Growth inhibition by self‐DNA: a phenomenon and its multiple explanationsписьмо
Аннотация: 'How can receivers benefit from a growth inhibition effect that is caused by the presence of their own DNA in the environment?' The effects were concentration-dependent and, most strikingly, the majority of the tested organisms were not inhibited by 'heterologous' eDNA, that is, exogenously applied DNA that was extracted from other, taxonomically distant species. Thus, it is essentially their own DNA that causes this striking inhibitory effect on the investigated organisms; for this reason Mazzoleni et al. (2015a) suggest growth inhibition by esDNA in litter as the causal mechanism of negative plant–soil feedback and, ultimately, as a means of maintaining biodiversity. Veresoglou et al. critically discuss this interpretation and stress that organisms should invest energy in deciphering eDNA only when the resulting response brings an adaptive benefit for the receiver. How can receivers benefit from a growth inhibition effect that is caused by the presence of their own DNA in the environment? In their Letter, Veresoglou et al. present nonexclusive alternative explanations for the observed phenomenon and suggest that a diminution of seed germination by esDNA could alleviate intraspecific competition, for example, by informing seeds that 'it is better to wait until intraspecific competition decreases', or that esDNA in soil might function as an intraspecific stress signal, that is, as an indicator of a hostile environment that has already caused the death of many conspecifics. Mazzoleni et al. (2015a,b) described a new phenomenon that, if confirmed, will have tremendous molecular and ecological implications, and Veresoglou et al. show that we will have to consider multiple and, perhaps, nonexclusive explanations if we aim to understand the underlying mechanisms and the biological relevance of the inhibitory effects of esDNA. In this context, we suggest that future research should be guided by several conceptual and empirical questions: Based on our own, recent observations (Duran-Flores & Heil, 2014), we provide some empirical support for the second explanation given by Veresoglou et al. and highlight the role of esDNA as a stress signal, that is, as a damage-associated molecular pattern (DAMP; see review by Heil & Land, 2014). Concretely, we observed that the application of conspecific leaf homogenates (which evidently contain esDNA) to leaves of common bean (Phaseolus vulgaris) induced the local development of reactive oxygen species (ROS) and further resistance-related responses, whereas homogenates produced from plants in other genera, families or divisions (which, from the perspective of the treated bean plant, contain 'nonself' DNA) did not elicit any statistically significant response (Duran-Flores & Heil, 2014). The taxonomic specificity was high in this experiment, as even 'nonself' extracts produced from genera in the same family did not elicit any significant effects. Unfortunately, we did not identify the concrete molecules that served as DAMPs in this situation. Extracellular ATP has been reported as a taxonomically widespread DAMP that induces resistance responses in plants (Tanaka et al., 2014), fungi (Medina-Castellanos et al., 2014), insects (Moreno-García et al., 2014) and mammals (reviewed in Heil & Land, 2014) and, thus, likely played a role in resistance induction. However, we cannot imagine how eATP could explain the observed specificity in the response to leaf homogenates from different congeneric species. Thus, it is tempting to speculate that esDNA functions as a DAMP that can facilitate taxonomic specificity in the recognition process. The allocation of resources to resistance expression comes at a cost and usually causes a transient decrease in primary metabolism and, thus, growth (Herms & Mattson, 1992). Therefore, resistance induction by esDNA could lead at the phenotypic level to the growth arrestment phenomenon that was observed by Mazzoleni et al. (2015a,b). In general terms, the release of fragmented molecules from cells occurs not only in decaying material, such as leaf-litter or in dead organisms, but also within any living organism that suffers injury, and all delocalized or fragmented molecules indicate cell damage and, thus, can serve as DAMPs. In this scenario (Fig. 1a), one category of relevant receivers of esDNA would be intact cells that are localized around damaged tissue in a multicellular organism. The same principle applies to colonies of genetically related unicellular organisms, particularly to clonal ones. Concentration does play an important role (Mazzoleni et al., 2015a,b), and the highest concentrations of esDNA arguably occur in the intercellular spaces around damaged tissues, rather than outside an organism. If we scale from the physiological to the ecological level, plants growing next to decomposing conspecifics would be exposed to lower – and distance-dependent – concentrations of eDNA, and they would face a mixture of self- and nonself-eDNA (Fig. 1b). Thus, it seems very important to repeat the experiments conducted by Mazzoleni et al. (2015a,b) with ecologically realistic concentrations of eDNA and with realistic ratios of self- to nonself-eDNA. Studies focused on soil-mediated plant–plant interactions will also have to consider the amount of free (vs bound) eDNA that occurs in natural substrates (Veresoglou et al.). To the best of our knowledge, specific receptors for eDNA have so far only been described in mammals, and there are no reports indicating that they distinguish self- from nonself-DNA, at least not within the same kingdom. In mammalian cells, Toll-like receptors (Fig. 2) are involved in the perception of mitochondrial eDNA and of cytosolic double-stranded RNA (reviewed in Heil & Land, 2014), and double-stranded eDNA can be sensed also indirectly by the NLRP3 (NOD-like receptor family protein 3) inflammasome (Patel et al., 2011). In the first case, the perception involves the extracellular domains of transmembrane receptor proteins, whereas in the second case eDNA is taken up by phagocytosis and then re-released and sensed inside the cell (Fig. 2). Thus, we will have to search for the eDNA receptors in plants, but we must also consider that no active perception mechanism might be involved at all. In fact, it is difficult to imagine that a cell carries specific receptors for all possible sequences that would characterize the fragments that result from the natural decomposition or experimental fragmentation of its own DNA. Therefore, additionally, it would be important to consider receptor-independent (and perhaps nonadaptive) mechanisms that can cause the observed concentration-dependent inhibitory effects of esDNA. Mazzoleni et al. (2015a,b) reported a taxonomically widespread growth inhibition by esDNA, whereas Paungfoo-Lonhienne et al. (2010) showed that eDNA can favour plant growth when it is taken up by roots as a source of nutrients, although it should be stated that herring sperm DNA fragments (that is, nonself-DNA) were used in the latter study. Veresoglou et al. focus on adaptive effects that could be achieved via the specific recognition of esDNA by living plants and stress that selective benefits for the receiver are mandatory for the evolution of any specific mechanism that an organism would require to correctly decipher eDNA. At the mechanistic level, eDNA can be perceived in the extracellular space or after its uptake into living cells, at least in mammals (Fig. 2). The observations made by Paungfoo-Lonhienne et al. (2010) show that plant cells can also take up small fragments of eDNA and use them as a substrate in their metabolism. Apart from these scattered pieces of information, the molecular mechanisms through which eDNA (both self- and nonself) interact with living cells remain a matter of speculation. We suggest that the most likely possibilities are either a receptor-dependent perception and downstream signalling processes, or the uptake of fragmented DNA into cells and its subsequent interference with essential biological processes, such as transcriptional or enzymatic activities. Future studies should use biologically realistic concentrations of eDNA and ratios of self- to nonself-DNA and must consider that (1) self- and nonself-DNA might have different targets within a cell, that (2) eDNA at the molecular, physiological and ecological level might have various, nonexclusive functions in (or 'meanings for') different receivers, and that (3) these multiple functions might be mediated through different mechanisms. The authors thank Editor Amy Austin and Nichola Hetherington for inviting this comment, Matthias C. Rillig for kindly reading an earlier version of the manuscript and Alejandro de León for preparing the figures.
Год издания: 2015
Авторы: Dalia Durán-Flores, Martin Heil
Издательство: Wiley
Источник: New Phytologist
Ключевые слова: Evolution and Genetic Dynamics, Insect and Arachnid Ecology and Behavior, Insect symbiosis and bacterial influences
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Том: 207
Выпуск: 3
Страницы: 482–485