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Genome size influences plant growth and biodiversity responses to nutrient fertilization in diverse grassland communities [1]
['Joseph A. Morton', 'School Of Biological', 'Behavioural Sciences', 'Queen Mary University Of London', 'London', 'United Kingdom', 'Department Of Trait Diversity', 'Function', 'Royal Botanic Gardens', 'Kew']
Date: 2024-12
Experiments comparing diploids with polyploids and in single grassland sites show that nitrogen and/or phosphorus availability influences plant growth and community composition dependent on genome size; specifically, plants with larger genomes grow faster under nutrient enrichments relative to those with smaller genomes. However, it is unknown if these effects are specific to particular site localities with speciifc plant assemblages, climates, and historical contingencies. To determine the generality of genome size-dependent growth responses to nitrogen and phosphorus fertilization, we combined genome size and species abundance data from 27 coordinated grassland nutrient addition experiments in the Nutrient Network that occur in the Northern Hemisphere across a range of climates and grassland communities. We found that after nitrogen treatment, species with larger genomes generally increased more in cover compared to those with smaller genomes, potentially due to a release from nutrient limitation. Responses were strongest for C 3 grasses and in less seasonal, low precipitation environments, indicating that genome size effects on water-use-efficiency modulates genome size–nutrient interactions. Cumulatively, the data suggest that genome size is informative and improves predictions of species’ success in grassland communities.
Funding: This work was generated using data from the Nutrient Network (
http://www.nutnet.org ) experiment, funded at the site‐scale by individual researchers. Specifically, NE acknowledges support for the German Centre for Integrative Biodiversity Research from the German Research Foundation (DFG-FZT 118, 202548816, www.dfg.de ). MWC acknowledges support from the Natural Sciences and Engineering Research Council of Canada (#386151, www.nserc-crsng.gc.ca ). XR acknowledges support for CEREEP-Ecotron IleDeFrance from the "Investissements d'Avenir" program launched by the French government and implemented by ANR (ANR-11-INBS-0001 AnaEE France and ANR-10-IDEX-0001-02 PSL, anr.fr). EB and ES acknowledge support from the National Science Foundation Research Coordination Network (NSF‐DEB‐1042132, nsf.gov) and Long-Term Ecological Research (NSF‐DEB‐1234162 to Cedar Creek LTER, nsf.gov) programs, and the Institute on the Environment (DG‐0001‐13, environment.umn.edu). YMB acknowledges financial support to the Burren field site from a Co-Centre award (22/CC/11103, www.sfi.ie ), managed by Science Foundation Ireland (SFI), Northern Ireland’s Department of Agriculture, Environment and Rural Affairs (DAERA) and UK Research and Innovation (UKRI), and supported via UK’s International Science Partnerships Fund (ISPF), and the Irish Government’s Shared Island initiative. Genome size plant sample collection and flow cytometry from North America sites and all cell size data collection was funded by an NSF CAREER grant awarded to EHG (NSF-DEB-Award #1941309, nsf.gov). JM’s PhD studentship was funded by Queen Mary University of London ( www.qmul.ac.uk ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Introduction
Genome size (GS) varies >2,400-fold across angiosperms [1], the largest range found in any comparable eukaryotic group. It has been proposed that GS variation impacts many aspects of a plant’s biology, including its life cycle, nutrient demands, water-use efficiency, and minimum cell size [2]. Considering nutrient demands, species with comparatively larger GS are hypothesized to be more growth-limited by low nitrogen (N) and/or phosphorus (P) availability, and to show greater positive growth responses following N and P additions than plants with comparatively smaller GS, owing to the hypothesized increased N and P costs of building and maintaining larger genomes [3,4]. In support of these hypotheses, greenhouse experiments comparing diploid and polyploid cytotypes have shown that plants with comparatively larger genomes exhibit faster growth relative to those with smaller genomes when grown under plentiful N- and P, but such advantages are lost when either of these nutrients are limiting [5–7]. In addition, experiments at single grassland sites have shown that plant species with larger GS are more productive on N and/or P-fertilized plots compared with low N and/or P plots [3,4,8,9]. What is not known to our knowledge is how widespread interactions between GS and nutrients on plant growth are across areas in separate geographical regions, characterized by different climatic conditions and species assemblages. Grassland ecosystems cover approximately 40% of global land area, providing diverse ecosystem services [10–12], and improved understanding of GS-nutrient interactions may lend increased predictive power in terms of how these ecosystems may change following anthropogenic eutrophication under climate change.
In grasslands worldwide, N and P fertilization has been shown to increase community productivity but lower species diversity [10,11]. This is because fertilization shifts communities towards those that compete more for light than for nutrients, with the most successful plants being those that are taller, which receive more light per unit size and are able to shade out competitors [12–14]. Furthermore, research has shown that when species compete for limiting resources (such as nutrients or water), those requiring lower levels of that resource are better able to outcompete other species [10,15]. Applied to grasslands, where N and/or P availability often limit productivity [16–18], we predict that species with smaller genomes exhibit faster growth rates under ambient site conditions relative to those with larger genomes, because they have lower cellular N and P requirements. Upon fertilization, however, we predict species with comparatively larger genomes are released from GS-nutrient constraints, enabling faster growth. In part, this faster growth may arise from increased rates of cell expansion, due to their increased minimum cell size [19,20] and/or from hybrid vigor in polyploids [21]; both allowing larger GS plants to outcompete smaller GS plants via shading [8].
Climatic factors, such as temperature and water availability, could also alter the effects of nutrient limitation on productivity [16,22] and differentially influence N and P treatment responses dependent upon species’ GS. For example, higher ambient temperatures favor growth by cell division rather than by cell expansion [19] resulting in faster biochemical reaction rates [23], which could potentially increase N and P demands and cellular N and P allocation trade-offs. Warmer climates would therefore be predicted to favor smaller GS species [24,25], which have lower N and P demands and faster cell division rates [26]. Low water availability may also influence plant growth rates dependent upon GS, although opposing hypotheses exist as to whether increased water availability will favor or disadvantage species with comparatively larger GS [27,28]. For example, increased stomatal size [29] of species with larger genomes could result in increased water loss [30] and lower water-use efficiency, if the increased size leads to increased overall stomatal pore area (area × density). Under such a scenario, low water availability should favor smaller GS species independent of nutrient availability [2,28]. Alternatively, the increased cell size of larger GS species may increase their water tissue storage capacity [27], and increase water-use efficiency if the total pore area per unit of leaf area does not increase [31], enabing them to store and conserve more water and hence maintain faster growth rates under drier conditions than smaller GS species. Furthermore, intra-annual fluctuations in temperature and precipitation could also affect GS-dependent growth nutrient interactions. Areas with more restricted growing seasons or with extreme wet and dry cycles might favor faster-growing species, which may benefit species with smaller genomes that have faster cell division rates and generation times [26,28]. In contrast, areas with longer, cooler growing seasons might favor growth by cell expansion [19] and thus species with larger GS, which have greater minimum cell sizes and can potentially grow while undergoing fewer costly cell cycles than those with smaller genomes.
Plant groups often differ in their resource requirements and allocation strategies [32,33] and such differences could also influence GS-dependent growth responses to nutrients. For example, C 4 plants are likely to respond less to N fertilization than C 3 plants, as they have a higher N-use efficiency [34,35]. Therefore, C 3 plants with larger genomes may be more sensitive to changes in nutrient availability than C 4 plants. Furthermore, it might be particularily advantageous for annual species growing in more seasonal climates with extreme fluctuations in climatic conditions to possess a small genome, as it would enable them to undergo faster cell cycles and grow quicker during the short periods when conditions are favorable for growth [36,37]. Lastly, rhizobium symbiosis in legumes and the ability of geophytes to store nutrients in underground storage organs [38,39] may increase the tolerance of species with larger genomes to N and/or P limitation [40], rendering them less responsive to N and P fertilization.
To decipher how these different factors might impact the GS-dependent growth responses to N and P, we address how GS and N and P fertilization affect plant growth on 27 grassland sites distributed across 2 continents in the Northern Hemisphere (S1 Fig and S1 Table). Sites varied in both climatic conditions (e.g., temperature, water availability, and seasonality) and in species assemblages (including species differing in their photosynthetic pathway (i.e., C 3 /C 4 ) and functional groups). All communities were on sites within the Nutrient Network, a global research collaboration that established the same experimental design which controls for nutrient treatment and which generates data on grassland productivity, diversity, and community composition (
https://nutnet.org/ [41]). By combining species GS, percent cover, functional group, and site climatic data, we tested the following 3 hypotheses using a range of approaches, including phylogenetically corrected models:
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