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Potential reinforcing role of earthworm species in plant resistance to parasitic nematodes

April 15, 2005

Parasitic nematodes of plants are microscopic soil-inhabiting organisms. Although they are present in all crop-growing areas, whether in the tropics or under temperate climes, it is predominantly in the tropical regions that these parasites perpetrate extensive damage and crop-yield losses. Market-garden produce, banana, sugar cane and rice are particularly prone to attack.
Chemical control strategies based on regular use of nematicides are to date still the usual recommended means of combating these pests. However, the products are costly, toxic for those who use them and harmful to the environment. Many of them are in any case being taken off the market, which intensifies the need to find other control strategies that are effective and carry no risk for either the users or the environment.
An alternative does present itself, according to IRD researchers and their partners (1). This is to be found among the soil fauna, although their precise role in plant-parasite interactions is still not clear. However, new results from experimentation by that team on the effect of certain earthworm species on the development of nematode-parasitized rice plants showed that these worms enable the plants to grow, in spite of still having substantial nematode populations in their roots. The damage usually caused to these crops is thus counteracted in some way.

The nematode species considered in this study, Heterodera sacchari, comes from rice-fields in the central region of the Ivory Coast. Earthworms of the species Millsonia anomala, originating from the same region, were used for introduction into the experimental system.
That nematode was chosen because it is strongly pathogenic for rice. The infesting larvae penetrate the rice-plant root system and colonize there. Salivary secretions from the young parasites alter root cells, which modifies the root metabolism for the benefit of the larvae's nutrition. The altered cells undergo excessive growth, or hypertrophy, which blocks the plant's sap-conducting vessels. The plant's supply of water and minerals is therefore cut off and the plant withers. Yield losses ranging from 20 to 50 % have been recorded in infected rice fields.

The research team compared the growth, over a 90-day cycle, of rice plantations placed under four different experimental regimes : without either nematodes or worms (control); with nematodes but no worms; with worms but no nematodes; with a mixture of both, introduced together into the experimental system. The photosynthetic activity was measured and gene-expression analysis was performed on several genes involved in the plant defence mechanisms, in order to assess the impact of the presence of earthworms on the parasite-infested rice.
When planted rice is subjected to nematodes only, the plants' photosynthesis declines and is practically obliterated by the end of a 90-day growing cycle. This leads to a loss of about 82 % plant dry weight. In contrast, this decrease does not occur when the earthworms and nematodes are introduced simultaneously. The presence of worms therefore counteracts the harmful effects of the parasites and allows the plant to grow normally, even though there is no reduction in the number of these parasites in the roots.
Certain genes in the rice phenotype, known as stress genes, are observed to change their expression in response to the earthworms' presence. The gene controlling the plant immune responses is indeed over-expressed. The worms appear to alter the plant's physiology by stimulating its defence mechanisms.

The earthworms therefore appear to exert some kind of action on the rice plant, directly or indirectly, and on its ability to minimize or even knock out the nematodes' pathogenic effect. Two main hypotheses have been proposed to explain the mechanisms involved. The first suggests that the worms' presence in the rice root system changes the composition and activity of microbe populations, inducing them to secrete growth hormones, liberate mineral nitrogen or to damage the nematodes' chemical receptors. These changes disturb the nematode larvae's root-location sensor mechanisms, reducing their ability to invade roots and holding back infestation until the rice is at a more advanced development stage. Such processes would thus dampen the virulence of the nematode pathogenic effect.
The second hypothesis envisages the earthworms acting on the plant by physical contact with the roots or by modifying the microbial environment. The general defence mechanisms of rice against attacking organisms would therefore be stimulated, leading to a reduction and delay in the nematodes' invasion of the root system.

The activity of earthworms and of belowground macrofauna as a whole, which is effective in the protection of plants against parasites, also keeps soil-system processes in good working order. This is particularly so for carbon fixing, retention and storage of water and the maintenance of a wide diversity of microscopic species. Only farming practices that involve input of organic matter and restrict ploughing and the use of chemically-based dressings can preserve this useful soil macrofauna.

(1) This research is conducted jointly by soil-fauna specialists and ecophysiologists in the IRD mixed research unit 137 " Biodiversité et fonctionnement du sol " (IRD-Universities of Paris VI and Paris XII), along with nematode specialists from IRD research unit UR 141 " Diversité et génomes des plantes cultivées " and Jérôme Tondoh, of Abobo-Adjamé University in the Ivory Coast.

Marie Guillaume -DIC
Translation : Nicholas Flay



Institut de Recherche pour le Développement, Paris (IRD)