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

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

doi:10.1111/tpj.14276

Cited by 30 publications

(24 citation statements)

References 77 publications

(161 reference statements)

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“…Our novel discovery will facilitate the progress of further studies focused on mycoheterotrophic evolution using albino mutants in not only Orchidaceae, but also now in Ericaceae. Such studies should provide valuable findings in terms of comparison with the many findings obtained from Orchidaceae (e.g., Abadie et al., ; Roy et al., ; Suetsugu et al., , ; Lallemand et al., ). Further, the albino mutants were fortunately found within the P. japonica species complex, which exhibits morphological similarities and continuous leaf size variation between partially mycoheterotrophic and nearly fully mycoheterotrophic species (Shutoh et al., , ).…”

Section: Discussionmentioning

confidence: 92%

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Evidence for newly discovered albino mutants in a pyroloid: implication for the nutritional mode in the genus Pyrola

Shutoh

Tajima²,

Matsubayashi

et al. 2020

American J of Botany

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Premise Difficulties in comparing extremely divergent features in fully mycoheterotrophic plants with those in closely related chlorophyllous plants have complicated attempts to reveal the evolutionary patterns and processes of fully mycoheterotrophic plants. Albino mutants of partially mycoheterotrophic plants, generally observed in Orchidaceae, have provided an ideal model for investigating the evolution of mycoheterotrophy within similar genetic backgrounds. In 2018, we found a putative albino population of Pyrola (Ericaceae). Here we aimed to reveal the identity of the albino pyroloid and confirm its fully mycoheterotrophic status. Methods To reveal the putative albino pyroloid's identity, we examined its morphology and sequenced its chloroplast DNA. In addition, we assessed the trophic status of the putative albino pyroloid by analyzing chlorophyll fluorescence, chlorophyll concentration, and natural 13C and 15N abundances. Results We identified albino individuals as P. japonica—otherwise a partially mycoheterotrophic species. We confirmed their albino status by their considerably lower chlorophyll fluorescence and concentrations than those of sympatrically occurring chlorophyllous plants. 13C abundance in the albino individuals was significantly higher than in the green individuals of P. japonica. Conclusions This first report of albino mutants from partially mycoheterotrophic species in angiosperms other than orchids will play a valuable role in further studies focused on mycoheterotrophy. For instance, their δ13C and δ15N values represent a reference for fully mycoheterotrophic plants in Pyrola. Our findings also indicate the strong dependence of some leafy Pyrola species on fungal C during their entire life cycle.

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Section: Discussionmentioning

confidence: 92%

“…The discovery of such albino orchids has provided an ideal model for investigating the evolution of mycoheterotrophy within similar genetic backgrounds (e.g., Abadie et al., ; Roy et al., ; Suetsugu et al., ). Recently, they were also used for studies focusing on genomics or metabolomics (Suetsugu et al., ; Lallemand et al., ).…”

mentioning

confidence: 99%

Evidence for newly discovered albino mutants in a pyroloid: implication for the nutritional mode in the genus Pyrola

Shutoh

Tajima²,

Matsubayashi

et al. 2020

American J of Botany

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“…However, it is an abundant storage carbohydrate in mycorrhizal fungi and it has been suggested that it is transferred to mycoheterotrophic orchids to be cleaved into glucose (Müller and Dulieu, 1998). A comparison between leaves of achlorophyllous mutants (thus with mycohetertrophic nutrition) and green individuals in mixotrophic orchids showed an upregulation of trehalase, but also of trehalose-6-P phosphatases (TPP) and trehalose-6-P synthase (TPS; Lallemand et al, 2019b). Similarly, the mycoheterotrophic orchids demonstrated a higher underground organ/stem ratio of trehalase and TPP expression (but not TPS) compared to photosynthetic grasses.…”

Section: An Upside-down Metabolic Architecturementioning

confidence: 99%

“…However, some species still recover carbon from the fungi at adulthood in addition to their photosynthesis (mixotrophy; Selosse and Roy, 2009 ), and from this nutrition some even evolved complete loss of photosynthesis and mycoheterotrophy at adulthood ( Merckx et al, 2009 ; Dearnaley et al, 2016 ). This versatile relation between orchids and their mycorrhizal partners provides an useful framework for understanding the metabolic evolution resulting in mycoheterotrophy ( Suetsugu et al, 2017 ; Lallemand et al, 2019b ).…”

Section: Introductionmentioning

confidence: 99%

The Genomic Impact of Mycoheterotrophy in Orchids

et al. 2021

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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.

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“…But this phenomenon has also been reported by Lallemand et al . (2019). They found a higher N content in albinos mixotrophic orchids ( Epipactis helleborine , E. purpurata and Cephalanthera damasonium Druce) compared with their green counterparts.…”

Section: Discussionmentioning

confidence: 99%

Effects of inoculated mycorrhizal fungi and non‐mycorrhizal beneficial micro‐organisms on plant traits, nutrient uptake and root‐associated fungal community composition of the Cymbidium hybridum in greenhouse

Liu

Liao

et al. 2020

J. Appl. Microbiol.

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Aims The aim of this study was to assess the effects of beneficial micro‐organisms on the growth, nutrient accumulation and root‐associated fungal species composition of pot orchids grown in the greenhouse. Methods and Results A greenhouse pot experiment was conducted to investigate the beneficial effects of a mycorrhizal fungus, Epulorhiza repens isolate ML01, an endophytic fungus, Umbelopsis nana isolate ZH3A‐3 and a mixed commercial inoculum Rem, alone or in combination. Nested PCR assays showed that both isolates ML01 and ZH3A‐3 can successfully establish in inoculated soil. All the inoculants significantly increased the plant total dry weight of Cymbidium hybridum ‘Golden Boy’, whereas only co‐inoculation with the endophytic fungus ZH3A‐3 and the Rem enhanced the fresh weight and height of host plants. The mycorrhizal fungus positively affected P, K, Ca, Mg content in shoots and Zn content in roots, while the endophytic fungus improved N, P, Ca accumulation in shoots and roots. Co‐inoculation with the Rem and ML01 improved root to shoot translocation of Fe and Zn. In addition, inoculation with ZH3A‐3, ML01+Rem and ZH3A‐3+Rem decreased the relative frequency of Fusarium sp. on orchid roots. Trichoderma sp. were isolated from the roots treated with ML01, ML01+Rem and ZH3A‐3+Rem. Conclusions Both mycorrhizal and endophytic fungi had the potential to create favourable microflora in the orchid roots and stimulate the growth of transplanted plantlets under greenhouse condition. Significance and Impact of the Study The newly isolated endophytic strain ZH3A‐3 showed significant application value in orchid production.

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

Cited by 30 publications

References 77 publications

Evidence for newly discovered albino mutants in a pyroloid: implication for the nutritional mode in the genus Pyrola

Evidence for newly discovered albino mutants in a pyroloid: implication for the nutritional mode in the genus Pyrola

The Genomic Impact of Mycoheterotrophy in Orchids

Effects of inoculated mycorrhizal fungi and non‐mycorrhizal beneficial micro‐organisms on plant traits, nutrient uptake and root‐associated fungal community composition of the Cymbidium hybridum in greenhouse

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