The Evolution of Organellar Genomes in Parasitic and Mycoheterotrophic Plants

Athanasios Zervas

The Evolution of Organellar Genomes in Parasitic and Mycoheterotrophic Plants

Athanasios Zervas

SCIENCE PhD theses

Abstract

Parasitic and mycoheterotrophic plants correspond to 1% of all angiosperms (>4.500 species), and they are characterized by covering a smaller or larger part of their nutritional requirements from their plant or fungal host, respectively. This lifestyle has evolved independently several times in the angiosperm phylogeny, and has led to a wide variety of morphological diversity. In general, similar patterns of chloroplast genome (plastome) degradation and gene loss have been observed, and evolutionary models have been proposed. Yet little is known about the molecular evolution of their mitochondrial genomes. The mitochondrial genomes of Viscum spp. were shown to have experienced a unique loss of all complex I genes, accompanied by elevated molecular evolution rates in their remaining mitochondrial genes. Expanding the analysis to incorporate more hemiparasites and holoparasites spread in the angiosperm phylogeny, including taxa from the closely related parasitic plants from Loranthaceae, Santalaceae, and Balanophoraceae, it was shown that this observation is unique to the Viscaceae. Statistical analyses also revealed that molecular evolution rates in this family alone are significantly different compared to other autotrophic, hemiparasitic and holoparasitic taxa, thus rejecting the previous finding that parasitic plants in general evolve faster than autotrophic relatives. The phylogenetic placement of Balanophoraceae in the Santalales was further supported by the results presented here. As DNA data showed quite divergent mitochondrial genes in the Viscaceae, including the loss of a whole complex, it was speculated that this might be the result of an unprecedented transfer to the nucleus of the complete cassette of nad genes. However, employing whole transcriptome sequencing in three members of this family, it was shown that: a) the remaining genes were actively transcribed, but they were not under heavy RNA editing, b) the NADH-ubiquinone oxidoreductase genes that were lost in their mitogenomes have not been transferred to their nuclear genome and c) a whole transcriptome sequencing approach, using oligo-dT beads to isolate mRNA molecules, was efficient in recovering plastid transcripts as well – at least in the Viscaceae –, thus offering the possibility to study RNA editing in the entire set of mitochondrial gene transcripts. Despite the plethora of studies focusing on plastome evolution and degradation in parasitic and mycoheterotrophic plants, many taxa still remain to be analyzed, in order to solidify the proposed models. Therefore, the first complete plastome of the mycoheterotroph orchid Lecanorchis aff. malaccensis (subfamily Vanilloideae) and the first three plastomes from the genus Odontochilus (subfamily Epidendroideae) were sequenced and assembled. The analyses revealed that L. aff. malaccensis followed the established model of gene loss and size reduction in chloroplast genomes of heterotrophic plants, but showed elevated GC contents across both coding and intergenic regions. Further, O. poilaneii is in the early stages of transitioning to the mycoheterotrophic lifestyle, has average GC contents, but does not exactly follow the suggested model, having lost the only one ndh gene, ndhF, but also psaC. Taken together, the results open up new directions in the respective research topics to better understand how the organellar genomes evolve in parasitic and mycoheterotrophic plants. Mitochondrial genome evolution in the Viscaceae and the closely related parasitic Amphorogynaceae needs to be further addressed and possibly models of gene loss in the mitogenomes of parasitic plants may be established. At the same time, the successful isolation of polyadenylated organellar mRNA molecules should be investigated in other parasitic and autotrophic plants to verify whether this is unique of the Viscaceae or expands to other families as well. Finally, although the established model of plastome evolution and degradation in parasitic plants applies to most cases, it is likely that variations of this model may exist, which calls for future work on parasitic and mycoheterotrophic plants from families not investigated so far.

Originalsprog	Engelsk

Forlag	Natural History Museum of Denmark, Faculty of Science, University of Copenhagen
Status	Udgivet - 2018

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Citationsformater

@phdthesis{e7ebaec0b5cd40dc8aea3f43aa08101e,

title = "The Evolution of Organellar Genomes in Parasitic and Mycoheterotrophic Plants",

abstract = "Parasitic and mycoheterotrophic plants correspond to 1% of all angiosperms (>4.500 species), and they are characterized by covering a smaller or larger part of their nutritional requirements from their plant or fungal host, respectively. This lifestyle has evolved independently several times in the angiosperm phylogeny, and has led to a wide variety of morphological diversity. In general, similar patterns of chloroplast genome (plastome) degradation and gene loss have been observed, and evolutionary models have been proposed. Yet little is known about the molecular evolution of their mitochondrial genomes. The mitochondrial genomes of Viscum spp. were shown to have experienced a unique loss of all complex I genes, accompanied by elevated molecular evolution rates in their remaining mitochondrial genes. Expanding the analysis to incorporate more hemiparasites and holoparasites spread in the angiosperm phylogeny, including taxa from the closely related parasitic plants from Loranthaceae, Santalaceae, and Balanophoraceae, it was shown that this observation is unique to the Viscaceae. Statistical analyses also revealed that molecular evolution rates in this family alone are significantly different compared to other autotrophic, hemiparasitic and holoparasitic taxa, thus rejecting the previous finding that parasitic plants in general evolve faster than autotrophic relatives. The phylogenetic placement of Balanophoraceae in the Santalales was further supported by the results presented here. As DNA data showed quite divergent mitochondrial genes in the Viscaceae, including the loss of a whole complex, it was speculated that this might be the result of an unprecedented transfer to the nucleus of the complete cassette of nad genes. However, employing whole transcriptome sequencing in three members of this family, it was shown that: a) the remaining genes were actively transcribed, but they were not under heavy RNA editing, b) the NADH-ubiquinone oxidoreductase genes that were lost in their mitogenomes have not been transferred to their nuclear genome and c) a whole transcriptome sequencing approach, using oligo-dT beads to isolate mRNA molecules, was efficient in recovering plastid transcripts as well – at least in the Viscaceae –, thus offering the possibility to study RNA editing in the entire set of mitochondrial gene transcripts. Despite the plethora of studies focusing on plastome evolution and degradation in parasitic and mycoheterotrophic plants, many taxa still remain to be analyzed, in order to solidify the proposed models. Therefore, the first complete plastome of the mycoheterotroph orchid Lecanorchis aff. malaccensis (subfamily Vanilloideae) and the first three plastomes from the genus Odontochilus (subfamily Epidendroideae) were sequenced and assembled. The analyses revealed that L. aff. malaccensis followed the established model of gene loss and size reduction in chloroplast genomes of heterotrophic plants, but showed elevated GC contents across both coding and intergenic regions. Further, O. poilaneii is in the early stages of transitioning to the mycoheterotrophic lifestyle, has average GC contents, but does not exactly follow the suggested model, having lost the only one ndh gene, ndhF, but also psaC. Taken together, the results open up new directions in the respective research topics to better understand how the organellar genomes evolve in parasitic and mycoheterotrophic plants. Mitochondrial genome evolution in the Viscaceae and the closely related parasitic Amphorogynaceae needs to be further addressed and possibly models of gene loss in the mitogenomes of parasitic plants may be established. At the same time, the successful isolation of polyadenylated organellar mRNA molecules should be investigated in other parasitic and autotrophic plants to verify whether this is unique of the Viscaceae or expands to other families as well. Finally, although the established model of plastome evolution and degradation in parasitic plants applies to most cases, it is likely that variations of this model may exist, which calls for future work on parasitic and mycoheterotrophic plants from families not investigated so far.",

author = "Athanasios Zervas",

year = "2018",

language = "English",

publisher = "Natural History Museum of Denmark, Faculty of Science, University of Copenhagen",

}

TY - BOOK

T1 - The Evolution of Organellar Genomes in Parasitic and Mycoheterotrophic Plants

AU - Zervas, Athanasios

PY - 2018

Y1 - 2018

N2 - Parasitic and mycoheterotrophic plants correspond to 1% of all angiosperms (>4.500 species), and they are characterized by covering a smaller or larger part of their nutritional requirements from their plant or fungal host, respectively. This lifestyle has evolved independently several times in the angiosperm phylogeny, and has led to a wide variety of morphological diversity. In general, similar patterns of chloroplast genome (plastome) degradation and gene loss have been observed, and evolutionary models have been proposed. Yet little is known about the molecular evolution of their mitochondrial genomes. The mitochondrial genomes of Viscum spp. were shown to have experienced a unique loss of all complex I genes, accompanied by elevated molecular evolution rates in their remaining mitochondrial genes. Expanding the analysis to incorporate more hemiparasites and holoparasites spread in the angiosperm phylogeny, including taxa from the closely related parasitic plants from Loranthaceae, Santalaceae, and Balanophoraceae, it was shown that this observation is unique to the Viscaceae. Statistical analyses also revealed that molecular evolution rates in this family alone are significantly different compared to other autotrophic, hemiparasitic and holoparasitic taxa, thus rejecting the previous finding that parasitic plants in general evolve faster than autotrophic relatives. The phylogenetic placement of Balanophoraceae in the Santalales was further supported by the results presented here. As DNA data showed quite divergent mitochondrial genes in the Viscaceae, including the loss of a whole complex, it was speculated that this might be the result of an unprecedented transfer to the nucleus of the complete cassette of nad genes. However, employing whole transcriptome sequencing in three members of this family, it was shown that: a) the remaining genes were actively transcribed, but they were not under heavy RNA editing, b) the NADH-ubiquinone oxidoreductase genes that were lost in their mitogenomes have not been transferred to their nuclear genome and c) a whole transcriptome sequencing approach, using oligo-dT beads to isolate mRNA molecules, was efficient in recovering plastid transcripts as well – at least in the Viscaceae –, thus offering the possibility to study RNA editing in the entire set of mitochondrial gene transcripts. Despite the plethora of studies focusing on plastome evolution and degradation in parasitic and mycoheterotrophic plants, many taxa still remain to be analyzed, in order to solidify the proposed models. Therefore, the first complete plastome of the mycoheterotroph orchid Lecanorchis aff. malaccensis (subfamily Vanilloideae) and the first three plastomes from the genus Odontochilus (subfamily Epidendroideae) were sequenced and assembled. The analyses revealed that L. aff. malaccensis followed the established model of gene loss and size reduction in chloroplast genomes of heterotrophic plants, but showed elevated GC contents across both coding and intergenic regions. Further, O. poilaneii is in the early stages of transitioning to the mycoheterotrophic lifestyle, has average GC contents, but does not exactly follow the suggested model, having lost the only one ndh gene, ndhF, but also psaC. Taken together, the results open up new directions in the respective research topics to better understand how the organellar genomes evolve in parasitic and mycoheterotrophic plants. Mitochondrial genome evolution in the Viscaceae and the closely related parasitic Amphorogynaceae needs to be further addressed and possibly models of gene loss in the mitogenomes of parasitic plants may be established. At the same time, the successful isolation of polyadenylated organellar mRNA molecules should be investigated in other parasitic and autotrophic plants to verify whether this is unique of the Viscaceae or expands to other families as well. Finally, although the established model of plastome evolution and degradation in parasitic plants applies to most cases, it is likely that variations of this model may exist, which calls for future work on parasitic and mycoheterotrophic plants from families not investigated so far.

AB - Parasitic and mycoheterotrophic plants correspond to 1% of all angiosperms (>4.500 species), and they are characterized by covering a smaller or larger part of their nutritional requirements from their plant or fungal host, respectively. This lifestyle has evolved independently several times in the angiosperm phylogeny, and has led to a wide variety of morphological diversity. In general, similar patterns of chloroplast genome (plastome) degradation and gene loss have been observed, and evolutionary models have been proposed. Yet little is known about the molecular evolution of their mitochondrial genomes. The mitochondrial genomes of Viscum spp. were shown to have experienced a unique loss of all complex I genes, accompanied by elevated molecular evolution rates in their remaining mitochondrial genes. Expanding the analysis to incorporate more hemiparasites and holoparasites spread in the angiosperm phylogeny, including taxa from the closely related parasitic plants from Loranthaceae, Santalaceae, and Balanophoraceae, it was shown that this observation is unique to the Viscaceae. Statistical analyses also revealed that molecular evolution rates in this family alone are significantly different compared to other autotrophic, hemiparasitic and holoparasitic taxa, thus rejecting the previous finding that parasitic plants in general evolve faster than autotrophic relatives. The phylogenetic placement of Balanophoraceae in the Santalales was further supported by the results presented here. As DNA data showed quite divergent mitochondrial genes in the Viscaceae, including the loss of a whole complex, it was speculated that this might be the result of an unprecedented transfer to the nucleus of the complete cassette of nad genes. However, employing whole transcriptome sequencing in three members of this family, it was shown that: a) the remaining genes were actively transcribed, but they were not under heavy RNA editing, b) the NADH-ubiquinone oxidoreductase genes that were lost in their mitogenomes have not been transferred to their nuclear genome and c) a whole transcriptome sequencing approach, using oligo-dT beads to isolate mRNA molecules, was efficient in recovering plastid transcripts as well – at least in the Viscaceae –, thus offering the possibility to study RNA editing in the entire set of mitochondrial gene transcripts. Despite the plethora of studies focusing on plastome evolution and degradation in parasitic and mycoheterotrophic plants, many taxa still remain to be analyzed, in order to solidify the proposed models. Therefore, the first complete plastome of the mycoheterotroph orchid Lecanorchis aff. malaccensis (subfamily Vanilloideae) and the first three plastomes from the genus Odontochilus (subfamily Epidendroideae) were sequenced and assembled. The analyses revealed that L. aff. malaccensis followed the established model of gene loss and size reduction in chloroplast genomes of heterotrophic plants, but showed elevated GC contents across both coding and intergenic regions. Further, O. poilaneii is in the early stages of transitioning to the mycoheterotrophic lifestyle, has average GC contents, but does not exactly follow the suggested model, having lost the only one ndh gene, ndhF, but also psaC. Taken together, the results open up new directions in the respective research topics to better understand how the organellar genomes evolve in parasitic and mycoheterotrophic plants. Mitochondrial genome evolution in the Viscaceae and the closely related parasitic Amphorogynaceae needs to be further addressed and possibly models of gene loss in the mitogenomes of parasitic plants may be established. At the same time, the successful isolation of polyadenylated organellar mRNA molecules should be investigated in other parasitic and autotrophic plants to verify whether this is unique of the Viscaceae or expands to other families as well. Finally, although the established model of plastome evolution and degradation in parasitic plants applies to most cases, it is likely that variations of this model may exist, which calls for future work on parasitic and mycoheterotrophic plants from families not investigated so far.

UR - https://rex.kb.dk/primo-explore/fulldisplay?docid=KGL01011963004&context=L&vid=NUI&search_scope=KGL&tab=default_tab&lang=da_DK

M3 - Ph.D. thesis

BT - The Evolution of Organellar Genomes in Parasitic and Mycoheterotrophic Plants

PB - Natural History Museum of Denmark, Faculty of Science, University of Copenhagen

ER -