Developmental and biophysical determinants of grass leaf size worldwide

One of the most notable ecological trends—described more than 2,300 years ago by Theophrastus—is the association of small leaves with dry and cold climates, which has recently been recognized for eudicotyledonous plants at a global scale. For eudicotyledons, this pattern has been attributed to the fact that small leaves have a thinner boundary layer that helps to avoid extreme leaf temperatures and their leaf development results in vein traits that improve water transport under cold or dry climates. However, the global distribution of leaf size and its adaptive basis have not been tested in the grasses, which represent a diverse lineage that is distinct in leaf morphology and that contributes 33% of terrestrial primary productivity (including the bulk of crop production). Here we demonstrate that grasses have shorter and narrower leaves under colder and drier climates worldwide. We show that small grass leaves have thermal advantages and vein development that contrast with those of eudicotyledons, but that also explain the abundance of small leaves in cold and dry climates. The worldwide distribution of leaf size in grasses exemplifies how biophysical and developmental processes result in convergence across major lineages in adaptation to climate globally, and highlights the importance of leaf size and venation architecture for grass performance in past, present and future ecosystems

Migration to colder climates in grasses involves pre-existing and adaptive traits

A large number of transitions between climates have been found in phylogenetic trees, but some clades with particular features are more likely to shift to new climates than others. Several traits have previously been associated with these multiple transitions. In order to understand how traits are involved in transitions between climates, the enabling effects of traits on transitions and the evolution of traits in new climates need to be identified. The diversity of species that have made multiple transitions between climates in grasses allows the phylogenetic comparative method to be used to address this issue. In this thesis, I investigated the morphological, physiological and genomic traits which have been hypothesised to be enablers of, or adaptations to, the transitions between climates. I provide evidence that pre-existing traits are important factors in facilitating the migration between climates. Using a biogeographical analysis, I first showed that the evolution of C4 photosynthesis in tropical climates facilitates transitions into cooler climates and expansion into warmer climates. This is consistent with modelling analyses which show that the benefits of C4 photosynthesis for canopy carbon gain are maximised at high temperatures, but remain significant at low temperatures if leaves can resist chilling and freezing. Using an experimental approach, I next showed that transitions into cold climates were facilitated by additional pre-existing traits that provide constitutive chilling and freezing resistances. These also arise initially in tropical species. Freezing resistance was determined by osmotic pressure, moisture content and cold acclimation, which influence the transition to cold climates, while chilling resistance was associated with culm height and leaf width. Therefore the combined facilitating effects of pre-existing traits determined the initiation of transitions into new climates. However, the adaptive evolution of traits to improve the efficiency of a plant after migration to new environments may also be required for specialism in cold climates. I found that cold acclimation to increase freezing tolerance evolved after migration to cold climates. This suggests that cold acclimation may enhance the efficiency of freezing resistance. In particular, I found signatures of adaptive evolution to cold climates in chloroplast genes encoding proteins which function in the structural stability of the photosystems. These findings suggest that pre-existing traits facilitate migration to new climates, but their efficiency depends on the total effect of related traits. Once in new climates, the additional adaptive evolution of multiple traits is required for a plant to become successful

Data from: C4 photosynthesis evolved in warm climates but promoted migration to cooler ones

C4 photosynthesis is considered an adaptation to warm climates, where its functional benefits are greatest and C4 plants achieve their highest diversity and dominance. However, whether inherent physiological barriers impede the persistence of C4 species in cool environments remains debated. Here, we use large grass phylogenetic and geographic distribution datasets to test whether (i) temperature influences the rate of C4 origins, (ii) photosynthetic types affect the rate of migration among climatic zones, and (iii) C4 evolution changes the breadth of the temperature niche. Our analyses show that C4 photosynthesis in grasses originated in tropical climates, and that C3 grasses were more likely to colonize cold climates. However, migration rates among tropical and temperate climates were higher in C4 grasses. Therefore, while the origins of C4 photosynthesis were concentrated in tropical climates, its physiological benefits across a broad temperature range expanded the niche into warmer and enabled diversification into cooler environments

grass_temp_data

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