Bet-hedging and variability in plant development: seed germination and beyond.

When future conditions are unpredictable, bet-hedging strategies can be advantageous. This can involve isogenic individuals producing different phenotypes, under the same environmental conditions. Ecological studies provide evidence that variability in seed germination time has been selected for as a bet-hedging strategy. We demonstrate how variability in germination time found in Arabidopsis could function as a bet-hedging strategy in the face of unpredictable lethal stresses. Despite a body of knowledge on how the degree of seed dormancy versus germination is controlled, relatively little is known about how differences between isogenic seeds in a batch are generated. We review proposed mechanisms for generating variability in germination time and the current limitations and new possibilities for testing the model predictions. We then look beyond germination to the role of variability in seedling and adult plant growth and review new technologies for quantification of noisy gene expression dynamics. We discuss evidence for phenotypic variability in plant traits beyond germination being under genetic control and propose that variability in stress response gene expression could function as a bet-hedging strategy. We discuss open questions about how noisy gene expression could lead to between-plant heterogeneity in gene expression and phenotypes. This article is part of a discussion meeting issue 'Causes and consequences of stochastic processes in development and disease'.

An ABA-GA bistable switch can account for natural variation in the variability of Arabidopsis seed germination time.

Genetically identical plants growing in the same conditions can display heterogeneous phenotypes. Here we use Arabidopsis seed germination time as a model system to examine phenotypic variability and its underlying mechanisms. We show extensive variation in seed germination time variability between Arabidopsis accessions and use a multiparent recombinant inbred population to identify two genetic loci involved in this trait. Both loci include genes implicated in modulating abscisic acid (ABA) sensitivity. Mutually antagonistic regulation between ABA, which represses germination, and gibberellic acid (GA), which promotes germination, underlies the decision to germinate and can act as a bistable switch. A simple stochastic model of the ABA-GA network shows that modulating ABA sensitivity can generate the range of germination time distributions we observe experimentally. We validate the model by testing its predictions on the effects of exogenous hormone addition. Our work provides a foundation for understanding the mechanism and functional role of phenotypic variability in germination time.

Formation of polarity convergences underlying shoot outgrowths.

The development of outgrowths from plant shoots depends on formation of epidermal sites of cell polarity convergence with high intracellular auxin at their centre. A parsimonious model for generation of convergence sites is that cell polarity for the auxin transporter PIN1 orients up auxin gradients, as this spontaneously generates convergent alignments. Here we test predictions of this and other models for the patterns of auxin biosynthesis and import. Live imaging of outgrowths from kanadi1 kanadi2 Arabidopsis mutant leaves shows that they arise by formation of PIN1 convergence sites within a proximodistal polarity field. PIN1 polarities are oriented away from regions of high auxin biosynthesis enzyme expression, and towards regions of high auxin importer expression. Both expression patterns are required for normal outgrowth emergence, and may form part of a common module underlying shoot outgrowths. These findings are more consistent with models that spontaneously generate tandem rather than convergent alignments.

Developmental mechanisms underlying variable, invariant and plastic phenotypes.

BACKGROUND: Discussions of phenotypic robustness often consider scenarios where invariant phenotypes are optimal and assume that developmental mechanisms have evolved to buffer the phenotypes of specific traits against stochastic and environmental perturbations. However, plastic plant phenotypes that vary between environments or variable phenotypes that vary stochastically within an environment may also be advantageous in some scenarios. SCOPE: Here the conditions under which invariant, plastic and variable phenotypes of specific traits may confer a selective advantage in plants are examined. Drawing on work from microbes and multicellular organisms, the mechanisms that may give rise to each type of phenotype are discussed. CONCLUSION: In contrast to the view of robustness as being the ability of a genotype to produce a single, invariant phenotype, changes in a phenotype in response to the environment, or phenotypic variability within an environment, may also be delivered consistently (i.e. robustly). Thus, for some plant traits, mechanisms have probably evolved to produce plasticity or variability in a reliable manner.

An intracellular partitioning-based framework for tissue cell polarity in plants and animals.

Tissue cell polarity plays a major role in plant and animal development. We propose that a fundamental building block for tissue cell polarity is the process of intracellular partitioning, which can establish individual cell polarity in the absence of asymmetric cues. Coordination of polarities may then arise through cell-cell coupling, which can operate directly, through membrane-spanning complexes, or indirectly, through diffusible molecules. Polarity is anchored to tissues through organisers located at boundaries. We show how this intracellular partitioning-based framework can be applied to both plant and animal systems, allowing different processes to be placed in a common evolutionary and mechanistic context.