Differential growth and flowering capacity of tulip bulbs and the potential involvement of PHOSPHATIDYLETHANOLAMINE-BINDING PROTEINS (PEBPs).

Background: Tulipa gesneriana reproduces vegetatively by the development of bulb clusters from axillary meristems in the scales of a mother bulb. While part of the daughter bulbs in a cluster develop into large, flowering bulbs, others stay small and vegetative under the same environmental conditions. This study aims to investigate how these different developmental fates are orchestrated.

Results: RNA-seq analysis revealed that the overall transcriptomic landscape of the two types of daughter bulbs does not differ substantially, but follows a similar trajectory over time. Nonetheless, the expression levels of genes related to proliferation already differ at early development stages. Surprisingly, at a later stage, transcriptomic changes related to flower induction are detectable in flowering as well as non-flowering bulbs, with some quantitative differences. However, genes linked with floral organ development are differentially expressed, as well as negative regulators of flowering and more basal metabolic processes. In search for the molecular determinants of daughter bulb size and developmental fate, we investigated members of the PHOSPHATIDYLETHANOLAMINE-BINDING PROTEIN (PEBP) gene family as candidates. Tulip FLOWERING LOCUS T1 (TgFT1), TgFT2, and TgFT3 are expressed in leaves and leaf-like organs of the mother plant, and their encoded proteins interact with the TCP transcription factor TEOSINTE BRANCHED1 (TgTB1). Therefore, we suggest that these three genes act as 'bulbigens', meaning regulators of axillary meristem outgrowth and hence, daughter bulb size. Furthermore, we found that TgFT2 and TgFT4 could constitute the main florigens in tulips, because of their expression pattern and the binding of their encoding proteins to the bZIP transcription factor FD (TgFD). Moreover, Arabidopsis lines ectopically expressing TgFT2 or TgFT4 flower significantly earlier than the wild type.

Conclusions: Differences in the developmental fate of tulip daughter bulbs are established early during development and are linked with differences in cell division and metabolism. The activity of members of the PEBP family, known for their role in flowering and storage organ formation in geophytes, appeared to be associated with the transcriptional switches observed during daughter bulb development. This points towards a functional role of these proteins in governing developmental trajectories underlying the mode of reproduction.