Functional diversification of phytoene desaturase (PDS) paralogs in diploid poplar: Catalytic PDS1 and a transcribed...

Phytoene desaturase (PDS) catalyzes the first committed step in carotenoid biosynthesis and represents a primary target of bleaching herbicides. However, the genomic architecture, evolutionary dynamics, and regulatory networks of PDS genes in woody perennials, particularly the economically important Populus L. species, remain poorly understood. Here we report a functional gene-pseudogene pair in Populus davidiana × P. bolleana Lauch cv. 'Shanxin': an enzyme-encoding PDS1 (PdaPboPDS1) and a transcriptionally active pseudogene (ΨPdaPboPDS2) with 13 premature termination codons. ΨPdaPboPDS2 is actively transcribed, implying functional regulatory roles rather than non-functional pseudogene status. Comparative genomic analyses of PDS1 across P. trichocarpa Torr. & A.Gray ex Hook., P. deltoides Bartr. ex Marsh. cv. 'I-69', and P. deltoides × P. euramericana (Dode) Guinier cv. 'Nanlin895' revealed exceptional evolutionary conservation, with identical coding sequence length (1731 bp / 576 amino acids), > 98% nucleotide identity, conserved exon-intron architecture (14 exons), consistent phylogenetic status, similar three-dimensional protein structure, functionally equivalent chloroplast-localized enzyme activity, and herbicide-binding affinity. Notably, tissue-specific and transgenic analyses revealed uncoupling of PdaPboPDS1 transcript and protein abundance, implicating pseudogene-derived lncRNAs as potential post-transcriptional regulators. Overexpression of PdaPboPDS1 led to a modest increase in phytoene desaturase abundance without enhancing lycopene or carotenoid accumulation, presumably due to feedback repression of downstream carotenoid pathway genes (e.g., ZDS and Z-ISO). These findings elucidate the evolutionary constraint and regulatory sophistication of carotenoid metabolism in trees, informing strategies for herbicide-resistant poplar breeding.