When enemies attack do plants get by with a little help from their friends?


  • Victoria A. Borowicz

    1. Behavior, Ecology, Evolution, and Systematics Section, Department of Biological Sciences, Illinois State University, Normal, IL 61790–4120, USA (tel +1 309 438 5208; fax +1 309 438 3722; email vaborow@ilstu.edu)
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Recognizing that mycorrhizal associations can alter plant physiology and allocation patterns leads to the question ‘What are the consequences of this partnership for plants and their enemies?’ Does the symbiosis reduce or exacerbate negative effects of pathogens or herbivores attacking a plant, that is, alter plant tolerance? Does the symbiosis make a plant more nutritious for pathogens or herbivores, or better defended against these antagonists, that is, alter resistance? These questions have been explored predominantly with crop plants and single arbuscular mycorrhizal fungus (AMF) isolates known to colonize the plants readily. Experiments with crop plants have provided significant insights into the mechanisms involved in plant-mycorrhiza–plant-pathogen interactions and have particular relevance for sustainable production of crops that can be inoculated with prepared AMF known to be effective mutualists (Pinochet et al., 1996; Harrier & Watson, 2004). However, studies with crop plants and selected single fungus isolates are not realistic representations of what happens in nature. Such studies are often conducted under conditions that bias results in favor of finding positive effects on plant growth. To understand the dynamics of a natural system it is important to pair plants with the suite of fungi they encounter in nature (Klironomos, 2003), whether or not the fungi are effective mutualists, and to conduct the experiment under conditions similar to those observed in the field. In this issue of New Phytologist de la Peña et al. (pp. 829–840) demonstrate how the AMF community can alter relationships between nematodes and the host plant, Ammophila arenaria, a dominant member of coastal dunes. In a pair of careful experiments they investigate the full range of interactions involving root symbionts, antagonists, and their host plant.

‘The negative interaction between AMF and nematodes may be eased or even eliminated when mycorrhizas are well established prior to challenge.’

In the shifting environment of dunes, sand accretion provides Ammophila arenaria with a zone for root growth free of root pathogens, including the root lesion nematode Pratylenchus penetrans (van der Stoel et al., 2002). This respite lasts only a few weeks before root antagonists colonize the rhizosphere and attack new roots. Failure to outrun nematodes and fungal pathogens reduces host vigor and is one explanation for eventual disappearance of A. arenaria (van der Stoel et al., 2002). However, Little & Maun (1996) demonstrated that sand burial is not the whole story for persistence of dune grasses, and suggested that AMF fungi are likely to be key players in this ecosystem. The experiments by de la Peña et al. continue this story.

Less tolerant, more resistant

Mycorrhizal fungi are generally assumed to increase plant growth, and this was the case in the first experiment by de la Peña et al. – but only in the absence of nematodes. This growth benefit from AMF was entirely negated when nematodes were added along with AMF (Fig. 1a). Such a negative interaction between AMF and nematodes suggests that AMF reduced plant tolerance, or the ability to regrow following damage (Strauss & Agrawal, 1999), a point that is missed if only main effects are examined. Improved plant growth with AMF is not, in itself, evidence of increased tolerance. The question is whether the damage caused by enemies is greater, the same, or less when plants are colonized by AMF. Here, that damage is greater. None the less, total biomass of AMF plants simultaneously infested with nematodes was similar to that of control plants (Fig. 1a), so AMF imposed no additional burden. Instead, gains in total biomass caused by AMF were eliminated if nematodes were present.

Figure 1.

Effects of sequential inoculation of Ammophila arenaria with arbuscular mycorrhizal fungi and Pratylenchus penetrans on (a) total dry mass (b) tiller production, and (c) plant nitrogen content. Data are means + SE. Nem, inoculation with nematodes only; AMF, inoculation with arbuscular mycorrhizal fungi (AMF) only; FN, inoculation with arbuscular mycorrhizal fungi and nematodes simultaneously; FN2, nematode inoculation 2 week after AMF; FN5, nematode inoculation 5 week after AMF. (Redrawn from de la Peña et al.)

Some of the mycorrhizal growth benefit removed by nematodes was restored when there was a sufficient lag between inoculation with AMF and subsequent challenge by nematodes (Fig. 1a). Certainly part of this effect could be the result of a briefer exposure to nematodes before harvest, or of greater age of roots when nematodes were finally added. However a greater lag time was also associated with reduced rate of nematode multiplication, which hints at the possibility that resistance mechanisms caused by nematodes had greater opportunity to kick in when AMF had a head start. In any event, nematode populations were lower in all AMF treatments, indicating that mycorrhizas increased host resistance to nematodes. Greater AMF benefit to plant growth, when nematode infestation lags behind AMF colonization, has been shown in other systems without a consistent association with increased resistance (Vaast et al., 1998; Talavera et al., 2001).

Although nematodes did not reduce total biomass of nonmycorrhizal plants, they did reduce tiller number, and again the effect of nematodes was more severe when AMF were added at the same time as the nematodes (Fig. 1b). Simultaneous colonization by AMF allowed nematode-infested plants to attain the same tiller production as nematode-free control plants, and greater tiller production than AMF-free, nematode-infested plants. By this measure, AMF reduced plant tolerance to nematodes, but still benefited plant growth. With sufficient lag time between colonization by AMF and challenge with nematodes, the negative interaction between nematodes and AMF disappears, yielding no effect of AMF on plant tolerance to nematodes.

In nature, AMF colonization may occur before or concurrently with nematode infestation (van der Stoel et al., 2002), and so this experiment provides a realistic estimate of the range of possible AMF effects on resistance and tolerance. Until nematodes arrive, AMF may increase A. arenaria growth. Once nematodes arrive, mycorrhizal plants may be more resistant to infestation, and this may have secondary effects. Pathology associated with nematodes is often a result of secondary infection by fungal pathogens that invade through wounds caused by nematodes, or are favored by changes in root exudates following nematode attack (van der Stoel et al., 2002). So AMF may reduce damage that leads to fungal infection, and may also stimulate resistance to fungal pathogens. This has implications for management. Restoration of beaches with seedlings preinoculated with resident AMF could give the plants two benefits during the establishment phase: (1) enhanced growth in the absence of nematodes; and (2) increased resistance to nematodes, and possibly fungal pathogens.

AMF–plant enemy antagonisms

Although the interaction between AMF and nematodes was negative or absent with respect to biomass, there was a pronounced positive interaction of AMF and nematodes on nitrogen content, with AMF increasing nitrogen concentration of the plant only when nematodes were present (Fig. 1c; de la Peña et al.). This inconsistency between the direction of interaction effects on plant growth vs biochemistry underscores the difficulty in identifying causes underlying antagonism between AMF and plant enemies. AMF can change plant chemistry, but causal connections between AMF colonization and effects on plant enemies, such as nematodes, have been devilishly difficult to resolve. Indirect effects mediated through the plant, such as changes in quality or quantity of the resource following AMF colonization, occur and may be expressed systemically or locally (Smith, 1988). Direct effects, such as pre-emption of infection sites, are another possibility. In a split-root experiment de la Peña et al. narrow the potential mechanisms of resistance to those acting locally. Nematode infection levels were reduced when roots were coinoculated with AMF and nematodes but not when AMF and nematodes occupied different subsystems of the roots, indicating that effects of AMF were chiefly induced locally rather than systemically. Interestingly, this suppressive effect of AMF on nematodes appears to be highly asymmetrical. In neither experiment did nematodes reduce root colonization by AMF. This is not unprecedented, but also it is not the usual pattern (Pinochet et al., 1996; Borowicz, 2001).

Is a negative interaction between AMF and nematodes, where growth reduction due to nematodes is greater when plants are mycorrhizal, unusual? Not really. This appears to be a common pattern for root-infecting nematodes (Borowicz, 2001), but de la Peña et al. demonstrate that the negative interaction may be eased or even eliminated when mycorrhizas are well established before challenge.

Future directions

Rather than a rare phenomenon, complex interactions among host plants, AMF, and root pathogens are likely to be the usual state of affairs, and de la Peña et al.'s study provides context for further investigation of these interactions. There is still much to learn about the dynamics in native populations of beach grass. For example, Kowalchuk et al. (2002) found differences in the AMF populations associated with vigorous vs degraded A. arenaria. Do effects of nematodes prompt succession in AMF communities, and result in reduced benefit to this host? Could succession in AMF communities heighten negative effects of nematodes? A. arenaria is host to several species of nematodes that differ in their effects on host growth and on each other (Brinkman et al., 2005a,b). Does the increased resistance conferred by AMF alter competitive relations among these nematodes?

A. arenaria is an invasive species in several parts of the world, including New Zealand, where its arrival has coincided not only with changes in plant community composition but also with physical structure of dunes (Hilton et al., 2005). Although escape from specialist nematodes may contribute to invasive success (van der Putten et al., 2005), invasiveness of beach grass cannot be fully explained by release from natural enemies (Beckstead & Parker, 2003). Other plant species may limit its spread via effects on root antagonists (Knevel et al., 2004). Host–symbiont–nematode interactions documented by de la Peña et al. support the argument that AMF effects must be included in investigations of plant communities if we are to understand conditions promoting invasion by A. arenaria, and also to understand invasiveness of plants in general (Klironomos, 2002; Bever, 2003; Wolfe & Klironomos, 2005).