Woodland strawberry axillary bud fate is dictated by a crosstalk of environmental and endogenous factors

Abstract

Plant architecture is defined by fates and positions of meristematic tissues and has direct consequences on yield potential and environmental adaptation of the plant. In strawberries (Fragaria vesca L. and F. × ananassa Duch.), shoot apical meristems (SAMs) can remain vegetative or differentiate into a terminal inflorescence meristem. Strawberry axillary buds (AXBs) are located in leaf axils and can either remain dormant or follow one of the two possible developmental fates. AXBs can either develop into stolons needed for clonal reproduction, or into branch crowns that can bear their own terminal inflorescences under favorable conditions. Although AXB fate has direct consequences on yield potential and vegetative propagation of strawberries, the regulation of AXB fate has so far remained obscure. We subjected a number of woodland strawberry (F. vesca L.) natural accessions and transgenic genotypes to different environmental conditions and growth regulator treatments to demonstrate that strawberry AXB fate is regulated either by environmental or endogenous factors, depending on the AXB position on the plant. We confirm that the F. vesca GIBBERELLIN20-oxidase4 (FvGA20ox4) gene is indispensable for stolon development and under tight environmental regulation. Moreover, our data show that apical dominance inhibits the outgrowth of the youngest AXB as branch crowns, although the effect of apical dominance can be overrun by the activity of FvGA20ox4. Finally, we demonstrate that the FvGA20ox4 is photoperiodically regulated via FvSOC1 (F. vesca SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1) at 18 °C, but at higher temperature of 22 °C an unidentified FvSOC1-independent pathway promotes stolon development.

Natural variation in the control of flowering and shoot architecture in diploid Fragaria species

“…We repeated the photoperiodic experiment at cooler temperature of 11°C and observed flowering and AXB fates by counting the number of stolons and branch crowns regularly. It has been earlier shown in F. vesca that cool temperature induces flowering independently of photoperiod (Heide and Sønsteby, 2007;Rantanen et al, 2015;Andrés et al, 2021). We found similar photoperiodindependent response in both F. vesca and F. bucharica after 6-week treatments at 11°C with significantly later flowering time in F. bucharica, while the control plants grown under LD conditions at 18°C remained vegetative until the end of the experiment (Figure 5).…”

“…The molecular mechanisms regulating floral induction and AXB fate as a response to environmental conditions are starting to emerge in the diploid model species F. vesca (Hytönen and Kurokura 2020;Andrés et al, 2021). To gain a broader view on the diversity of regulation of flowering and AXB fate within the Fragaria genus, we studied these responses in a panel of wild diploid strawberry species originating from diverse geographical origins ranging from Asia to Europe.…”

“…Regulation of AXB fate in Rosaceae has been mainly studied at the phenotype level, perhaps because the molecular processes taking place within the well-protected AXB are difficult to examine. However, a recent reports in F. vesca demonstrated that stolon development in this species requires GIBBERELLIN 20-OXIDASE4 (FvGA20ox4) that is activated within the AXBs under LD conditions via an FvSOC1-dependent photoperiodic pathway at 18°C (Mouhu et al, 2013;Tenreira et al, 2017;Andrés et al, 2021). Higher temperature of 22°C upregulates FvGA20ox4 independently of FvSOC1, whereas at cooler temperature (11°C), FvGA20ox4 is de-activated in both SD and LD conditions (Andrés et al, 2021).…”

“…However, a recent reports in F. vesca demonstrated that stolon development in this species requires GIBBERELLIN 20-OXIDASE4 (FvGA20ox4) that is activated within the AXBs under LD conditions via an FvSOC1-dependent photoperiodic pathway at 18°C (Mouhu et al, 2013;Tenreira et al, 2017;Andrés et al, 2021). Higher temperature of 22°C upregulates FvGA20ox4 independently of FvSOC1, whereas at cooler temperature (11°C), FvGA20ox4 is de-activated in both SD and LD conditions (Andrés et al, 2021). Cool temperatures, as well as SDs at 18°C, promote BC development instead of stolons in the seasonal flowering F. vesca, and although the same environmental cues induce flowering, these two processes can occur independently (Andrés et al, 2021).…”

“…Cool temperatures, as well as SDs at 18°C, promote BC development instead of stolons in the seasonal flowering F. vesca, and although the same environmental cues induce flowering, these two processes can occur independently (Andrés et al, 2021). However, the fate of the youngest AXB located immediately below the SAM is directly dependent on the vegetative/generative status of the SAM; if the SAM is induced to flower, the youngest AXB develops a branch crown to continue the growth of the plant in a sympodial fashion (Sugiyama et al, 2004;Andrés et al, 2021). Based on similar phenotypic effects from growth regulator applications (Ramina et al, 1985;Reekie and Hicklenton 2002;Webster, 2004;Hytönen et al, 2009), similar mechanisms may be involved in the control of AXB development to short or long shoots in different Rosaceous species.…”