Herbivory is a common phenomenon in most natural habitats, while grazing cattle constitute a major part of the human food supply (Strauss & Agrawal, 1999). Herbivory entails a direct loss of resources and a reduction in future resource acquisition when roots or leaves are affected, and should be expected to negatively impact plant performance. Yet, even severe levels of herbivory may have relatively small effects on plant fitness and can even stimulate it (Paige & Whitham, 1987; Stowe et al., 2000). This indicates that plants have evolved compensatory growth traits that enable them to mitigate the negative effects of herbivory. Relatively little is known about these compensatory traits, their physiological regulation and their quantitative significance for plant performance. Research has focused on compensatory photosynthesis, shifts in branching patterns and pre-existing storage of carbohydrates. The results presented by Gómez et al. (pp. 835–844) in this issue of New Phytologist, however, suggest that plants may also respond to leaf damage through a shift in resource allocation by which nitrogen (N) is re-allocated from damaged leaves to the roots. They argue that N is thus safe from folivores and available for regrowth once the threat of herbivory has passed. Here, we discuss the documentation, physiological regulation and possible adaptive significance of this response.
‘Given the importance of tolerance in herbivory-imposed selection, more research is needed to quantify the physiological regulation and adaptive significance of moving resources away from the herbivore.’
Moving resources away from the herbivore
Several compensatory mechanisms by which plants can mitigate the negative effects of herbivory have been discussed in the literature, including: increases in leaf photosynthesis, activation of dormant buds, changes in the allocation of new assimilates, and the re-allocation of pre-existent stores of carbohydrates and other resources (e.g. Anten et al., 2003; Newingham et al., 2007). The last mechanism (i.e. the use of stored resources) is believed to be the most common compensatory mechanism in herbaceous plants (see Gómez et al.), but may entail lower performance in the absence of herbivory, as stored resources are not being deployed in other plant functions (Stowe et al., 2000).
Recent research has started to focus on rapid shifts in resource allocation immediately following the onset of herbivory (e.g. Babst et al., 2005, 2008; Schwachtje et al., 2006; Newingham et al., 2007; Gómez et al.). Measuring this type of short-term dynamics in resource allocation has been made possible through the application of radioisotopes (e.g. 11CO2 or 13NH3) to plants, in combination with strategically located sensors that measure radioactivity in different parts of the plant (Fig. 1). This method allows changes in allocation to be detected within minutes after herbivory takes place. It was found that both leaf herbivory and the application of either herbivore saliva or a defence elicitor (e.g. jasmonic acid (JA)) to leaves resulted in increased export of carbon (C) from leaves and that this C tended to be preferentially allocated towards the roots (Babst et al., 2005; Schwachtje et al., 2006). This response may be beneficial as it entails a re-allocation of resources away from the site of damage to a part of the plant that is relatively safe from herbivory.
Earlier work on herbivory-induced re-allocation of resources focused on C and did not consider N (Babst et al., 2005, 2008; Schwachtje et al., 2006). For many herbivores, N is the most limiting element in their diet, while in many growth environments, N is also the primary limiting growth factor (Stockhoff, 1994). Recently, however, several studies have documented shifts in N allocation either from roots to leaves upon root herbivory (Newingham et al., 2007) or from leaf to roots after application of the defense elicitor methyl jasmonate (MeJA) (Gómez et al.). Changes in N allocation appeared to be stronger than those in C allocation.
An important question is how this rapid response is regulated. As with many other tolerance-related traits, very little research has been carried out to unravel this mechanism. Re-allocation of sugars following herbivory might be regulated by changes in sink strength of different plant organs, which can be induced by the treatment of single leaves in Populus with JA (Babst et al., 2005) and may be associated with the well-documented control of photosynthesis and senescence by JA (Creelman & Mullet, 1997). Consistently, Gómez et al. also observed increased export of C from the leaves and increased transport of C towards the roots upon treatment with MeJA. However, in Nicotiana attenuata the herbivory-induced increase of C allocation to roots may be JA independent. Schwachtje et al. (2006) observed that herbivory by Manduca sexta larvae increased C allocation to roots and concomitantly stimulated the activity of sugar cleavage enzymes, believed to play a role in regulating sink strength, in roots. Importantly, this response was preserved in asLOX transgenic N. attenuata plants that have reduced wounding-induced JA levels and consequently have attenuated defence responses (Halitschke & Baldwin, 2003). Further studies are needed that combine herbivory, JA treatment and JA-deficient or JA-insensitive plants to show conclusively whether herbivore-induced changes in C allocation act through the JA pathway. Schwachtje et al. (2006) showed that an SNF1 (sucrose non-fermenting 1)-related kinase (SnRK1) is required for the herbivore-induced change of C allocation in N. attenuata using asGAL83 transgenic plants with silenced SnRK1 expression. Because SnRK1s are central regulators of cell-energy metabolism (Polge & Thomas, 2006), these findings tie herbivore-induced changes in C allocation to central cellular metabolic control. The molecular mechanism underpinning this regulation remains unknown, but probably does not involve the JA pathway because the observed change in C allocation is preserved in transgenic plants with reduced herbivore-induced JA accumulation (Schwachtje et al., 2006). With respect to the re-allocation of N from leaves to roots, Gómez et al. are the first to show that JA can induce this response. Further studies are required to identify whether this re-allocation still occurs during herbivore attack, and, if so, whether it occurs in a JA-dependent manner.
As already noted, it can be argued that sequestration of resources away from the site of damage in response to herbivory can be beneficial because these resources are spared and can be utilized for regrowth while at least partly preventing the costs associated with pre-existent storage. Yet, this response may also have detrimental effects and it is still unclear if, and under what conditions, it is adaptive. In the first place, this response would probably not work in the case of large herbivores that consume a large fraction of the plant in one or a few bites. Second, re-allocation of N from leaves in response to folivores might induce additional feeding to compensate for the lower nutritional quality (Gómez et al.). Finally, plants are often attacked by several different types of herbivores that may act both aboveground and belowground, which diminishes the reliability of re-allocating resources to another plant compartment (Dicke et al., 2009).
The ecological and evolutionary significance of compensatory traits can only be assessed by comparing the performance of a normal damaged plant with that of a noncompensating damaged plant (Anten et al., 2003). This is experimentally complicated because herbivory induces compensatory responses and thus prevents the noncompensating phenotype from occurring.
One possibility entails the use of genetically modified plants that are the same as wild-type plants in all respects except for one or more compensatory traits. Given the above-mentioned scant knowledge regarding the molecular and physiological regulation of compensatory traits, this option has rarely been used and we know of only one study (Schwachtje et al., 2006) that has taken this approach to analyse the adaptive significance of the rapid re-allocation of resources following herbivory. Schwachtje et al. (2006) compared the asGAL83 transgenic N. attenuata plants (mentioned earlier in this article) that exhibit a constitutive, enhanced C re-allocation from leaves to roots with wild-type plants that only show this response under herbivory and not when damaged artificially. In the absence of damage, asGAL83 plants had overall lower fitness but they performed better than wild-type plants when exposed to nonherbivore damage. These results suggest that the plastic response, whereby C is re-allocated from leaves upon herbivory, might indeed be adaptive.
In short, given the prevalence of herbivory in nature and the importance of tolerance in herbivore-imposed selection (Stowe et al., 2000), more research is needed to quantity the physiological regulation and adaptive significance of moving resources away from the herbivore, possibly along the lines depicted in Table 1.
Table 1. Putative agenda for research towards understanding the occurrence, the physiological regulation and the adaptive significance of the response whereby plants move resources away from damaged areas upon herbivory
We note that this list is by no means complete.
Further studies addressing whether nitrogen (N) re-allocation is stronger than carbon (C) re-allocation
Further assess the involvement of the jasmonic acid (JA) pathway
Further use of plant types genetically manipulated in key parts of the response
Document response in more species and growth forms
Unravel signal transduction components of herbivore-induced changes in C and N allocation
Analyses under natural conditions, for example, in the presence of both aboveground and belowground herbivory
Studying the potential occurrence and effects of additional feeding by herbivores