI 13 June 2006 13:56 related to fitness under the new climate sce. such as Phyllosticta minima.126. Karnosky et al. or increased intervals between precipitation www. They sug- vantage over plants because of their shorter gested that one result of climate change for generation times and. Temperature governs the rate of re. tion. Climate variability itself may be an important The effects of elevated ozone on disease form of selection: Koelle et al. necrotrophic fungi studied. so increased overwintering and over. and a decrease for the other four.128 on 10/08/07. predicting climate change effects. ele- under more variable environments. pathogen load. Climate disease will make predictions of plant pro- change may also influence whether pathogen ductivity even more challenging. disease severity. anced negative effects from ozone but did not thus increasing the evolutionary potential of a compensate for the effects of fungal infec- population. In a study of plant disease in tallgrass Under climate change. ity for six of ten biotrophic fungi studied.org rapid when large pathogen populations are duced (86). Some mechanisms of effects of rascus cannonballus reproduces more quickly elevated CO2 on plants are fairly well un- at higher temperatures (143).annualreviews. Even without the added impetus of Charkraborty et al. leaf surface characteristics. such as reduced stomatal opening sons that result from higher temperatures and changes in leaf chemistry. Phytopathol. ple. (30) have reviewed the ef. pathogens. and 2 remained un- Puccinia substriata increases with increasing changed. altered temperatures may fa. For biotrophic tion is of primary importance for predicting fungi. the abil. For personal use only. Mitchell et al. spore germination of the rust fungus 4 exhibited a decrease. But combining the direct effects present. such that vated ozone has been found to increase (74) sensitivity to environmental fluctuations can and decrease (139) infection. may be re- Annu. Pathogen evolution may also be more ata.

Disease management strategies may require ological Station (121). Such risk models are of great economic importance when they Population Biology bear on what trade restrictions may be ap- Plant exposure to pathogens may increase un. have been predicted for a greater range” may be important. biocontrol agent popu- toric British wheat samples was closely cor. many adjustment under climate change. atures and moisture availability may also al- olina (84) and Septoria musiva causing canker ter disease severity. of climatic conditions and requirements need Both the “absolute range” and the “seasonal to be supplemented by information about 498 Garrett et al. newer work has also addressed temperature effects in a natural Plant Disease Management montane meadow in Rocky Mountain Bi. Strategies pathogens and herbivores were more abun. cent decades when it is actually only regain. Downloaded from arjournals. and may not recover (15). ties could result in rapid pathogen evolution While effects of temperature on disease (107). consistently available. centration of carbohydrates in host tissues as a Depending on the life history of the pathogen. leaf rust epidemics in the Great Plains are very Drought stress and disease stress may have different from year to year as a function of additive effects on plants. epidemiology also have a long history of study in agricultural systems. agent populations to environmental variation served specimens may reveal surprising cor. conducive conditions and the duration of con- fects on their hosts under drought conditions. . For many invasive pathogens. If environmental increased infection rates under drought or be. Changes in the timing of conducive temper- Other pathogens. ANRV283-PY44-21 ARI 13 June 2006 13:56 events. this may lead Annu. and humidity (133).128 on 10/08/07. Rev. Tilletia indica. both the likelihood of in poplar (83).annualreviews. The propriate temperature and moisture are not ratio of Stagnospora and Septoria species in his. Beet yellows ter or was reintroduced from further south. For personal use only. climatic variables such as temperature. 147). In this study. 2006. such as Macrophomina phase. phaseolina that can survive in ranges and exposure to new plant communi- by 190. for example. may cause more deleterious ef. not only to more disease in the short run. as observed for in. result of drought stress may benefit pathogens new interactions brought about by expanding such as M. (84) suggest that the con.40.44:489-509.org cause of increased impacts per infection event. conditions are more conducive. plied against regions where a pathogen such as der predicted climate change scenarios be. Phytopathol. wheat geographic area than are increases (69). causal agent of Karnal bunt. and Maize dwarf mosaic virus (102). virus (36). ducive conditions may increase. extremely dry soils. with nonad- though it is unclear whether this is because of ditive effects on disease risk. such as delaying planting to avoid a pathogen dant on plant populations with the longer may become less reliable. field has been the vulnerability of biocontrol New approaches to the study of pre. ducive conditions recur (57. jor problems with applications of biological but some were more abundant in the ambient control for plant disease management in the cooler conditions. models ranges for overwintering or oversummering. whether the pathogen was able to overwin- fection by Xyllela fastidiosa (87). This is also an illustration of how one as rapidly as pathogen populations when con- pathogen might appear to “emerge” in re. Models of the risk of movement of invasive ing its historical advantage from the previous pathogens to a new area are typically based on century. lations may reach densities that are too small related with the levels of environmental SO2 to have important effects.126. rain- fall. And one of the ma- growing season produced by artificial heating. is cause of longer growing seasons and expanded present. but Mayek-Perez et al. also more potential for pathogen evolution. If ap- relations with environmental variables. and environmental extremes (59. 61).

proaches that have been used for modeling Johnson (70) defined durable resistance as the effect of climate change on disease. www. Cli- resistance “that remains effective during its mate matching is applied by quantifying the prolonged and widespread use in an environ- climatic features of locations so that the suc- ment favorable to the disease. it to result in reduced durability of resistance. teff. model inputs have a high degree climate variability and uncertainty and less of uncertainty (75. Garrett pirical models. Downloaded from arjournals. Em- Annu. will tend to add extra Scherm (126. Phytopathol. (38) discussed several ap- and other human networks (10). sweet potato. Tem- such as frequent sexual reproduction (85a). can be used pathogen population to host populations with to predict the success of organisms across the a resistance gene is more likely and more im- range of conditions studied (18).” If resistance cess of an organism in a reference climate can is “inherently” durable. decision making by subsistence farmers in (38). But “realized durability” will vary de- the organism has not yet been introduced or pending on the extent to which the condi- where the climate is expected to change to tions defined by Johnson (70) can be avoided become similar to the reference climate. El Nino˜ patterns was found useful for general At the time of the review by Coakley et al.44:489-509. 128) make it crops include plantain. L.126. Because that pathogen characteristics that will tend climate change occurs slowly and variably. For example. the poten- changing disease-management needs will be tial for adaptation by plants and pathogens particularly important for such crops.org through deployment decisions (K. climate change through the argument that One conclusion about the effects of temporary effects of a year with unusual cli- climate change for disease management is matic features are likely to represent the ef- that changes. “orphan crops” (97) of particular linear relationships (21) and thresholds in the regional importance that have received less relationship between climatic variables and research attention than dominant temperate epidemiological responses (104. such as regression models with & R.org • Climate Change Effects on Plant Disease 499 . Third. ANRV283-PY44-21 ARI 13 June 2006 13:56 the availability of susceptible hosts and the Models for Disease Prediction likelihood of transport of pathogens by trade Coakley et al. poral variability in climate can be used to will also tend to facilitate adapation to a new draw inference about the potential effects of climate. Information about predictive understanding. variability in climate. is another complicating factor that is often incorporating climatic predictions based on ignored in models. For surprisingly difficult to acquire.128 on 10/08/07. there may tend to be both greater ease. In tropical uing problems with the application of models regions where food security is a particular for predicting climate change effects on dis- concern. difficult to collect sufficient data for a clear millets. non- example. data on investment in technologies supporting pro- the geographic distribution of disease are still duction of regionally important crops. 2006. portant if pathogen overwintering increases olation a possibility when the mechanisms of along with the number of pathogen gener- relationship are sufficiently understood. is difficult to study its effects directly. For personal use only. Bowden. manuscript in preparation).annualreviews. with extrap- by 190. cassava. The frequency with which ulation models are based on theoretical re- environments favorable for infection occur lationships and can be used to predict out- will also be an important factor. especially if they lead to greater fects of longer-term changes.annualreviews. In fact. It is notable comes under a range of scenarios.40. Sim- ations possible. Rev. climatic variables as predictors and epidemic Prolonged and widespread exposure of the parameters as response variables. First. no studies had been published using Zimbabwe (109). More recently. and quinoa. A. 125). 127) has identified three contin- uncertainty to decision making. Second. then climate change be used to predict the success of that organism may have no influence on its continued effi- in other locations with similar climates where cacy.

Asynchrony between pathogen. (e) rate of pathogen effects on hosts in relation ward over 100 years. if climate change produces major shifts caution in tallying such a prediction as a pos.128 on 10/08/07. sessment such as the Global Change and Ter- corporating insect and pathogens as “biotic restrial Ecosystems Core Project of the Inter- disturbance agents” (76) in models of vege. to rate of response/recovery by hosts or indi- perature of phloem in infected trees to evalu. possible that. Bergot et al. Many of these factors have ing or flowering (53). Of course. field (146). Ultimately. 68. and/or reproduction. and.org cinnamomi of up to a few hundred km east. Since then. potential adap. ing ecosystems. mote sensing of plant populations. pathogen effect on host survival. Newman (99) change. 2006.40. in which agricultural species are present in a itive potential outcome from climate change. (16) have used a GCM tion of individuals/biomass infected at a site. physiology. region. & Likens (51) have developed a framework for evaluating likely ecosystem effects for a pathogen and. It is (43). national Geosphere-Biosphere Programme tation change in response to climate. ically studied (14. viduals replacing hosts. been addressed in other sections of this review. as in most models. (c) propor- 105). ments. (b) life stages up from small-scale predictions (5. in models of climate ef. at this portance. 130) and for scaling behavior. . even in the extreme event that a tems such as Fusarium head blight for which plant species should go extinct due to greater there is a specific window of time during pathogen effects resulting from climate which flowers can be infected. 129. predictions may vary with re. Phytopathol. portant factors (39). Annu. fect. but suggests hand. this may result in important changes since many “desirable” insects may experience in nutrient loss from agriculture to surround- a similar decline. by extension. most studies had been based changes in land use patterns will also be im- on fixed changes in temperature or precipi. there are still challenges to identifying Ecosystem Level Effects particular plant species and to distinguishing The implications of plant disease at the between different types of plant stress in the ecosystem level have rarely been addressed. 33. the topic has been reviewed and 500 Garrett et al. Chuine et al.126. For personal use only. vector. Although remote sensing technologies have advanced rapidly. by modeling the tem. but the sixth is of particular interest for scal- and host may be an effect of climate change ing up predictions to the ecosystem level. ( f ) functional simi- ate overwintering probabilities. plant species that replace it could has predicted that cereal aphids will decline maintain ecosystem function. larity of infected individuals versus replace- (35) have argued for the inclusion of phenol. 79. Instead. Eviner will provide context for evaluation (128a). Rev. the study of such gion.44:489-509. Downloaded from arjournals. such as the time of bud and leaf open. the potential CONCLUSIONS ecosystem and “meta-ecosystem” (80) impacts Since climate change effects are challeng- of a pathogen when its epidemiology shifts ing to study but of potentially great im- with a shifting climate. the number of interactions and even sophisticated General Circulation Models types of interactions rapidly increases. But it is relevant to con- tation. Global networking for impact as- Malmstrom & Raffa (82) have addressed in. This could be important for pathosys. ANRV283-PY44-21 ARI 13 June 2006 13:56 climate variables generated by the more scale.annualreviews. modelers have developed sider Eviner & Likens’ factors for predicting approaches for scaling from the coarse GCM ecosystem effects and how pathogen charac- predictions down to the smaller scales at terization might shift with climate change: (a) which plant disease epidemics are more typ. and (GCM). and ( g ) frequency and duration of by 190. On the other significantly in southern Britain. pathogen impact. ogy. to predict a range expansion of Phytophthora (d ) spatial extent and distribution of infection. large-scale processes will be facilitated by re- tation by cereal aphids is not evaluated. of a host vulnerable to a pathogen.

cies in tropical areas will face related chal- ther decreasing or increasing the encounter lenges to maintenance of agricultural pro- rate between pathogens and host by chang.org populations and pathogen populations? Are itive effects of climate change on encounter invasive plant species better able to adapt to rates. once pathogens themselves. ANRV283-PY44-21 ARI 13 June 2006 13:56 recommendations put forward almost as fre. 138)? ultimately be modified by the evolutionary Closer links between empirical and model. What pathogen characteristics. affect rates of adaptation in both host an increase in disease will be those with pos- Annu. If agricultural land use decreases in dressed (37). counter rates. new vectors shifts in many climatic variables and perhaps that may alter epidemic dynamics. Widespread changes as modules for inclusion in larger modeling in land-use patterns will alter the potential systems. such as life in disease impact. both the host and its pathogens (17).126. If bor. Climate 44). Downloaded from arjournals. and new also about the potential for adaptation. tion.40. The ing their evolutionary options through bot.annualreviews. For personal use only.128 on 10/08/07. species. Species at highest risk for span. as shifts in the availability of agricultural la- ticular genes are better understood (20). or virulence. temperate areas and expands in the trop- The impact of climate change on disease ics. potential of host and pathogen. Social changes. advances in technologies for the high-throughput analysis of gene expression have made it possible to begin discriminating host. while the development of land use poli- change could first affect disease directly by ei. 2006. environmental conduciveness to infec- climate change and move to new areas rapidly. in terms of new hosts that may tic predictions about responses to complex boost pathogen inoculum levels. potential problems in calibrating ex. tlenecks (1. policies in temperate areas may support for a given plant species will depend on the restoration of natural areas or they may sup- nature of the effects climate change has on port expansion of suburban development (9. should be positively correlated with increases quently as climate change effects have been in virulence and aggressiveness of pathogens. affect the rate of adap. ing studies could support more rapid progress Finally. ductivity and plant biodiversity in a changing ing ranges of the two species. We have discussed the in plant gene expression in response to dif. SUMMARY POINTS 1. aggressiveness. At the genomic level. which in turn are potentially mendation would be an increased focus on affected by climate change. 90. yielding no net change tation? What host characteristics. neutral or negative effects on resistance. Phytopathol. such the costs and benefits of expression of par. effects of climate change on all these traits will by 190. Disease severity world. 42). will also change options available for dis- these more detailed studies can be developed ease management (124). scapes. for populations of plants and plant pathogens periments in more controlled environments (71) to migrate through fragmented land- with field experiments will also need to be ad. Rev. potential effects of introductions of new ferent stressors will allow more mechanis. both of these effects on disease have supplied recommendations for needed will be mediated by host resistance and en- research and syntheses. global climate change will affect in understanding climate change effects. Thus a number of authors However. pathogen. understanding trade-offs change phenomena. One broad recom. Thus a positive how a changing environment affects evolution effect of climate change on conduciveness to (11.44:489-509. such infection or pathogen aggressiveness or vir- as frequency of generations and proportion of ulence could be offset by a concurrent in- sexual reproduction. but with leaving pathogens behind or at least limit. studied empirically. and . crease in resistance. At plant disease in concert with other global the smallest scales.

by the Eco- logical Genomics Initiative of Kansas through NSF Grant No. Garrett KA. Agrawal AA. E. Morales FJ. National Science Foundation under Grants DEB-0130692. LITERATURE CITED 1. Models of plant disease have now been developed to incorporate more sophisticated climate predictions from General Circulation Models.S. 89:419–24 4. an anony- mous reviewer. For personal use only. At the scale of the individual plant. DE-FG02-04ER63892. 19:535–44 502 Garrett et al. enough experiments have been performed to begin synthesizing the effects of climate variables on infection rates. Grant No. This is Kansas State Experiment Station Contribution No. Anderson PK.org quickly enough to keep pace with climate change.126. It is also a pleasure to acknowledge support by the U. Power AG. 4. the adaptive potential of plant and pathogen populations may prove to be one of the most important predictors of the magnitude of climate change effects on plant disease. EPP-A-00-04-00013-00 to the Office of Interna- tional Research and Development at Virginia Tech and for the Integrated Pest Management CRSP. Ecology 86:2979–89 2. Kotanen PM. 2004. L. E. 2005. Leach. Garfinkel. populations will not be able to migrate Annu. 2005. Patel NG. Almeida RPP. Department of Energy. Emerging infectious diseases of plants: pathogen pollution. Department of Agriculture under Grant No. 2006. 06-311-J. since. by the U. 3. and by The Land Institute. ANRV283-PY44-21 ARI 13 June 2006 13:56 vector responses to different biotic and abiotic stressors and potential trade-offs in responses. for many species. facilitation. and niche differentiation in two foliar pathogens.S. Ecosystem ecologists are now addressing the role of plant disease in ecosystem pro- cesses. Gould. H. U.128 on 10/08/07.S. with the potential for greater understanding of the large-scale impacts of disease. Wistrom C. Plant Dis. At the population level. and members of the KSU Ecological Genomics Community for discussions and comments that improved this manuscript. by 190. Daszak P. Mitchell CE. Rev. EPS-0236913 with matching funds from the Kansas Technology Enterprise Corporation. Phytopathol.annualreviews. by the U. Godsoe W. Cunningham AA. Klironomos J. though pathosystem- specific characteristics make synthesis challenging. Enemy release? An experiment with congeneric plant pairs and diverse above. A. J. Purcell AH. climate change and agrotech- nology drivers. Hashim J. Jewett. Vector transmission of Xylella fastidiosa to dormant grape. Hill BL. by the Office of Science (Program in Ecosystem Research). Oecologia 143:449–57 3. Competition. Al-Naimi FA. Bowden. 5. Epstein PR. 2005.44:489-509. ACKNOWLEDGMENTS Thanks to R. Downloaded from arjournals. 2. Bockus WW. Evol. Ecol. and EF- 0525712 (as part of the joint NSF-NIH Ecology of Infectious Disease program). . Saleh. P. 2002-34103-11746.S. DEB-0516046.40. by the NSF Long Term Ecological Research Program at Konza Prairie.and belowground enemies. Agency for International Development for the Sustainable Agriculture and Natural Resources Management Collaborative Research Support Program (SANREM CRSP) under terms of Cooperative Agreement Award No.

2005. 2005. Rev. Climate change and plant diseases in Ontario.annualreviews. Rev. 170:201–4 9. 2005. 2005. and pathogenicity of Puccinia striiformis f. Leadley PW. Biogeogr. Phytopathol. Change Biol. The effects of long-term exposure to simulated acid rain on the development of pine wilt disease caused by Bursaphelenchus xylophilus. Sci. Soc. Traore S. Babbitt B. Fitt BDL. 2005. Baron C. Bergot M. van Niekerk BD. Cooke DEL. Global change. Jovanovic T. Acad. Erhard M. Sci. 1999. Leadley PW. B 360:2095–108 15.org The role of climatic mapping in predicting the potential geographical distribution of non-indigenous pests under current and future climates. Cities in the Wilderness: A New Vision of Land Use in America. Araujo impact models under climate change. 2005. Marc¸ais B. tritici in South Africa. 55:2331–41 www. 2004. Plant Pathol. Bray EA. Glob. 2005. Brasier CM. Effects of inoculum density of pinewood nematode on the devel- opment of pine wilt disease in Japanese black pine seedlings pretreated with simulated acid rain. Duncan JM. J. Bale JS. Philos. ANRV283-PY44-21 ARI 13 June 2006 13:56 ´ MB. Change Biol. 82:57–71 11. 2005. Natl. 86:485–92 20. Bezemer TM. Phytopathol. USA 102:5438– 42 16. Jarvis CH. 2006. Acta Oecol. For. Bostock RM. Natl. 108:365–72 19. Pretorius ZA. Barthes L. Asai E. Annu. Plant Pathol. Pathol. 2000. 26:284–90 22. Fraaije BA. 26:335–50 18.40. Barnard R. Pearson RG. Bourgeois G. Cycles 19:GB1007 13. Agric. From GCM grid cell to agricultural plot: scale issues affecting modelling of climate impact. R. Plant. Emberson L. Glob. Rapid evolution of introduced plant pathogens via interspecific hy- bridization. Change Biol. BioScience 51:123–33 23. Proc. Baker RHA. Desprez-Loustau M-L. Boland GJ. Lensi R. Pollut. Glob. soil microbial and soil inor- ganic nitrogen responses to elevated CO2 : a study in microcosms of Holcus lanatus. J. Old KM. 2000. Barnard R.annualreviews.org • Climate Change Effects on Plant Disease 503 . J. Exp. Downloaded from arjournals. Bourque A. Melzer MS. Sarr B. Ozone—a significant threat to future world food production? New Phytol. Environ. Cannon RJC. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. Walters KFA. Validation of species-climate 5. Origin of a new Phytophthora pathogen through interspecific hybridization. Nassuth A. Signal crosstalk and induced resistance: straddling the line between cost and benefit. 35:135–44 8. MacLeod A. Environ. sp. Bot. Modelling the impact of climate change on disease incidence: a bioclimatic challenge. 2001. 2001. Hopkin A. et al. Pathol. 8:1–16 by 190. 2006. Washington. Ecosyst. Trans. D´equ´e M. Dudzinski MJ. Shaw MW. distribution. 27:171–78 14. 10:1539–52 17. 11:1504–13 6. Booth TH. and denitri- fication: a review. Can. 2004. Climatic mapping to identify high-risk areas for Cylindrocladium quinqueseptatum leaf blight on eucalypts in mainland South East Asia and around the world. DC: Island Press 10. Plant Dis. Higgins V. For. Sultan B. Thuiller W. nitrification.126. Awmack C. Ashmore M. 31:241–53 7. Hodkinson ID. Masters GJ.128 on 10/08/07. et al. For personal use only. Hungate BA. Wheat archive links long-term fun- gal pathogen population dynamics to air pollution. Sansford CE. Balme M. Asai E. Cloppet E. Acad. Annu. Boshoff WHP. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Futai K. Can. Futai K. Establishment. Proc. Glob. 2004. Brasier CM. 12. Bearchell SJ. 2004.44:489-509. Deaudelin G. 2002. London Ser. 43:545–80 21. Simulation of potential range expansion of oak disease caused by Phytophthora cinnamomi under climate change. 2002. P´erarnaud V. Toet S. USA 96:5878–83 24.

Emanuel K. Davis MB. London Ser. Phytopathol. Phylloclimate or the climate perceived by individual plant organs: What is it? How to model it? What for? New Phytol. 28:380– evaluates adaptive 81 potential as a feature that may 44. 2005. Teng PS. ANRV283-PY44-21 ARI 13 June 2006 13:56 25. Browder LE. Rev. Comtois P. Appl. 54:1305–11 47. Plant Biol. Hovmoller M. Interactions of temperature and time with some Puccinia recondita:Triticum corresponding gene pairs.126. Agric. Shaw RG. 14:103–20 in determining the 45.) in sunflower (Helianthus annuus L. Shaw RG. Trans. 1986. 2006. How will plant pathogens adapt to host plant resistance at elevated CO2 under a changing climate? New Phytol. perspective in 70:1051–58 1999. 34. Wheeler TR. Lewis CF. Davelos AL. 1987. Davis MB. Environ. 133:251–61 37. Resistance to organisms under broomrape (Orobanche spp. Soc. Chuine I. 2005. Burdon JJ. Aerial dispersal of pathogens on the global and con- tinental scales and its impact on plant disease. New York: Cambridge Univ. 2000. Climate change: potential impact on plant diseases. Etterson JR. Ecol. Phytopathol. Entomol. Chakraborty S.128 on 10/08/07. Scherm H. Doos BR. Understanding plant responses to drought- from genes to the whole plant. The problem of predicting global food production. The effects of drought on sugar beet growth in isolation and in combination with beet yellows virus infection. Exp. 2003. Dale VH.) is temperature depen- climate change scenarios.org day and doubled CO2 climates. dent. 2005. Breeding Plants for Less Favorable Environments. 37:399–426 of climate change 39. Brown JKM. 7:753–69 from a 40. Chelle M. Ambio 31:417–24 success of 46. Press 28. Annu. Microbiol. 1997. Chakraborty S. Tiedemann AV. Potential impact of climate change on plant pathogen interactions. Coakley SM. Evolutionary responses to changing climate. Science 292:673–79 42. Plakhine D. Chaves MM. Climate change and phenological asynchrony. 1999. Appleton K. Kleifeld Y. 159:733–42 30. 166:781–90 by 190. Smith HG. Range shifts and adaptive responses to quaternary climate analysis. Plant Pathol. Samac DA. 1982. Nature 436:686–88 504 Garrett et al. 1995. Bone A. on plant disease Appl. Plant Pathol. Coakley SM. Phytopathology 76:1286–88 26.annualreviews. Spatial variation in frequency and intensity of management antibiotic interactions among streptomycetes from prairie soil. Jaggard KW. 2006. Eversmeyer MG. Datta S. Increasing destructiveness of tropical cyclones over the past 30 years. Slingo JM. Environ. Ecosyst. Agric. 2000. Dockerty T. 2003. 2003. Environ. 2002. Challinor AJ. Hershenhorn J. Hemming D. Clover GRG. . Christiansen MN. Ecology 86:1704–14 This review 43. change. Rubin B. Aust. Funct. 108:317–26 31. Science 297:537–41 27. Rev. J. In press 29. Bot. Chakraborty S. Sci. Change Biol. 2005. B 360:2085–94 32. Dixon AFG. R. Our review builds on this 41. Climate change and plant disease provides the context for effects management. Quantification of physical and biological uncertainty in the simulation of the yield of a tropical crop using present- Annu. The relationship between land-use change and climate change. Biospheric change: will it matter in plant pathology? Can. 2001. Pereira JS. 2004. Azam-Ali SN. Kinkel LL. 17:147–53 This review 38. 2003. Philos. 30:239–64 33. Glob. Ecol. Eizenberg H. J. 1999. Cambon G. Scaling phenology from the local to the regional level: advances from species-specific phenological models. J. Sunnenberg¨ G. 2002. Pollut. Developing sce- often prove to be narios and visualisations to illustrate potential policy and climatic influences on future the most important agricultural landscapes. For personal use only. New York: Wiley 35. Chakraborty S.40. Lovett A.44:489-509. 6:943–52 36. Maroco JP. Downloaded from arjournals. Diseases and Population Biology. 2006.

Chapin FC III. Clinal patterns of selection along an environmental gradient in the Great Plains. 2004. 2001. 2002. 1996. 2006. 15:56–61 67. Climate warming and disease risks for terrestrial and marine biota. 2006. Shaw RG. Agroecosystern responses to combinations of elevated CO2 . Plant Pathol. Effects of disease on biogeochemical cycling. I. 102:133–42 62. London Ser. Downloaded from arjournals. 7:417–26 www. R. 2003.org • Climate Change Effects on Plant Disease 505 . 2002. Eviner VT. 2004. 160:21–42 61. Huntley B. Evolutionary ecology of plant diseases in natural ecosystems. Collingham YC. 2003. F Keesing. Science 308:1431–35 63. Garrett KA. and global climate change. For personal use only. Evol. Science 296:1689–91 54. Evolutionary potential of Chamaecrista fasciculata in relation to climate change. Gutschick VP. Etterson JR. 1992. Harvell CD. Sato M. Willis J. Nature 409:188–91 65. Epstein PR. Chapin FS III. ecology. Fitter RSR. Appl. Rev. Rev. Agric. Hungate BA. Biological consequences of global warming: Is the signal already ap- parent? Trends Ecol. Travers SE. Ecosyst. 2002. 1999. 1996. An Allee effect reduces the invasive potential of Tilletia indica.annualreviews. Leach JE. 3:747–54 49. et al. Climate change and emerging infectious diseases. Effects of climate and land use on the occurrence of viruliferous aphids and the epi- Annu. Fuhrer J. 97:1–20 by 190. New Phytol. relative humidity and biological control agents on grey mold of bean. J. Kleczkowski A.44:489-509. Phytopathology 92:1152–59 56. Canadell J. Hulbert SH. Microbes Infect. Leterrier JL. Agric. Science 296:2158–62 64. 2001. Modeling leaf wetness in relation to plant disease epi- demiology. Grevstad FS. 2000. Bowden RL.40. In Cary Conference XI: Infectious Disease Ecology: The Effects of Ecosystems on Disease and of Disease on Ecosystems. 2002. B 266:1743–53 58. 9:1439–47 60. Mitchell CE. Annu. Gilligan CA. Boland GJ. Etterson JR. 2005. Rapid changes in flowering time in British plants. Hughes L. Green RE. Firestone MK. Ward JR. et al. 2005. V Eviner. Interactions of air temperature. Ecosyst.126. Ecol. Ecological genomics and epi- demiology. Nazarenko L. Field CB. Environ. In press 52. Altizer S. Extreme events as shaping physiology. Phytopathol. The performance of models relating species geographical distributions to climate is independent of trophic level. Press. Soc. Dobson AP. Predicting variability in biological con- trol of a plant-pathogen system using stochastic models. 40:13–43 59. Likens GE. Ecology 77:2505–15 68. Gibson GJ. Dedryver CA. Plant Pathol. J.org demiology of barley yellow dwarf disease. Hansen J. Huber L. 2006. Eur. Factors influencing the chance of population establishment: impli- cations for release strategies in biocontrol. Garrett KA. Ecol. ANRV283-PY44-21 ARI 13 June 2006 13:56 48. Hannusch DJ. et al. Evolution 58:1446–58 50. Earth’s energy imbalance: confirmation and implications. Rev. Jacquot E. New York: Princeton Univ. Plantegenest M. Hill JK. ed. Phytopathol. Constraint to adaptive evolution in response to global warming. Chiariello NR. Fabre F. Environ.annualreviews. 55. Hu S. Eur. 2001. Lett. 1999. Annu. Willis SG. Proc. Mieuzet L. Nitrogen limitation of microbial decomposition in a grassland under elevated CO2 . In press 57. R Ostfeld. Ruedy R.128 on 10/08/07. BassiriRad H. Phytopathol. Fitter AH. 106:49–55 53. Plant species mediate changes in soil microbial N in response to elevated CO2 . ozone. and evolution of plants: toward a unified definition and evaluation of their consequences. 30:553–77 66. Gillespie TJ. Gilbert GS. Science 294:151–54 51.

6:654–64 79a. Raffa KF. Conserv. Vera Cruz CM. Res. Potential impact of global warm- ing on deciduous oak dieback caused by ambrosia fungus Raffaelea sp. Malmstrom ¨ CM. Hoye KA. Annu. 2006. Ecol. tremuloidae). Climate Change 2001: The Scientific Basis. Change. Rev. Wada K. Ritts WD. et al. 2005. JT Houghton. 6:673–79 81. 2003. Loreau M. Pathogen population genetics. histopathology and growth of common bean (Phaseolus vulgaris L. Holbrook CC. carried by am- Annu.126. Glob. Contrib. Simpson J. sp. 2001. Luo M. et al. UK/New York: the climatology Cambridge Univ.40. McElrone AJ. Biol. Lafferty KD. Johnson R. 8:329–38 by 190. Water relations. Phytopathol. 2005.128 on 10/08/07. understanding of DJ Griggs. Glob. Bai J. 2005. 2002. Kamata N. Intergov. 2001. 39:187–224 80. Percy KE. et al. Spread of an invasive pathogen is scheduled to be over a variable landscape: a nonnative root rot on Port Orford cedar. M Noguer. 92:119–26 74. Koelle K.org brosia beetle Platypus quercivorus (Coleoptera: Platypodidae) in Japan. Callan B. Interacting elevated CO2 and tropospheric O3 predisposes aspen (Populus tremuloides Michx. Deleted in proof 78. 2002. Bausher MG. Mayek-Perez N. Group This document summarizes the I Third Assess. Penuelas J. Xiang B. Lopez-Castaneda C. Igeta Y. Change Biol. Katz RW. How should environmental stress affect the population dynamics of disease? Ecol. Techniques for estimating uncertainty in climate change scenarios and impact studies. 2003. Glob. Panel Clim. Katz RW. Yunus M. Y Ding. Lett. Phytopathol. and durable resistance. Lett. Dang P. Running to stand still: adaptation and the response of plants to rapid climate change. 15:320–31 85a. Rep. Parlange MB. Work. Ecology 83:3167–81 updated in 2007. Hart E. Statistics of extremes: modeling ecological disturbances. 2002. 2005. Change Biol. Kauffman MJ. Brush GS. Jules ES. McDonald BA. Ecol. 40:349–79 86. Annu. London Ser. PJ van der Linden. Acosta-Gallegos JA. 20:167–85 76. Noormets A. Biotic disturbance agents in the boreal forest: consid- erations for vegetation change models. 75. Reid CD. 1984. 2000. Rev. 8:1010–20 73. Kruger EL. 2002. Soc. Pascual M. Microarray-based screening of differentially expressed genes in peanut in response to Aspergillus parasiticus infection and drought stress. Pathogen adaptation to seasonal forcing and climate change. R. evolutionary potential. Physiol. . Rev. Mouquet N. For personal use only. Elevated CO2 reduces disease incidence and severity of a red maple fungal pathogen via changes in host phys- iology and leaf chemistry. Res.) during pathogenesis of Macrophomina phaseolina under drought stress. ed. 22:309– the state of current 30 understanding of climate change and 71. Phytopathol.44:489-509. Karnosky DF. 2005. 2001. Jump AS. Phytopathol. 11:1828–36 506 Garrett et al. Linde C. Effects of water stress on colonization of poplar stems and excised leaf disks by Septoria musiva. 2002. Cambridge. Esaki K. Lett. Plant Pathol. Maxwell DL. Plant Sci. 60:185–95 85. Annu. Rev. 169:695–703 82. Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Clim. Carroll AL. IPCC. Entomol. 1997. Proc.) to infection by rust (Melampsora medusae f. Liang XQ. Leach JE. Mol. Kato K. Leung H. Press community about 70. 6:35–48 83. Holt RD. Garcia-Espinosa R. ANRV283-PY44-21 ARI 13 June 2006 13:56 69. Phytopathology 87:381–88 84. Holt RD. Ecology 86:1124–34 77. B 272:971–77 79. Stanosz GR. ˜ 72. 2002. Change Biol. Pathogen fitness penalty as a predictor of durability of disease resistance genes.annualreviews. Jackson RB. Bull. Ecological consequences of recent climate change. Downloaded from arjournals. A critical analysis of durable resistance. McCarty JP.

Lett.org Plant Sci. Acad. Olson AJ.128 on 10/08/07. Mitchell CE. Glob. A globally coherent fingerprint of climate change impacts across natural systems. Annu. Glob. Ecology 86:2088–98 89. Eur. Mitchell CE. Ford RE. Change Biol. Otten W. 2004. Interactive effects of water stress and xylem- limited bacterial infection on the water relations of a host vine. Biogeogr. Ecol. 1996. Gilligan CA. Effects of drought stress and infection by maize dwarf mosaic virus in sweet corn. 2005. New Phytol. Change Biol. Empirical evidence of spatial thresholds to control invasion of fungal parasites and saprotrophs. 2006. DC: Natl. 2004. Forseth IN. Newman JA. Anim. Young IM.annualreviews. Effects of elevated CO2 . Ecol. Release of invasive plants from fungal and viral pathogens. Climate change and the fate of cereal aphids in Southern Britain. D’Arcy CJ. Phytopathol. Rev. 72:556–66 101. Awmack CS. Nature 421:625–27 91. 74:147–51 103.40. Power AG. Change Biol. ANRV283-PY44-21 ARI 13 June 2006 13:56 87. Gibson DJ. Change Biol. 6:147–55 90. 2004. Yates D. Manos PS. 2003. Tilman D. 2001. J. Transgenerational phenotypic plastic- by 190. Gilligan CA. Newman JA. 2004. Naylor RL. Syst. Sherald JL. The role of genomics research in improvement of “orphan” crops. 30:1221–32 104. de Rautenbach CJD. Yohe G. Divergent pheromone- mediated insect behaviour under global atmospheric change. Erasmus BFN. National Research Council. Soil structure and soil-borne diseases: using epidemiolog- ical concepts to scale from fungal spread to plant epidemics. Jahn MM. McElrone AJ. Simulating tick distributions over sub-Saharan Africa: the use of observed and simulated climate surfaces. 10:1820– 24 96. Phytopathology 94:221–27 107. Parker IM. 2003. Mondor EB. Tremblay MN. Tremblay MN. Nelson RJ. Glob. Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres. 2003. 11:15–19 93.126. 45:973–77 102. Pataky JK. Climate change and cereal aphids: the relative effects of increasing CO2 and temperature on aphid population dynamics. and decreased species diversity on foliar fungal plant disease. Newton AC. 2004. Grand Challenges in Environmental Sciences. Downloaded from arjournals. 44:1901–4 98. Clark JS. Awmack CS. Groth JV. 2003. 11:1990–96 94. J.org • Climate Change Effects on Plant Disease 507 . Mittler R. Evol. Trophic control of grassland production and biomass by pathogens. Parmesan C.annualreviews. Reich PB. Rev. Mondor EB. 2004. McLachlan JS. For personal use only. Parsons AJ. 2004. Engelbrecht FA. Glob. Gilbert GS. 7:941–46 95. 10:5–15 99. 35:675–700 108. 9:438–51 92. Lindroth RL. Glob. 2005. Soil Sci. Bailey DJ. Tremblay MN. Ecol. nitrogen deposition. Chakraborty S. Mondor EB. Trends Annu. Washington. 2005. Olwoch JM. 163:125–32 105. Molecular indicators of tree migration ca- pacity under rapid climate change.44:489-509. Abiotic stress. 2003. Nature 421:37–42 www. Plant Dis. Crop Sci. Lett. 1990. 2006. Mitchell CE. 57:26–37 106. Newman J. Exp. How predictable are aphid population responses to elevated CO2 ? J. Plant Pathol. Pangga IB. the field environment and stress combination. Lindroth RL. ity under future atmospheric conditions. 54:419–30 88. Press 97. 11:940–44 100. Ecol. Temporary partial breakdown of mlo-resistance in spring barley by the sudden relief of soil water stress. Canopy size and induced resistance in Sty- losanthes scabra determine anthracnose severity at high CO2 . Change Biol. The evolutionary ecology of novel plant-pathogen inter- actions. Lindroth RL. J. Otten W. Bot. 2003. 2006. 2003. Thornley JHM. van Jaarsveld AS.

Rogers HH.128 on 10/08/07. Mitchell CE. Climate change and plant pathosystems—future disease prevention starts here. Rosenzweig C. Sandermann H Jr.40. Scherm H. Plazek A. 2005. Pritchard SG. Sutherst RW. Simulating uncertainty in climate-pest models with fuzzy numbers. Appl. 2000. Proc. Response of plant pathogens and herbivores to a warming experiment. Global warming and nonlinear growth—how important are changes in average temperature? Phytopathology 84:1380–84 128a. cv. New Phytol. . Plant Pathol. 7:694–705 116. 2005. Prior SA. Pollut. Percy KE. Awmack CS. Sci. Freezing temperature effect on survival of Puccinia graminis subsp. Environ. Sheehy JE. Genet. Vollmer SS. Ozone/biotic disease interactions: molecular biomarkers as a new experimental tool. Leath KT. 1999. Power AG. 2005. Harte J. Environ. et al. Pennypacker BW. 190 113. Patt A. Elevated CO2 and plant structure: a review. 2003. Rapacz H. Acad. by 190. 2004. 2004. Multiple effects of two drivers of agricultural change. Roy BA. Scherm H. J. Visperas RM. 2003. Phytopathol. 108:333–41 508 Garrett et al. 108:327–32 124. Coakley SM. Proc. Global networking for as- sessment of impacts of global change on plant pests. Teng PS. Savary S. labour shortage and water scarcity. Lindroth RL. Schloss PD. Pollut. Annu. Hall KR. Rust Diseases of Wheat: Concepts and Methods of Disease Management. Scherm H. Impact of drought stress on the expres- sion of resistance to Verticillium albo-atrum in alfalfa. Aust. Root TL. Natl. 83:1058– Annu. 2001. graminicola in Festuca arundinacea and Lolium perenne. The influence of ozone fumigation on metabolic efficiency and plant resistance to fungal pathogens. Effects of seasonal climate forecasts and participa- tory workshops among subsistence farmers in Zimbabwe. Scarlett) grown at elevated ozone and carbon dioxide concentrations. 1991. et al. Mexico. 159:531–38 123. Elstner EF.44:489-509. Payer HD. Gwata C. Price JT. Heiser I. 32:157–65 128.org 62 114. Downloaded from arjournals. on rice pest profiles in tropical Asia. Change Biol. Peterson CM. Altered per- formance of forest pests under atmospheres enriched by CO2 and O3 . Huang J. Suarez P. 1999. 75:8–13 115. Plessl M. 5:807–37 118. Phytopathology 81:1014–24 112. Pfender WF. Pounds JA. Ingram JSI. J. Laza RC. 2004. 2004. 91:263–71 125. 1994. Natl. Am. Handelsman J. 108:373–79 126. Hill RR Jr. Metagenomics: genomic analysis of microbial communities. Poll. Riesenfeld CS. Nature 421:57–60 121. Castilla NP. 26:267–73 127. 2000. Glob. Growth parameters and resistance against Drechslera teres of spring barley (Hordeum vulgare L. Acad. Ecology 85:2570–81 122. Kubiske ME.126. Heller W. Plant pathogens in a changing world. Plant Dis. For personal use only. Zur I. Nature 420:403–7. Peng S. Kopper BJ. Habermeyer J. 2003. Gusewell S. Roelfs AP. Plant Pathol. 38:525–52 119. Hura K. Saari EE. Nat. 1992. Scherm H. ANRV283-PY44-21 ARI 13 June 2006 13:56 109. Rice yields decline with higher night temperature from global warming. USA 101:9971–75 111. DF: CIMMYT 120. Plant Biol. van Bruggen AHC. Schneider SH. 164:S79–89 117. Harrington R. 2000. Runion GB. Scherm H.annualreviews. Singh RP. Sci. Climate change: can we predict the impacts on plant pathology and pest management? Can. Environ. Rev. Finger- prints of global warming on wild animals and plants. Field Crops Res. 2006. Pathogen spillover in disease epidemics. 2002. Rev. Bot. Elazegui FA. 2004. USA 102:12623–28 110.

annualreviews. Walther G-R. Nature 427:145–48 137. soil type and Trichoderma species on the survival of Fusarium pseudograminearum in wheat straw. 1997. Agric. Melcher U. Zack JW. Oberti R. 6:169–85 142. Wilson JP. Interactive effects of elevated ozone and carbon dioxide on growth and yield of leaf rust-infected versus non-infected wheat. 2004. 2005. Can. 2003. Dyn. 2005. 31:253–57 148. Downloaded from arjournals. and intensity in a warming environment. Bravo C. 103:73–82 135. Syst. 2000. Russo JM. Lafferty KD. McCartney HA. Seem RC. Aust. For. Plant Dis. indica.40. 31:81–92 134. Beaumont LJ. 168:661–70 145. 2000. Nelson RS. Mead JA. Way H. 2004. 87:45–50 144. Coates KD. Puccinia substriata var. Waugh MM.44:489-509.annualreviews. Post E. Field CB. McKenzie VJ. Stanghellini ME. Forecasting climate suitability for karnal bunt of wheat: a comparison of two meteorological methods. Kim DH. Evol. Environ. 2002. Menzel A. Firsching KH. Is an unprecedented Dothistroma needle blight epidemic related to climate change? BioScience 55:761–69 www. J. 26:274–83 130. Dobson AP. Scheets K. Green RE. Plant Dis. Hamann A. Climate change and crop production: contributions. 108:357–63 140.org • Climate Change Effects on Plant Disease 509 . Convey P. 4:e80 147. 25:739–53 143. Wang G. Environ. Plant Pathol. Thomas CD. Palmer MW. Sci- ence 298:1987–90 132. Strand JF. Some agrometeorological aspects of pest and disease magagement for Annu. For personal use only. Smith DL. J. Woods A. Nature 421:628–30 139. Changes in tropical cyclone number. 2005. Plant Pathol. Perspect. 81:1049–52 136. Introduced species and their missing parasites. 2006. Plants in a warmer world. Phytopathol. Plant virus biodiversity and ecology. and adaptations. Plant Sci. moisture. Plant Ecol. Extinction by 190. Parmesan C. Mooney HA. Annu. Wong PTW. Forecasting plant disease in a changing climate: a question of scale. Moshou D. Chiariello NR. Zavaleta ES. Meteor. Ecological re- sponses to recent climate change. Wren JD. et al. Pollut. Clim. West JS. 26:253–66 133. Croft MC. Science 299:1735–37 138. Shaw MR. Curry JA. Cleland EE. Roossinck MJ. Stansbury CD. 2003. Xue GP. Chang HR. Casu R.org the 21st century. et al. Science 309:1844–46 146. McKirdy SJ. et al. Bakkenes M. Aust. 2002. PLoS Biol. 2005. Thrall PH. Burdon JJ. Effects of temperature and light on germination of ure- diniospores of the pearl millet rust pathogen. Kuris AM. Nature 416:389–95 141. Pollut. Identification of differen- tially expressed genes in wheat undergoing gradual water deficit stress using a subtractive hybridisation approach. 2003. duration. Phytopathol. Reproductive potential of Monosporascus cannonballus. Estimating disease risk at the whole plant level with General Circulation Models. Ferrin DM. 2002. Plant Pathol. Cameron A. Torchin ME. 2000. Walther G-R. Lemaire D.126. Almaraz JJ. risk from climate change. 2006. 2003. 2004. im- pacts. Magarey RD. 2003. Agricultural drought in a future climate: results from 15 global climate models participating in the IPCC 4th assessment. Plant Pathol. von Tiedemann A. 41:593–614 146a. Grassland responses to global environmental changes suppressed by elevated CO2 .128 on 10/08/07. Rev. McIntyre L. 2002. 108:389–95 131. Webster PJ. Rev. Seem RC. ANRV283-PY44-21 ARI 13 June 2006 13:56 129. Can. Chapman S. Evolution of virulence in a plant host-pathogen metapop- ulation. Tapsoba H. Effect of temperature. The potential of optical canopy measurement for targeted control of field crop diseases. Holland GJ.

Jr. Carris. p p p p p p p p p p p p p89 Nonsystemic Bunt Fungi—Tilletia indica and T.C.annualreviews. G. Phytopathol. Fauquet. Yong-Hu Huang.J.M. Ngugi and Harald Scherm p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 261 v . Falk p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 183 Breeding for Disease Resistance in the Major Cool-Season Turfgrasses Stacy A. Konaté. E. and Blair J. Fitt. Peterschmitt. and C. and William A. Nutter.126. van Loon. Meyer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 213 Molecular Ecology and Emergence of Tropical Plant Viruses D. West p p p p p p 163 Virus-Vector Interactions Mediating Nonpersistent and Semipersistent Transmission of Plant Viruses James C.44:489-509. Rep. 2006 A Retrospective of an Unconventionally Trained Plant Pathologist: Plant Diseases to Molecular Plant Pathology Annu. For personal use only. M. Teng. horrida: A Review of History.128 on 10/08/07. 2006. Muller.K. Downloaded from arjournals. Clarke.org Seiji Ouchi p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 The Current and Future Dynamics of Disease in Plant Communities Jeremy J. Peter H. Laetitia Willocquet. Ng and Bryce W. Goates p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 113 Significance of Inducible Defense-related Proteins in Infected Plants L. M. Systematics. Frank van den Bosch. Fargette. Pieterse p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 135 Coexistence of Related Pathogen Species on Arable Crops in Space and Time Bruce D. Contents ARI 1 July 2006 4:28 Annual Review Contents of Phytopathology Volume 44. Thrall. Rao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p61 Quantification and Modeling of Crop Losses: A Review of Purposes Serge Savary. Lisa A. Bruce B. Burdon.40.N. C. Paul S. and Jonathan S. Castlebury.L. Bonos. and Biology Lori M. and J. and Forrest W. and Lars Ericson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p19 A Catalogue of the Effector Secretome of Plant Pathogenic Oomycetes by 190. L.M. Rev. Thresh p p p 235 Biology of Flower-Infecting Fungi Henry K. Sophien Kamoun p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p41 Genome Packaging by Spherical Plant RNA Viruses A.

Biosynthesis and Regulation Dmitri V. Mavrodi. Leighton Pritchard.J. and Madhumita Joshi p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 469 Climate Change Effects on Plant Disease: Genomes to Ecosystems K. the Soybean Cyst Nematode T. M. Cammue p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 393 by 190. Martin B. Contents ARI 1 July 2006 4:28 A Model Plant Pathogen from the Kingdom Animalia: Heterodera glycines.128 on 10/08/07.40. Frank. and Bruno P.A. Travers p p p p p p p p p p p p p p p p p 489 INDEX Subject Index p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 599 ERRATA An online log of corrections to Annual Review of Phytopathology chapters (if any.org/ vi Contents . Miguel F.44:489-509. Thomashow p p p p p p p p p p p p p p p p p p p p p p 417 Long-Distance RNA-RNA Interactions in Plant Virus Gene Expression and Replication W. Allen Miller and K. Phytopathol. Wulf Blankenfeldt.A. Garrett. and Linda S. Broekaert.N. For personal use only. 1977 to the present) may be found at http://phyto. Toth. Stijn L. Rouse. Johan Kers.N.org Maria T. and G. K. Tylka p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 283 Comparative Genomics Reveals What Makes an Enterobacterial Plant Pathogen Ian K. You-Liang Peng. Lambert.annualreviews. and Amir Sharon p p p p p p p p p p p p p p p p 337 Fitness of Human Enteric Pathogens on Plants and Implications for Food Safety Annu. De Bolle.annualreviews. Dendy. Rev. Andrew White p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 447 Evolution of Plant Pathogenicity in Streptomyces Rosemary Loria.126. Downloaded from arjournals. and S. Phenazine Compounds in Fluorescent Pseudomonas Spp.E. 2006. E. Dickman. Birch p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 305 The Dawn of Fungal Pathogen Genomics Jin-Rong Xu. and Paul R. S.L. Niblack.L.P. Brandl p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 367 The Role of Ethylene in Host-Pathogen Interactions Willem F.C.E. Delauré.