Fungal & Oomycete Pathogenesis
- According to Agrios, >8,000 species of fungi can cause plant disease
Latijnhouwers et al. 2003. Trends in
Microbiology 11:462-469
Topics for today
Mechanisms of pathogenesis
Effector functions
Uptake of effectors into host cells
Powdery mildew can suppress senescence
Can biotrophs help to keep their hosts alive?
Schulze-Lefert and Vogel. 2000, Trends in Plant Sci. 5:343-348
Question: If you were a typical fungus, what key
activities/functions might you need in order to
infect a susceptible host?
Would needs be different for biotroph versus necrotroph?
General mechanisms involved in pathogenesis
- Mechanical forces
Formation of appressoria and penetration of the host cuticle and cell wall
- Chemical weapons
Enzymes: cutinases, pectinases, cellulases, hemicellulases, ligninases
proteinases, amylases, lipases
Toxins:
non-host specific, host specific
- Growth regulators
auxins, gibberellins, cytokinins, ethylene, abscisic acid
- Polysaccharides
See chapter 3 of “Plant Pathology” by Agrios.
Examples of appressoria and
haustoria of fungi and Oomycetes
Features of appressoria of fungi:
- Adhere to plant surface
- Melanization
- High turgor pressures
- Form in response to appropriate signals
Magnaporthe grisea, 3M
glycerol, 8 MPa/1160 psi
Latijnhouwers et al. 2003. Trends in Microbiology 11:462-469
Signaling pathway leading to appressorium development in rice blast fungus
Caracuel-Rios & Talbot. 2007. Current Opinion in Microbiology 2007, 10:339–345
Plant surface cues induce gene expression changes in Ustilago maydis
DSM = sho1 msb2 mutant
Differentially expressed genes include:
Cell wall degrading enzymes
Effectors
Lanver. 2014. PLoS Pathog. 10:e1004272
Infection cycles of Ustilago maydis and Cladosporiuim fulvum
Okmen. 2014. Curr. Opin. Plant Biol. 20:19-25
Haustoria form contact between fungus and host
Panstruga. 2003. Curr. Op. Plant Biol. 6:320-326
Secretion of effectors into intercellular and intracellular spaces
Examples of fungal and oomycete effectors
Okmen. 2014. Curr. Opin. Plant Biol. 20:19-25
Cladosporium fulvum Avr4 binds to chitin
van den Burg. 2006. Mol. Plant Microbe Interact. 19:1420-1430
Avr4 prevents chitin hydrolysis by tobacco chitinase
van den Burg. 2006. Mol. Plant Microbe Interact. 19:1420-1430
Avr4 promotes growth of fungi in presence of chitinases
van den Burg. 2006. Mol. Plant Microbe Interact. 19:1420-1430
Ustilago maydis Pep1 suppresses defense responses
Hemetsberger. 2012. PLoS Pathog. 8:e1002684
Pep1 inhibits peroxidase activity and binds peroxidase 12 (POX12)
Hemetsberger. 2012. PLoS Pathog. 8:e1002684
Silencing pox12 promotes infection by pep1 mutant
Hemetsberger. 2012. PLoS Pathog. 8:e1002684
Over expression of Pi03192
increases P. infestans
virulence
Pi03192 interacts with two
NAC transcription factors
McLellan. 2013. PLoS Pathog. 9:e1003670
Silencing NAC transcription factors increases susceptibility to P. infestans
McLellan. 2013. PLoS Pathog. 9:e1003670
Silencing Pi03192 compromises
pathogenicity
Pathogenicity can be restored
by silencing NAC transcription
factors
McLellan. 2013. PLoS Pathog. 9:e1003670
Layers of interaction between U. maydis and C. fulvum with hosts
Okmen. 2014. Curr. Opin. Plant Biol. 20:19-25
Analysis of fungal genomes
- Secretome
- M. larici-populina – 1184 SSPs
- P. graminis – 1106 SSPs
- Effectoromics
Schmidt & Panstruga (2011) Curr. Opin. Plant
Biol. 14:392-399
Fungal and oomycete structures for effector secretion
Petre. 2014. PLoS Biol. 12:e1001801
The RXLR motif present in a large class of oomycete effector proteins
(Peronosporales – Phytophthora & downy mildews primarily)
Rehmany et al. 2005. Plant Cell 17:1839–1850,
RXLR is a conserved host targeting signal
Bhattacharjee et al. 2006. PLoS Pathog 2(5): e50
RXLR is followed by sequences enriched for amino acids E, D, & R
required for host targeting
Bhattacharjee et al. 2006. PLoS
Pathog 2(5): e50
Assays for detecting pathogen-independent entry of effectors
Kale and Tyler (2011) Cell. Microbiol. 13:1839-1848
PI3P binding mediates entry of RXLR effectors
Kate et al. (2010) Cell 142:284-295
Model for entry of fungal and oomycete effectors
Kale and Tyler (2011) Cell. Microbiol. 13:1839-1848
Controversy over model for entry of fungal and oomycete effectors
Ellis and Dodds (2011) Showdown at the RXLR motif: Serious differences of
opinion in how effector proteins from filamentous eukaryotic pathogens enter plant cells.
PNAS. 108:14381-14382
RXLR motif of AVR1b is not
required for PIP binding
Yaeno et al. (2011) PNAS
108:14682-14687
Wawra et al. (2012) Host-targeting protein 1 (SpHtp1) from the oomycete Saprolegnia
parasitica translocates specifically into fish cells in a tyrosine-O-sulphate–dependent manner
PNAS. 109:2096–2101
Avr3a triggers HR in plants expressing R3a resistance gene
Bos et al. 2006. Plant J. 48:165–176
AVR3a suppresses INF1-elicited cell death in N. benthamiana
Avr3a is a cell death suppressor
Different amino acids affect R3a HR and suppression of cell death
Bos et al. 2009. MPMI. 22:269-81
CRINKLER (CRN) type effectors are common in oomycetes
LXLFLAK translocation domain
Schornack et al. (2010) PNAS. 107:17421-17426
CHXC effector candidates represent a third delivery motif in oomycetes
Found first in
Albugo laibachii
Kemen et al. (2011) PLoS Biology. 9:e1001094
N-terminal effector domains proposed to mediate host-cell entry
Petre. 2014. PLoS Biol. 12:e1001801
Integrated process of effector translocation
Petre. 2014. PLoS Biol. 12:e1001801
Petre. 2014. PLoS
Biol. 12:e1001801
Hypothetical involvement of epigenetic mechanisms in pathogen invasion
Kasuga. 2013. Trends Micro. 21:575
Summary
Fungi and oomycetes have a variety of different lifestyles
Common themes in fungal signal transduction controlling development
and pathogenicity
Oomycetes and fungi can form appressoria and haustoria
Oomycetes and fungi can secrete a variety of effector proteins into
intracellular and intercellular spaces
Effectors perform functions in fungal walls, apoplast, and inside host cells
RXLR & dEER, LXLFLAK, and CHXC motifs mediate delivery into host cells
Controversy over mechanisms of entry mediated by RXLR – Question remains open
on how effectors enter host cells.