Molecular mechanisms governing differential robustness of development and environmental responses in plants

Abstract

Background: Robustness to genetic and environmental perturbation is a salient feature of multicellular organisms. Loss of developmental robustness can lead to severe phenotypic defects and fitness loss. However, perfect robustness, i.e. no variation at all, is evolutionarily unfit as organisms must be able to change phenotype to properly respond to changing environments and biotic challenges. Plasticity is the ability to adjust phenotypes predictably in response to specific environmental stimuli, which can be considered a transient shift allowing an organism to move from one robust phenotypic state to another. Plants, as sessile organisms that undergo continuous development, are particularly dependent on an exquisite fine-tuning of the processes that balance robustness and plasticity to maximize fitness.

Scope and conclusions: This paper reviews recently identified mechanisms, both systems-level and molecular, that modulate robustness, and discusses their implications for the optimization of plant fitness. Robustness in living systems arises from the structure of genetic networks, the specific molecular functions of the underlying genes, and their interactions. This very same network responsible for the robustness of specific developmental states also has to be built such that it enables plastic yet robust shifts in response to environmental changes. In plants, the interactions and functions of signal transduction pathways activated by phytohormones and the tendency for plants to tolerate whole-genome duplications, tandem gene duplication and hybridization are emerging as major regulators of robustness in development. Despite their obvious implications for plant evolution and plant breeding, the mechanistic underpinnings by which plants modulate precise levels of robustness, plasticity and evolvability in networks controlling different phenotypes are under-studied.

Keywords: Developmental robustness; Hsp90; canalization; capacitor; chromatin; hormones; network hubs; network motifs; noise; plasticity; rDNA; redundancy; species diversity.

Fig. 1.

Changing environments induce phenotype-specific responses. Phenotypic responses to changing environments range from plastic to robust. Environmental changes that occur predictably lead to programmed responses. Shown here is the transition between vegetative and reproductive growth induced by seasonal exposures to low and then high temperatures. Other environmental challenges are unpredictable, such as pathogen attacks (red bacteria), which trigger immune responses in plants, including the hypersensitive response (yellowed leaf). In contrast, some traits are largely robust to changing environments. For example, most floral morphs are invariant to both predictable and unpredictable environmental changes. Invariant floral forms are important for reproductive success.

Fig. 2.

Network motifs associated with robustness and plasticity. Several network motifs are associated with robust phenotypes. (A) Coherent feed-forward loops (left), such as those acting in secondary cell wall synthesis (right), maintain robust development (TF, transcription factors). (B) An incoherent feed-forward loop (left) triggered by pathogens induces plant immunity (right), a plastic response. (C) An autoregulatory loop (left) in which EPR1 negatively regulates itself is important for the plastic developmental process of photomorphogenesis (right). The EPR1 autoregulatory loop is not present in the dark or upon initial light exposure but emerges with increased exposure to light. (D) A variant of an extended biparallel motif (left) is important for robust floral and shoot determinacy (right). (E) Phyllotaxy relies on a fan-in motif (left) for robust patterning of leaf emergence (right).