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Photosynthetic costs and benefits of abaxial versus adaxial anthocyanins in Colocasia esculenta ‘Mojito’

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Abstract

Main conclusion

Anthocyanins in upper (adaxial) leaf tissues provide greater photoprotection than in lower (abaxial) tissues, but also predispose tissues to increased shade acclimation and, consequently, reduced photosynthetic capacity. Abaxial anthocyanins may be a compromise between these costs/benefits.

Plants adapted to shaded understory environments often exhibit red/purple anthocyanin pigmentation in lower (abaxial) leaf surfaces, but rarely in upper (adaxial) surfaces. The functional significance of this color pattern in leaves is poorly understood. Here, we test the hypothesis that abaxial anthocyanins protect leaves of understory plants from photo-oxidative stress via light attenuation during periodic exposure to high incident sunlight in the forest understory, without interfering with sunlight capture and photosynthesis during shade conditions. We utilize a cultivar of Colocasia esculenta exhibiting adaxial and abaxial anthocyanin variegation within individual leaves to compare tissues with the following color patterns: green adaxial, green abaxial (GG), green adaxial, red abaxial (GR), red adaxial, green abaxial (RG), and red adaxial, red abaxial (RR). Consistent with a photoprotective function of anthocyanins, tissues exhibited symptoms of increasing photoinhibition in the order (from least to greatest): RR, RG, GR, GG. Anthocyanic tissues also showed symptoms of shade acclimation (higher total chl, lower chl a/b) in the same relative order. Inconsistent with our hypothesis, we did not observe any differences in photosynthetic CO2 uptake under shade conditions between the tissue types. However, GG and GR had significantly (39 %) higher photosynthesis at saturating irradiance (A sat) than RG and RR. Because tissue types did not differ in nitrogen content, these patterns likely reflect differences in resource allocation at the tissue level, with greater nitrogen allocated toward energy processing in GG and GR, and energy capture in RG and RR (consistent with relative sun/shade acclimation). We conclude that abaxial anthocyanins are likely advantageous in understory environments because they provide some photoprotection during high-light exposure, but without the cost of decreased A sat associated with adaxial anthocyanin-induced shade syndrome.

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Acknowledgments

We kindly thank Dr. Anita McCauley and the microscopy facility at Wake Forest University for assistance with microscopy.

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Authors and Affiliations

  1. Department of Biology, High Point University, University Station 3591, High Point, NC, 27262, USA

    Nicole M. Hughes, Kaylyn L. Carpenter, Timothy S. Keidel & Charlene N. Miller

  2. Department of Biology, Valdosta State University, 1500 N Patterson St., Valdosta, GA, 31698, USA

    Matthew N. Waters

  3. Department of Biology, Wake Forest University, P.O. Box 7325 Reynolda Station, Winston-Salem, NC, 271069-7325, USA

    William K. Smith

Authors
  1. Nicole M. Hughes
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  2. Kaylyn L. Carpenter
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Correspondence to Nicole M. Hughes.

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Special topic: Anthocyanins. Guest editor: Stefan Martens.

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Hughes, N.M., Carpenter, K.L., Keidel, T.S. et al. Photosynthetic costs and benefits of abaxial versus adaxial anthocyanins in Colocasia esculenta ‘Mojito’. Planta 240, 971–981 (2014). https://doi.org/10.1007/s00425-014-2090-6

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  • DOI: https://doi.org/10.1007/s00425-014-2090-6

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