Smith Chelsea R, Kaltenegger Elisabeth, Teisher Jordan, Moore Abigail J, Straub Shannon C K, Livshultz Tatyana
Botany Department, Academy of Natural Sciences of Drexel University, Philadelphia, PA, USA.
Department of Biodiversity, Earth, and Environmental Sciences, Drexel University, Philadelphia, PA, USA.
Am J Bot. 2025 Feb;112(2):e16458. doi: 10.1002/ajb2.16458. Epub 2025 Jan 30.
Enzymes that are encoded by paralogous genes and produce identical specialized metabolites in distantly related plant lineages are strong evidence of parallel phenotypic evolution. Inference of phenotypic homology for metabolites produced by orthologous genes is less straightforward, since orthologs may be recruited in parallel into novel pathways. In prior research on pyrrolizidine alkaloids (PAs), specialized metabolites of Apocynaceae, the evolution of homospermidine synthase (HSS), an enzyme of PA biosynthesis, was reconstructed and a single origin of PAs inferred because HSS enzymes of all known PA-producing Apocynaceae species are orthologous and descended from an ancestral enzyme with the motif (VXXXD) of an optimized HSS.
We increased sampling, tested the effect of amino acid motif on HSS function, revisited motif evolution, and tested for selection to infer evolution of HSS function and its correlation with phenotype.
Some evidence supports a single origin of PAs: an IXXXD HSS-like gene, similar in function to VXXXD HSS, evolved in the shared ancestor of all PA-producing species; loss of HSS function occurred multiple times via pseudogenization and perhaps via evolution of an IXXXN motif. Other evidence indicates multiple origins: the VXXXD motif, highly correlated with the PA phenotype, evolved two or four times independently; the ancestral IXXXD gene was not under positive selection, while some VXXXD genes were; and substitutions at sites experiencing positive selection occurred on multiple branches in the HSS-like gene tree.
The complexity of the genotype-function-phenotype map confounds the inference of PA homology from HSS-like gene evolution in Apocynaceae.
由旁系同源基因编码并在远缘植物谱系中产生相同特殊代谢产物的酶是平行表型进化的有力证据。对于直系同源基因产生的代谢产物，表型同源性的推断则不那么直接，因为直系同源基因可能会平行地被招募到新的途径中。在先前对夹竹桃科特殊代谢产物吡咯里西啶生物碱（PAs）的研究中，重建了PA生物合成酶高刺桐碱合酶（HSS）的进化过程，并推断PAs有单一的起源，因为所有已知产生PA的夹竹桃科物种的HSS酶都是直系同源的，并且起源于具有优化HSS基序（VXXXD）的祖先酶。
我们增加了样本量，测试了氨基酸基序对HSS功能的影响，重新审视了基序进化，并测试了选择作用以推断HSS功能的进化及其与表型的相关性。
一些证据支持PAs有单一的起源：一个功能与VXXXD HSS相似的IXXXD类HSS基因在所有产生PA的物种的共同祖先中进化；HSS功能的丧失通过基因假化多次发生，也许还通过IXXXN基序的进化发生。其他证据表明有多个起源：与PA表型高度相关的VXXXD基序独立进化了两次或四次；祖先的IXXXD基因没有受到正选择，而一些VXXXD基因受到了正选择；在类HSS基因树的多个分支上，经历正选择的位点发生了替换。
基因型-功能-表型图谱的复杂性混淆了从夹竹桃科类HSS基因进化推断PA同源性的过程。
