Fluorescent protein-mediated colour polymorphism in reef corals: multicopy genes extend the adaptation/acclimatization potential to variable light environments.

John R Gittins,Richard J Edwards,Cecilia D'Angelo,Jörg Wiedenmann,Franz Oswald

doi:10.1111/mec.13041

John R Gittins, Richard J Edwards + Show 3 more

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https://doi.org/10.1111/mec.13041

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Abstract

The genomic framework that enables corals to adjust to unfavourable conditions is crucial for coral reef survival in a rapidly changing climate. We have explored the striking intraspecific variability in the expression of coral pigments from the green fluorescent protein (GFP) family to elucidate the genomic basis for the plasticity of stress responses among reef corals. We show that multicopy genes can greatly increase the dynamic range over which corals can modulate transcript levels in response to the light environment. Using the red fluorescent protein amilFP597 in the coral Acropora millepora as a model, we demonstrate that its expression increases with light intensity, but both the minimal and maximal gene transcript levels vary markedly among colour morphs. The pigment concentration in the tissue of different morphs is strongly correlated with the number of gene copies with a particular promoter type. These findings indicate that colour polymorphism in reef corals can be caused by the environmentally regulated expression of multicopy genes. High‐level expression of amilFP597 is correlated with reduced photodamage of zooxanthellae under acute light stress, supporting a photoprotective function of this pigment. The cluster of light‐regulated pigment genes can enable corals to invest either in expensive high‐level pigmentation, offering benefits under light stress, or to rely on low tissue pigment concentrations and use the conserved resources for other purposes, which is preferable in less light‐exposed environments. The genomic framework described here allows corals to pursue different strategies to succeed in habitats with highly variable light stress levels. In summary, our results suggest that the intraspecific plasticity of reef corals’ stress responses is larger than previously thought.

Highlights

Shallow-water coral reefs owe their success in well-lit tropical waters to the symbiosis of scleractinian corals with dinoflagellates of the genus Symbiodinium
We focused on three colonies representing morphs with distinct levels of redness: high-level red (HR), mediumlevel red (MR) and low-level red (LR)
We studied colour polymorphisms of Acropora millepora to understand the plasticity of corals’ responses to environmental stimuli and to elucidate the genomic basis for large differences in the constitutive expression of environmentally regulated genes

Summary

Introduction

Colour morphs often display an overlapping distribution (Wiedenmann et al 1999; Kelmanson & Matz 2003; Salih et al 2006; Leutenegger et al 2007a), and conspecific corals containing widely different concentrations of the same types of GFP-like proteins can be found side by side in the most light-exposed reef sites (Figs 1a and S1, Supporting information) This coexistence suggests that the benefits afforded by these pigments are not essential, but that they offer more subtle advantages, such as enabling corals to acclimate to a broader range of conditions or to survive extreme stress events (Smith et al 2013). The red FP amilFP597 is ideally suited for the analysis of the genomic basis of the intraspecific colour variability as it (i) is defined by a distinct nucleotide/amino acid sequence, (ii) displays a characteristic fluorescence signature that permits its optical quantification even in complex FP mixtures and (iii) shows a uniform upregulation in response to increased light levels (D’Angelo et al 2008b)

Materials and methods

Results and discussion

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