The modified underground architecture enhances carbon gains through not photosynthesis but fungal parasitism

Suetsugu, Kenji; Matsubayashi, Jun

(a) Mature Calypso bulbosa plant without a coral-shaped rhizome. (b) Mature Calypso bulbosa plant with a coral-shaped rhizome.
(a) Mature Calypso bulbosa plant without a coral-shaped rhizome. (b) Mature Calypso bulbosa plant with a coral-shaped rhizome.

Green coloration is a defining feature of the plant kingdom, and plants are mostly autotrophic, i.e. they make their own nutrients through photosynthesis. However, several hundreds of plants have lost their photosynthetic ability and have evolved to depend entirely on mycorrhizal fungi (known as full mycoheterotrophy). Since photosynthesis is a fundamental process for plant survival, its loss is one of the most exciting and challenging topics in plant evolution. Interestingly, recent studies have shown that green coloration is insufficient to confirm complete autotrophy in plants. Growing evidence suggests that many green orchids have adopted a kind of mixotrophy, through which they obtain carbon by autotrophy as well as mycoheterotrophy. These mixotrophic orchids are a suitable model for investigating mycoheterotrophic evolution, as they are in an evolutionary transition from autotrophy to heterotrophy. Here we focused Calypso bulbosa (fairy slipper), a green orchid widely distributed in north temperate regions of the world. In spring, the plants develop a beautiful flower whose shape resembles an elegant fairy slipper. Interestingly, the subterranean parts of fairy slipper are dimorphic concerning the presence of underground coralloid rhizomes, a morphological character associated with fully mycoheterotrophic orchids. We hypothesized that since fairy slipper bears coralloid rhizomes, it may exhibit a high level of mycoheterotrophy. Our results showed that fairy slipper plants bearing coral-shaped rhizomes were more dependent on mycorrhizal fungi than those without coral-shaped rhizomes. These results confirm our hypothesis that underground morphology is the key factor contributing to the difference in the degree of mycoheterotrophy in fairy slipper. The dimorphic underground morphology (i.e., high mycoheterotrophy in those with coral-shaped rhizomes vs. low mycoheterotrophy in those without coral-shaped rhizomes) in fairy slipper offers a unique opportunity to investigate mycoheterotrophic evolution, because both types of nutrition occur in plants of the same species with similar genetic backgrounds. Our study provides novel insights into the important question of how plants have evolved to abandon photosynthesis and become parasitic on fungi.

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