Nematodes and Plant Damage

Rev 10/30/2019

 


Function of roots

Terrestrial plants are estimated to have annual production of 120 billion tons of biomass - 5% minerals = 6 billion tons of minerals mined from the soil each year.
 

A plant may transpire its own weight in water in a day.
 

The integrity of Casparian strip (waxy layer around endodermis cells) is important - nutrients, and sometimes water, are taken up against a gradient.

Secondary roots and endoparasites are disruptive to the Casparian strip.


Components of Damage

A. Demand

Total energy consumption during the lifecycle of a female root-knot nematode (Meloidogyne spp.) is 1 calorie.

The total biomass of a female root-knot nematode is 200 g, including the egg mass (Melakerberhan and Ferris).  For say 100,000 nematodes in a root system, the total nematode biomass is 20 g! Allowing for 50% production efficiency, total material extracted from the plant would be 40 g. So, the demand effect on the plant may be minimal unless plant is very stressed and resources are limited.

An adult Heterodera schachtii consumes 11 nL/day of cell content (Muller et al, 1981).  So, it would take 1,000,000 such females to remove 11 ml of cell content in a day.

B. Mechanical Disturbance

a. Penetration of cells - relative to length of stylet. Damage will depend on types of cells affected - storage tissues, cortex, or functional vascular.

b. Migration through tissues - intercellular and intracellular requiring dissolution of cell walls, middle lamellae. Suggests cellulase and pectinase enzymes - spongy tissues, sloughing, e.g. damage caused by Pratylenchus and Ditylenchus.  Allows ingress of other organisms.  Root-knot (Meloidogyne spp.) and cyst (Heterodera spp.) produce endogluconase (cellulase) enzymes and pectate lyase which are presumable involved in the passage through plant tissues.

c. Leakage from damaged tissues - it is estimated that up to 20% or more of photosynthate partitioned to roots may leak into rhizosphere soil without root damage. "Root exudation" nurturing organisms in rhizosphere - presumably to plant benefit - but speculate that selection has optimized the costs and benefits. Enhancing root leakage through nematode damage must reduce plant productivity.

C. Physiological Disturbance

a. Nematode secretions - associated with establishment and maintenance of feeding sites. Effects increase with sedentary endoparasitism.  Secretions from the nematode digestive glands may polymerize into a feeding tube inside the cell.  The feeding tube remains associated with the stylet during ingestion.  When the stylet is withdrawn the opening in the cell wall is sealed with an electron-dense feeding plug.

b. Physiological effects -  

c. Whole-plant effects - Disturbance of the biochemical network. Wallace (1987) points to the complexity of the biochemical pathways:
Photosynthesis divided into two basic phases - a light phase when light energy is converted into chemical energy, and a synthetic phase in which carbohydrates are formed in a series of reactions accelerated by light. Photosynthesis involves a chain of metabolic events cross-linked to other physiological processes, so disruption of one may have effects throughout system.
For example, Bird suggested that photosynthesis is reduced in tomato by
Meloidogyne javanica by inhibiting production of cytokinins and gibberellins in roots, and/or by increased stomatal resistance due to water stress.
Fatemy et al. indicate that the response of potato to
Globodera rostochiensis is due to stomatal closure through water stress; the result is reduced photosynthesis.
However, generally the mechanisms by which root-infecting pathogens, including nematodes, affect physiological processes have been insufficiently studied.

d. Plant as an Integrator - Metabolic pool concept - plant as an integrator - concepts of demand and damage. Melakeberhan and Ferris characterized five effects of root-knot nematode infection in grape while exploring the impact in an energy partitioning and flow model:

D.  Molecular Events:

Successful Parasitism by Plant-parasitic Nematodes

Suppression of Plant Defenses by Nematodes

(Powepoint overview

Biotrophic Pathogens

 Innate Immunity

Plant Defenses

  1. Pre-existing Defenses – Basal Resistance

a.    Structural – cuticle, wax, wall thickness, spines that suppress penetration of cells.

b.    Chemical-phenolic and other compounds that inhibit or kill invading organisms.

    2.  Systemic Induced Resistance

  1. PAMP Signals

    b. 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).

 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, the first line of defense, may involve 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) which may initiate localized programmed cell death – hypersensitive response.

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 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. 

One possible candidate is the Hg30C02 effector protein of Heterodera glycines which may be involved in active suppression of host defenses (Hamamouch et al., 2012).  

Another is the 8D05 parasitism gene of Meloidogyne incognita which is required for successful infection of host roots.  The gene codes for a protein that is secreted from the subventral glands duriing initiation of the feeding site (Xue et al., 2013).

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.

 

 

The Evolutionary Response: Effector-triggered Immunity (ETI)

In effect, the sources of specific ETIs are resistance genes.  Thus, the Mi gene of tomato codes for receptors to the effector molecules introduced by root-knot nematodes to suppress plant defenses and, perhaps, facilitate the development of feeding sites. 

However, although they are known for some other pathogens, the nematode effector molecules that trigger ETIs have not yet been determined and are the focus of several active research programs.

Although the nature of nematode effector products has still to be determined, the hypersensitive response of cells to the activated ETI effectively disrupts the feeding and development of sedentary endoparasitic nematode species.

 

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 reduce active oxygen plant defenses.

Many plant-parasitic nematodes produce glutathione S tranferases that detoxify endogenous toxic molecules.  They also produce superoxide dismutase that breaks down active oxygen plant defenses.

A recent (2011) compilation of the understanding of actions of Nematode Effector Proteins in host plant cells

The above compilation by Gheysen and Mitchum (2011) is based mainly on research on cyst and root-knot nematodes.

 

Cell wall degrading enzymes (CWDEs) and chorismate mutase are secreted by both root-knot and cyst nematodes while 16D10 is specific for root-knot nematodes.

Effector proteins originating from the subventral and dorsal esophageal gland cells are secreted into plant tissues through tthe nematode stylet.

  • CWDEs facilitate nematode migration through root tissues.

  • Effector proteins containing a nuclear localization signal affect the plant nucleus.

  • Nematode secreted ubiquitin extension proteins may alter cellular protein degradation pathways or function as signaling molecules.

  • Chorismate mutase changes the subcellular balance of chorismate.

  • Upregulation of the auxin influx transport proteins, AUX1 and LAX3, and downregulation of PIN1 leads to a local accumulation of auxin (IAA) in the initial feeding cell.

  • Relocalization of PIN3 to the lateral plasma membranes delivers auxin to adjacent cells.

  • LAX3 regulates auxin influx in adjacent cells stimulating cell wall hydrolysis for subsequent incorporation into the developing feeding site.

  • Other putative nematode effectors  include proteases, venom-allergen proteins (VAPs),calreticulin, MAP-1, RBP-1, and NodL.

Synopsis from Gheysen and Mitchum (2011).

E. Evolutionary Events:

The genome of plant-feeding nematodes of the sub-order Tylenchina includes genes that encode for endoglucanases. Endogluconases are cellulases, a family of enzymes formerly thought to be restricted to prokaryotes. Other plant-cell wall digesters such as termites and ruminants use symbiotic and commensal bacteria to achieve dissolve cellulose.  The presence of these and other genes suggests that horizontal or lateral gene transfer has occurred between bacteria and nematodes.

 

F.  Proof of pathogenicity:

Koch, Pasteur - the germ theory - required rules of proof.

Mountain provided guidelines for obligate parasite nematodes:

Predisposition

Interaction with other organisms

Note - term "interaction" is loosely used - implies that effect in combination is different than sum of individual effects - not additivity. Three descriptions of the result of combinations of organisms: -synergistic, -suppressive, -no interaction.

Mechanisms of interactions

        Synergistic:

        Suppressive:

Importance of Nematodes in World Agriculture

See Sasser and Freckman in Vistas on Nematology.
Questionnaires returned by 371 nematologists worldwide (handout with Tables 2 and 3)
Consider inherent biases in data of this kind.
Consider means and variance in crop loss data.
- almost nobody had 10% yield loss
- include management costs as part of the loss

Ranking of important genera and relative weight:

Genus

Relative Damage Importance

Meloidogyne 1.00
Pratylenchus 0.57
Heterodera 0.44
Ditylenchus 0.18
Globodera 0.19
Tylenchulus 0.17
Xiphinema 0.15
Radopholus 0.12
Rotylenchulus 0.10
Helicotylenchus 0.09

Note - considerable variation by region, so questionnaire data biased by number of respondents per region.

International Survey of Crop Losses due to Nematodes

Life-sustaining Crops

Annual Loss (%)

Economically-important Crops

Annual Loss (%)

Banana

19.7

Cacao

10.5

Barley

6.3

Citrus

4.2

Cassava

8.4

Coffee

15.0

Chickpea

13.7

Cotton

10.7

Coconut

17.1

Cowpea

15.1

Corn

10.2

Eggplant

16.9

Field bean

10.9

Forages

8.2

Millet

11.8

Grape

12.5

Oat

4.2

Guava

10.8

Peanut

12.0

Melons

13.8

Pigeon pea

13.2

Misc. other

17.3

Potato

12.2

Okra

20.4

Rice

10.0

Ornamentals

11.1

Rye

3.3

Papaya

15.1

Sorghum

6.9

Pepper

12.2

Soybean

10.6

Pineapple

14.9

Sugar beet

10.9

Tea

8.2

Sugar cane

15.3

Tobacco

14.7

Sweet potato

10.2

Tomato

20.6

Wheat

7.0

Yam

17.7

 

 

 

 

Average

10.7%

Average

14.0%

 

Overall Average 12.3%

 

 

 

 

 

Information based on a worldwide survey with 371 responses.

Source: Sasser, J.N., Freckman, D.W., 1987. A world perspective on Nematology: the role of the society.  Pp 7-14 in J.A. Veech and D.W. Dickson (eds) Vistas on Nematology. Society of Nematologists, Hyattsville, Maryland. 509p.

 Crop losses - measurement and estimates

Estimated Crop Losses 2008

Crop Number of estimates per crop FAO production estimates (1000 metric tons) Estimated price per metric ton -2008 (U.S.$) Estimated yield losses due to nematodes (%) Estimated monetary loss due to nematodes - 2008 (x1000 U.S.$)
Banana 78 81,263 928 19.7 14,855,056
Barley 49 136,209 238 6.3 2,044,978
Cassava 25 228,138 175 8.4 3,353,629
Citrus 102 105,000 711 14.2 10,601,170
Cocoa 13 4,012 2,693 10.5 1,134,626
Coffee 36 7,742 1,915 15 2,223,425
Corn 125 637,444 183 10.2 11,895,929
Cotton (lint only) 85 112 1,040 10.7 12,463
Field bean 70 6,371 1,200 10.9 833,327
Oat 37 25,991 117 4.2 127,327
Peanut 69 30,670 1,470 12 5,410,188
Potato 141 321,736 264 12.2 10,362,473
Rice 64 432 624 10 26,957
Sorghum 53 64,589 59 6.9 262,942
Soybean 91 56,389 339 10.6 2,024,967
Sugar beet 51 247,878 47 10.9 1,258,234
Sugar cane 65 1,557,664 36 15.3 8,462,835
Sweet potato 67 126,299 407 10.2 5,242,210
Tea 16 3,871 282 8.2 89,637
Tobacco 92 6,326 6,600 14.7 6,137,485
Wheat 89 676,300 237 7 11,237,807
Sources:
http://www.fas.usda.gov/wap/circular/2008/08-09/productionfull09-08.pdf
http://usda.mannlib.cornell.edu/usda/current/PeanPrice/PeanPrice-10-10-2008.pdf
http://usda.mannlib.cornell.edu/usda/current/CropProdSu/CropProdSu-01-11-2008.pdf
http://www.nass.usda.gov/Publications/Ag_Statistics/2008/index.asp

References:

Bird, A.F.

Davis. E.L., R.S. Hussey, T.J. Baum, J. Bakker, A. Schotts, M.N. Rosso and P. Abad. 2000. Nematode parasitism genes.  Ann. Rev. Phytopathol. 38:365-396.

Dropkin, V.

Garrett

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 Hg30C02 cyst nematode effector protein with a plant b-1,3-endoglucanase may suppress host defence to promote parasitism.  Journal of Experimental Botany.

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.

Jones, J.D.G, Dangl, J.L. 2006. The plant immune system. Nature 444:323-329.

Jones, J. 2012.  Lectures in the EUMAINE program, University of Ghent.

Gheysen, G.  1998.  Chemical signals in the plant-nematode interaction.  A complex system? In Romeo et al.  Phytochemical signals and plant-microbe interactions.

Gheysen, G. and Mitchum, M.G. 2011. How nematodes manipulate plant development pathways for Infection. Current Opinion in Plant Biology 14:415-421.

Hussey, R.S. and V.M. Williamson 1998.  Physiological and molecular aspects of nematode parasitism.  Agronomy Monograph 36.

Koenning, S.R.,  Overstreet, C., Noling,, J.W., Donald, P.A., Becker, J.O., Fortnum B.A. 1999. Survey of Crop Losses in Response to Phytoparasitic Nematodes in the United States for 1994.  Journal of Nematology 31:587-618.

Melakeberhan and Ferris

McClure

Muller et al, 1981

Sasser, J.N., Freckman, D.W., 1987. A world perspective on Nematology: the role of the society.  Pp 7-14 in J.A. Veech and D.W. Dickson (eds) Vistas on Nematology. Society of Nematologists, Hyattsville, Maryland. 509p.

Seinhorst

Wallace, 1986

Wyss U., F.M.W. Grundler and A. Munch. 1992. The parasitic behaviour of second-stage juveniles of Meloidogyne incognita in roots of Arabadopsis thaliana. Nematologica 38:98-111.

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