Plant Phenotypes as Distributions: Johannsen's Beans Revisited.

AbstractIn the early twentieth century, Wilhelm Johannsen's breeding experiments on pure lines of beans provided empirical support for his groundbreaking distinction between phenotype and genotype, the foundation stone of classical genetics. In contrast with the controversial history of the genotype concept, the notion of phenotype has remained essentially unrevised since then. The application of the Johannsenian concept of phenotype to modularly built, nonunitary plants, however, needs reexamination. In the first part of this article it is shown that Johannsen's appealing solution for dealing with the multiplicity of nonidentical organs produced by plant individuals (representing individual plant phenotypes by arithmetic means), which has persisted to this day, reflected his intellectual commitment to nineteenth-century typological thinking. Revisitation of Johannsen's results using current statistical tools upholds his major conclusion about the nature of heredity but at the same time falsifies two important ancillary conclusions of his experiments-namely, the alleged homogeneity of pure lines (genotypes) regarding seed weight variability and the lack of transgenerational effects of within-line (within-genotype) seed weight variation. The canonical notion of individual plant phenotypes as arithmetic means should therefore be superseded by a concept of phenotype as a dual property, consisting of central tendency and variability components of organ trait distribution. Phenotype duality offers a unifying framework applicable to all nonunitary organisms.

Lifetime genealogical divergence within plants leads to epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae).

Epigenetic mosaicism is a possible source of within-plant phenotypic heterogeneity, yet its frequency and developmental origin remain unexplored. This study examines whether extant epigenetic heterogeneity within Lavandula latifolia (Lamiaceae) shrubs reflects recent epigenetic modifications experienced independently by different plant parts or, alternatively, it is the cumulative outcome of a steady lifetime process. Leaf samples from different architectural modules (branch tips) were collected from three L. latifolia plants and characterized epigenetically by global DNA cytosine methylation and methylation state of methylation-sensitive amplified fragment-length polymorphism (MS-AFLP) markers. Epigenetic characteristics of modules were then assembled with information on the branching history of plants. Methods borrowed from phylogenetic research were used to assess genealogical signal of extant epigenetic variation and reconstruct within-plant genealogical trajectory of epigenetic traits. Plants were epigenetically heterogeneous, as shown by differences among modules in global DNA methylation and variation in the methylation states of 6 to 8% of MS-AFLP markers. All epigenetic features exhibited significant genealogical signal within plants. Events of epigenetic divergence occurred throughout the lifespan of individuals and were subsequently propagated by branch divisions. Internal epigenetic diversification of L. latifolia individuals took place steadily during their development, a process which eventually led to persistent epigenetic mosaicism.

Within-plant heterogeneity in fecundity and herbivory induced by localized DNA hypomethylation in the perennial herb Helleborus foetidus.

PREMISE: Phenotypic heterogeneity of reiterated, homologous structures produced by individual plants has ecological consequences for plants and their animal consumers. This paper examines experimentally the epigenetic mosaicism hypothesis, which postulates that within-plant variation in traits of reiterated structures may partly arise from different parts of the same genetic individual differing in patterns or extent of genomic DNA methylation. METHODS: Leaves of paired ramets borne by field-growing Helleborus foetidus plants were infiltrated periodically over the entire flowering period with either a water solution of the demethylating agent zebularine or just water as the control. The effects of the zebularine treatment were assessed by quantifying genome-wide DNA cytosine methylation in leaves and monitoring inflorescence growth and flower production, number of ovules per flower, pollination success, fruit set, seed set, seed size, and distribution of sap-feeding insects. RESULTS: Genomic DNA from leaves in zebularine-treated ramets was significantly less methylated than DNA from leaves in control ones. Inflorescences in treated ramets grew smaller and produced fewer flowers, with fewer ovules and lower follicle and seed set, but did not differ from inflorescences in untreated ramets in pollination success or seed size. The zebularine treatment influenced the within-plant distribution of sap-feeding insects. CONCLUSIONS: Experimental manipulation of genomic DNA methylation level in leaves of wild-growing H. foetidus plants induced considerable within-plant heterogeneity in phenotypic (inflorescences, flowers, fecundity) and ecologically relevant traits (herbivore distribution), which supports the hypothesis that epigenetic mosaicism may partly account for within-plant variation.

Plant subindividual functional diversity and carbon cycling.

Plant subindividual trait variation is a neglected level of functional diversity that contributes to the variation of phenotypes and ecological communities. Disregarding the role of subindividual functional diversity (SFD) in nature may lead to incorrect understanding of spatial and temporal scales of relationships between trait diversity, ecosystem function, and carbon cycling.

Phenotypic, epigenetic, and fitness diversity within plant genotypes.

Plant plastic responses to environmental variation, at scales smaller than the individual plant size, promote phenotypic and epigenetic diversity among repeated structures within genotypes. Different epigenetic marks in the somatic line can translate to the germline and seeds, generating a fitness patchwork in the progeny with unexplored effects on plant evolutionary dynamics.