Climate change and plant disease

Karen A. Garrett Kansas State University

Photos: Gordon, UCD

Outline
Plant disease and ecosystem services The usual challenges for managing plant disease Implications of climate change Potential interactions and thresholds Responding to climate change

Ecosystem services: Services provided to humans by ecosystems, including services provided by plants and their pathogens
(see Millennium Ecosystem Assessment 2005)

Provisioning services Food Fiber Fuel Fresh water Genetic resources

Photo: CIP

Other forms of services include:

Supporting services Soil formation Nutrient cycling Primary production

Provisioning services Food Fiber Fuel Fresh water Genetic resources

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Regulating services Climate regulation Disease regulation Water regulation Water purification

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Regulating services Climate regulation Disease regulation Water regulation Water purification

Damage by disease and insect pests results in approx. 42% loss in the eight most important food and cash crops
(Oerke et al. 1994)

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

This is a loss of > $300 billion

Plant disease pressure

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

A broader definition of successful management: Plant disease and ecosystem services Cheatham et al., in preparation

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Methods for disease management

Plant disease pressure

Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Plant biodiversity Alternate hosts Non-hosts Insect biodiversity Pathogen vectors Natural enemies of vectors Microbial biodiversity Pathogens Biocontrol organisms/ Disease suppressive soils

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Plant disease pressure

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Plant disease pressure

Plant biodiversity Alternate hosts Non-hosts

Insect biodiversity Pathogen vectors Natural enemies of vectors

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Biological impacts from beyond target region Global genetic resources: Provisioned by many different ecosystems Disease resistance genes in crops New invasive pathogens
Plant disease pressure
Plant biodiversity Alternate hosts Non-hosts

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Insect biodiversity Pathogen vectors Natural enemies of vectors

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Biological impacts from beyond target region Global genetic resources: Provisioned by many different ecosystems Disease resistance genes in crops New invasive pathogens

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Plant disease pressure

Plant biodiversity Alternate hosts Non-hosts

Insect biodiversity Pathogen vectors Natural enemies of vectors

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Policy

Biological impacts from beyond target region Global genetic resources: Provisioned by many different ecosystems

Support for conserving and utilizing genetic Disease resistance genes in crops resources New invasive
pathogens

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Policies to control movement of plant materials

Plant biodiversity Alternate hosts Non-hosts

Plant disease pressure

Insect biodiversity Pathogen vectors Natural enemies of vectors

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Policy
Support for conserving and utilizing genetic resources Policies to control movement of plant materials

Biological impacts from beyond target region Global genetic resources: Provisioned by many different ecosystems Disease resistance genes in crops New invasive pathogens

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Plant disease pressure

Plant biodiversity Alternate hosts Non-hosts

Insect biodiversity Pathogen vectors Natural enemies of vectors

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Farm Bill: in US, subsidies Support for conserving and Global genetic resources: provide pressure for great utilizing genetic resources Provisioned by many different ecosystems abundance of a few crop Policies to control Disease resistance genes in crops movement of plant materials species Payment for ecosystem services: e.g., US Conservation Plant disease Reserve Program pressure
Plant biodiversity Alternate hosts Non-hosts Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides New invasive pathogens

Policy

Biological impacts from beyond target region

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Insect biodiversity Pathogen vectors Natural enemies of vectors

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Policy
Support for conserving and utilizing genetic resources Policies to control movement of plant materials Farm Bill: in US, subsidies provide pressure for great abundance of a few crop species Payment for ecosystem services: e.g., US Conservation Reserve Program

Biological impacts from beyond target region Global genetic resources: Provisioned by many different ecosystems Disease resistance genes in crops New invasive pathogens

Provisioning services Food Fiber Fuel Fresh water Genetic resources Supporting services Soil formation Nutrient cycling Primary production

Plant disease pressure

Plant biodiversity Alternate hosts Non-hosts

Insect biodiversity Pathogen vectors Natural enemies of vectors

Methods for disease management Tillage for disease management Need for resistant varieties (with potentially lower value) Application of pesticides

Regulating services Climate regulation Disease regulation Water regulation Water purification Cultural services Ecotourism Agrotourism Aesthetics Education Recreation Inspiration

Microbial biodiversity Pathogens Biocontrol organisms/Disease suppressive soils

Outline
Plant disease and ecosystem services The usual challenges for managing plant disease Implications of climate change Potential interactions and thresholds Responding to climate change

Management options
Disease resistance is generally the best option, if available Pesticides are often an option, sometimes with associated health and environmental risks, not to mention economic costs Particular diseases may have other options, such as sanitation, biocontrol, tillage, and use of certified seed

For rice blast, single R genes have not offered long-lasting protection

Blast R gene

lea

1965

Br ea

Re

1970

kd ow n

se

1975

1980

1985

1990

Adapted from Lee and Cho, International Rice Research Conference, Seoul, 1991

Connected regions for pathogen types with different tolerances to the cost of limited host availability

Margosian, Garrett, Hutchinson, and With

Farm policies that support vast acreages of a single crop species increase the risk of rapid pathogen movement throughout the highly connected plantings

Rice blast management through genotype mixtures (Yunnan Province) - Zhu et al. 2000 Nature The rice variety mixtures are now used on over 1 million hectares in China More recently, studies indicate that microclimate changes from mixing varieties play an important role in reduced disease in this system

Strategically selected intraspecific plant diversity can be effective for disease management, especially as a component in an integrated disease management plan

Potato late blight can only be managed in some regions with more than 10 pesticide applications a season

Image c/o CIP and CARE farmer field schools and collaborators

Fungicide applications as a function of climate

Estimates of regional reliance on fungicides for management of potato late blight around Lake Titicaca

For well-known diseases, we can make rough predictionsUsing about the late blight demands for management as forecasting models based on meteorological temperature and precipitation variables change
Forbes, Raymundo, Garrett

Outline
Plant disease and ecosystem services The usual challenges for managing plant disease Implications of climate change Potential interactions and thresholds Responding to climate change

Garrett et al. 2006

Ecogen KSU Conceptual Model

ECOLOGY
ECOSYSTEM RESPONSE POPULATION AND COMMUNITY RESPONSE

ECOLOGICAL GENOMICS

ORGANISMAL RESPONSE

GENETICS

GENOTYPIC CONTRAINTS

PHENOTYPIC EFFECT ON DEVELOPMENT/PHYSIOLOGY

GENE EXPRESSION

Ecogen KSU Conceptual Model

ECOLOGY
ECOSYSTEM RESPONSE POPULATION AND COMMUNITY RESPONSE

ECOLOGICAL GENOMICS

GENETICS

In the long run, understanding the genetic constraints for pathogen ORGANISMAL RESPONSE and plant adaptation will allow better mechanistic models of GENOTYPIC responses to climate PHENOTYPIC change EFFECT ON
CONTRAINTS

DEVELOPMENT/PHYSIOLOGY

GENE EXPRESSION

Lower expression of HR and other genes associated with disease resistance in big bluestem in response to simulated precipitation change Travers et al. 2007

Steve Travers

Phytohormone responses to disease and drought stress in big bluestem Jasmonic acid and salicylic acid increase in response to rust infection in plants without drought stress Under drought stress, plants dont respond in this way Drought stress doubles disease severity in this system

Erin Frank

Xa resistance genes, except Xa7, are less effective at higher temperatures

Lesion length (cm) 3.5 a 2.5 1.5 b 0.5 b a b a b a a a 35 C day/29 C night 29 C day/21 C night

Xa3 Xa4 xa5 Xa7 Xa10 Rice bacterial blight resistance gene
c/o Jan Leach
Webb et al., unpubl.

Stomatal closure and leaf growth inhibition during drought (e.g., Chaves et al. 2003) Plant structural changes in response to CO2 (Pritchard et al. 1999) Higher fecundity of Colletotrichum gloeosporioides under increased CO2 (Chakraborty and Datta 2003)

Garrett et al. 2006

Increased CO2 increased fungal pathogen load in tallgrass prairie (Mitchell et al. 2003) Heating of montane prairie had mixed effects on pathogens (Roy et al. 2004)

Needle blight moving northward in North America as temperature and precipitation patterns change (Woods et al. 2005)

Phytophthora cinnamomi predicted expansion in Europe due to temperature change from General Circulation Models (Bergot et al. 2004)

Soybean rust pathogen immigration to US potentially via Hurricane Ivan Invasive species Kudzu will probably play important role in epidemiology Dry conditions have probably slowed movement through the US

Factors for prediction of disease effects on ecosystems (Eviner and Likens, in press) Pathogen effect on host survival, physiology, behavior, and/or reproduction Life stages of a host vulnerable to a pathogen Proportion of individuals/biomass infected at a site Spatial extent and distribution of infection Rate of pathogen effects on hosts in relation to rate of response/recovery by hosts of individuals replacing hosts Frequency and duration of pathogen impact Functional similarity of infected individuals versus replacements

Outline
Plant disease and ecosystem services The usual challenges for managing plant disease Implications of climate change Potential interactions and thresholds Responding to climate change

Policy supporting extensive plowing + drought = dustbowl

Plant disease triangle

Susceptible host Generalization: Fungal pathogens benefit from Virulent pathogen more precipitation

Conducive environment

Plant disease triangle

Susceptible host An environment that is not conducive may obscure the fact that a susceptible host and virulent pathogen are both present Virulent pathogen

Conducive environment

For potato late blight, the effects of Susceptible potatoes climatic variables for a particular pathogen genotype and host genotype, within a field, are fairly well understood Phytophthora infestans Conducive environment

+ reliance on potatoes as primary food = Irish potato famine

The local inoculum load builds during the period of conducive weather
Percentage inoculum saturation
70 60 50 40 30 20 10 0 Month 1 Month 2 Month 3 Month 4 Month 5 Month 6 Month 7

Because plant disease pressure often increases following a compound interest model, increasing the length of the growing season slightly can have a very large impact on inoculum load

A conceptual model of the relationship between season length and local potato late blight severity

Local processes (Field)

Pathogen: Local inoculum load

Local disease severity

Environment: Local environmental conduciveness to disease during season

Host: Local host susceptibility

Garrett, Zuniga, Roncal, Mundt, Forbes, Su, and Nelson

Regional processes (Valley)

Environment: Regional environmental conduciveness to disease during season

Host: Regional host susceptibility

Pathogen: Regional inoculum load

Regional disease severity Local disease severity

Local processes (Field)

Pathogen: Local inoculum load

Environment: Local environmental conduciveness to disease during season

Host: Local host susceptibility

Garrett, Zuniga, Roncal, Mundt, Forbes, Su, and Nelson

Regional processes (Valley)

Environment: Regional environmental conduciveness to disease during season

Host: Regional host susceptibility

Pathogen: Regional inoculum load Length of season Local processes (Field) Pathogen: Local inoculum load

Regional disease severity Local disease severity

Environment: Local environmental conduciveness to disease during season

Host: Local host susceptibility

Garrett, Zuniga, Roncal, Mundt, Forbes, Su, and Nelson

Regional processes (Valley)

Environment: Regional environmental conduciveness to disease during season

Host: Regional host susceptibility Effect of regional host diversity Regional disease severity Local disease severity Effect of local host diversity

Pathogen: Regional inoculum load Length of season Local processes (Field) Pathogen: Local inoculum load

Environment: Local environmental conduciveness to disease during season

Host: Local host susceptibility

Garrett, Zuniga, Roncal, Mundt, Forbes, Su, and Nelson

Regional processes (Valley)

Length of season Local processes (Field)

of regional Changes in season length Effect may host diversity affectPathogen: the utility of management Regional practices that depend on Regional disease inoculum load severity reducing inoculum load at a local level Local disease Pathogen: Local inoculum load severity

Environment: Regional environmental conduciveness to disease during season

Host: Regional host susceptibility

Effect of local host diversity Environment: Local environmental conduciveness to disease during season Host: Local host susceptibility

Garrett, Zuniga, Roncal, Mundt, Forbes, Su, and Nelson

An Allee effect may produce thresholds for pathogen reproduction Results for Tilletia indica, causing Karnal bunt of wheat
(Garrett and Bowden 2002; Garrett, Sharma, Tang, Yang and Bowden, in preparation)

1.2 Infected kernels (Proportion of maximum)

b
1 0.8 0.6

b
spray

syringe

c a a d e a

0.4 0.2 0 0

50000

100000

150000

200000

Inoculum concentration

An Allee effect may produce thresholds for pathogen reproduction Results for Tilletia indica, causing Karnal bunt of wheat
(Garrett and Bowden 2002; Garrett, Sharma, Tang, Yang and Bowden, in preparation)

1.2 Infected kernels (Proportion of maximum)

b
1 0.8 0.6 0.4 0.2 0 0

b
spray

syringe

c Changes in processes at small a pathogen population sizes may a d on pathogen have major effects dispersal and establishment e a
50000 100000 150000 200000

Inoculum concentration

Outline
Plant disease and ecosystem services The usual challenges for managing plant disease Implications of climate change Potential interactions and thresholds Responding to climate change

Consistent support for plant disease research spanning from basic to applied is needed in order to manage plant disease well - with or without new challenges from climate change

Research needs I
Better understanding of gene expression in plants and pathogens in response to climatic factors Integrated omic studies of host and pathogen responses, as well as communities of soil and plantassociated microbes Multifactor studies of climate change effects

Research needs II
Better models of adaptation rates Better data and models related to dispersal, current levels of intraspecific diversity, strength of selection under different climate change scenarios, and heritability of traits

Research needs III

Long-term large-scale records of pathogen and host distributions Models of regional processes that incorporate disease Data and models describing dispersal of propagules and vectors Integrated multi-disciplinary international networks for data collection and synthesis

US National Plant Diagnostic Network

Implemented in part in response to concerns about bioterrorism Will enhance our ability to respond to plant disease Needs to be linked with global networks

Need for genetic resources to respond to changing climates

International institutions such as the CGIAR center network, with responsibility for maintaining and characterizing plant genetic resources, generally have shoestring budgets

Orphan crops such as quinoa, cassava, sweet potato, millets, and teff are of particular regional importance but receive relatively little research attention (Nelson et al., 2004). In tropical regions where food security is a particular concern, there may be greater climate variability and uncertainty combined with less investment in technologies to support crop production.

Quinoa variety trial in Bolivia

Photo: P. Motavalli

Conclusions
Plant disease has a major impact on agricultural and natural systems Current strategies for management need to be maintained and improved, even if the climate did not change Climate change will increase some disease risks and decrease others The effects of climate change will be most important when thresholds and interactions occur to produce unanticipated large responses Systems may change more rapidly than in the past, requiring more research and policy attention

Acknowledgements
US-NSF, USDA, US-DOE, USAIDSANREM, USAIDIPM, NCEAS Ecological Genomics Jianfa Bai Erin Frank Mike Herman Scot Hulbert Loretta Johnson Alan Knapp Jan Leach George Milliken Amgad Saleh Pat Schnable Mendy Smith Steve Travers NCEAS Plant Disease & Ecosystem Services Group Melissa Cheatham Severo Cardenas I. Greg Forbes Tom Gordon Willy Pradel Rubi Raymundo Matthew Rouse Adam Sparks And many other collaborators

Disease Ecology Helen Alexander Bob Bowden Shauna Dendy Phil Fay Greg Forbes Greg Gilbert Shaun Hutchinson Peg Margosian Chris Mundt Rebecca Nelson Sunny Power Rubi Raymundo Erminia Roncal Indu Sharma Zhaohui Su Zhongwen Tang Corinne Valdivia Nollie Vera Cruz Cam Webb Kim With Noemi Zuniga

Postdoc position

Mean proportion plants diseased at Konza Prairie Biological Station

0.16 0.14 0.12 0.10 0.08 0.06 0.04 0.02 Upland Lowland

2002

2003

2004

2005

Proportion of P

0.00 (39, 116) (24, 37, 55, 69) (30, 50, 71) (50)

Days After June 1 of Each Year