New insights into the functional roles of reactive oxygen species during embryo sac development and fertilization in Arabidopsis thaliana

Abstract

Previously considered as toxic by-products of aerobic metabolism, reactive oxygen species (ROS) are emerging as essential signaling molecules in eukaryotes. Recent evidence showed that maintenance of ROS homeostasis during female gametophyte development is crucial for embryo sac patterning and fertilization. Although ROS are exclusively detected in the central cell of mature embryo sacs, the study of mutants deficient in ROS homeostasis suggests that controlled oxidative bursts might take place earlier during gametophyte development. Also, a ROS burst that depends on pollination takes place inside the embryo sac. This oxidative response might be required for pollen tube growth arrest and for sperm cell release. In this mini-review, we will focus on new insights into the role of ROS during female gametophyte development and fertilization. Special focus will be made on the mitochondrial Mn-Superoxide dismutase (MSD1), which has been recently reported to be essential for maintaining ROS homeostasis during embryo sac formation.

Figure 1. Illustration showing ROS domains during megasporogenesis and female gametogenesis in Arabidopsis. thaliana. During megasporogenesis, an oxidative domain that corresponds to cytosolic peroxide is detected in the nucellus of the developing ovule. The location corresponds to the position of the dying megaspores. ROS cannot be detected during early megagametogenesis, suggesting a tight control of the embryo sac oxidative status. Accordingly, high expression of MSD1 is detected. ROS oscillations might control mitosis progression as reported for other systems. At maturity, mitochondrial superoxide and cytosolic peroxide are detected exclusively in the central cell of the embryo sac. MMC: megaspore mother cell; FM: functional megaspore.

Figure 2. ROS-mediated signaling pathways proposed to control pollen tube growth arrest/burst in A. thaliana. Pollination triggers an oxidative burst in the synergid cells inside the unfertilized embryo sac. This oxidative environment induced by the accumulation of mitochondrial superoxide and cytosolic peroxide is restricted to the synergid cells and maintained until pollen tube arrival. ROS production inside the embryo sac might be dependent on FER signaling. As described for root hairs, FER might interact with ROPGEF which in turn interacts and activates RAC/ROP. Downstream signaling might lead to the activation of NADPH oxidase to produce ROS. ROS increase inside the receptive synergid cell might be necessary for pollen tube growth arrest or burst. Additionally, it might lead to an influx of Ca²⁺ from the extracellular space. The increase in Ca²⁺ concentration could in turn promote synergid cell death.