Homeologue differential expression in the flavonoid biosynthetic pathway underlies flower colour variation in natural and synthetic polyploids of Nicotiana tabacum (Solanaceae)

Abstract Homeologue expression bias occurs when one progenitor copy of a gene is expressed at a higher level than the other in allopolyploids. Morphological variation, including differences in flower colour, exists between natural and synthetic allopolyploids of Nicotiana tabacum and their progenitors. In this study, we use a comparative transcriptomic approach to investigate gene expression differences as well as homeologue bias in the flavonoid biosynthetic pathway (FBP) in these accessions. We do not observe reciprocal homeologue bias between dark and light pink allopolyploids, but the production of light pink flowers is correlated with high FLAVONOL SYNTHASE:DIHYDROFLAVONOL-4-REDUCTASE (FLS:DFR) ratio at 60% of anthesis length due to delayed activation of DFR in these accessions. We do find that natural allopolyploids have stronger homeologue bias than synthetic allopolyploids in both FBP genes and across the transcriptome. While there is no overall subgenome dominance, there is a bias towards expression of N. tomentosiformis homeologues in FBP genes; however, the magnitude of this bias is reduced in allopolyploids compared to the progenitors, suggesting that N. sylvestris homeologues play an active role in the development of flower colour in N. tabacum allopolyploids. In addition, synthetic allopolyploids tend to exhibit trans regulation of homeologues whereas natural allopolyploids often have evolved cis-regulatory differences between homeologues since their origin.