Transcript Successful Parasitism by Plant

Successful Parasitism by Plantparasitic Nematodes
Suppression of Plant Defenses
by Nematodes
Biotrophic Pathogens
Pathogens that can only feed on a living host and must keep the host and its cells alive are
termed biotrophic pathogens.
Sedentary ecto- and endoparasitic nematodes are in this category, for example, species of
Meloidogyne, Heterodera, Xiphinema, Tylenchulus, Rotylenchulus.
Nematodes that withdraw contents from individual cells and then move to new feeding
sites are considered cell grazers.
Innate Immunity
Most plants are resistant to most pathogens; they have highly effective immune systems.
Host defense mechanisms may be as extreme as programmed cell death, the hypersensitive
response.
All biotrophic pathogens must suppress host defenses. The feeding site must be induced
without host detection or without induction of host defenses.
Following establishment of the feeding site by sedentary nematodes, it must be maintained
for up to 5 or 6 weeks to allow the nematode to achieve its reproductive potential. That time
scale is much greater than that required by many bacterial and fungal pathogens of plants.
Failure to establish and maintain the feeding site may prevent reproduction and therefore is
catastrophic to the nematode genotype. Consequently, there is strong selection pressure on
nematodes to suppress host defenses.
Plant Defenses
a. Pre-existing Defenses – Basal Resistance
Structural – cuticle, wax, wall thickness, spines that suppress penetration of cells.
Chemical-phenolic and other compounds that inhibit or kill invading organisms.
b. Systemic Induced Resistance
(i) PAMP Signals
Organisms attempting to feed on plant cells, or to invade plant tissues, betray their presence
with recognizable molecular signals on their surfaces. Such signals are termed pathogen
associated molecular patterns (PAMPs) and are recognized by pattern recognition receptors
on cell surfaces.
Chitins in fungal cell walls are PAMPS which trigger immunity responses (pathogen-triggered
immunity – PTI). The PAMP signals of nematodes are unknown; chitin is not present in the
cuticle although it does occur in egg shells and perhaps in the stylet.
(ii) DAMP Signals
Another set of signals that may trigger PTI responses in plants are cell-degradation products
resulting from damage caused by the invasion, damage-associated molecular patterns
(DAMPs).
(iii) The Defense Mechanisms
Plants characteristically deposit callose to strengthen cell walls at the point of invasion,
including at the point of nematode stylet insertion.
PAMP-triggered PTI, the first line of defense, may involve production of salicylic acid (SA) as a
signal to invoke defense mechanisms including callose thickening of cell walls and suppression
of active oxygen defense responses (H2O2, superoxide) which may initiate localized
programmed cell death – the hypersensitive response.
Also, pathogen invasion triggers the jasmonic acid signaling pathway (JA) which stimulates
production of protease inhibitors and the release of toxins.
Induced Resistance
JA = jasmonic acid
SA = salicylic acid
ISR = Induced Systemic Resistance
SAR = Systemic Acquired Resistance
PR = Pathogenesis-Related genes
> peroxidase and catalase
Effector Suppression of Plant Defenses and PTI
Invading bacteria and fungi, and probably nematodes, release effector molecules into plant
cells to suppress PTI and render the plant susceptible to infection or invasion.
PAMP-triggered PTI may result in production of salicylic acid (SA) as a signal to invoke defense
mechanisms. In that case, successful nematode infections would involve suppression of SA
production, reduction of callose thickening of cell walls and suppression of active oxygen
defense responses (H2O2, superoxide), and the hypersensitive response of localized
programmed cell death.
SA signaling is possibly disrupted by chorismate mutase produced in the esophageal glands. In
the PTI signaling pathway, chorismate is converted to salicylic acid. Chorismate mutase from
the nematode reduces chorismate and thus SA, so defense mechanisms are not triggered.
Incidentally, like cellulases, chorismate mutase is an example of horizontal gene transfer from
bacteria. Nematodes are the only metazoan with the enzyme.
An alternative mechanism of PTI suppression by nematodes is the production of effectors
which cause ubiquitin to attach to plant signal proteins and thus reduce their levels and
effectiveness in triggering PTI responses.
the evolution of plant parasitism
Rhabditoidea
Cephaloboidea
horizontal gene transfer- HGT
cellulases – GHF5- glycoside hydrolase family
chorismate mutase
bacteria
Tylenchoidea
the evolution of plant parasitism
Aphelenchoidea
fungus
Bursaphelenchus xylophilus
horizontal gene transfer- HGT
cellulases – GHF45- glycoside hydrolase family
Note: GHF5 glycoside hydrolases are expressed in Aphelenchoides fragariae when feeding on plant tissue; the
expression decreases x1800 when transferred to fungus for several generations (Fu et al., 2012).
The Evolutionary Response: Effector-triggered Immunity
The evolution of effector suppression of PTI has resulted in evolution of immune receptors,
with a nucleotide-binding domain and a leucine-rich domain (NB-LRR), in plants that
recognize the effector molecules and activate effector-triggered immunity (ETI).
However, successful pathogens have evolved next-generation effectors that suppress ETI.
Plants have responded with more specific ETIs and the evolutionary treadmill continues.
PTI responses to PAMPs and DAMPs are relatively general in their effect but higher level
ETIs are progressively more specific to individual pathogens.
The cyclical evolutionary process of plant-nematode interactions with regard to plant
immunity and susceptibility is depicted by the zig-zag-zig model (Jones and Dangl, 2006).
Initially PAMPs trigger PTI which reduces susceptibility. Then nematodes develop effectors
that suppress PTI and plants evolve immunity responses to the effectors.
Mechanisms of Effector-triggered Immunity and Effector-triggered Susceptibility
The sources of specific ETIs are resistance genes. The hypersensitive response of cells to the
activated ETI effectively disrupts the feeding and development of sedentary endoparasitic
nematode species.
The Mi gene of tomato codes for receptors to the effector molecules introduced by root-knot
nematodes that would otherwise suppress plant defenses and facilitate the development of
feeding sites.
Examples of ETS genes and products include:
• The Hg30C02 effector protein of Heterodera glycines which may be involved in active
suppression of host defenses. Hg30C02 specifically interacts with a plant ß-1,3endoglucanase (Hamamouch et al., 2012).
• The Mi8D05 parasitism gene of Meloidogyne incognita which peaks in expression in the
parasitic J2 stage of M. incognita when induction and early formation of giant-cells
occurs. The gene encodes a protein of 382 amino acids which is located in the subventral
gland cells of M. incognita J2 and is probably secreted into host plant tissues. RNA
interference tests using a double-stranded RNA complementary to Mi8D05 reduced by 90%
M. incognita infection of Arabidopsis (Xue et al., 2013).
Suppression and Avoidance of Host Defenses
Nematodes are protected by the cuticle and surface coat.
The surface coat of lipid and protein molecules is shed as the nematode moves, shedding
bacteria but also confusing the plants as to its whereabouts.
Glutathione peroxidases on surface coats of nematodes reduce active oxygen plant
defenses.
Many plant-parasitic nematodes produce glutathione S tranferases that detoxify
endogenous toxic molecules.
Nematodes also produce superoxide dismutase that breaks down active oxygen plant
defenses
References
Fu, Z., Agudelo, P., Wells, C.E. 2012. Differential expression of a β-1,4-endoglucanase induced by diet change in the foliar nematode
Aphelenchoides fragaria. Phytopathology 102:804-811.
Hamamouch, N., Li, C., Hewezi, T., Baum, T.J., Mitchum, M.G., Hussey, R.S., Vodkin, L.O., Davis, E.L. 2012. The interaction of the novel 30C02
cyst nematode effector protein with a plant b-1,3-endoglucanase may suppress host defence to promote parasitism. Journal of Experimental
Botany.
Huang, G., Dong, R., Allen, R., Davis, E.L., Baum, T.J., Hussey, R.S. 2005. Two chorismate mutase genes from the root-knot nematode
Meloidogyne incognita. Molecular Plant Pathology 6:23-30.
Jones, J.D.G, Dangl, J.L. 2006. The plant immune system. Nature 444:323-329.
Jones, J.T., Gheysen, G. and Fenoll, C. (eds) 2011. Genomics and molecular genetics of plant-nematode interactions. Springer Academic
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Jones, J.T. 2012. Lectures in the EUMAINE program, University of Ghent.
Jones, J.T., Furlanetto, C., Bakker, E., Banks, B., Blok, V., Chen, Q., Phillips, M. and Prior, A. 2003. Characterization of a chorismate mutase from
the potato cyst nematode Globodera pallida. Molecular Plant Pathology 4:43–50.
Lambert, K.N., Allen, K.D. and Sussex, I.M. 1999. Cloning and characterization of an esophageal-gland-specific chorismate mutase from the
phytoparasitic nematode Meloidogyne javanica. Molecular Plant-Microbe Interactions 12:328–336.
Smant, G., Jones, J. 2011. Suppression of plant defences by nematodes. Chapter 13, pp 273-286. In Jones, J., Gheysen, G., Fenoll, C. (eds).
Genomics and Molecular Genetics of Plant-Nematode Interactions. Springer, NY.
Xue, B., Hamamouch, N., Li, C., Huang, G., Hussey, R.S., Baum, T.J., Davis, E.L. 2013. The 8D05 parasitism gene of Meloidogyne incognita is
required for successful infection of host roots. Phytopathology 103:175-181.