A DELLA protein contributes to seed protein storage

Seeds and their reserve stores of carbohydrates, oils, and proteins provide the plant with a robust means of propagation and survival and thus are important evolutionary adaptation. These seed stores are also crucial for human nutrition (Verdier and Thompson, 2008). The synthesis and accumulation of seed storage proteins (SSPs) is tightly controlled by developmental and environmental cues, many of which are not yet fully understood.

At the heart of many plants physiological processes are the finely tuned hormone signaling pathways. Gibberellins (GAs) were first discovered over 90 years ago (Yabuta, 1938). Since then, GAs have been recognized as key regulators of plant growth and development, mediating tissue elongation, flowering, seed dormancy, and seed germination among numerous other processes (Tai-ping, 2008; Davière and Achard, 2013). Chemically, GAs constitute an extensive family of diterpenoid acids, where only few are physiologically active (Hedden and Thomas, 2012). The diversity of processes that are regulated by GAs stems from their interaction with the DELLA (Asp–Glu–Leu–Leu–Ala motif containing) proteins. DELLAs act as repressors of GA signaling activity (Hauvermale et al., 2012). Upon binding with its receptor GIBBERELLIN-INSENSITIVE DWARF1, GA promotes DELLA ubiquitination and subsequent proteasome-dependent degradation. The degradation of DELLAs releases downstream processes that depend on GA. Thus, DELLAs act as the gatekeepers for the many processes that are regulated by GAs.

Five DELLA proteins are known in Arabidopsis thaliana: GIBBERELLIN-INSENSITIVE (Peng et al., 1997), REPRESSOR OF ga1–3 (RGA; Silverstone et al., 1998), and RGA-LIKE1 (RGL1), 2, RGL2, and RGL3 (Lee et al., 2002). Of these, RGL2 and RGL3 have been implicated in seed germination, but the specific mechanism of this involvement was not previously known. In this issue of Plant Physiology, Hu et al. (2021) explore the role of the DELLA protein RGL3 in the accumulation of SSPs in Arabidopsis. Using mutants unable to synthesize GA (ga3ox 1/2/3) in combination with exogenous GA applications in Col-0, this study first establishes the direct relationship between the absence of GA and increased amounts of SSPs in Arabidopsis seeds. Furthermore, the study shows the link between the pattern of SSP accumulation and RGL3 transcript and protein levels during seed development. Compared to transcripts encoding other DELLA proteins, RGL3 transcripts exhibit a much higher increase at 11 d after pollination, the time when SSPs start to accumulate in seeds (Baud et al., 2008). Moreover, complementation of an rgl3 mutant showing reduced levels of SSP transcript and protein accumulation was fully recovered in the wild-type phenotype. Similarly, overexpression of RGL3 using the 35S promoter resulted in increased amounts of accumulated SSPs.

Although DELLAs localize in the nucleus (Hauvermale et al., 2012) and regulate gene expression, they do not directly interact with promoter regions; instead, they exert their regulatory function by interacting with diverse transcription factors. ABSCISIC ACID-INSENSITIVE 3 (ABI3) is a transcription activator required for the accumulation of SSPs during the seed filling phase (Verdier and Thompson, 2008). Hu et al. (2021) used pull-down assays and bimolecular fluorescence complementation in Arabidopsis mesophyll protoplasts to demonstrate that RGL3 and ABI3 interact in vitro and in vivo. Furthermore, chromatin immunoprecipitation assays showed that these two proteins are associated with promoter regions of SSP-encoding genes and act as co-activators.

Phytohormones are the focus of programs dedicated to breeding desirable traits since they are key regulators of plant tolerance to biotic and abiotic stress as well as productivity. SSPs are hugely important for human nutrition. The study by Hu et al. (2021) adds to our understanding of the important process of seed maturation and protein storage as regulated by GAs, and the role of the RGL3-type DELLA gene as a potential breeding target.