- Award ID(s):
- 1939226
- NSF-PAR ID:
- 10401879
- Date Published:
- Journal Name:
- BMC Genomics
- Volume:
- 23
- Issue:
- 1
- ISSN:
- 1471-2164
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Here we respond to the paper entitled “ Contribution of anthocyanin pathways to fruit flesh coloration in pitayas ” (Fan et al., BMC Plant Biol 20:361, 2020). In this paper Fan et al. 2020 propose that the anthocyanins can be detected in the betalain-pigmented genus Hylocereus , and suggest they are responsible for the colouration of the fruit flesh. We are open to the idea that, given the evolutionary maintenance of fully functional anthocyanin synthesis genes in betalain-pigmented species, anthocyanin pigmentation might co-occur with betalain pigments, as yet undetected, in some species. However, in absence of the LC-MS/MS spectra and co-elution/fragmentation of the authentic standard comparison, the findings of Fan et al. 2020 are not credible. Furthermore, our close examination of the paper, and re-analysis of datasets that have been made available, indicate numerous additional problems. Namely, the failure to detect betalains in an untargeted metabolite analysis, accumulation of reported anthocyanins that does not correlate with the colour of the fruit, absence of key anthocyanin synthesis genes from qPCR data, likely mis-identification of key anthocyanin genes, unreproducible patterns of correlated RNAseq data, lack of gene expression correlation with pigmentation accumulation, and putative transcription factors that are weak candidates for transcriptional up-regulation of the anthocyanin pathway.more » « less
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Summary In this study, we investigate the genetic mechanisms responsible for the loss of anthocyanins in betalain‐pigmented Caryophyllales, considering our hypothesis of multiple transitions to betalain pigmentation.
Utilizing transcriptomic and genomic datasets across 357 species and 31 families, we scrutinize 18 flavonoid pathway genes and six regulatory genes spanning four transitions to betalain pigmentation. We examined evidence for hypotheses of wholesale gene loss, modified gene function, altered gene expression, and degeneration of the MBW (MYB‐bHLH‐WD40) trasnscription factor complex, within betalain‐pigmented lineages.
Our analyses reveal that most flavonoid synthesis genes remain conserved in betalain‐pigmented lineages, with the notable exception of
TT19 orthologs, essential for the final step in anthocyanidin synthesis, which appear to have been repeatedly and entirely lost. Additional late‐stage flavonoid pathway genes upstream ofTT19 also manifest strikingly reduced expression in betalain‐pigmented species. Additionally, we find repeated loss and alteration in the MBW transcription complex essential for canonical anthocyanin synthesis.Consequently, the loss and exclusion of anthocyanins in betalain‐pigmented species appear to be orchestrated through several mechanisms: loss of a key enzyme, downregulation of synthesis genes, and degeneration of regulatory complexes. These changes have occurred iteratively in Caryophyllales, often coinciding with evolutionary transitions to betalain pigmentation.
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Summary The evolution of
l ‐DOPA 4,5‐dioxygenase activity, encoded by the gene , was a key step in the origin of betalain biosynthesis in Caryophyllales. We previously proposed thatDODA l ‐DOPA 4,5‐dioxygenase activity evolved via a single Caryophyllales‐specific neofunctionalisation event within the gene lineage. However, this neofunctionalisation event has not been confirmed and theDODA gene lineage exhibits numerous gene duplication events, whose evolutionary significance is unclear.DODA To address this, we functionally characterised 23 distinct
DODA proteins forl ‐DOPA 4,5‐dioxygenase activity, from four betalain‐pigmented and five anthocyanin‐pigmented species, representing key evolutionary transitions across Caryophyllales. By mapping these functional data to an updatedDODA phylogeny, we then explored the evolution ofl ‐DOPA 4,5‐dioxygenase activity.We find that low
l ‐DOPA 4,5‐dioxygenase activity is distributed across the gene lineage. In this context, repeated gene duplication events within theDODA gene lineage give rise to polyphyletic occurrences of elevatedDODA l ‐DOPA 4,5‐dioxygenase activity, accompanied by convergent shifts in key functional residues and distinct genomic patterns of micro‐synteny.In the context of an updated organismal phylogeny and newly inferred pigment reconstructions, we argue that repeated convergent acquisition of elevated
l ‐DOPA 4,5‐dioxygenase activity is consistent with recurrent specialisation to betalain synthesis in Caryophyllales. -
Abstract The R2R3-MYB transcription factor FveMYB10 is a major regulator of anthocyanin pigmentation in the red strawberry fruits. fvemyb10 loss-of-function mutants form yellow fruits but still accumulate purple-colored anthocyanins in the petioles, suggesting that anthocyanin biosynthesis is under distinct regulation in fruits and petioles. We identified a green petioles (gp)-1 mutant from chemical mutagenesis in the diploid wild strawberry Fragaria vesca that lacks anthocyanins in petioles. Using mapping-by-sequencing and transient functional assays, we confirmed that the causative mutation resides in a FveMYB10-Like (MYB10L) gene and that FveMYB10 and FveMYB10L function independently in the fruit and petiole respectively. In addition to their tissue-specific regulation, FveMYB10 and FveMYB10L respond differently to changes in light quality, produce distinct anthocyanin compositions, and preferentially activate different downstream anthocyanin biosynthesis genes in their respective tissues. This work identifies a new regulator of anthocyanin synthesis and demonstrates that two paralogous MYB genes with specialized functions enable tissue-specific regulation of anthocyanin biosynthesis in fruit and petiole tissues.more » « less
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