Artificial selection of two antagonistic E3 ubiquitin ligases finetunes soybean photoperiod adaptation and grain yield.

Abstract

The precise control of flowering time is of utmost importance for crop adaptation to varying environmental conditions and consequently determines grain yield and plant fitness. Soybean <i>E2</i>, the homolog of Arabidopsis <i>GIGANTEA</i>, is a major locus contributing to high-latitude adaptation and is involved in photoperiod sensitivity. However, due to major effects of <i>E2</i>, additional genetic loci controlling soybean flowering and adaptation have historically been masked and difficult to identify. Here, by eliminating the effect of <i>E2</i>, we identified a <i>Tof9</i> locus controlling flowering in which <i>ZEITLUPE 2</i> (<i>ZTL2</i>) is the causal gene. <i>ZTL2</i> encodes an F-box E3 ubiquitin ligase with homology to Arabidopsis ZEITLUPE and is shown to play a key role in the soybean photoperiodic flowering pathway. ZTL2 physically interacts with E2 to mediate its degradation. Intriguingly, ZTL2 and FKF1, both belong to the F-box-type E3 ubiquitin-ligase family, exhibit opposite roles in regulating soybean flowering. ZTL2 degrades E2, leading to early flowering, while FKF1 stabilizes E2, resulting in delayed flowering. The balance between ZTL2-mediated degradation and FKF1-mediated stabilization enables soybeans to finetune flowering time and maximize grain yield. Field-grown <i>ztl2</i> mutants are taller, flower late, and have increased yield parameters. <i>ZTL2</i> and <i>FKF1b</i> bear contrasting artificial-selection patterns to adapt to different latitudes. This antagonistic regulation is crucial for soybean adaptation to diverse ecological settings and allows plants to fine-tune their flowering time in response to photoperiod and latitudinal changes.