Comparative Analysis of Plastid Genomes in the Non-photosynthetic Genus Thismia Reveals Ongoing Gene Set Reduction

Yudina, Sophia V.; Schelkunov, Mikhail I.; Nauheimer, Lars; Crayn, Darren M.; Chantanaorrapint, Sahut; Hroneš, Michal; Sochor, Michal; Dančák, Martin; Mar, S.S.; Lưu, Hồng Trường; Nuraliev, Maxim S.; Logacheva, Maria D.

doi:10.3389/fpls.2021.602598

Cited by 17 publications

(44 citation statements)

References 72 publications

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“…The impact of mycoheterotrophy on plant physiology can be analyzed through the changes in genomes of mycoheterotrophs compared to autotrophic relatives. As mycoheterotrophy is associated with the loss of photosynthesis, sequencing of the plastid genome has been targeted first, thanks to next-generation methods (e.g., Logacheva et al, 2014 ; Schelkunov et al, 2015 ; Lim et al, 2016 ; Ravin et al, 2016 ; Yudina et al, 2021 ). A common feature among plastid genomes of mycoheterotrophs is a strong reduction in size and gene content, especially with, as expected, a loss of all photosynthetic genes ( Graham et al, 2017 ; Hadariová et al, 2018 ).…”

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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Section: Introductionmentioning

confidence: 99%

The Genomic Impact of Mycoheterotrophy in Orchids

et al. 2021

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“…1 and 2, Supplementary Material online , Naumann et al 2016 ; Jost et al 2020 ). Although this fraction is generally high among highly condensed plastomes ( Bellot and Renner 2016 ; Lim et al 2016 ; Roquet et al 2016 ; Arias-Agudelo et al 2019 ; Su et al 2019 ; Yudina et al 2021 ), comparatively those genes appear to occupy the most space in the Hydnoraceae plastomes. In contrast to the studied species of Hydnora (excluding H. esculenta ), plastomes of other highly condensed holoparasitic plants generally lack their quadripartite structure, due to IR loss ( Bellot and Renner 2016 ; Roquet et al 2016 ; Arias-Agudelo et al 2019 ; Su et al 2019 ).…”

Section: Discussionmentioning

confidence: 97%

“…In contrast to the studied species of Hydnora (excluding H. esculenta ), plastomes of other highly condensed holoparasitic plants generally lack their quadripartite structure, due to IR loss ( Bellot and Renner 2016 ; Roquet et al 2016 ; Arias-Agudelo et al 2019 ; Su et al 2019 ). The plastomes of mycoheterotrophic Thismia on the other hand contain two IR copies, occupying a large portion of the total plastomes sequence ( Lim et al 2016 ; Yudina et al 2021 ). Currently, there are no highly condensed plastomes for which Prosopanche -like DR structures have been reported.…”

Section: Discussionmentioning

confidence: 99%

“…Whether the putatively nonfunctional status of trn W can be translated to the other Prosopanche species is uncertain. The loss of tRNAs Y and W in Hydnora , as opposed to a gain in Prosopanche , is supported by the general consensus that gene loss during heterotrophic plastome condensation is presumed to be irreversible and therefore one-directional ( Barrett and Davis 2012 ; Graham et al 2017 ; Yudina et al 2021 ).…”

Section: Discussionmentioning

confidence: 99%

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Structural Plastome Evolution in Holoparasitic Hydnoraceae with Special Focus on Inverted and Direct Repeats

Jost

Naumann

Bolin

et al. 2022

Genome Biology and Evolution

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Plastome condensation during adaptation to a heterotrophic lifestyle is generally well understood and lineage-independent models have been derived. However, understanding the evolutionary trajectories of comparatively old heterotrophic lineages, that are on the cusp of a minimal plastomes, is essential to complement and expand current knowledge. We study Hydnoraceae, one of the oldest and least investigated parasitic angiosperm lineages. Plastome comparative genomics, using seven out of eight known species of the genus Hydnora and three species of Prosopanche, reveal a high degree of structural similarity and shared gene content; contrasted by striking dissimilarities with respect to repeat content (inverted and direct repeats). We identified varying IR content and positions, likely resulting from multiple, independent evolutionary events and a direct repeat gain in Prosopanche. Considering different evolutionary trajectories and based on a fully resolved and supported species-level phylogenetic hypothesis, we describe three possible, distinct models to explain the Hydnoraceae plastome states. For comparative purposes we also report the first plastid genomes for the closely related autotrophic genera Lactoris (Lactoridaceae) and Thottea (Aristolochiaceae).

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“…The genus is distributed across tropical and subtropical regions of Asia, Australasia and America, extending into some temperate regions (Yudina et al 2021). Over a third of the known species of Thismia have been recorded to occur in Malaysia where the majority have very local distributions.…”

Section: Introductionmentioning

confidence: 99%

Thismia sitimeriamiae (Thismiaceae), an extraordinary new species from Terengganu, Peninsular Malaysia

Siti‐Munirah¹,

Dome²,

Thorogood³

2021

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We describe an extraordinary new species in the genus Thismia from the Terengganu State of Malaysia in the Malay Peninsula. The new species, which we name Thismia sitimeriamiae, is distinct from all other Thismia species known to science, most notably in its unique mitre configuration formed by the inner tepals and its floral surface morphology characterised by conspicuous orange trichomes. We discuss our findings in the context of underestimated species diversity in the genus Thismia and implications for their conservation. We recommend assigning T. sitimeriamiae the conservation status as Critically Endangered (CR) according to IUCN criteria.

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Comparative Analysis of Plastid Genomes in the Non-photosynthetic Genus Thismia Reveals Ongoing Gene Set Reduction

Cited by 17 publications

References 72 publications

The Genomic Impact of Mycoheterotrophy in Orchids

The Genomic Impact of Mycoheterotrophy in Orchids

Structural Plastome Evolution in Holoparasitic Hydnoraceae with Special Focus on Inverted and Direct Repeats

Thismia sitimeriamiae (Thismiaceae), an extraordinary new species from Terengganu, Peninsular Malaysia

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