In situ transcriptomic and metabolomic study of the loss of photosynthesis in the leaves of mixotrophic plants exploiting fungi

Félix Lallemand , Marie-Laure Martin-Magniette , Françoise Gilard , Bertrand Gakière , Alexandra Launay‐Avon , Étienne Delannoy , Marc-Andre Selosse

Abstract

Mycoheterotrophic plants have lost photosynthesis and obtain carbon through mycorrhizal fungi colonizing their roots. They are likely to have evolved from mixotrophic ancestors, which rely on both photosynthesis and fungal carbon for their development. Whereas our understanding of the ecological and genomic changes associated with the evolutionary shift to mycoheterotrophy is deepening, little information is known about the specific metabolic and physiological features driving this evolution. We investigated this issue in naturally occurring achlorophyllous variants of temperate mixotrophic orchids. We carried out an integrated transcriptomic and metabolomic analysis of the response to achlorophylly in the leaves of three mixotrophic species sampled in natura. Achlorophyllous leaves showed major impairment of their photosynthetic and mineral nutrition functions, strong accumulation of free amino acids, overexpression of enzymes and transporters related to sugars, amino acids and fatty acid catabolism, as well as induction of some autophagy‐related and biotic stress genes. Such changes were reminiscent of these reported for variegated leaves and appeared to be symptomatic of a carbon starvation response. Rather than decisive metabolic innovations, we suggest that the evolution towards mycoheterotrophy in orchids is more likely to be reliant on the versatility of plant metabolism and an ability to exploit fungal organic resources, especially amino acids, to replace missing photosynthates.
Author Félix Lallemand
Félix Lallemand,,
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, Marie-Laure Martin-Magniette
Marie-Laure Martin-Magniette,,
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, Françoise Gilard
Françoise Gilard,,
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, Bertrand Gakière
Bertrand Gakière,,
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, Alexandra Launay‐Avon
Alexandra Launay‐Avon,,
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, Étienne Delannoy
Étienne Delannoy,,
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, Marc-Andre Selosse (FB / DPTNC)
Marc-Andre Selosse,,
- Department of Plant Taxonomy and Nature Conservation
Journal seriesPlant Journal, ISSN 0960-7412, (N/A 140 pkt)
Issue year2019
Vol98
No5
Pages826-841
Publication size in sheets0.75
Keywords in Englishmycorrhiza, mycoheterotrophy, mixotrophy, albinos, orchids, Neottieae, metabolomic, transcrip-tomic, carbon starvation response
ASJC Classification1307 Cell Biology; 1110 Plant Science; 1311 Genetics
DOIDOI:10.1111/tpj.14276
URL https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.14276
Languageen angielski
Score (nominal)140
Score sourcejournalList
ScoreMinisterial score = 140.0, 29-11-2019, ArticleFromJournal
Publication indicators WoS Citations = 0; Scopus SNIP (Source Normalised Impact per Paper): 2017 = 1.669; WoS Impact Factor: 2018 = 5.726 (2) - 2018=6.467 (5)
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