Getting sick may help plants overcome abiotic stress
Article first published online: 6 NOV 2008
© The Authors (2008). Journal compilation © New Phytologist (2008)
Volume 180, Issue 4, pages 738–741, December 2008
How to Cite
Rouhier, N. and Jacquot, J.-P. (2008), Getting sick may help plants overcome abiotic stress. New Phytologist, 180: 738–741. doi: 10.1111/j.1469-8137.2008.02673.x
- Issue published online: 6 NOV 2008
- Article first published online: 6 NOV 2008
- oxidative stress;
- reactive oxygen species (ROS)
In their environment, plants establish relationships with many microorganisms such as fungi, bacteria and viruses which can be either pathogens or symbionts. Common wisdom states that mutualistic/symbiotic associations are beneficial to the plant but pathogen associations deleterious. However, recent papers in New Phytologist by Xu et al. (this issue; pp. 911–921) and Baltruschat et al. (2008; issue 180 (2); pp. 501–510) underline the point that this view is perhaps too simplistic. In the case of pathogenesis, one possibility for the plant to prevent or minimize microbe infection is to generate an oxidative burst, the purpose of which is to kill bacteria and plant cells surrounding the infection site. However, recent data indicate that reactive oxygen and nitrogen species (ROS and RNS, respectively) are produced by both partners in many symbiotic and pathogenic systems (Delledonne et al., 2001; Tanaka et al., 2006; Baptista et al., 2007; Jones et al., 2007; Molina & Kahmann, 2007; Shetty et al., 2007). Therefore, in a pathogenic or symbiotic association, both the plant and the microbe must be able to deal with a complex mixture of ROS coming from both sides. ROS are not necessarily harmful for the partners and, depending on the model considered, they can also help to signal and limit/control the interaction. For example, the development of a mutualistic association between Epichloë festucae, a fungal endophyte, and the grass Lolium perenne requires the production of superoxide or hydrogen peroxide by a fungal NADPH oxidase, whilst inactivation of this gene changes the interaction from mutualistic to antagonistic (Tanaka et al., 2006). In any case, both partners (the plant and the microbe) have developed an impressive array of nonenzymatic and enzymatic antioxidant systems, whose function is to maintain adequate concentrations of ROS in their own cells. Indeed, low ROS concentrations are known to be required for signalling, growth and development, while high concentrations are detrimental to the cell and can damage various macromolecules. The antioxidants include the low-molecular-weight compounds glutathione, ascorbate and tocopherol and the enzymes superoxide dismutases, catalases, ascorbate- or thiol-dependent peroxidases, glutathione reductases, dehydroascorbate reductases and monodehydroascorbate reductases (Rouhier et al., 2008). These enzymes are involved in the removal of ROS either directly (superoxide dismutases, catalases, and ascorbate- or thiol-dependent peroxidases) or indirectly through the regeneration of the two major redox molecules in the cell, ascorbate and glutathione (glutathione reductases, dehydroascorbate reductases and monodehydroascorbate reductases). An interesting feature of the interplay between oxidants and antioxidants is that it occurs in all subcellular compartments including plastids and mitochondria, two sites of extensive ROS production (Navrot et al., 2007). Of primary importance for the development of plant–microbe interactions are the ROS produced at the interface between the partners, that is, in the extracellular matrices, cell walls and more generally the apoplast compartment. NADPH oxidases, plasma membrane-situated proteins, are key players in this subcellular compartment for the generation of ROS species including superoxide ions and hydrogen peroxide.
‘... the molecular limits between pathogenic and mutualistic associations are sometimes very narrow ...’
It has long been assumed that symbioses such as ectomycorrhizas, arbuscular mycorrhizas and rhizobial–leguminous interactions can be, in several aspects, beneficial to the plant partner (Jones et al., 2007; Finlay, 2008). It has been shown that these interactions can contribute to increased plant resistance or tolerance to several biotic or abiotic constraints. The recent paper by Baltruschat et al. (2008) demonstrated that the root endophytic basidiomycete Piriformospora indica increases the tolerance of a salt-sensitive barley (Hordeum vulgare) cultivar to severe salt stress. This paper follows a previous article indicating that this fungus also improves plant resistance against root and leaf diseases (Waller et al., 2005). Under these salt stress conditions, P. indica-colonized plants contained higher ascorbate concentrations in roots compared with noncolonized plants, while the ratio of ascorbate vs dehydroascorbate was not significantly altered and catalase, ascorbate peroxidase, glutathione reductase, dehydroascorbate reductase and monodehydroascorbate reductase activities were increased. These modifications are consistent with the decrease of leaf lipid peroxidation observed in these experiments.
In this issue of New Phytologist, the paper by Xu et al. describes an unexpected beneficial aspect of plant–pathogen interactions. They used 10 monocot and dicot plant species (Beta vulgaris, Capsicum annuum, Cucumis lanatus, Cucumis sativus, Solanum lycopersicum, Oryza sativa, Cucurbita pepo, Chenopodium amaranthicolor, Nicotiana benthamiana and Nicotiana tabacum) and inoculated them with the specific RNA viruses CMV (Cucumber Mosaic Virus), BMV (Brome Mosaic Virus), TMV (Tobacco Mosaic Virus) and TRV (Tobacco Rattle Virus). The infected plants exhibited better tolerance and survival in response to drought and/or cold stress, suggesting that the viral infection induced a reaction that may be part of an elaborate mechanism used by plants to survive under various environmental challenges. It is likely that the presence of the viruses up-regulated a specific set of stress-related genes which allows the infected plant to survive for a longer period when subjected to additional abiotic stresses, which are also known to generate the production and accumulation of ROS (Apel & Hirt, 2004). The findings of this study are consistent with the improved thermal tolerance observed for the plant and fungal partners of a tripartite mutualistic interaction between the fungal endophyte Curvularia protuberata and the tropical grass Dichantelium lanuginosum only when a virus is present in the fungal isolates (Márquez et al., 2007). In these cases, the contact with the virus or pathogen induced molecular changes in the plant hosts which made them more tolerant to other stresses. Following these experiments, one wonders whether pathogens can also provide useful metabolites or enzymes that could be of benefit to their hosts. These studies demonstrate that the molecular limits between pathogenic and mutualistic associations are sometimes very narrow, as shown for the interaction between Epichloë festucae and Lolium perenne, where the inactivation of one gene results in a different life style (see above; Tanaka et al., 2006).
Overall, these studies indicate that the increased plant tolerance to abiotic stresses (whether drought, salt or cold/thermal stress) recorded when plants are in contact with a microbe, either a pathogen or a mutualist, is in part correlated with an increase in antioxidant or osmolyte concentrations and/or in the activities of antioxidant enzymes, with ascorbate apparently playing a major role in the plant cells (Baltruschat et al., 2008), as illustrated in Fig. 1. These observations may somehow be related to the systemic acquired resistance observed in some pathogenic interactions where healthy parts of the host plant become more resistant to a subsequent infection by either the same microbe or another one. As far as we know, there is no molecular evidence for the involvement of the above-mentioned antioxidants in this process. Of course, in addition to ascorbate, several other compounds are also crucial and it is well known that glutathione and several hormones (abscisic acid (ABA), salicylic acid (SA), jasmonic acid (JA) and ethylene) are important players both in the abiotic stress response of plants and in plant–microbe interactions (Chamnongpol et al., 1998; Asselbergh et al., 2007; Vadassery et al., 2008). Following the reports of Xu et al. and Baltruschat et al., it will be of interest to determine the concentrations and qualities of antioxidants generated in various plant–microbe systems and to test whether this antioxidant generation results in improved stress protection for one or the other partner. Such data would allow further testing of the hypothesis that we have made in this commentary, i.e. that the biotic stress generates various antioxidants that help withstand an additional biotic stress.
Another important area of research would be to determine whether the converse is true; that is, do plants subjected to an abiotic stress become more resistant to other abiotic or biotic stresses? Although it is expected that a prolonged exposure to an abiotic stress would weaken plant defences and thus render the plants more susceptible to pathogen infection, there are a few contradictory examples. Bilgin et al. (2008) showed that ozone stress enhanced soybean (Glycine max) tolerance to a virus attack and Chamnongpol et al. (1998) demonstrated that a tobacco (Nicotiana tabacum) plant deficient for catalase, and thus more sensitive to photooxidative stress, exhibited enhanced tolerance against a pathogen attack. In their natural environment, plants may indeed be subjected simultaneously or sequentially to a combination of biotic or abiotic stresses. This might result in conflictive situations, because abiotic stress would promote an increase in antioxidant defences to scavenge the ROS produced, while the pathogen challenge would require a lowering of those defences for increased production of ROS, at least at the infection sites. In addition, it is worth mentioning that all oxidative stress conditions do not lead to identical patterns of response; although there are general oxidative stress response markers, additional unique and specific pathways are induced by specific stresses and specific ROS (Gadjev et al., 2006, Laloi et al., 2007).
In conclusion, the beneficial effect of viral infection for abiotic stress tolerance is still no more than a ‘pis-aller’ in terms of improving agricultural yields. Indeed, whilst the beneficial effect of viral infection can temporarily delay the negative effects of a given abiotic stress, it cannot protect indefinitely against them. Nevertheless, the papers discussed here provide an interesting molecular paradox that might help in the engineering of more stress-resistant plants to mitigate against the impacts of global climate change on agricultural and native plant communities via the enhancement of their redox defences, for example through the use of disarmed viral strains or fungal symbionts.
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