- Email: [email protected]
Impact of genomic diversity in river ecosystems
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Opinion
Impact of genomic diversity in river ecosystems Andrew R. Leitch1*, Ilia J. Leitch2*, Mark Trimmer1, Maite´ S. Guignard1, and Guy Woodward3 1
School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK 3 Imperial College London, Department of Life Sciences, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire, SL5 7PY, UK 2
We propose that genomic diversity in aquatic macrophytes of rivers, driven by the underlying genomic processes of interspecific hybridization and polyploidy (whole-genome duplication), play a significant role in ecosystem functioning. These genomic processes generate individuals which might differ in their demands for nitrogen (N) and phosphorus (P). This is significant because (i) N and/or P are frequently limiting nutrients in freshwater ecosystems, and (ii) nucleic acids are demanding in N and P. We suggest that N and P availability will provide a selection pressure for genetic variants in macrophytes which will, in turn, influence the nutritional quality of plant biomass, and hence their consumption by herbivores and detritivores as well as the energy flux of their biomass through the food web. Freshwater macrophyte ecology and genomic diversity The ecological significance of freshwater plants (macrophytes) in lakes and ponds is well known, where they contribute to producing a complex 3D habitat, as well as driving key nutrient cycles and acting as keystone species maintaining a clear water state (e.g., [1–3]). Far less is known about the role of macrophytes in rivers and streams, particularly in terms of how they influence the higher levels of biological organization (communities, food webs, ecosystems), and most studies of primary producers in rivers and streams only focus on the trophic roles of algae or terrestrial plant detritus at the base of the food web (e.g., reviewed in [4,5]) and on the role of macrophytes in fluvial dynamics and the physical habitat [6,7]. As with terrestrial plants, submerged or emergent macrophytes have long been assumed to enter the food web primarily as detritus after autumn die-back, rather than playing a major role as a living resource for consumers. More recently, however, it has become clear that macrophytes are also important in river ecosystems (i) by providing energy from their living and dead tissues, and (ii) by Corresponding author: Woodward, G. ([email protected]). Keywords: ecology; food webs; genome size; selection; nutrient stoichiometry. * Joint first authors. 1360-1385/$ – see front matter ß 2014 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.tplants.2013.12.005
playing a crucial role in the major nutrient cycles. Support for the first case includes isotope data which suggest a tight coupling between river macrophytes and key macroinvertebrates [8,9]. There is also direct evidence that river macrophytes are eaten by macroinvertebrates [10] and water birds [11,12]. Indeed, in some angiosperms that can be either aquatic or terrestrial it was shown that leaf loss through grazing was higher in the river populations when measured by leaf area and the same as terrestrial populations when measured by mass per unit area [13]. The second case is supported by strong empirical evidence showing how river macrophytes not only assimilate nutrients in their own tissues [6], but can also trap organic sediment [14] and facilitate the mineralization of organic carbon (C) and nitrogen (N) [15–17]. River macrophytes also provide conduits for the efflux of methane and other greenhouse gases from sediments [18]. Despite the growing appreciation of the ecological role of macrophytes in river ecosystems, we argue that the significance of their biodiversity is still underestimated. The use of macrophyte bioindicators of river ecosystem status have led to a focus on river biodiversity in terms of species richness and/or species assemblages, in conjunction with river characteristics [19]. However, some have doubted the efficacy of such approaches [20], and we suggest this may be because they miss a more fundamental aspect of biodiversity at the genomic level, a deficiency which restricts our understanding of the influence of higher plants on fluvial ecology. Glossary Allochthonous: imported from outside the system; in other words, ex situ in origin. Autochthonous: generated from within the system; in other words, in situ in origin. Dysploidy: variation in chromosome numbers arising through chromosome fusion, fission, and rearrangement events, as well chromosome number losses and gains. Food web: a schematic depicting the feeding connections between organisms, usually species, in an ecological community. Genome size: the total amount of DNA in an unreplicated gametic nucleus. Interspecific hybridization: hybridization between two or more species. Backcrossing of hybrids to parents can lead to introgression of DNA from one species to another. Polyploidy: whole-genome multiplication leading to 3 multiples of the chromosome number found in an unreplicated gametic nucleus. Reticulate evolution: the pattern of evolution arising from interspecific hybridization, which is often associated with polyploidy. RNA pool: the total RNA content of a cell, the transcriptome. Trends in Plant Science xx (2014) 1–6
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Opinion There are many evolutionary processes that influence genetic diversity – for example, genetic drift (e.g., especially associated with founder events and small populations) and selection (e.g., against herbivory) – over different geographic and temporal scales (e.g., post-glacial expansions). Here we focus on three processes which substantially influence genomic diversity in terms of genome size (see Glossary) and RNA usage. These processes are: polyploidy, interspecific hybridization, and dysploidy, which can generate substantial intra- and interspecific variation upon which selection can act over both time and space. Indeed, they are major driving forces in angiosperm evolution [21–23] and are particularly prevalent in aquatic plants [24]. Genome size varies because polyploids and dysploids have multiples (or part multiples) of the diploid DNA content, and the RNA content of cells can also be highly variable [25], especially in the context of hybrids and polyploids [26]. In this opinion article we propose that variation in the DNA and RNA content of river plants generated by these genomic processes, coupled with selection driven by the availability of the nutrients N and P, will significantly influence the nutrient stoichiometry of macrophytes and hence their nutritional quality, dead or alive, in the food web. Furthermore, we propose that this resulting genomic variation is likely to influence the consumption of macrophytes by herbivores and detritivores, and hence the flux of their biomass through the food web (summarized in Figure 1). Essentially, by ignoring such molecular aspects of plant diversity we could be missing a key link between ‘true’ biodiversity and ecosystem processes in rivers and streams. Nucleic acids are major sinks for N and P in the cell Genomic variation in plants is important because: (i) both N and P are frequently limiting nutrients in freshwater ecosystems [27], and (ii) nucleic acids (DNA and RNA) are demanding in both N and P (i.e., by mass, they are approximately 39% N and nearly 9% P assuming a 1:1 ratio for purines and pyridines [25]). Indeed, nucleic acids contain more P than any other major biomolecule [25]. For example, in aquatic invertebrates, up to 80% of organic P is tied up in nucleic acids [28] whereas, in plants, nucleic acids account for up to 40% of the total cell P content in some species [29,30]. Consequently, we propose that the availability of N and P provides a selection pressure that influences RNA use and genome size in macrophytes. Although it is often stated that RNA forms the largest component of the nucleic acid fraction in the cell [31], the cellular content of P and N made up by the RNA component of nucleic acids, including ribosomal RNA, is extremely variable, can be regulated, and depends on (i) tissue, (ii) metabolic activity of the cell, (iii) species, and (iv) the growth conditions in which the species is found [26,28,32,33]. For DNA, we are unaware of data for angiosperms reporting the proportion of cellular P invested, but it is likely that DNA comprises at least 5–10% of cellular P, as in haploid and diploid algae respectively [33]. Similarly, we are unaware of the proportion of cellular N invested in DNA in angiosperms; nevertheless, this too must be significant, not least because of the high levels of N in their nitrogenous bases and in the 2
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histones that package DNA (histones account for 10% of all cellular proteins in mouse fibroblasts [34]). Certainly, it is unknown how N and P investment in DNA and RNA scales across the 2 400-fold range of genome sizes encountered in angiosperms [35]. Given the variation in both RNA and DNA content of cells, it is not unsurprising that RNA:DNA ratios have also been reported to vary from <1 to >10, although they are often around 2–3 except when growth is slow, when the ratio is likely to be <1 [28,31]. Genome size also correlates with other cellular properties which will impact on N and P demands of the cell. For example, there is a significant positive correlation between nucleus size and cell size in angiosperms [36]. Thus, as genome size increases, the cellular demand for other N and P-containing molecules (e.g., phospholipid membranes) will also increase [25,33] (although how cell size scales with cell number in tissues in angiosperms is unknown). Evidence that there is indeed selection at the genomesize level under limiting N and P comes from several studies. Certainly, in suspended algae in freshwaters and oceans, diploids are favored when nutrients are abundant, and haploids favored under nutrient limitation [33]. Although we are unaware of comparable data in freshwater macrophytes, in a long-term (60 year) grassland nutrient-enrichment field experiment, there is evidence for selection of plants with lower mean genome sizes on plots receiving least P [37]. There is also evidence that plants have responded to N-limitation through selection for nucleotides and amino acids which require less N, a feature that is lost in crop plants where that selection pressure has been reduced by fertilizers [38]. There may also be a response to limiting N and P – mediated by selection for individuals with lower amounts of DNA – via its elimination (i.e., genome downsizing [39]) in polyploid genomes. Indeed, DNA elimination following polyploidy is likely to be one of the main reasons why genome sizes in angiosperms are heavily skewed towards small genomes, despite the prevalence of recurrent polyploidy in many lineages [40–42]. Polyploids, hybrids, and aquatic macrophytes If selection is indeed acting in macrophytes at the genomesize level under limiting nutrient conditions, then it is important to consider the major processes that generate such variation. Reticulate evolution, polyploidy, and dysploidy are certainly significant processes in relation to aquatic macrophyte biology [24]. Much has been written about the ecological and evolutionary advantages associated with polyploidy, including the fixing of heterozygosity and hybrid vigor over the short term [43], and the generation of multiple gene copies from which new functions can evolve (neofunctionalization [44]) in the longer term. Furthermore, when polyploidy is coupled with interspecific hybridization (i.e., allopolyploidy), novel characters not found in either parent can evolve through the ‘mixand-match’ of biochemical pathways (i.e., transgressive characters [45]). In addition, from its onset, interspecific hybridization and polyploidy can generate enormous genetic variation upon which selection can act. Indeed, such advantages have been proposed to explain the high
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Opinion
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Genomic processes Hybridizaon/Polyploidy/Dysploidy
Crypc genomic variaon DNA amount
RNA amount
Different genome sizes Different chromosome numbers
Size of RNA pool (transcriptome) Amount of ribosomal RNA
Diversity in [DNA] and [RNA] and thus [N] and [P]
Selecon based on [N] and [P] availability
Crypc macrophyte diversity Low [N] and [P]
High [N] and [P]
• Selecon for small genome sizes and low levels of polyploidy • Selecon for efficient RNA usage
• Larger range of genomes and ploidy levels possible • Relaxed selecon for efficient RNA usage
Impacts on ecosystem funconing • Nutrional quality of plant biomass • Nutrient cycling through food web
• Plant decomposion rate • Energy flux through ecosystem/food webs • Food web complexity
Impact on ecosytem services • • • •
Regulatory services (e.g., water purificaon) Supporng services (e.g., fish producon) Provisioning services (e.g., reeds for thatching) Cultural and aesthec services
TRENDS in Plant Science
Figure 1. Ecological and evolutionary consequences of genomic processes operating in freshwater macrophytes. Hypothesized scenario for the effect of nitrogen (N) and phosphorus (P) selection on genomic variability, cryptic macrophyte diversity, and ecosystem functioning. Top left, plant chromosomes stained with a blue fluorochrome (40 ,6-diamidino-2-phenylindole, DAPI); middle left, Nymphaea alba (white waterlily); bottom left, food web.
frequency of polyploids in many extant angiosperms, as has the suggestion that most, if not all, angiosperms have experienced polyploidy in their evolutionary history [46]. Rather less attention has been paid to the biological and biochemical costs of polyploidy, and these need to be explored more fully. Paramount among these is that polyploids, with multiples of the genome size of diploid relatives, are likely to require more N and P from the environment to build their cells [22,47]. Interspecific
hybridization and polyploidy are also known to alter the size and nature of the RNA pool in unpredictable ways [26], and there may be selection for the efficient use of N and P through the reallocation of resources from DNA (via genome downsizing) to RNA (especially ribosomal RNA needed for protein synthesis) to facilitate growth [28]. Among aquatic macrophytes, reticulate evolution, polyploidy, and dysploidy have generated extensive chromosome number diversity, with variations in chromosome 3
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Opinion number between species reported in 80% of aquatic macrophyte genera [24]), including in many iconic submerged macrophytes, such as water lilies (Nymphaea L.) and water crowfoot (Ranunculus L.), and emergents such as Phragmites [24,48,49]. Within species there is also considerable chromosome number variation; for example, Aponogeton distachyon ranges from diploid to decaploid [24]. The variants caused by these genomic changes, from an ecological perspective, provide huge scope for selection; for example, for different genome sizes or efficiency of RNA usage (e.g., quicker RNA cycling, and targeted gene transcription). River N and P, and macrophytes Potentially, rivers differ from lakes in the strength, duration and nature of these N- and P-based selection pressures because rivers act more similarly to chemostat cultures whereas lakes more resemble batch cultures. In lakes rapid nutrient depletion is associated with seasonal macrophyte and algal growth. Certainly there is a succession of suspended algal communities in lakes and oceans associated with this depletion, and it is noteworthy that diploid species predominate over haploid species when nutrient levels are high [33]. In rivers, the selection pressures of a more regular supply of nutrients on genome size is likely to be more uniform over the year, reducing the option to assimilate and store N and P in times of plenty. In rivers, therefore, it should be more apparent if N and P are limiting, and if so this will likely have an effect on biomass-scaled genome size (genome size multiplied by the proportion of biomass contributed by the species), as shown in the grassland nutrient-enrichment field experiment noted above [37]. The concept of eutrophication is well established for both lakes and coastal seas, with primary productivity being strongly correlated with anthropogenic nutrient enrichment, either as N or P. Even so, our understanding of the effects of nutrient availability for river networks, especially at both ends of the spectrum and over continental scales, is lacking [50,51]. Furthermore, in the context of macrophytes, little is known about how much N and P is sequestered to storage organs, or are lost by plant succession or through die-back each season. Nevertheless, there is an emerging consensus that increases in nutrients (N or P) can increase algal and macrophyte biomass. For example, Ranunculus penicillatus (Stream water crowfoot) biomass increased with the concentration of P across 14 UK rivers [52], as was Potamogeton pectinatus (Sago pondweed) in artificial streams [53], whereas N and P accounted for 27% of the variability in macrophytes biomass in 28 Canadian rivers [54]. There is also equivocal evidence to suggest that changes in biodiversity and species composition in response to available nutrients [51,55] can influence plant palatability. However, a confounding problem is that reticulate evolution in macrophytes frequently leads to complex, obscure, and imprecise systematics and taxonomy. This may be why macrophyte species composition was found to be a poor bioindicator of surrounding nutrient status [56]. Indeed, in many cases the traditional biodiversity measures, that use Latin binomial names as fundamental units 4
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of measurement, are inadequate [20]. Certainly, such taxonomy may obscure more appropriate measures of biological variation mediated at the cellular level. We predict that selection pressures favor particular genetic variants in the macrophyte assemblage, variants selected from the widespread interspecific hybrids, and/or polyploid/dysploid forms. Such selection might act quickly, particularly because macrophytes show high vagility, meaning that well-adapted clones may readily colonize a river catchment [19,24,57]. This line of reasoning leads us to predict that, in rivers with low available N and/or P, there will be selection for individuals with low ploidy and/or genome size, and for efficient use of RNA, and we would expect this selection pressure to manifest itself in terms of biomass-scaled genome size, as mentioned above. Consequences of hidden genomic diversity for ecosystem processes It is generally assumed that plants are more stoichiometrically flexible (lower degree of homeostasis) in relation to the C, N, and P content of their tissues than are animals [25,58–60]. Nevertheless, genome size will affect the amount and distribution of C, N and P in plant tissues, and this will, in turn, influence nutrient availability to consumers. For example, there is evidence that plants with larger genomes may be more palatable because of low C:N or C:P ratios, and hence may be assimilated more efficiently [61,62]. Thus, limitations in available N and P in aquatic plants (macrophytes and/or algae) may reverberate upwards through the food web. Indeed, in shallow fresh waters it is known that growth rates in the water flea Daphnia magna are strongly and negatively impacted by low-quality food (high C:P ratio) at high temperatures [63] (at lower temperature the effect is lost, potentially because of decreased growth rates and hence reduced P demand). In the freshwater snail Potamopyrgus antipodarum (New Zealand mud snail), body P and nucleic acid content per unit mass increases with ploidy level [64]. When triploid and tetraploid representatives of this species are grown in culture and fed low-P diets, the tetraploids showed a twofold decrease in growth rate compared with the triploids. Such data suggest that food quality may well provide cryptic selection also on the animal genomes, as well as influencing species composition and abundance in food webs, and energy flux through the ecosystem: polyploidy could therefore have numerous important, but overlooked, effects in freshwater ecosystems from streams to rivers and lakes. The vast majority of research conducted on biodiversity and ecosystem processes in river organisms has focused on consumption of allochthonous terrestrial leaf-litter (e.g., [65–68]), while largely ignoring the autochthonous macrophyte production that can enter the food web via primary consumers (but see [69]). Much of this is because it is often assumed that living higher plants are less grazed relative to algae or terrestrial leaf litter, perhaps owing to their effective chemical defenses. Nevertheless, there is increasing evidence that macrophyte herbivory is significant, perhaps comparable to terrestrial systems [10–13]. In addition, macrophytes represent a large input of detrital biomass when they senesce, especially in lowland systems
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Opinion [68]. Because C, N, and P content of allochthonous detritus largely determines its decomposition rates within streams [70,71], we predict the same is likely to be true for autochthonous (macrophyte) detritus, as has been demonstrated, for instance, in field bioassays in wetlands [71]. Concluding remarks In conclusion, our synthesis of the literature leads us to propose that aquatic macrophytes may indeed respond to the prevailing nutrient conditions in rivers through the selection of variants with differing genome size and RNA usage. Given that this in turn has the potential to generate plant material of variable nutritional quality for consumers, and hence the efficiency and magnitude of energy flux to the food web, the impact of diversity at the genomic level has the potential to reverberate through the whole river ecosystem (Figure 1). There is now clearly a need to obtain the necessary empirical genomic data such that a more holistic understanding of river ecosystems can be achieved. Acknowledgments We thank the Research Council of Norway (RCN grant no. 196468/V40) and the National Environmental Research Council (ERC) Macronutrients Cycle Programme NE/J012106/1 for support. This work was also partly supported by the Grand Challenges in Ecosystems and the Environment initiative at Imperial College London. We thank A. Hildrew and B. Demars and two anonymous reviewers for thought-provoking and critical comments on this manuscript.
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Opinion
Impact of genomic diversity in river ecosystems Andrew R. Leitch1*, Ilia J. Leitch2*, Mark Trimmer1, Maite´ S. Guignard1, and Guy Woodward3 1
School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK 3 Imperial College London, Department of Life Sciences, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire, SL5 7PY, UK 2
We propose that genomic diversity in aquatic macrophytes of rivers, driven by the underlying genomic processes of interspecific hybridization and polyploidy (whole-genome duplication), play a significant role in ecosystem functioning. These genomic processes generate individuals which might differ in their demands for nitrogen (N) and phosphorus (P). This is significant because (i) N and/or P are frequently limiting nutrients in freshwater ecosystems, and (ii) nucleic acids are demanding in N and P. We suggest that N and P availability will provide a selection pressure for genetic variants in macrophytes which will, in turn, influence the nutritional quality of plant biomass, and hence their consumption by herbivores and detritivores as well as the energy flux of their biomass through the food web. Freshwater macrophyte ecology and genomic diversity The ecological significance of freshwater plants (macrophytes) in lakes and ponds is well known, where they contribute to producing a complex 3D habitat, as well as driving key nutrient cycles and acting as keystone species maintaining a clear water state (e.g., [1–3]). Far less is known about the role of macrophytes in rivers and streams, particularly in terms of how they influence the higher levels of biological organization (communities, food webs, ecosystems), and most studies of primary producers in rivers and streams only focus on the trophic roles of algae or terrestrial plant detritus at the base of the food web (e.g., reviewed in [4,5]) and on the role of macrophytes in fluvial dynamics and the physical habitat [6,7]. As with terrestrial plants, submerged or emergent macrophytes have long been assumed to enter the food web primarily as detritus after autumn die-back, rather than playing a major role as a living resource for consumers. More recently, however, it has become clear that macrophytes are also important in river ecosystems (i) by providing energy from their living and dead tissues, and (ii) by Corresponding author: Woodward, G. ([email protected]). Keywords: ecology; food webs; genome size; selection; nutrient stoichiometry. * Joint first authors. 1360-1385/$ – see front matter ß 2014 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.tplants.2013.12.005
playing a crucial role in the major nutrient cycles. Support for the first case includes isotope data which suggest a tight coupling between river macrophytes and key macroinvertebrates [8,9]. There is also direct evidence that river macrophytes are eaten by macroinvertebrates [10] and water birds [11,12]. Indeed, in some angiosperms that can be either aquatic or terrestrial it was shown that leaf loss through grazing was higher in the river populations when measured by leaf area and the same as terrestrial populations when measured by mass per unit area [13]. The second case is supported by strong empirical evidence showing how river macrophytes not only assimilate nutrients in their own tissues [6], but can also trap organic sediment [14] and facilitate the mineralization of organic carbon (C) and nitrogen (N) [15–17]. River macrophytes also provide conduits for the efflux of methane and other greenhouse gases from sediments [18]. Despite the growing appreciation of the ecological role of macrophytes in river ecosystems, we argue that the significance of their biodiversity is still underestimated. The use of macrophyte bioindicators of river ecosystem status have led to a focus on river biodiversity in terms of species richness and/or species assemblages, in conjunction with river characteristics [19]. However, some have doubted the efficacy of such approaches [20], and we suggest this may be because they miss a more fundamental aspect of biodiversity at the genomic level, a deficiency which restricts our understanding of the influence of higher plants on fluvial ecology. Glossary Allochthonous: imported from outside the system; in other words, ex situ in origin. Autochthonous: generated from within the system; in other words, in situ in origin. Dysploidy: variation in chromosome numbers arising through chromosome fusion, fission, and rearrangement events, as well chromosome number losses and gains. Food web: a schematic depicting the feeding connections between organisms, usually species, in an ecological community. Genome size: the total amount of DNA in an unreplicated gametic nucleus. Interspecific hybridization: hybridization between two or more species. Backcrossing of hybrids to parents can lead to introgression of DNA from one species to another. Polyploidy: whole-genome multiplication leading to 3 multiples of the chromosome number found in an unreplicated gametic nucleus. Reticulate evolution: the pattern of evolution arising from interspecific hybridization, which is often associated with polyploidy. RNA pool: the total RNA content of a cell, the transcriptome. Trends in Plant Science xx (2014) 1–6
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Opinion There are many evolutionary processes that influence genetic diversity – for example, genetic drift (e.g., especially associated with founder events and small populations) and selection (e.g., against herbivory) – over different geographic and temporal scales (e.g., post-glacial expansions). Here we focus on three processes which substantially influence genomic diversity in terms of genome size (see Glossary) and RNA usage. These processes are: polyploidy, interspecific hybridization, and dysploidy, which can generate substantial intra- and interspecific variation upon which selection can act over both time and space. Indeed, they are major driving forces in angiosperm evolution [21–23] and are particularly prevalent in aquatic plants [24]. Genome size varies because polyploids and dysploids have multiples (or part multiples) of the diploid DNA content, and the RNA content of cells can also be highly variable [25], especially in the context of hybrids and polyploids [26]. In this opinion article we propose that variation in the DNA and RNA content of river plants generated by these genomic processes, coupled with selection driven by the availability of the nutrients N and P, will significantly influence the nutrient stoichiometry of macrophytes and hence their nutritional quality, dead or alive, in the food web. Furthermore, we propose that this resulting genomic variation is likely to influence the consumption of macrophytes by herbivores and detritivores, and hence the flux of their biomass through the food web (summarized in Figure 1). Essentially, by ignoring such molecular aspects of plant diversity we could be missing a key link between ‘true’ biodiversity and ecosystem processes in rivers and streams. Nucleic acids are major sinks for N and P in the cell Genomic variation in plants is important because: (i) both N and P are frequently limiting nutrients in freshwater ecosystems [27], and (ii) nucleic acids (DNA and RNA) are demanding in both N and P (i.e., by mass, they are approximately 39% N and nearly 9% P assuming a 1:1 ratio for purines and pyridines [25]). Indeed, nucleic acids contain more P than any other major biomolecule [25]. For example, in aquatic invertebrates, up to 80% of organic P is tied up in nucleic acids [28] whereas, in plants, nucleic acids account for up to 40% of the total cell P content in some species [29,30]. Consequently, we propose that the availability of N and P provides a selection pressure that influences RNA use and genome size in macrophytes. Although it is often stated that RNA forms the largest component of the nucleic acid fraction in the cell [31], the cellular content of P and N made up by the RNA component of nucleic acids, including ribosomal RNA, is extremely variable, can be regulated, and depends on (i) tissue, (ii) metabolic activity of the cell, (iii) species, and (iv) the growth conditions in which the species is found [26,28,32,33]. For DNA, we are unaware of data for angiosperms reporting the proportion of cellular P invested, but it is likely that DNA comprises at least 5–10% of cellular P, as in haploid and diploid algae respectively [33]. Similarly, we are unaware of the proportion of cellular N invested in DNA in angiosperms; nevertheless, this too must be significant, not least because of the high levels of N in their nitrogenous bases and in the 2
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histones that package DNA (histones account for 10% of all cellular proteins in mouse fibroblasts [34]). Certainly, it is unknown how N and P investment in DNA and RNA scales across the 2 400-fold range of genome sizes encountered in angiosperms [35]. Given the variation in both RNA and DNA content of cells, it is not unsurprising that RNA:DNA ratios have also been reported to vary from <1 to >10, although they are often around 2–3 except when growth is slow, when the ratio is likely to be <1 [28,31]. Genome size also correlates with other cellular properties which will impact on N and P demands of the cell. For example, there is a significant positive correlation between nucleus size and cell size in angiosperms [36]. Thus, as genome size increases, the cellular demand for other N and P-containing molecules (e.g., phospholipid membranes) will also increase [25,33] (although how cell size scales with cell number in tissues in angiosperms is unknown). Evidence that there is indeed selection at the genomesize level under limiting N and P comes from several studies. Certainly, in suspended algae in freshwaters and oceans, diploids are favored when nutrients are abundant, and haploids favored under nutrient limitation [33]. Although we are unaware of comparable data in freshwater macrophytes, in a long-term (60 year) grassland nutrient-enrichment field experiment, there is evidence for selection of plants with lower mean genome sizes on plots receiving least P [37]. There is also evidence that plants have responded to N-limitation through selection for nucleotides and amino acids which require less N, a feature that is lost in crop plants where that selection pressure has been reduced by fertilizers [38]. There may also be a response to limiting N and P – mediated by selection for individuals with lower amounts of DNA – via its elimination (i.e., genome downsizing [39]) in polyploid genomes. Indeed, DNA elimination following polyploidy is likely to be one of the main reasons why genome sizes in angiosperms are heavily skewed towards small genomes, despite the prevalence of recurrent polyploidy in many lineages [40–42]. Polyploids, hybrids, and aquatic macrophytes If selection is indeed acting in macrophytes at the genomesize level under limiting nutrient conditions, then it is important to consider the major processes that generate such variation. Reticulate evolution, polyploidy, and dysploidy are certainly significant processes in relation to aquatic macrophyte biology [24]. Much has been written about the ecological and evolutionary advantages associated with polyploidy, including the fixing of heterozygosity and hybrid vigor over the short term [43], and the generation of multiple gene copies from which new functions can evolve (neofunctionalization [44]) in the longer term. Furthermore, when polyploidy is coupled with interspecific hybridization (i.e., allopolyploidy), novel characters not found in either parent can evolve through the ‘mixand-match’ of biochemical pathways (i.e., transgressive characters [45]). In addition, from its onset, interspecific hybridization and polyploidy can generate enormous genetic variation upon which selection can act. Indeed, such advantages have been proposed to explain the high
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Opinion
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Genomic processes Hybridizaon/Polyploidy/Dysploidy
Crypc genomic variaon DNA amount
RNA amount
Different genome sizes Different chromosome numbers
Size of RNA pool (transcriptome) Amount of ribosomal RNA
Diversity in [DNA] and [RNA] and thus [N] and [P]
Selecon based on [N] and [P] availability
Crypc macrophyte diversity Low [N] and [P]
High [N] and [P]
• Selecon for small genome sizes and low levels of polyploidy • Selecon for efficient RNA usage
• Larger range of genomes and ploidy levels possible • Relaxed selecon for efficient RNA usage
Impacts on ecosystem funconing • Nutrional quality of plant biomass • Nutrient cycling through food web
• Plant decomposion rate • Energy flux through ecosystem/food webs • Food web complexity
Impact on ecosytem services • • • •
Regulatory services (e.g., water purificaon) Supporng services (e.g., fish producon) Provisioning services (e.g., reeds for thatching) Cultural and aesthec services
TRENDS in Plant Science
Figure 1. Ecological and evolutionary consequences of genomic processes operating in freshwater macrophytes. Hypothesized scenario for the effect of nitrogen (N) and phosphorus (P) selection on genomic variability, cryptic macrophyte diversity, and ecosystem functioning. Top left, plant chromosomes stained with a blue fluorochrome (40 ,6-diamidino-2-phenylindole, DAPI); middle left, Nymphaea alba (white waterlily); bottom left, food web.
frequency of polyploids in many extant angiosperms, as has the suggestion that most, if not all, angiosperms have experienced polyploidy in their evolutionary history [46]. Rather less attention has been paid to the biological and biochemical costs of polyploidy, and these need to be explored more fully. Paramount among these is that polyploids, with multiples of the genome size of diploid relatives, are likely to require more N and P from the environment to build their cells [22,47]. Interspecific
hybridization and polyploidy are also known to alter the size and nature of the RNA pool in unpredictable ways [26], and there may be selection for the efficient use of N and P through the reallocation of resources from DNA (via genome downsizing) to RNA (especially ribosomal RNA needed for protein synthesis) to facilitate growth [28]. Among aquatic macrophytes, reticulate evolution, polyploidy, and dysploidy have generated extensive chromosome number diversity, with variations in chromosome 3
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Opinion number between species reported in 80% of aquatic macrophyte genera [24]), including in many iconic submerged macrophytes, such as water lilies (Nymphaea L.) and water crowfoot (Ranunculus L.), and emergents such as Phragmites [24,48,49]. Within species there is also considerable chromosome number variation; for example, Aponogeton distachyon ranges from diploid to decaploid [24]. The variants caused by these genomic changes, from an ecological perspective, provide huge scope for selection; for example, for different genome sizes or efficiency of RNA usage (e.g., quicker RNA cycling, and targeted gene transcription). River N and P, and macrophytes Potentially, rivers differ from lakes in the strength, duration and nature of these N- and P-based selection pressures because rivers act more similarly to chemostat cultures whereas lakes more resemble batch cultures. In lakes rapid nutrient depletion is associated with seasonal macrophyte and algal growth. Certainly there is a succession of suspended algal communities in lakes and oceans associated with this depletion, and it is noteworthy that diploid species predominate over haploid species when nutrient levels are high [33]. In rivers, the selection pressures of a more regular supply of nutrients on genome size is likely to be more uniform over the year, reducing the option to assimilate and store N and P in times of plenty. In rivers, therefore, it should be more apparent if N and P are limiting, and if so this will likely have an effect on biomass-scaled genome size (genome size multiplied by the proportion of biomass contributed by the species), as shown in the grassland nutrient-enrichment field experiment noted above [37]. The concept of eutrophication is well established for both lakes and coastal seas, with primary productivity being strongly correlated with anthropogenic nutrient enrichment, either as N or P. Even so, our understanding of the effects of nutrient availability for river networks, especially at both ends of the spectrum and over continental scales, is lacking [50,51]. Furthermore, in the context of macrophytes, little is known about how much N and P is sequestered to storage organs, or are lost by plant succession or through die-back each season. Nevertheless, there is an emerging consensus that increases in nutrients (N or P) can increase algal and macrophyte biomass. For example, Ranunculus penicillatus (Stream water crowfoot) biomass increased with the concentration of P across 14 UK rivers [52], as was Potamogeton pectinatus (Sago pondweed) in artificial streams [53], whereas N and P accounted for 27% of the variability in macrophytes biomass in 28 Canadian rivers [54]. There is also equivocal evidence to suggest that changes in biodiversity and species composition in response to available nutrients [51,55] can influence plant palatability. However, a confounding problem is that reticulate evolution in macrophytes frequently leads to complex, obscure, and imprecise systematics and taxonomy. This may be why macrophyte species composition was found to be a poor bioindicator of surrounding nutrient status [56]. Indeed, in many cases the traditional biodiversity measures, that use Latin binomial names as fundamental units 4
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of measurement, are inadequate [20]. Certainly, such taxonomy may obscure more appropriate measures of biological variation mediated at the cellular level. We predict that selection pressures favor particular genetic variants in the macrophyte assemblage, variants selected from the widespread interspecific hybrids, and/or polyploid/dysploid forms. Such selection might act quickly, particularly because macrophytes show high vagility, meaning that well-adapted clones may readily colonize a river catchment [19,24,57]. This line of reasoning leads us to predict that, in rivers with low available N and/or P, there will be selection for individuals with low ploidy and/or genome size, and for efficient use of RNA, and we would expect this selection pressure to manifest itself in terms of biomass-scaled genome size, as mentioned above. Consequences of hidden genomic diversity for ecosystem processes It is generally assumed that plants are more stoichiometrically flexible (lower degree of homeostasis) in relation to the C, N, and P content of their tissues than are animals [25,58–60]. Nevertheless, genome size will affect the amount and distribution of C, N and P in plant tissues, and this will, in turn, influence nutrient availability to consumers. For example, there is evidence that plants with larger genomes may be more palatable because of low C:N or C:P ratios, and hence may be assimilated more efficiently [61,62]. Thus, limitations in available N and P in aquatic plants (macrophytes and/or algae) may reverberate upwards through the food web. Indeed, in shallow fresh waters it is known that growth rates in the water flea Daphnia magna are strongly and negatively impacted by low-quality food (high C:P ratio) at high temperatures [63] (at lower temperature the effect is lost, potentially because of decreased growth rates and hence reduced P demand). In the freshwater snail Potamopyrgus antipodarum (New Zealand mud snail), body P and nucleic acid content per unit mass increases with ploidy level [64]. When triploid and tetraploid representatives of this species are grown in culture and fed low-P diets, the tetraploids showed a twofold decrease in growth rate compared with the triploids. Such data suggest that food quality may well provide cryptic selection also on the animal genomes, as well as influencing species composition and abundance in food webs, and energy flux through the ecosystem: polyploidy could therefore have numerous important, but overlooked, effects in freshwater ecosystems from streams to rivers and lakes. The vast majority of research conducted on biodiversity and ecosystem processes in river organisms has focused on consumption of allochthonous terrestrial leaf-litter (e.g., [65–68]), while largely ignoring the autochthonous macrophyte production that can enter the food web via primary consumers (but see [69]). Much of this is because it is often assumed that living higher plants are less grazed relative to algae or terrestrial leaf litter, perhaps owing to their effective chemical defenses. Nevertheless, there is increasing evidence that macrophyte herbivory is significant, perhaps comparable to terrestrial systems [10–13]. In addition, macrophytes represent a large input of detrital biomass when they senesce, especially in lowland systems
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Opinion [68]. Because C, N, and P content of allochthonous detritus largely determines its decomposition rates within streams [70,71], we predict the same is likely to be true for autochthonous (macrophyte) detritus, as has been demonstrated, for instance, in field bioassays in wetlands [71]. Concluding remarks In conclusion, our synthesis of the literature leads us to propose that aquatic macrophytes may indeed respond to the prevailing nutrient conditions in rivers through the selection of variants with differing genome size and RNA usage. Given that this in turn has the potential to generate plant material of variable nutritional quality for consumers, and hence the efficiency and magnitude of energy flux to the food web, the impact of diversity at the genomic level has the potential to reverberate through the whole river ecosystem (Figure 1). There is now clearly a need to obtain the necessary empirical genomic data such that a more holistic understanding of river ecosystems can be achieved. Acknowledgments We thank the Research Council of Norway (RCN grant no. 196468/V40) and the National Environmental Research Council (ERC) Macronutrients Cycle Programme NE/J012106/1 for support. This work was also partly supported by the Grand Challenges in Ecosystems and the Environment initiative at Imperial College London. We thank A. Hildrew and B. Demars and two anonymous reviewers for thought-provoking and critical comments on this manuscript.
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