Surprisingly weak coordination between leaf structure and function among closely-related tomato species

Muir, Christopher D.; Conesa, Miquel À.; Roldán, Emilio J.; Molins, Arántzazu; Galmés, Jeroni

doi:10.1101/031328

Cited by 4 publications

(1 citation statement)

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“…(), Muir et al . () and Mason & Donovan () also failed to find a number of LES trait relationships among species within the Viburnum , Solanum and Helianthus genera, respectively. Conversely, studying tropical trees, Santiago & Mulkey () found correlations between traits from the LES and CR.…”

Section: Discussionmentioning

confidence: 96%

Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network

et al. 2017

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Summary Plant phenotypic diversity is shaped by the interplay of trade‐offs and constraints in evolution. Closely integrated groups of traits (i.e. trait dimensions) are used to classify plant phenotypic diversity into plant strategies, but we do not know the degree of interdependence among trait dimensions. To assess how selection has shaped the phenotypic space, we examine whether trait dimensions are independent. We gathered data on saplings of 24 locally coexisting tree species in a temperate forest, and examined the correlation structure of 20 leaf, branch, stem and root traits. These traits fall into three well‐established trait dimensions (the leaf economic spectrum, the wood spectrum and Corner's Rules) that characterize vital plant functions: resource acquisition, sap transport, mechanical support and canopy architecture. Using ordinations, network analyses and Mantel tests, we tested whether the sapling phenotype of these tree species is organized along independent trait dimensions. Across species, the sapling phenotype is not structured into clear trait dimensions. The trait relationships defining trait dimensions are either weak or absent and do not dominate the correlation structure of the sapling phenotype as a whole. Instead traits from the three commonly recognized trait dimensions are organized into an integrated trait network. The effect of phylogeny on trait correlations is minimal. Our results indicate that trait dimensions apparent in broad‐based interspecific surveys do not hold up among locally coexisting species. Furthermore, architectural traits appear central to the phenotypic network, suggesting a pivotal role for branching architecture in linking resource acquisition, mechanical support and hydraulic functions. Synthesis. Our study indicates that local and global patterns of phenotypic integration differ and calls into question the use of trait dimensions at local scales. We propose that a network approach to assessing plant function more effectively reflects the multiple trade‐offs and constraints shaping the phenotype in locally co‐occurring species.

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Section: Discussionmentioning

confidence: 96%

Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network

et al. 2017

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Independent evolution of ab- and adaxial stomatal density enables adaptation

Muir

Conesa

Galmés

2015

Preprint

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1• Are organisms free to reach their adaptive optima or constrained by hard-2 wired developmental programs? Recent evidence suggests that the arrangement 3 of stomata on abaxial (lower) and adaxial (upper) leaf surfaces may be an 4 important adaptation in plants, but stomatal traits on each surface likely share 5 developmental pathways that could hamper evolution. 6 • We reviewed the quantitative genetics of stomatal density to look for loci that 7 (1) affected ab-or adaxial density independently or (2) pleiotropically affected 8 stomatal density on both surfaces. We also used phylogenetic comparative 9 methods to test for independent versus correlated evolution of stomatal traits 10 (density, size, and pore index) on each surface from 14 amphistomatous wild 11 tomato taxa (Solanum; Solanaceae). 12• Naturally occurring and laboratory-induced genetic variation alters stomatal 13 density on one surface without affecting the other, indicating that develop-14 ment does not strongly constrain the spectrum of available mutations. Among 15 wild tomato taxa, traits most closely related to function (stomatal pore index 16 and density) evolved independently on each surface, whereas stomatal size was 17 constrained by correlated evolution. 18• Genetics and phylogenetics demonstrate mostly independent evolution of stom-19 atal function on each leaf surface, facilitating largely unfettered access to fitness 20 optima. 21 2 Keywords 22 Adaptation, correlated evolution, developmental constraint, phylogenetic compara-23 tive methods, quantitative genetics, Solanum, stomata, stomatal ratio 24 Introduction 25 Are traits able to evolve independently of one another or they constrained by de-26 velopment, genetic, or functional connections? Here, we examine whether stomata 27 on the abaxial ('lower') surface of the leaf evolve independently of adaxial ('upper') 28 stomata. Stomata are microscopic pores on the leaf surface formed by a pair of guard 29cells. The density, size, and arrangement of stomata on a leaf set the maximum stom-30 atal conductance to CO 2 diffusing into a leaf and the amount of water that transpires 31 from it (Parkhurst, 1978; Sack et al., 2003; Franks and Farquhar, 2001; Galmés et al., 32 1975). Hence, stomatal traits like density, size, and ratio of upper to lower stomata 33 have strong effects on carbon assimilation and water-use efficiency. 34An unresolved question is whether stomatal size and density on each leaf surface 35 can evolve independently or are tethered together by shared development. Stomata 36 are most often found only on the lower leaf surface (hypostomy), but occur on both 37 surfaces (amphistomy) in some species (Metcalfe and Chalk, 1950; Parkhurst, 1978; 38 Mott et al., 1984), especially herbs (Salisbury, 1927; Muir, 2015) and plants from 39 open habitats (Mott et al., 1984; Gibson, 1996; Jordan et al., 2014). The proportion 40 of stomata found on the upper surface also tends to increase during domestication, 41 even as the total stomatal density stays constant (...

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Genetic Architecture and Molecular Networks Underlying Leaf Thickness in Desert-Adapted TomatoSolanum pennellii

Coneva

Frank

Balaguer

et al. 2017

Preprint

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Thicker leaves allow plants to grow in water-limited conditions. However, our understanding of the genetic underpinnings of this highly functional leaf shape trait is poor. We used a custom-built confocal profilometer to directly measure leaf thickness in a set of introgression lines (ILs) derived from the desert tomato species Solanum pennellii, and identified quantitative trait loci (QTL). We report evidence of a complex genetic architecture of this trait and roles for both genetic and environmental factors. Several ILs with thick leaves have dramatically elongated palisade mesophyll cells and, in some cases, increased leaf ploidy. We characterized thick ILs 2-5 and 4-3 in detail and found increased mesophyll cell size and leaf ploidy levels, suggesting that endoreduplication underpins leaf thickness in tomato. Next, we queried the transcriptomes and inferred Dynamic Bayesian Networks of gene expression across early leaf ontogeny in these lines to compare the molecular networks that pattern leaf thickness. We show that thick ILs share S. pennellii-like expression profiles for putative regulators of cell shape and meristem determinacy, as well as a general signature of cell cycle related gene expression. However, our network data suggest that leaf thickness in these two lines is patterned by at least partially distinct mechanisms. Consistent with this hypothesis, double homozygote lines combining introgression segments from these two ILs show additive phenotypes including thick leaves, higher ploidy levels and larger palisade mesophyll cells. Collectively, these data establish a framework of genetic, anatomical, and molecular mechanisms that pattern leaf thickness in desert-adapted tomato.

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Surprisingly weak coordination between leaf structure and function among closely-related tomato species

Cited by 4 publications

References 3 publications

Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network

Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network

Independent evolution of ab- and adaxial stomatal density enables adaptation

Genetic Architecture and Molecular Networks Underlying Leaf Thickness in Desert-Adapted TomatoSolanum pennellii

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