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

Authors: MCCARTHY, ELIZABETH - State University Of New York (SUNY); LANDIS, JACOB - Cornell University; MCCOY, ABIGAIL - State University Of New York (SUNY); LAWHORN, AMBER - University Of California, Riverside; KURTI, AMMELDA - University Of California, Riverside; XU, YIMIN - Boyce Thompson Institute; Giovannoni, James; LITT, AMY - University Of California, Riverside

Submitted to: Botanical Journal of the Linnean Society
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/17/2023
Publication Date: 4/1/2024
Citation: Mccarthy, E., Landis, J., Mccoy, A., Lawhorn, A., Kurti, A., Xu, Y., Giovannoni, J.J., Litt, A. 2024. Homeologue differential expression in the flavonoid biosynthetic pathway underlies flower colour variation in natural and synthetic polyploids of Nicotiana tobacum (Solanaceae). Botanical Journal of the Linnean Society. 2024 (4), 283-303. https://doi.org/10.1093/botlinnean/boad052.
DOI: https://doi.org/10.1093/botlinnean/boad052

Interpretive Summary: Flower color differences in blue, purple, pink, red, and white hues are often due to differences in expression and/or function of the genes that make up or regulate the flavonoid biosynthetic pathway, a branched pathway that produces both anthocyanin and flavonol pigments. Multiple types of anthocyanin and flavonol pigments are produced that differ by the number of hydroxyl groups present on the beta ring of their chemical structures. Flavonols include kaempferol with one hydroxyl group, quercetin with two hydroxyl groups, and myricetin with three hydroxyl groups; these pigments are often colourless to humans, but absorb UV and have antioxidant potential that protects plant tissues from light and other stresses and have nutritional value to humans. Here we studied the genetic contributions to color of leaf petals using the model species tobacco which produces large colorful flowers. We demonstrate that color variation results from gene dosage of key genes in the flavonoid synthesis pathway and that contributions can also differ depending on parental origin of said genes. The combination of gene product function, gene dosage and genetic origin results in the diverse array of colors displayed in floral organs.

Technical 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.