Accelerated Flowering and Differential Florigen Gene Expression of Seagrass Zostera marina Under Experimental Warming

Flowering is an important trait for the resilience of marine angiosperms (seagrasses) as they face rising seawater temperatures, more frequent extreme weather events, and anthropogenic disturbances. Using the seagrass Zostera marina, we applied a common garden approach to experimentally test how flowering and its underlying molecular mechanisms responded to elevated water temperature (+3°C). We focused on developmental and reproductive traits paired with florigen gene expression to gain insight into the molecular mechanism underpinning differences in flowering responses. We compared annual seedlings from two source populations (Willapa Bay along the coast and Padilla Bay in the Salish Sea, Washington, USA) to understand natural variation not only in morphological and reproductive traits but also in the gene-environment interactions governing flowering onset. At the individual and population levels, annual seedlings in the +3°C heated treatment produced more spathes and accelerated the development of inflorescences, so seeds dispersed sooner. Seedlings from Padilla Bay flowered at greater rates and earlier than those from Willapa Bay, and these differences were exaggerated by the +3°C heated treatment. A predicted repressor of flowering onset, ZmaFT9, was expressed at lower levels in the shoots grown in the +3°C heated treatment, and even more so in the Padilla Bay population, which flowered earlier than the Willapa Bay population. For two predicted floral activators, ZmaFT2 and ZmaFT4, expression increased throughout the summer regardless of population and showed no response to the temperature treatment. ZmaTFL1a, a gene predicted to be involved with downstream flowering processes, showed no significant response to the temperature treatment. Together, these results support a key role for antiflorigen (ZmaFT9) in the molecular control of flowering in Z. marina, and ZmaFT9 expression contributes to the temperature-based response of the timing of flowering onset. Impacts of elevated seawater temperature on flowering timing and spathe production, with different responses by population, have potential consequences for seed yield and variation in meadow resilience.