The Genomic Impact of Mycoheterotrophy in Orchids.

Marcin Jąkalski,Etienne Delannoy,José Caius,Marc-André Selosse,Michał May,Julita Minasiewicz

doi:10.3389/fpls.2021.632033

Abstract

Mycoheterotrophic plants have lost the ability to photosynthesize and obtain essential mineral and organic nutrients from associated soil fungi. Despite involving radical changes in life history traits and ecological requirements, the transition from autotrophy to mycoheterotrophy has occurred independently in many major lineages of land plants, most frequently in Orchidaceae. Yet the molecular mechanisms underlying this shift are still poorly understood. A comparison of the transcriptomes of Epipogium aphyllum and Neottia nidus-avis, two completely mycoheterotrophic orchids, to other autotrophic and mycoheterotrophic orchids showed the unexpected retention of several genes associated with photosynthetic activities. In addition to these selected retentions, the analysis of their expression profiles showed that many orthologs had inverted underground/aboveground expression ratios compared to autotrophic species. Fatty acid and amino acid biosynthesis as well as primary cell wall metabolism were among the pathways most impacted by this expression reprogramming. Our study suggests that the shift in nutritional mode from autotrophy to mycoheterotrophy remodeled the architecture of the plant metabolism but was associated primarily with function losses rather than metabolic innovations.

Highlights

More than 85% of vascular plants grow in association with soil fungi, forming a mycorrhizal symbiosis (Wang and Qiu, 2006; van der Heijden et al, 2015; Brundrett and Tedersoo, 2018).Thanks to this symbiosis, plant growth, and fitness are substantially improved by better mineral nutrition and increased resistance to biotic and abiotic stresses.In this mutualism, the fungal partner provides mineral nutrients in exchange for organic compounds from the photosynthesis of the plant
Twenty-two of these orthogroups contained only unannotated genes and the 16 remaining did not have specific annotations (Supplementary Data 4). These results suggest that the switch to mycoheterotrophy in orchids does not involve new pathways or functions
Repertoires, we were not able to identify new functions associated with mycoheterotrophy, and large losses appeared to be restricted to genes exclusively involved in photosynthetic functions

Summary

Introduction

More than 85% of vascular plants grow in association with soil fungi, forming a mycorrhizal symbiosis (Wang and Qiu, 2006; van der Heijden et al, 2015; Brundrett and Tedersoo, 2018) Thanks to this symbiosis, plant growth, and fitness are substantially improved by better mineral nutrition and increased resistance to biotic and abiotic stresses (see Jung et al, 2012 for a review). Plant growth, and fitness are substantially improved by better mineral nutrition and increased resistance to biotic and abiotic stresses (see Jung et al, 2012 for a review) In this mutualism, the fungal partner provides mineral nutrients (e.g., water, N, P, and K) in exchange for organic compounds from the photosynthesis of the plant (see Rich et al, 2017 for a review).

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Discussion

Conclusion