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Coordinating Development: How Do Animals Integrate Plastic and Robust Developmental Processes? - PubMed

  • ️Tue Jan 01 2019

Review

Coordinating Development: How Do Animals Integrate Plastic and Robust Developmental Processes?

Christen K Mirth et al. Front Cell Dev Biol. 2019.

Abstract

Our developmental environment significantly affects myriad aspects of our biology, including key life history traits, morphology, physiology, and our susceptibility to disease. This environmentally-induced variation in phenotype is known as plasticity. In many cases, plasticity results from alterations in the rate of synthesis of important developmental hormones. However, while developmental processes like organ growth are sensitive to environmental conditions, others like patterning - the process that generates distinct cell identities - remain robust to perturbation. This is particularly surprising given that the same hormones that regulate organ growth also regulate organ patterning. In this review, we revisit the current approaches that address how organs coordinate their growth and pattern, and outline our hypotheses for understanding how organs achieve correct pattern across a range of sizes.

Keywords: eco-evo-devo; environmentally-sensitive growth; morphogenetic growth; nutrition; patterning; phenotypic plasticity; robustness.

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Figures

FIGURE 1
FIGURE 1

While growth of the hand may differ between individuals, due to genetic or environmental factors, the number of digits on a normally-developing hand do not. This illustrates that the hand formation requires the integration of both plastic and robust developmental processes.

FIGURE 2
FIGURE 2

Final size of insect organs, like the wing, is a product of morphogenetic and environmentally-sensitive growth. Signaling pathways that are thought to regulate morphogenetic growth in insects include morphogen-induced signaling, as well as the signaling pathways responding to the systemic hormones, juvenile hormone (JH) and ecdysone. Environmentally-sensitive growth is regulated by a number of systemic signals, including JH, ecdysone, and insulin signaling, as well as cell-autonomous nutrient-sensing pathways like the Target of Rapamycin pathway.

FIGURE 3
FIGURE 3

Morphogens, developmental hormones, and environmentally-sensitive signaling pathways each exert effects on growth and patterning of the wing disc. (A) The morphogens Decapentaplegic (Dpp), Hedgehog (Hh), and Wingless (Wg) act through morphogen-specific signaling pathways to regulate the growth and patterning of the developing wing. Abbreviations: Frizzled (Fz), Dachshund (Dsh), Zeste White 3 (Zw3), Adenomatous Polyposis Coli (APC), Armadillo (Arm), Thick Veins (Tkv), Mother’s Against Dpp (Mad), Brinker (Brk), Smoothened (Smo), Patched (Ptc), Cubitus Interruptus – Activator (CiA), Cubitus Interruptus – Repressor (CiR). (B) Developmental hormones like ecdysone act to regulate growth and patterning in the wing disc. By binding to its receptor, a heterodimeric complex of Ecdysone Receptor (EcR) and Ultraspiracle (Usp), ecdysone stimulates growth of the wing disc. It further relieves the repression of patterning imposed by unliganded EcR/Usp complexes in early third instar wing discs. (C) Environmental conditions affect wing disc growth by acting systemically, via the insulin-like peptides, or on cell autonomous nutrient sensing pathways like the Target of Rapamycin (TOR pathway). To date, we know little about how insulin and TOR signaling affect patterning in the wing disc. Abbreviations: Insulin Receptor (InR), Phosphatidylinositide 3-Kinase (PI3K), 3 Phosphoinositide-Dependent protein Kinase (PDK), Phosphatase and Tensin homolog (PTEN), Forkhead Box O (FoxO), Tuberous Sclerosis Complex 1/2 (TSC1/2), Ras Homolog Enhanced in Brain (Rheb).

FIGURE 4
FIGURE 4

Three non-mutually exclusive models of the coordination of morphogenetic and environmentally-sensitive growth. (A) Hypothesis 1: Environmental signals regulate growth both via environmentally-sensitive signaling pathways, and via patterning signaling pathways. The effect of the environment on patterning is either direct, via environmentally-sensitive signaling pathways, or indirect, via the environmentally-regulated size of the imaginal disc. The ontogenetic relationship between disc size (relative to final size) and pattern is stereotyped and maintained across environmental conditions. (B) Hypothesis 2: Both environmental and patterning signals are coordinated by a single mechanism, possibly Hippo signaling, to drive growth. Again, the ontogenetic relationship between disc size (relative to final size) and pattern is stereotyped and maintained across environmental conditions. (C) Hypothesis 3: There is a complex relationship between pattern and growth, such that multiple patterning and environmentally-sensitive signaling pathways crosstalk, potentially independently from one another. The ontogenetic relationship between disc size (relative to final size) is complex and rates of pattern formation vary across environmental conditions.

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