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The tiny-leaved orchid Cephalanthera subaphylla obtains most of its carbon via mycoheterotrophy

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Abstract

The evolution of mycoheterotrophy has been accompanied by extreme reductions in plant leaf size and photosynthetic capacity. Partially mycoheterotrophic plants, which obtain carbon from both photosynthesis and their mycorrhizal fungi, include species with leaves of normal size and others that are tiny-leaved. Thus, plant species may lose their leaves in a gradual process of size reduction rather than through a single step mutation. Little is known about how the degree of mycoheterotrophy changes during reductions in leaf size. We compared the degree of mycoheterotrophy among five Japanese Cephalanthera species, four with leaves of normal size (Cephalanthera falcata, Cephalanthera erecta, Cephalanthera longibracteata and Cephalanthera longifolia), one with tiny leaves (Cephalanthera subaphylla), and one albino form of C. falcata (as reference specimens for fully mycoheterotrophic plants). The levels of mycoheterotrophy were determined by stable isotope natural abundance analysis. All Cephalanthera species were relatively enriched in 13C and 15N in comparison with surrounding autotrophic plants. Cephalanthera subaphylla was strongly enriched in 13C and 15N to levels similar to the albinos. Species with leaves of normal size were significantly less enriched in 13C than C. subaphylla and the albinos. Thus, C. subaphylla was strongly mycoheterotrophic, obtaining most of its carbon from mycorrhizal fungi even though it has tiny leaves; species with leaves of normal size were partially mycoheterotrophic. Hence, during the evolutionary pathway to full mycoheterotrophy, some plant species appear to have gained strong mycoheterotrophic abilities before completely losing foliage leaves.

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Acknowledgments

We thank T. Itagaki, T. Yamada, H. Nomura, N. Takano, Y. Waki, and T. Kimura for their advice and/or assistance in the field, and Jindai Botanical Gardens for permission to collect plants. We also thank Professor Gerhard Gebauer of the University of Bayreuth for his helpful comments on our data. This study was partly supported by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

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Correspondence to Masayuki Maki.

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Y. Sakamoto and Y. Ogura-Tsujita contributed equally.

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Sakamoto, Y., Ogura-Tsujita, Y., Ito, K. et al. The tiny-leaved orchid Cephalanthera subaphylla obtains most of its carbon via mycoheterotrophy. J Plant Res 129, 1013–1020 (2016). https://doi.org/10.1007/s10265-016-0856-6

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