Do we Underestimate the Importance of Leaf Size in Plant Economics? Disproportional Scaling of Support Costs Within the Spectrum of Leaf Physiognomy

Niinemets, Ülo; Portsmuth, Angelika; Tena, David; Tobias, Mari; Matesanz, Silvia; Valladares, Fernando

doi:10.1093/aob/mcm107

Cited by 206 publications

(183 citation statements)

References 70 publications

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“…The negative relationship was strongest in LiC, and smaller and not significant in LiN, indicating that extent of the trade-off may be conditiondependent. A similar negative relationship was recently shown between N percentage, as a proxy of protein concentration, and the dry to fresh mass ratio in 122 vascular plant species 39 as well as between N content and leaf weight in barley 40 , demonstrating the generality of the trade-off between size and protein concentration within and across species, as well as its importance in an ecological context and in crop plants.…”

Section: Resultssupporting

confidence: 79%

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

et al. 2014

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Growth often involves a trade-off between the performance of contending tasks; metabolic plasticity can play an important role. Here we grow 97 Arabidopsis thaliana accessions in three conditions with a differing supply of carbon and nitrogen and identify a trade-off between two tasks required for rosette growth: increasing the physical size and increasing the protein concentration. We employ the Pareto performance frontier concept to rank accessions based on their multitask performance; only a few accessions achieve a good trade-off under all three growth conditions. We determine metabolic efficiency in each accession and condition by using metabolite levels and activities of enzymes involved in growth and protein synthesis. We demonstrate that accessions with high metabolic efficiency lie closer to the performance frontier and show increased metabolic plasticity. We illustrate how public domain data can be used to search for additional contending tasks, which may underlie the sub-optimality in some accessions. L iving organisms perform many different and sometimes contending tasks, leading to trade-offs in which optimal performance of one task comes at the cost of a sub-optimal performance of another task. Trade-offs are influenced by the environment and their resolution depends on metabolic resources and plasticity 1,2 . One important environmental variable affecting plant growth is resource availability 3-6 . We first ask whether there is a trade-off between two tasks during vegetative growth of Arabidopsis thaliana: the maximization of physical size and the maximization of protein concentration. We then apply two methods to rank accessions: the first based solely on the performance of tasks, and the second based on the efficiency with which metabolic resources are deployed to perform tasks. In addition, we investigate whether the trade-off and the ranking of accessions are affected by the availability of carbon (C) and nitrogen (N) and the way in which it shapes the accession-specific metabolic profiles.Plants use light energy to transform CO 2 and inorganic nutrients into a plethora of metabolic precursors that are used to drive growth. As plants are sessile, resource acquisition is constrained by their physical size. In land plants, the majority of a mature cell is occupied by the vacuole, allowing the generation of a much larger physical size per unit protein than is usually obtained by microbes or animals 7 . For simplification, we do not consider the impact of shape and phenology on the relation between physical size and resource acquisition. On the other hand, proteins are required to catalyse the transformation of resources into biomass. In particular, the majority of the protein in a plant leaf is involved in photosynthesis [8][9][10] . We hypothesize that there is a trade-off between physical size and protein concentration. While production of leaves with a higher protein concentration will allow higher rates of photosynthesis and metabolism per unit biomass, it also increases the costs of growth a...

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Section: Resultssupporting

confidence: 79%

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

et al. 2014

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“…The needles and scale leaves of conifers are successful in high light but there are clear limits on the utility of this hydraulic design where competition for light is intense in the forest understorey. A general trend of increased leaf size in plants grown under low light (Givnish 1987;Abrams and Kubiske 1990) suggests that the economic benefits of large leaf size for reducing the proportion of mechanical support costs (Westoby and Wright 2003;Niinemets et al 2007a) become important in the understorey (Saldaña et al 2007). Because of the hydraulic constraint on maximum width, needles can increase in size only by increasing length.…”

Section: Needles and Scalesmentioning

confidence: 99%

“…Explicit determination of the construction costs of venation (cf. Niinemets et al 2006Niinemets et al , 2007aNiinemets et al , 2007b should be a priority for future work on leaf hydraulics. Formulating the details of cost v. benefit as it applies to hydraulic investment and photosynthetic gain will provide a basis for interpreting patterns of leaf hydraulic architecture in extant natural vegetation as well as in fossil floras.…”

Section: Hydraulic Supply and Leaf Economicsmentioning

confidence: 99%

Viewing leaf structure and evolution from a hydraulic perspective

Brodribb

Feild

Sack³

2010

Functional Plant Biol.

254

230

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Abstract. More than 40 000 km 3 year -1 of water flows through the intricate hydraulic pathways inside leaves. This water not only sustains terrestrial productivity, but also constitutes nearly 70% of terrestrial evapotranspiration, thereby influencing both global and local climate (Chapin et al. 2002). Thus, the central role played by leaf vascular systems in terrestrial biology provides an important context for research into the function and evolution of water transport in leaves. Significant progress has been made recently towards understanding the linkages between anatomy and water transport efficiency in leaves, and these discoveries provide a novel perspective to view the evolution of land plants.

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“…However, right-skewed leaf size frequency distributions may also reflect biologically prevalent allometric trends whose adaptive significance remains problematic or obscure. For example, it has been suggested that plant height and twig size have significant effects on leaf size optimization (e.g., Ackerly and Donoghue 1998;Cornelissen 1999;Westoby and Wright 2003;Sun et al 2006;Xiang et al 2009) and that large leaves require disproportionally more mechanical tissues (both within the leaf lamina and within subtending stems) than do smaller leaves (Givnish 1984;Niklas 1999;Niinemets and Kullm 1999;Niinemets et al 2006Niinemets et al , 2007aLi et al 2008). Due to these allometry relationships, small leaves may confer adaptive benefits indirectly, i.e., the focus of natural selection may not be directly on leaf size per se.…”

Section: Leaf Size Frequency Distributions Within Habitatsmentioning

confidence: 99%

“…However, for interspecific variation within habitats with similar macroclimatic conditions, leaf size has been assumed to be a neutral trait confounded by community phylogenetic composition, or simply an allometric consequence of plant size, anatomy, or architecture. For example, leaf size has been found to be significantly correlated with plant height (Ackerly and Donoghue 1998;Cornelissen 1999), subtending twig size (Brouat et al 1998;Westoby and Wright 2003;Sun et al 2006), within-leaf biomass allocation and physiology (Niinemets et al 2006(Niinemets et al , 2007aNiklas et al 2007;Li et al 2008), and seed or fruit size (Ackerly and Donoghue 1998;Cornelissen 1999;Westoby and Wright 2003).…”

Section: Introductionmentioning

confidence: 99%

Testing the generality of the ‘leafing intensity premium’ hypothesis in temperate broad-leaved forests: a survey of variation in leaf size within and between habitats

Sun

2009

Evol Ecol

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Because leaf size scales negatively and isometrically with leaf number per shoot size (leafing intensity) in woody species, and because most tree and shrub species have small leaves, Kleiman and Aarssen (J Ecol 95:376-382, 2007) recently proposed that natural selection favors high leafing intensity resulting in small leaves, i.e., the leafingintensity-premium hypothesis. However, empirical evidence for or against this hypothesis is still lacking. In addition, this hypothesis has not been examined in the context of how leaf size varies among habitats. To fill this void, we investigated leaf size frequency distributions of woody species from temperate China and explored the relationships among leaf mass, leaf number, and stem mass of current-year shoots of 133 woody species at low and high altitudes of three mountain ranges. The scaling relationships between leaf size and leafing intensity (leaf number per stem mass) were determined using both standardized major axis regression analyses and phylogenetically independent comparative techniques. In light of the leafing-intensity-premium hypothesis, we made three predictions: (1) leaf size frequency distributions should be right-skewed for each local study area and for the entire study region, (2) leafing intensities at different altitudes at different sites should differ while leafing intensities at comparable altitudes should be similar baring large taxonomic differences among sites, and (3) that leafing intensity should be higher for any given leaf size in habitats with small-leaved species. Significant negative and isometric scaling relationships between leaf size and leafing intensity were found to be consistently conserved independent of habitat type, both across species and across correlated evolutionary divergences. Within each mountain range or across the entire study region, leaf size frequency distributions were right-skewed, in accordance with our prediction. However, leafing intensity was smaller for any given leaf size at the altitude with smaller leafed 123Evol Ecol (2010) 24:685-701 DOI 10.1007 species than for altitudes characterized by large leafed species, i.e., altitudes characterized by species with small leaves did not have consistently higher leafing intensities than other altitudes on each mountain range. Our analyses therefore indicate the direct adaptive value of leaf size but not the selective advantage in high leafing intensity as posited by the leafing-intensity-premium hypothesis. We suggest that this hypothesis explains less about the variation of leaf size among different habitats as it does about variation within habitats, i.e., the relative importance of the adaptive significance of leafing intensity and leaf size can and does vary with habitats.

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Do we Underestimate the Importance of Leaf Size in Plant Economics? Disproportional Scaling of Support Costs Within the Spectrum of Leaf Physiognomy

Cited by 206 publications

References 70 publications

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

Viewing leaf structure and evolution from a hydraulic perspective

Testing the generality of the ‘leafing intensity premium’ hypothesis in temperate broad-leaved forests: a survey of variation in leaf size within and between habitats

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