Fighting for their lives: Plants and

pathogens

Photos courtesy of CIMMYT, Scott Bauer, USDA Agricultural Research Service, IRRI, IRRI, IITA

Nematodes are

large,

multicellular

animals

Bacteria are

prokaryotes

Viruses are

non-cellular,

and merely

packaged

nucleic acids

Fungi and

oomyctes are

eukaryotes

Bacteria

Oomycete

Fungus Fungus

Many kinds of organisms

cause plant disease

Large, E.C. 1940. Advance of the Fungi. Jonathan Cape, London.

What makes an interaction into a

disease? (Disease triangle)

Plants are exposed to

countless microbes, but

very, very few of these

interactions lead to

disease. Why?

Environment

The disease

triangle

(it takes three)

The pathogen must

be able to overcome

plant defenses

The environment must

tip the balance in favor

of the pathogen

The host plant

must be

susceptible to

the pathogen

Humans influence diseases

Photos courtesy Scott Bauer and Bob Nichols, USDA, and Geovantage, Inc.

Monoculture

Introduced pathogens

and vectors

Growing

practices

Migrations

of people

and plants Humans add another

dimension (making a

disease pyramid….)

Strategies of pathogenicity

A successful pathogen must:

• Find the host and attach to it

• Gain entry through the plant’s

impermeable defenses

• Avoid the plant’s defense

responses

• Grow and reproduce

• Spread to other plants

Clemson University - USDA Cooperative Extension Slide Series, Bugwood.org

Gray mold (Botrytis cinerea)

Wind, water, insects and chemotaxis

help pathogens reach their hosts

Jim Plaskowitz, USDA, and Stan Diffie, University of Georgia

Pathogens must be able to penetrate

or circumvent physical barriers

Reprinted by permission from Macmillan Publishers Ltd: Giraldo, M.C., Valent, B. (2013). Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11: 800-814; Kleemann, J., Rincon-Rivera, L.J., Takahara,

H., Neumann, U., van Themaat, E.V.L., van der Does, H.C., Hacquard, S., Stüber, K., Will, I., Schmalenbach, W., Schmelzer, E. and O'Connell, R.J. (2012). Sequential delivery of host-induced virulence effectors by

appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog. 8: e1002643;

Appressorium

Some pathogens

produce non-

melanized but

effective

appressoria

Melanized

appressoria

build up high

pressure to

puncture the

cell wall

Some pathogens

enter through

stomata and grow

extracellularly

Pathogens are biotrophs,

necrotrophs or hemibiotrophs

Reprinted by permission from Macmillan Publishers Ltd: Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S. and Van Wees, S.C.M.

(2009). Networking by small-molecule hormones in plant immunity. Nat Chem Biol. 5: 308-316, copyright 2009.

Necrotrophs kill

cells and then

consume the

contents Biotrophs live

within host tissue

without causing

death

Hemibiotrophs can

switch from biotroph

to necrotroph

Summary - strategies of

pathogenicity

Pathogens must overcome

formidable plant defenses

Once inside the plant, they

can either co-habitate or kill

Plant immune responses

Plants resist pathogens

through active processes that

include recognition of the

pathogen and defense

responses to fight it

The zig-zag model of plant –

pathogen interactions

Adapted from Jones and Dangl (2006) The plant immune system. Nature. 444: 323-329.

Am

plit

ude o

f defe

nse

Low

High

Pathogen is

recognized:

Pattern

Triggered

Immunity

Effector is

“recognized”:

Effector

Triggered

Immunity

Pathogen effectors

suppress defense

response:

Effector Triggered

Susceptibility

Defense responses

Defense responses

How are pathogens recognized?

Pattern recognition receptors (PRRs)

Many PRRs have an

extracellular leucine-

rich repeat domain

that recognizes

conserved microbial

elements…..

….and an intracellular

kinase domain

They are leucine-rich

repeat receptor

kinases (LRR-RKs)

Bacterial pathogen

Fungal or

oomycete

pathogen

PRRs recognize

pathogens

outside the cell

and initiate

defense

responses

Pathogens produce effectors that

enhance their virulence

Kinase cascade

leading to

transcriptional

responses

Calcium

ion influx

Reactive

oxygen

production

Microbial

effectors

suppress the

plant’s immune

response and /

or contribute to

the pathogen’s

viability

enzymes

Some effectors alter plant behaviour

and development

Reprinted from Hogenhout, S.A., Van der Hoorn, R.A.L., Terauchi, R. and Kamoun, S. (2009). Emerging concepts in

effector biology of plant-associated organisms. Mol. Plant-Microbe Interact. 22: 115-122.

Resistance proteins – intracellular

immune receptors

effector

R protein

R protein

R proteins recognize

effectors intracellularly

Defense

responses

R protein activation leads to

enhanced defense: ETI

Adapted from Jones and Dangl (2006) The plant immune system. Nature. 444: 323-329.

Am

plit

ude o

f defe

nse

Low

High

PTI

ETI

Activated R proteins signal

danger, and trigger a heightened

defense response that includes:

• Production of the stress

hormone salicylic acid (SA)

• Production of reactive oxygen

species (ROS)

• The hypersensitive cell death

response (HR)

• Expression of pathogenesis-

related (PR) proteins

• Systemic signals and systemic

acquired resistance (SAR)

Summary - PTI is suppressed by

effectors, which sometimes trigger ETI

Effectors

suppress PTI

R proteins

recognize

effectors and

induce ETI

PAMP-triggered

immunity

Defense

Responses Defense

Responses

Effector-triggered

immunity

Defense

Responses

Effector triggered

suppression

Adapted from Macmillan Publishers Ltd: Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S. and Van Wees, S.C.M. (2009). Networking by small-molecule hormones in plant immunity. Nat Chem Biol. 5: 308-316,

Strategies to prevent and manage

disease

Environment

The disease

triangle

(it takes three)

Avoid or eliminate

the pathogen

Manipulate the

environment to favor

the plant

Make the plant

resistant through

genetic or other

methods

Photos by Photo by James Tourtellotte, US Customs and Border Protection : Keith Parker, Marin County Fire Department.

The best way to prevent disease is

to keep pathogens away

Agricultural inspectors check imported

plants for pest and pathogens, but

many pathogens are spread by wind

and water….

Phytophthora ramorum causes

sudden oak death

Pathogens’ effects can be minimized

by hygiene and rotation

Courtesy J.H. Graham (left) and G. Allen (right). Reproduced by permission from Maloy, O. C. (2005). Plant Disease Management. The Plant Health Instructor. DOI: 10.1094/PHI-I-2005-0202-01.

Rotating crops helps reduce

pathogen load in soils

Continuously

cultivated Rotated with corn

Removing and burning an infected citrus

grove to eradicate bacterial canker

Chemical controls are critical for

eradicating pathogens

Photos by Ken Hammond; J.K. Lindsey

Azostrobulin, a widely used

fungicide derived from a

defensive compound

produced by Strobilurus fungi

Compounds must

be safe and

effective, and

application

protocols must be

followed to slow

the development of

resistance

Because pathogens

develop resistance,

finding novel compounds

to eradicate pathogens is

an ongoing process

Biocontrol agents:

• attack the pathogen

• compete with the pathogen

• enhance the plant’s

defenses through induced

systemic resistance (ISR)

• often have multiple effects

Biocontrol refers to the

use of other organisms

to ward off pathogenic

microorganisms and

disease

Reprinted by permission from Macmillan Publishers Ltd: Haas, D. and Defago, G. (2005). Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Micro. 3: 307-319.

Biological control of

pathogens

Summary – strategies to prevent and

manage disease

Quarantines

Crop rotation

Good hygiene

Control of viral vectors

Biocontrols

Chemical

controls

• Adequate nutrition

• Well drained soils

• Genetic diversity to

avoid epidemics

• R-gene mediated

resistance

• Quantitative

disease resistance

• Enhancement of

immune and

defense responses

Weaken

pathogen

Separate plant

& pathogen

Strengthen

plant

Plants and Pathogens: Summary

• Plant diseases are major

threats to food production

• Pathogens have diverse

modes of pathogenicity and

rapidly evolving effectors

• Plants are not passive victims

- they have sophisticated

surveillance and defense

mechanisms

• Human practices, particularly

migrations and monocultures,

have contributed to the

magnitude of plant diseases