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Plastid genome evolution in mycoheterotrophic Ericaceae

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Abstract

Unlike parasitic plants, which are linked to their hosts directly through haustoria, mycoheterotrophic (MHT) plants derive all or part of their water and nutrients from autothrophs via fungal mycorrhizal intermediaries. Ericaceae, the heather family, are a large and diverse group of plants known to form elaborate symbiotic relationships with mycorrhizal fungi. Using PHYA sequence data, we first investigated relationships among mycoheterotrophic Ericaceae and their close autotrophic relatives. Phylogenetic results suggest a minimum of two independent origins of MHT within this family. Additionally, a comparative investigation of plastid genomes (plastomes) grounded within this phylogenetic framework was conducted using a slot-blot Southern hybridization approach. This survey encompassed numerous lineages of Ericaceae with different life histories and trophic levels, including multiple representatives from mixotrophic Pyroleae and fully heterotrophic Monotropeae and Pterosporeae. Fifty-four probes derived from all categories of protein coding genes typically found within the plastomes of flowering plants were used. Our results indicate that the holo-mycoheterotrophic Ericaceae exhibit extensive loss of genes relating to photosynthetic function and expression of the plastome but retain genes with possible functions outside photosynthesis. Mixotrophic taxa tend to retain most genes relating to photosynthetic functions but are varied regarding the plastid ndh gene content. This investigation extends previous inferences that the loss of the NDH complex occurs prior to becoming holo-heterotrophic and it shows that the pattern of gene losses among mycoheterotrophic Ericaceae is similar to that of haustorial parasites. Additionally, we identify the most desirable candidate species for entire plastome sequencing.

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Acknowledgments

For providing generous access to their live plant collections, the authors are grateful to directors/managers of the following greenhouses: Indiana University (Bloomington, IN, USA), the University of Toronto (Toronto, ON, Canada), and the University of Washington (Seattle, WA, USA). We would also like to thank Masha Kuzmina for collecting and providing plant material. Special thanks are due to Dan Nickrent and two anonymous reviewers for their valuable suggestions that considerably improved earlier versions of the manuscript. Financial support from the Natural Sciences and Engineering Research Council of Canada (grant no. 326439), the Canada Foundation for Innovation (grant no. 12810), and the Ontario Research Funds to S. Stefanović is gratefully acknowledged. We also thank the Natural Sciences and Engineering Research Council of Canada for the scholarship award provided to T. Braukmann.

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Braukmann, T., Stefanović, S. Plastid genome evolution in mycoheterotrophic Ericaceae. Plant Mol Biol 79, 5–20 (2012). https://doi.org/10.1007/s11103-012-9884-3

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