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Shaping the evolutionary tree of green plants: evidence from the GST family.

ABSTRACT: Glutathione-S-transferases (GSTs) are encoded by genes belonging to a wide ubiquitous family in aerobic species and catalyze the conjugation of electrophilic substrates to glutathione (GSH). GSTs are divided in different classes, both in plants and animals. In plants, GSTs function in several pathways, including those related to secondary metabolites biosynthesis, hormone homeostasis, defense from pathogens and allow the prevention and detoxification of damage from heavy metals and herbicides. 1107 GST protein sequences from 20 different plant species with sequenced genomes were analyzed. Our analysis assigns 666 unclassified GSTs proteins to specific classes, remarking the wide heterogeneity of this gene family. Moreover, we highlighted the presence of further subclasses within each class. Regarding the class GST-Tau, one possible subclass appears to be present in all the Tau members of ancestor plant species. Moreover, the results highlight the presence of members of the Tau class in Marchantiophytes and confirm previous observations on the absence of GST-Tau in Bryophytes and green algae. These results support the hypothesis regarding the paraphyletic origin of Bryophytes, but also suggest that Marchantiophytes may be on the same branch leading to superior plants, depicting an alternative model for green plants evolution.

SUBMITTER: Monticolo F

PROVIDER: S-EPMC5662610 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Shaping the evolutionary tree of green plants: evidence from the GST family.

Monticolo Francesco F Colantuono Chiara C Chiusano Maria Luisa ML

Scientific reports 20171030 1

Glutathione-S-transferases (GSTs) are encoded by genes belonging to a wide ubiquitous family in aerobic species and catalyze the conjugation of electrophilic substrates to glutathione (GSH). GSTs are divided in different classes, both in plants and animals. In plants, GSTs function in several pathways, including those related to secondary metabolites biosynthesis, hormone homeostasis, defense from pathogens and allow the prevention and detoxification of damage from heavy metals and herbicides. 1 ...[more]

PMID: 29084977

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Project description:BackgroundThe degree of metal binding specificity in metalloproteins such as metallothioneins (MTs) can be crucial for their functional accuracy. Unlike most other animal species, pulmonate molluscs possess homometallic MT isoforms loaded with Cu(+) or Cd(2+). They have, so far, been obtained as native metal-MT complexes from snail tissues, where they are involved in the metabolism of the metal ion species bound to the respective isoform. However, it has not as yet been discerned if their specific metal occupation is the result of a rigid control of metal availability, or isoform expression programming in the hosting tissues or of structural differences of the respective peptides determining the coordinative options for the different metal ions. In this study, the Roman snail (Helix pomatia) Cu-loaded and Cd-loaded isoforms (HpCuMT and HpCdMT) were used as model molecules in order to elucidate the biochemical and evolutionary mechanisms permitting pulmonate MTs to achieve specificity for their cognate metal ion.ResultsHpCuMT and HpCdMT were recombinantly synthesized in the presence of Cd(2+), Zn(2+) or Cu(2+) and corresponding metal complexes analysed by electrospray mass spectrometry and circular dichroism (CD) and ultra violet-visible (UV-Vis) spectrophotometry. Both MT isoforms were only able to form unique, homometallic and stable complexes (Cd(6)-HpCdMT and Cu(12)-HpCuMT) with their cognate metal ions. Yeast complementation assays demonstrated that the two isoforms assumed metal-specific functions, in agreement with their binding preferences, in heterologous eukaryotic environments. In the snail organism, the functional metal specificity of HpCdMT and HpCuMT was contributed by metal-specific transcription programming and cell-specific expression. Sequence elucidation and phylogenetic analysis of MT isoforms from a number of snail species revealed that they possess an unspecific and two metal-specific MT isoforms, whose metal specificity was achieved exclusively by evolutionary modulation of non-cysteine amino acid positions.ConclusionThe Roman snail HpCdMT and HpCuMT isoforms can thus be regarded as prototypes of isoform families that evolved genuine metal-specificity within pulmonate molluscs. Diversification into these isoforms may have been initiated by gene duplication, followed by speciation and selection towards opposite needs for protecting copper-dominated metabolic pathways from nonessential cadmium. The mechanisms enabling these proteins to be metal-specific could also be relevant for other metalloproteins.

Project description:Lycopods are tracheophytes in the Kingdom Plantae and represent one of the oldest lineages of living vascular plants. Symbiotic interactions between these plants with fungi and bacteria, including fine root endophytes in Endogonales, have been hypothesized to have helped early diverging plant lineages colonize land. However, attempts to study the lycopod rhizobiome in its natural environment are still limited. In this study, we used Illumina amplicon sequencing to characterize fungal and bacterial diversity in nine Lycopodiaceae (club moss) species collected in New Zealand. This was done with generic fungal ITS rDNA primers, as well as Endogonales- and arbuscular mycorrhizal fungi (AMF)-selective primer sets targeting the 18S rDNA, and generic bacterial primers targeting the V4 region of the 16S rDNA. We found that the Lycopodiaceae rhizobiome was comprised of an unexpected high frequency of Basidiomycota and Ascomycota coincident with a low abundance of Endogonales and Glomerales. The distribution and abundance of Endogonales varied with host lycopod, and included a novel taxon as well as a single operational taxonomic unit (OTU) that was detected across all plant species. The Lycopodiaceae species with the greatest number and also most unique OTUs was Phlegmariurus varius, while the plant species that shared the most fungal OTUs were Lycopodiella fastigiatum and Lycopodium scariosum. The bacterial OTU distribution was generally not consistent with fungal OTU distribution. For example, community dissimilarity analysis revealed strong concordance between the evolutionary histories of host plants with the fungal community but not with the bacterial community, indicating that Lycopodiaceae have evolved specific relationships with their fungal symbionts. Notably, nearly 16% of the ITS rDNA fungal diversity detected in the Lycopodiaceae rhizobiome remained poorly classified, indicating there is much plant-associated fungal diversity left to describe in New Zealand.

Dataset Information

Shaping the evolutionary tree of green plants: evidence from the GST family.

Publications

Shaping the evolutionary tree of green plants: evidence from the GST family.

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