Diversity of woodland strawberry inflorescences arises from heterochrony regulated by TERMINAL FLOWER 1 and FLOWERING LOCUS T

Sergei Lembinen1, Mikolaj Cieslak2, Teng Zhang1, Kathryn Mackenzie1, Paula Elomaa1, Przemyslaw Prusinkiewicz2, and Timo Hytönen1
1 University of Helsinki
2 University of Calgary

Abstract

A vast variety of inflorescence architectures have evolved in angiosperms. Here, we analyze the diversity and development of the woodland strawberry (Fragaria vesca) inflorescence. Contrary to historical classifications, we show that it is a closed thyrse: a compound inflorescence with determinate primary monopodial axis and lateral sympodial branches, thus combining features of racemes and cymes. We demonstrate that this architecture is generated by 2 types of inflorescence meristems differing in their geometry. We further show that woodland strawberry homologs of TERMINAL FLOWER 1 (FvTFL1) and FLOWERING LOCUS T (FvFT1) regulate the development of both the racemose and cymose components of the thyrse. Loss of functional FvTFL1 reduces the number of lateral branches of the main axis and iterations in the lateral branches but does not affect their cymose pattern. These changes can be enhanced or compensated by altering FvFT1 expression. We complement our experimental findings with a computational model that captures inflorescence development using a small set of rules. The model highlights the distinct regulation of the fate of the primary and higher-order meristems, and explains the phenotypic diversity among inflorescences in terms of heterochrony resulting from the opposite action of FvTFL1 and FvFT1 within the thyrse framework. Our results represent a detailed analysis of thyrse architecture development at the meristematic and molecular levels.

Reference

Sergei Lembinen, Mikolaj Cieslak, Teng Zhang, Kathryn Mackenzie, Paula Elomaa, Przemyslaw Prusinkiewicz, and Timo Hytönen. Diversity of woodland strawberry inflorescences arises from heterochrony regulated by TERMINAL FLOWER 1 and FLOWERING LOCUS T. The Plant Cell, koad086, 2023.

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Download the supporting information from the publisher's site or download the Supplemental Model Description from here and the Supplemental Data from here.

Download Movie 1 here -- Simulated WT woodland strawberry development calibrated to the GER12 x FIN2 cross (Phenotype 0).(MP4, 0.58 MB)
Download Movie 2 here -- Simulated development of the inflorescence Phenotype 1 shown in Figure 8. (MP4, 0.39 MB)
Download Movie 3 here -- Simulated development of the inflorescence Phenotype 2 shown in Figure 8. (MP4, 0.35 MB)
Download Movie 4 here -- Simulated development of the inflorescence Phenotype 3 shown in Figure 8. (MP4, 0.32 MB)
Download Movie 5 here -- Simulated development of the inflorescence Phenotype 4 shown in Figure 8. (MP4, 0.30 MB)
Download Movie 6 here -- Simulated development of the inflorescence Phenotype 5 shown in Figure 8. (MP4, 0.19 MB)
Download Movie 7 here -- Simulated development of the inflorescence Phenotype 6 shown in Figure 8. (MP4, 0.22 MB)
Download Movie 8 here -- Simulated development of the inflorescence Phenotype 7 shown in Figure 8. (MP4, 0.24 MB)

Download Model Strawberry-basic here (TGZ archive, 0.37 MB)
Download Model Strawberry-calibrating here (TGZ archive, 2.65 MB)
Download Model Strawberry-diversity here (TGZ archive, 0.55 MB)

You will need VLAB to run the models. They were tested using VLAB verison 5.0 on macOS 10.13 (High Sierra).