Nematodes and Plant Damage

Rev 12/05/2007

Function of roots

• absorb water
• absorb nutrient ions
• storage
• anchorage
• dynamic mining function, regeneration.

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 µg, 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.

• Cell wall permeability and surface enlargement - transfer cells, cell wall thickening.
• Increase in cytoplasm density, metabolic activity.
• Hypertrophy - cell enlargement, 500 to 1000x increase in volume (Meloidogyne) - nuclear division without cytoplasmic division (karyokinesis without cytokinesis). But different strategies in different genera - eg cell wall dissolution in Heterodera. Multinucleate cells, nuclei larger.
• Hyperplasia - tissue enlargement - mitotic activity -galling, root tip galls etc.
• Disruption of normal meristem activity - Xiphinema, Trichodorus, Hemicycliophora (different taxonomic groups). Damage to meristems.
• Physiological control of carbohydrate partitioning - Metabolic sink - McClure, ¹⁴CO₂ studies.

b. Physiological effects -  

• increased root respiration (more mass), 
• increased growth respiration - repair, 
• mobilization of defense mechanisms.
• increased levels of plant hormones (indole acetic acid, cytokinins) in galled tissue, but source uncertain.

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:

• Reduction (disruption) of water uptake. Seinhorst, however, asserted that there is little evidence of reduction of water uptake in response to nematodes. He measured daily water uptake on a water usage basis - rate of water loss from pots minus increase in dry wt minus evaporation from surface. The rate was a linear function of total dry wt. So, he argued that rate of use per g tissue is constant. However, root damage could result in lower water uptake, and final dry weight could be a function of the rate of water uptake.
• Reduction in rate of photosynthesis.
• Reduced leaf expansion and total photosynthesis.
• Alteration of partitioning of photosynthate- change in root/shoot ratio.
• Increased leakage - direct effect and affect on other pathogens energy supply (Garrett - inoculum potential as a function of the abundance of infective units and the energy resources available to them).

D.  Molecular Events:

Plant responses to nematode indection (from various plant and nematode systems):

• Pathogenesis-related proteins (similar to those after fungal or viral infections) are induced.
• Non-local induction of proteinase inhibitor proteins occurs.
• Local and systemic induction of a gene encoding catalase occurs.  Catalase may protect the plant from oxidative stress associated with nematode feeding.
• Expression of a gene encoding extensins, which are hydroxyproline-rich glycoproteins that are components of plant cell walls.

Changes in gene expression at feeding sites is probably localized in a few cells.  Identifying the small amount of product is technically difficult.  Use of reporter genes such as GUS which can be attached to promoter regions of other genes are among useful new indicators of localized gene activity.

E. Evolutionary Events:

The genome of plant-feeding nematodes of the Order Tylenchida 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:

• - establish association - ecological phase
• - establish parasitic capabilities - biological phase
• - establish host-parasite relations - etiological phase

Predisposition

Interaction with other organisms

• a. other nematodes
• b. fungi
• c. bacteria
• d. viruses
• e. abiotic/physical stresses

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:

• Reduced tolerance - multiple stress
• Vectoring - Longidoridae and Trichodoridae
• Change in substrate - fungi?
• Routes of ingress - fungi, bacteria
• Leakage - energy source - fungi, bacteria

        Suppressive:

• Induced resistance - any examples?
• Reduction of stress - mycorrhizae
• Biological antagonists - but not an interaction of two pathogens
• Reduced substrate availability

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:

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

International Survey of Crop Losses due to Nematodes

 Crop losses - measurement and estimates

• - Problem of reference yield - how do you isolate one pest effect?
• - Need for holistic approach.
• - How to remove one stress from system without changing system.

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

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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