Advances on Post-translational Modifications Involved in Seed Germination

Abstract

Seed germination and subsequent seedling establishment are important developmental processes that undergo extremely complex changes of physiological status and are precisely regulated at transcriptional and translational levels. Phytohormones including abscisic acid (ABA) and gibberellin (GA) are the critical signaling molecules that modulate the alteration from relative quiescent to a highly active state in seeds. Transcription factors such as ABA insensitive5 (ABI5) and DELLA domain-containing proteins play the central roles in response to ABA and GA, respectively, which antagonize each other during seed germination. Recent investigations have demonstrated that the regulations at translational and post-translational levels, especially post-translational modifications (PTMs), play a decisive role in seed germination. Specifically, phosphorylation and ubiquitination were shown to be involved in regulating the function of ABI5. In this review, we summarized the latest advancement on the function of PTMs involved in the regulation of seed germination, in which the PTMs for ABI5- and DELLA-containing proteins play the key roles. Meanwhile, the studies on PTM-based proteomics during seed germination and the crosstalk of different PTMs are also discussed. Hopefully, it will facilitate in obtaining a comprehensive understanding of the physiological functions of different PTMs in seed germination.

Keywords: ABI5; phosphorylation; post-translational modification; seed germination; ubiquitylation.

FIGURE 1

The diverse post-translation modifications (PTMs) involved in seed germination. (A) The key genes regulated by PTMs involved in seed germination. (B) The PTMs identified by proteomics techniques involved in seed germination. The phytohormones GA and ABA function antagonistically with each other in regulating seed germination, of which the signal transduction is largely coordinated by PTMs. ABI5, a key transcription factor in response to ABA, suppresses the seed germination, and it is phosphorylated by different kinases such as SnRK2, BIN2, CIPK26, PKS5, and KEG. KEG also ubiquitinates ABI5, CIPK26, and ABF1/3 to directly inhibit seed germination. DWA1, DWA2, and DDB1 interact with each other forming a complex that elevates the level of ABI5, in which DWA1 and DWA2 are ubiquitinated by CUL4. CUL4 also ubiquitinated ABD1 targeted for ABI5 degradation through 26S proteasome. The phosphatase FyPP1/2 and SIZ1 dephosphorylated and sumoylated ABI5, respectively. GA facilitated the expression of SLY1, which ubiquitinated two DELLA containing proteins RGA and RGL2 to derepress for germination. MADS-box transcription factor AGL67 acetylated the promoter of zinc-finger protein SOM to promote its expression that inhibited seed germination, and AtMIA40 formed the complex with AtSLP2 to coordinate its phosphatase activity, which negatively regulated the GA-related process under seed germination. Furthermore, the PTMs including phosphorylation, ubiquitination, carbonylation, glycosylation, acetylation, and succinylation were also involved in multiple metabolism processes such as protein processing, ribosome complex, brassinosteroid signal transduction, and reactive oxygen species. GA, gibberellin; ABA, abscisic acid; ABI5, ABA insensitive 5; SnRK2s, SNF1-related kinases 2; BIN2, BRASSINOSTEROID-INSENSITIVE 2; CIPK26, Calcineurin B-like Interacting Protein Kinase 26; PKS5, SOS2-like protein kinase 5; KEG, KEEP ON GOING; ABF1/3: ABRE binding factor 1/3; DWA1/2, DWD hypersensitive to ABA1; CUL4, CULLIN4; DDB1, damaged DNA binding1; ABD1, ABA-hypersensitive DCAF1; SIZ1, SUMO E3 ligases; SLY1, F-box-containing proteins SLEEPY1; RGA, REPRESSOR OF ga1-3; RGL2, RGA-like 2; SOM, SOMNUS; AGL67, AGAMOUS-LIKE67; AtSLP2, Arabidopsis Shewanella-like protein phosphatase 2; AtMIA40, Arabidopsis mitochondrial oxidoreductase import and assembly protein 40; P, phosphorylation; U, ubiquitination; carb, carbonylation; glyc, glycosylation; acet, acetylation; succ, succinylation; sumo, sumoylation.