Cellular recycling of proteins in seed dormancy alleviation and germination
Oracz and Stawska, Front. Plant Sci.(2016) https://doi.org/10.3389/fpls.2016.01128
Each step of the seed-to-seed cycle of plant development including seed germination is characterized by a specific set of proteins. The continual renewal and/or replacement of these biomolecules are crucial for optimal plant adaptation. As proteins are the main effectors inside the cells, their levels need to be tightly regulated. This is partially achieved by specific proteolytic pathways via multicatalytic protease complexes defined as 20S and 26S proteasomes. In plants, the 20S proteasome is responsible for degradation of carbonylated proteins, while the 26S being a part of ubiquitin-proteasome pathway is known to be involved in proteolysis of phytohormone signaling regulators.
Figure 1. The model of protein recycling in cells of germinating seeds. During translation preformed on ribosomes associated with particular mRNAs, a wide range of proteins are synthetized, and the energy in the form of ATP is required for this process. The specific regulatory proteins which have completed their mission in various cellular processes can be polyubiquitinated by the cascade of three enzymes E1, E2, and E3. The attachment of at least 4 ubiquitin (Ub) molecules target proteins for proteolysis via 26S proteasome in an ATP-dependent manner. As soon as the substrate is degraded, Ub are released and can be reused in the labeling and degradation of another target protein. On the contrary, storage and other (e.g., damaged) proteins, which are irreversibly oxidized (carbonylated) during seed germination, undergo ATP- and Ub-independent degradation by 20S proteasome. Short peptides resulting from proteasomal proteolysis are then cleaved by the peptidases to single amino acids, which then can be re-used by complexes of ribosomes and mRNA during de novo protein biosynthesis and/or used in the citric acid cycle (TCA) to generate energy – ATP. The balance between protein synthesis and degradation determines the germination potential of the seed (Oracz and Stawska, Front. Plant Sci., 2016, https://doi.org/10.3389/fpls.2016.01128).
On the other hand, the role of translational control of plant development is also well-documented, especially in the context of pollen tube growth and light signaling. Despite the current progress that has been made in seed biology, the sequence of cellular events that determine if the seed can germinate or not are still far from complete understanding. The role and mechanisms of regulation of proteome composition during processes occurring in the plant’s photosynthetic tissues have been well-characterized since many years, but in non-photosynthetic seeds it has emerged as a tempting research task only since the last decade. This review discusses the recent discoveries providing insights into the role of protein turnover in seed dormancy alleviation, and germination, with a focus on the control of translation and proteasomal proteolysis.
Figure 2. The 26S proteasome as a regulatory hub of GA, ABA, and light signaling. The complex of proteases called as the proteasome 26S together with various types of E3 ligases ubiquitinating target proteins are key components of the mechanism controlling accumulation of regulatory proteins involved in GA, ABA, and light signaling pathways, determining the germination potential of the seed. Proteasome modulate GA signaling by degradation of DELLA proteins, which in the presence of GA can bind to GID1 receptors and SCF complex resulting in DELLA ubiquitination, allowing recognition of targeted proteins by the 26S complex. ABA signaling is controlled by the degradation of ABI3 and ABI5 transcription factors, as well as CIPK26 regulatory proteins, by 26S proteasome after ubiquitination of these proteins by different types of E3 ligases, such as AIP2, KEG, and CUL4. Light signal perception by germinating seeds rely mostly on the modulation of abundance of PHYB, which depends on the activity of CDD-CUL4 ligase complex, as well as LRB1/2 regulatory proteins allowing ubiquitination of PHYB and degradation by 26S proteasome. Degradation of regulatory proteins involved in GA and ABA signaling leads to stimulation of germination, while degradation of regulators of light signaling affects germination (indicated by up- or down-oriented arrows). Ub, ubiquitin (Oracz and Stawska, Front. Plant Sci., 2016, https://doi.org/10.3389/fpls.2016.01128).
The presented novel data of translatome profiling in seeds highlighted that post-transcriptional regulation of germination results from a timely regulated initiation of translation. In addition, the importance of 26S proteasome in the degradation of regulatory elements of cellular signaling and that of the 20S complex in proteolysis of specific carbonylated proteins in hormonal- and light-dependent processes occurring in seeds is discussed. Based on the current knowledge the model of cellular recycling of proteins in germinating seeds is also proposed.
Funding: Krystyna Oracz and Marlena Stawska are grateful for the financial support from the HOMING PLUS/2012-5/10 grant of the Foundation for Polish Science.