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Nutritional regulation in mixotrophic plants: new insights from Limodorum abortivum

  • Plant-microbe-animal interactions - Original research
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Abstract

Partially mycoheterotrophic (mixotrophic) plants gain carbon from both photosynthesis and their mycorrhizal fungi. This is considered an ancestral state in the evolution of full mycoheterotrophy, but little is known about this nutrition, and especially about the physiological balance between photosynthesis and fungal C gain. To investigate possible compensation between photosynthesis and mycoheterotrophy in the Mediterranean mixotrophic orchid Limodorum abortivum, fungal colonization was experimentally reduced in situ by fungicide treatment. We measured photosynthetic pigments of leaves, stems, and ovaries, as well as the stable C isotope compositions (a proxy for photosynthetic C gain) of seeds and the sizes of ovaries and seeds. We demonstrate that (1) in natural conditions, photosynthetic pigments are most concentrated in ovaries; (2) pigments and photosynthetic C increase in ovaries when fungal C supply is impaired, buffering C limitations and allowing the same development of ovaries and seeds as in natural conditions; and (3) responses to light of pigment and 13C contents in ovaries shift from null responses in natural conditions to responses typical of autotrophic plants in treated L. abortivum, demonstrating photoadaptation and enhanced use of light in the latter. L. abortivum thus preferentially feeds on fungi in natural conditions, but employs compensatory photosynthesis to buffer fungal C limitations and allow seed development.

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Acknowledgments

This unfunded work was performed due to the courtesy and generosity of those who helped the authors—lending their instruments, sharing their knowledge and time—without any financial interest. To them we express our gratitude. We are infinitely grateful to Prof. Kazuhide Nara (University of Tokyo, Japan), who provided us with the plates containing Russula, and to Mr. Mario Corrado for giving us his permission to perform the field trial in his estate. We must also thank Dr. Agostino Menna and Dr. Beatrice Cocozziello (ARPA Campania, Italy) for giving us their permission to use—and their help in using—the HPLC system; Dr. Mathieu Sauve (CEFE-CNRS, France) for help with fungal barcoding; Prof. Roberto Ligrone (Seconda Università di Napoli, Italy) for his helpful review of the manuscript; and Dr. David Marsh for revising the English.

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Authors and Affiliations

  1. Dipartimento di Chimica e Biologia, Università degli Studi di Salerno, Via Giovanni Paolo II 132, 84084, Fisciano, Salerno, Italy

    Alessandro Bellino, Anna Alfani & Daniela Baldantoni

  2. Département Systématique et Evolution (UMR 7205 OSEB), Muséum national d’Histoire naturelle, CP 50, 45 rue Buffon, 75005 , Paris, France

    Marc-André Selosse

  3. Dipartimento di Scienze dei Sistemi Colturali, Forestali e dell’Ambiente, Università della Basilicata, Viale dell’Ateneo Lucano 10, 85100, Potenza, Italy

    Rossella Guerrieri & Marco Borghetti

  4. Earth Systems Research Center, University of New Hampshire, 8 College Road, Durham, NH, 03824, USA

    Rossella Guerrieri

Authors
  1. Alessandro Bellino
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  2. Anna Alfani
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  3. Marc-André Selosse
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  4. Rossella Guerrieri
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  5. Marco Borghetti
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  6. Daniela Baldantoni
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Corresponding authors

Correspondence to Alessandro Bellino or Daniela Baldantoni.

Additional information

Communicated by Caroline Müller.

Alessandro Bellino began this research, then Daniela Baldantoni worked alongside him in every phase of this project, from devising the experimental plan to the samplings, analyses, and interpretation of data. Marc-André Selosse proposed additional experiments and measurements, and carried out some of them in his lab. Rossella Guerrieri and Marco Borghetti performed the \(\delta ^{13}\)C measurements. Anna Alfani coordinated the work. All contributed to writing the paper.

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Bellino, A., Alfani, A., Selosse, MA. et al. Nutritional regulation in mixotrophic plants: new insights from Limodorum abortivum . Oecologia 175, 875–885 (2014). https://doi.org/10.1007/s00442-014-2940-8

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  • DOI: https://doi.org/10.1007/s00442-014-2940-8

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