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G. Ledyard Stebbins and the evolutionary synthesis.

More than any other individual, Stebbins synthesized knowledge from a disparate set of areas that included plant genetics, systematics, and evolution. This work culminated in 1950 with the appearance of his magnum opus, Variation and Evolution in Plants. This book gave plant evolution a coherent framework that was compatible with that emerging from the work of Theodosius Dobzhansky, Ernst Mayr, G. G. Simpson, and Julian Huxley, and others associated with establishing the synthetic theory of evolution. For this work he is regarded as the botanical "architect" of the evolutionary synthesis.

Biological Evolution↗

Photoprotection by Cichorum endivia extracts: prevention of UVB-induced erythema, pyrimidine dimer formation and IL-6 expression.

In the gradual process of evolution, plants have developed natural sun protecting substances that enable continuous survival under direct and intense ultraviolet (UV) radiation. As part of our studies of plant-derived pigments that might constitute an alternative to conventional sunscreens, we have tested the ethanolic extracts of roots, stalks, and inflorescences of populations of wild Cichorum endivia subsp. Divaricatum (Asteraceae) in terms of protection against sunburn, and in prevention of UVB-induced pyrimidine dimer formation and IL-6 mRNA expression in the human keratinocyte cell line, HaCaT. Using ELISA technique for detection of pyrimidine dimers and RT-PCR for detection of IL-6, we found that the ethanolic extract of C. endivia roots absorbs radiation in the UVB spectrum and partially prevents induction of pyrimidine dimers and IL-6 expression. Application of the root extract on the skin prior to UVB irradiation totally prevented erythema. Our findings suggest that C. endivia extracts might possess sun-protective qualities that make them useful as sunscreens.

Administration, Cutaneous↗

MEANtools integrates multi-omics data to identify metabolites and predict biosynthetic pathways.

During evolution, plants have developed the ability to produce a vast array of specialized metabolites, which play crucial roles in helping plants adapt to different environmental niches. However, their biosynthetic pathways remain largely elusive. In the past decades, increasing numbers of plant biosynthetic pathways have been elucidated based on approaches utilizing genomics, transcriptomics, and metabolomics. These efforts, however, are limited by the fact that they typically adopt a target-based approach, requiring prior knowledge. Here, we present MEANtools, a systematic and unsupervised computational integrative omics workflow to predict candidate metabolic pathways de novo by leveraging knowledge of general reaction rules and metabolic structures stored in public databases. In our approach, possible connections between metabolites and transcripts that show correlated abundance across samples are identified using reaction rules linked to the transcript-encoded enzyme families. MEANtools thus assesses whether these reactions can connect transcript-correlated mass features within a candidate metabolic pathway. We validate MEANtools using a paired transcriptomic-metabolomic dataset recently generated to reconstruct the falcarindiol biosynthetic pathway in tomato. MEANtools correctly anticipated five out of seven steps of the characterized pathway and also identified other candidate pathways involved in specialized metabolism, which demonstrates its potential for hypothesis generation. Altogether, MEANtools represents a significant advancement to integrate multi-omics data for the elucidation of biochemical pathways in plants and beyond.

Metabolomics↗

Herbivory could unlock mutations sequestered in stratified shoot apices of genetic mosaics.

Many higher plants have shoot apical meristems that possess discrete cell layers, only one of which normally gives rise to gametes following the transition from vegetative meristem to floral meristem. Consequently, when mutations occur in the meristems of sexually reproducing plants, they may or may not have an evolutionary impact, depending on the apical layer in which they reside. In order to determine whether developmentally sequestered mutations could be released by herbivory (i.e., meristem destruction), a characterized genetic mosaic was subjected to simulated herbivory. Many plants develop two shoot meristems in the leaf axils of some nodes, here referred to as the primary and secondary axillary meristems. Destruction of the terminal and primary axillary meristems led to the outgrowth of secondary axillary meristems. Seed derived from secondary axillary meristems was not always descended from the second apical cell layer of the terminal shoot meristem as is expected for terminal and primary shoot meristems. Vegetative and reproductive analysis indicated that secondary meristems did not maintain the same order of cell layers present in the terminal shoot meristem. In secondary meristems reproductively sequestered cell layers possessing mutant cells can be repositioned into gamete-forming cell layers, thereby adding mutant genes into the gene pool. Herbivores feeding on shoot tips may influence plant evolution by causing the outgrowth of secondary axillary meristems.

Journal Article↗

Costs of plasticity in foraging characteristics of the clonal plant Ranunculus reptans.

In clonal plants, evolution of plastic foraging by increased lengths of leaves and internodes under unfavourable conditions may be constrained by costs and limits of plasticity. We studied costs and limits of plasticity in foraging characteristics in 102 genotypes of the stoloniferous herb Ranunculus reptans. We grew three replicates of each genotype with and three without competition by the naturally co-occuring grass Agrostis stolonifera. We used regression and correlation analyses to investigate potential costs of plasticity in lengths of leaves and stolon internodes, developmental instability costs of these traits, and a developmental range limit of these traits. We used randomization procedures to control for spurious correlations between parameters calculated from the same data. Under competition the number of rosettes, rooted rosettes, and flowers was 58%, 40%, and 61% lower, respectively, than in the absence of competition. Under competition lengths of leaves and stolon internodes were 14% and 6% smaller, respectively, than in the absence of competition. We detected significant costs of plasticity in stolon internode length in the presence of competition when fitness was measured in terms of the number of rosettes and the number of flowers (selection gradients against plasticity were 0.250 and 0.214, respectively). Within-environment variation (SD) in both foraging traits was not positively correlated with the corresponding plasticity, which indicates that there were no developmental instability costs. More plastic genotypes did not have less extreme trait values than less plastic genotypes for both foraging traits, which indicates that there was no developmental range limit. We conclude that in R. reptans costs of plasticity more strongly constrain evolution of foraging in the horizontal plane (i.e., stolon internode length) than in the vertical plane (i.e., leaf length).

Adaptation, Physiological↗

Architecture of the sperm cell of Psilotum.

In this correlated SEM (scanning electron microscope) and TEM (transmission electron microscope) investigation, we describe architectural details of the multiflagellated sperm cell of Psilotum nudum. Comparisons with other pteridophytes are made to (1) assess the placement of Psilotum among pteridophyte taxa and (2) evaluate structural modifications of sperm cells during land plant evolution. The released spermatozoid of Psilotum coils 2.0 revolutions and is outlined by a parallel band of up to 190 microtubules. The elongated nucleus is highly compacted and parallels the cellular coils with numerous mitochondria and starch-laden plastids distributed along its length. Along the anterior coil is an elaborate locomotory apparatus that includes ∼36 flagella that are inserted into the cell by basal bodies. Subtending the basal bodies is the multilayered structure, which consists of a long narrow lamellar strip and an overlying band of microtubules. An elongated anterior mitochondrion underlies the multilayered structure. Additional amyloplasts and mitochondria are aggregated along the anterior coil in association with the locomotory apparatus, while a fibrous band encircles the leading edge of the cell. Salient features of this cell, including details of the locomotory apparatus, structure and position of organelles, and arrangement of the spline, are shared by spermatozoids of Equisetum and ferns (including eusporangiate and leptosporangiate taxa). Thus, this study provides morphological support for the hypothesis that Psilotum nudum is a member of an assemblage that includes ferns and Equisetum. However, the less streamlined architecture of Psilotum gametes and the lack of architectural features shared with any specific taxon examined to date suggest that Psilotum is an early divergent fern, with relatively remote affinities to Ophioglossaceae and Equisetaceae.

Journal Article↗

The evolution of a plant globin gene family.

We have analyzed the sequences of soybean leghemoglobin genes as an initial step toward understanding their mode of evolution. Alignment of the sequences of plant globin genes with those of animals reveals that based on the proportion of nucleotide substitutions that have occurred at the first, second, and third codon positions, the time of divergence of plant and animal globin gene families appears to be extremely remote (between 900 million and 1.4 billion years ago, if one assumes constancy of evolutionary rate in both the plant and animal lineages) and in addition to the normal regulatory sequences on the 5' end, an approximately 30-base-pair sequence, specific to globin genes, that surrounds the cap site is conserved between the plant and animal globin genes. Comparison of the leghemoglobin sequences with one another shows that the relative amount of sequence divergence in various coding and noncoding regions is roughly similar to that found for animal globin genes and as in animal globin genes, the positions of insertions and deletions in the intervening sequences often coincide with the locations of direct repeats. Thus, the mode of evolution of the plant globin genes appears to resemble, in many ways, that of their animal counterparts. We contrast the overall intergenic organization of the plant globin genes with that of animal genes, and discuss the possibility of the concerted evolution of the leghemoglobin genes.

Animals↗

The Arabidopsis SHAGGY-related protein kinase (ASK) gene family: structure, organization and evolution.

Higher plants contain a multigene family encoding proteins that share a highly conserved catalytic protein kinase domain about 70% identical to SHAGGY protein kinase (SGG) and glycogen synthase kinase-3 (GSK-3), respectively, from Drosophila and mammals. In this study we have characterized the structure and evolution of the Arabidopsis SHAGGY-related protein kinase (ASK) gene family. At least ten ASK genes are present per haploid genome of Arabidopsis. The genomic sequences of five ASK genes show a strikingly high conservation of intron positions and exon lengths. Phylogenetic analyses suggested that the Arabidopsis gene family contains at least three ancient classes of genes that diverged early in land plant evolution. The different classes may reflect specificity of substrates and/or biological functions. Eight out of the ten predicted ASK genes were mapped and shown to be dispersed over the five Arabidopsis chromosomes. A tentative model for the organization and evolution of the Arabidopsis ASK genes is presented.

Arabidopsis↗

The Ty1-copia group of retrotransposons in plants: genomic organisation, evolution, and use as molecular markers.

The genomic organisation and diversity of the Ty1-copia group retrotransposons has been investigated in several crop plants and their relatives from both dicotyledonous and monocotyledonous families, including potato (Solanum tuberosum), faba beans (Vicia faba), Vicia melanops, Vicia sativa, barley (Hordeum vulgare), rye (Secale cereale), and onion (Allium cepa). Extreme heterogeneity in the sequence of the Ty1-copia retrotransposons from all these plants was revealed following sequence analysis of reverse transcriptase fragments. The estimated copy numbers of the Ty1-copia group retrotransposons for the genomes of S. tuberosum, L. esculentum, A. cepa, S. cereale, and V. faba is highly variable, ranging from a few hundred to approximately a million copies per genome. In situ hybridisation data from metaphase and prophase chromosomes of V. faba, S. cereale, and H. vulgare suggest that retrotransposon sequences are dispersed throughout the euchromatic regions of the genome but are almost undetectable in most heterochromatic regions. In contrast, similar data from metaphase chromosomes of A. cepa suggests that although retrotransposon sequences are dispersed throughout the euchromatic regions of the genome, they are predominantly concentrated in the terminal heterochromatin. These results are discussed in the context of the role played by the Ty1-copia group retrotransposons in the evolution of the plant genome. Lastly, the application of retrotransposon sequences as genetic markers for mapping genomes and for studying genetic biodiversity in plants is presented.

Chromosome Mapping↗

Markers derived from amplified fragment length polymorphism gels for plant ecology and evolution studies.

We describe the types of polymerase chain reaction (PCR) markers that we have isolated using amplified fragment length polymorphisms (AFLP) in closely related taxa from diverse plant genera. With these markers, both inter- and intraspecific differences have been identified. The characterization of the nucleotide sequences and fragment length polymorphisms of such AFLP-derived PCR markers is promising for investigating the ecology and evolution of closely related plant taxa.

Ecosystem↗

Function and evolution of the plant MADS-box gene family.

The function of MADS-box genes in flower and fruit development has been uncovered at a rapid pace over the past decade. Evolutionary biologists can now analyse the expression pattern of MADS-box genes during the development of different plant species, and study the homology of body parts and the evolution of body plans. These studies have shown that floral development is conserved among divergent species, and indicate that the basic mechanism of floral patterning might have evolved in an ancient flowering plant.

Animals↗

Plant snoRNAs: functional evolution and new modes of gene expression.

Small nucleolar RNAs (snoRNAs) are a well-characterized family of non-coding RNAs whose main function is rRNA modification. The diversity and complexity of this gene family continues to expand with the discovery of snoRNAs with non-rRNA or unknown targets. Plants contain more snoRNAs than other eukaryotes and have developed novel expression and processing strategies. The increased number of modifications, which will influence ribosome function, and the novel modes of expression might reflect the environmental conditions to which plants are exposed. Polyploidy and chromosomal rearrangements have generated multiple copies of snoRNA genes, allowing the generation of new snoRNAs for selection. The large snoRNA family in plants is an ideal model for investigation of mechanisms of evolution of gene families in plants.

Base Sequence↗

The evolution of plant-insect mutualisms.

Mutualisms (cooperative interactions between species) have had a central role in the generation and maintenance of life on earth. Insects and plants are involved in diverse forms of mutualism. Here we review evolutionary features of three prominent insect-plant mutualisms: pollination, protection and seed dispersal. We focus on addressing five central phenomena: evolutionary origins and maintenance of mutualism; the evolution of mutualistic traits; the evolution of specialization and generalization; coevolutionary processes; and the existence of cheating. Several features uniting very diverse insect-plant mutualisms are identified and their evolutionary implications are discussed: the involvement of one mobile and one sedentary partner; natural selection on plant rewards; the existence of a continuum from specialization to generalization; and the ubiquity of cheating, particularly on the part of insects. Plant-insect mutualisms have apparently both arisen and been lost repeatedly. Many adaptive hypotheses have been proposed to explain these transitions, and it is unlikely that any one of them dominates across interactions differing so widely in natural history. Evolutionary theory has a potentially important, but as yet largely unfilled, role to play in explaining the origins, maintenance, breakdown and evolution of insect-plant mutualisms.

Animals↗

Comprehensive identification and analysis of clusters of tandemly duplicated genes reveal their contributions to adaptive evolution of green plants.

Tandem gene duplication occurred more frequently compared with the episodic whole-genome duplication (WGD), providing a continuous supply of genetic material for evolutionary innovation and adaptation to changing environments. The rising roles of clusters of tandemly duplicated genes (CTDGs) in the evolution of phenotypic diversity have been unraveled in mammals. However, the content and biological roles of CTDGs remain largely unknown in plants. Here, we comprehensively identified CTDGs in 220 published plant genomes representing major lineages of green plants. The number of CTDGs showed great variation across taxa, ranging from 0 to 6028. The size of CTDGs varied from 2 to 47 genes, with small clusters containing two members predominating. Interestingly, significant expansion of CTDGs was found in early-diverging land plants and is closely associated with the evolution of key traits (e.g., ABA response, plant cuticle, UV-B resistance) required for plants to conquer terrestrial environments. Functional enrichment analysis revealed conserved and specialized functional profiles among different sizes of CTDGs in both Arabidopsis thaliana and the bryophyte Physcomitrium patens. Small CTDGs were enriched in fundamental stress responses, including protein modification, signal transduction, and responses to diverse stress stimuli, while large CTDGs were enriched in more sophisticated processes such as plant hormone biosynthesis and signaling, plant-microbe interactions, and reproductive processes. Expression pattern analyses of CTDGs under different stress conditions in A. thaliana and P. patens revealed that the highest number of CTDGs showed differential expression under drought stress, suggesting important roles of CTDGs in the evolution of desiccation tolerance in early land plants. The results of this study provide new additions to our knowledge about the abundance of CTDGs across green plants and reveal their important contributions to enable plants to overcome stressful environments on land.

Gene Duplication↗

Predicting evolution of floral traits associated with mating system in a natural plant population.

Evolution of floral traits requires that they are heritable, that they affect fitness, and that they are not constrained by genetic correlations. These prerequisites have only rarely been examined in natural populations. For Mimulus guttatus, we found by using the Riska-method that corolla width, anther length, ovary length and number of red dots on the corolla were heritable in a natural population. Seed production (maternal fitness) was directly positively affected by corolla width and anther size, and indirectly so by ovary length and number of red dots on the corolla. The siring success (paternal fitness), as estimated from allozyme data, was directly negatively affected by anther-stigma separation, and indirectly so by the corolla length-width ratio. Genetic correlations, estimated with the Lynch-method, were positive between floral size measures. We predict that larger flowers with larger reproductive organs, which generally favour outcrossing, will evolve in this natural population of M. guttatus.

Biological Evolution↗

The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants.

The entire mitochondrial genome of rice (Oryza sativa L.), a monocot plant, has been sequenced. It was found to comprise 490,520 bp, with an average G+C content of 43.8%. Three rRNA genes, 17 tRNA genes and five pseudo tRNA sequences were identified. In addition, eleven ribosomal protein genes and two pseudo ribosomal protein genes were found, which are homologous to 13 of the 16 genes for ribosomal proteins in the mitochondrial genome of the liverwort (Marchantia polymorpha). A greater degree of variation in terms of presence/absence and integrity of genes was observed among the ribosomal protein genes and tRNA genes of rice, Arabidopsis and sugar beet. Transcription and post-transcriptional modification (RNA editing) in the rice mitochondrial sequence were also examined. In all, 491 Cs in the genomic DNA were converted to Ts in cDNA. The frequency of RNA editing differed markedly depending upon the ORF considered. Sequences derived from plastid and nuclear genomes make up 6.3% and 13.4% of the mitochondrial genome, respectively. The degree of conservation of plastid sequences in the mitochondrial genome ranged from 61% to 100%, suggesting that sequence migration has occurred very frequently. Three plastid DNA fragments that were incorporated into the mitochondrial genome were subsequently transferred to the nuclear genome. Nineteen fragments that were similar to transposon or retrotransposon sequences, but different from those found in the mitochondrial genomes of dicots, were identified. The results indicate frequent and independent DNA sequence flow to and from the mitochondrial genome during the evolution of flowering plants, and this may account for the range of genetic variation observed between the mitochondrial genomes of higher plants.

Biological Evolution↗

Molecular evolution of the plant R regulatory gene family.

Anthocyanin pigmentation patterns in different plant species are controlled in part by members of the myc-like R regulatory gene family. We have examined the molecular evolution of this gene family in seven plant species. Three regions of the R protein show sequence conservation between monocot and dicot R genes. These regions encode the basic helix-loop-helix domain, as well as conserved N-terminal and C-terminal domains; mean replacement rates for these conserved regions are 1.02 x 10(-9) nonsynonymous nucleotide substitutions per site per year. More than one-half of the protein, however, is diverging rapidly, with nonsynonymous substitution rates of 4.08 x 10(-9) substitutions per site per year. Detailed analysis of R homologs within the grasses (Poaceae) confirm that these variable regions are indeed evolving faster than the flanking conserved domains. Both nucleotide substitutions and small insertion/deletions contribute to the diversification of the variable regions within these regulatory genes. These results demonstrate that large tracts of sequence in these regulatory loci are evolving at a fairly rapid rate.

Amino Acid Sequence↗