Pseudogenization and Resurrection of a Speciation Gene

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Pseudogenization and Resurrection of a Speciation Gene

Petunia is a model system for the study of floral pigmentation and genetic architecture of evolutionary shifts in pigmentation[43]. For example, the loss of color (purple to white) during the transition from bee to hawkmoth pollination in P. axillaris is simple and involves inactivating mutations in the gene encoding the R2R3-MYB transcription factor AN2 [13, 26]. Likewise, loss of UV pigmentation in the transition from hawkmoth to hummingbird pollination was accompanied by a frameshift mutation in the R2R3-MYB transcription factor MYB-FL, leading from UV-absorbent flowers in P. axillaris to UV-reflective ones in P. exserta [16]. Thus, shifts in visible and UV color are attributed to mutations in MYB transcription factors with large phenotypic effect, allowing for subsequent adaptation to different pollinators. However, our understanding of the evolution of flower color in Petunia remains incomplete. The observed color variation among species of the long-tube clade could be the result of either an independent loss of color in the white P. axillaris or a reacquisition of color in the purple P. secreta and red P. exserta. Re-gain of anthocyanin pigmentation is a less likely scenario: first, because reacquiring a gene function is more demanding than losing it and, second, because once a pathway becomes obsolete, release from selective pressure will leave its genes free to accumulate deleterious mutations [44, 45], making reversal less likely with the passing of time. Indeed, observed losses of floral pigmentation appear to be largely unidirectional, reviewed in [4].

Here, we used phylogenetic reconstructions, sequence comparisons, as well as functional analyses to demonstrate that P. secreta is colored due to the improbable and independent reacquisition of AN2 function. This rare example of gene resurrection and trait reversal conforms to the essence of Dollo’s second law [46–49] and contributes to long-standing questions of how evolution proceeds

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@pnelson should look at this example closely. It shows convergence at a functional level, convergence at a gene level (vis vi: Winston Ewert: The Dependency Graph of Life), but divergence at a sequence level. Is that right @davecarlson?

FIgure 3 appears to be the key data:

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A) Bayesian inference of coding sequences of the Petunia AN2 gene. H1 and H11 encode functional proteins, whereas H2–H10 are pseudogenes.

(B) Graphical display of the coding region of AN2 ordered into the eleven haplotypes (H) classified according to the nature and position of the inactivating mutations. ATG, start codon: nt380: nucleotide 380; inverted triangle, indel, with number above indicating number of bases deleted or inserted; red star, stop codon.

(C) Partial nucleotide and translated protein sequences of the short-tube species P. inflata (H1), P. axillaris / P. exserta (H10), and P. secreta (H11). The 1-bp deletion in P. axillaris / P. exserta translates into a truncated protein. A compensatory 2-bp deletion leads to the functional AN2 of P. secreta .

(D) Introduction and silencing of the P. secreta AN2 gene modify floral color (from left to right): P. axillaris; transgenic P. axillaris :: AN2 P. secreta; P. secreta; P. secreta AN2-VIGS; note the white spots on the purple flower. Starred accessions are based on the coding sequence, see Table S1.

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I also wonder how much of this pathway is IC1 and how much represents “novel” function by the definitions of Behe and Axe/@Agauger…

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FIgure 1:

(A) Schematic representation of the flavonoid biosynthetic pathway genes with transcription factors MYB-FL and AN2 (circled). Transcription factor MYB-FL induces FLS, whereas AN2 activates DFR and downstream anthocyanin biosynthetic genes.

(B) Depiction of the Petunia flavonoid biosynthetic pathway where flavonol (UV color) as well as anthocyanin (visible color) pigments are produced (division indicated by the dashed arrows). DHK, DHQ, and DHM are the last common dihydroflavonol precursors to both flavonols and anthocyanins. Dihydroflavonols are modified by the pathway branching enzymes F3′H and F3′5′H, which add hydroxyl groups to the flavonoid B ring. At each branching node of this series of hydroxylating steps, FLS and DFR can compete for dihydroflavonol substrate. FLS action yields the flavonols kaempferol, quercetin, and myricetin, in increasing B-ring hydroxylation order. The anthocyanins are produced by the sequential action of DFR and ANS. Further modifications by a suite of six enzymes yield, in increasing B-ring hydroxylation order: the brick-red to orange pelargonidin; the red to magenta cyanidin and peonidin; as well as the blue to purple delphinidin, petunidin, and malvidin. In Petunia , the enzyme DFR does not accept DHK as a substrate, causing the absence of the orange-red pelargonidin (indicated in light gray arrows). The enzyme FLS has low activity on DHM, causing the severely reduced presence of myricetin. Increased hydroxylation of anthocyanidins through the action of F3′H/HT1 and F3′5′H/HF shift color from red toward purple-blue. Glycosylation, acylation, and methylation of the anthocyanidin backbone by a set of six enzymes have a similar effect.

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That sounds right to me, though to be honest I had not actually read most of the paper when I made the OP! :smiley:

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