Multilayered Regulation in Senescence

Sakuraba et al. show the existence of multilayered regulation systems for the rice ONAC054 transcription factor, which is involved in abscisic acid-induced leaf senescence in rice. Plant Cell

By Nam-Chon Paek, Department of Plant Science, Seoul National University, Seoul 08826, Republic of Korea

Background: In most plants, abscisic acid (ABA) induces premature leaf senescence. However, the mechanisms of ABA signaling during leaf senescence still remain largely unknown. The NAC genes (NAM, ATAF1/2, and CUC2) encode plant-specific transcription factors (TFs) and are one of the largest TF families in plants. NAC TFs are involved in multiple developmental processes, such as lateral root formation, phytohormone signaling, abiotic stress responses, and leaf senescence. Among NAC TFs, the activity of certain NAC TFs is post-translationally regulated by the C-terminal transmembrane domain (TMD). Under normal growth conditions, TMD-containing NAC TFs localize in the cytoplasm. Under unfavorable growth conditions, however, the cleavage of the TMD allows NAC TFs to translocate to the nucleus. In Arabidopsis, TMD containing NAC TFs have pivotal roles in the regulation of abiotic stress responses and leaf senescence.

Question: As described above, while the physiological roles of TMD-containing NAC TFs have been widely studied in Arabidopsis, those of rice TMD-containing NAC TFs are largely unknown.

Findings: We show that ONAC054, a rice TMD-containing NAC TF, is tightly associated with the regulation of ABA-induced leaf senescence. The onac054 knockout mutants maintained green leaves, while ONAC054-overexpressing plants showed an early leaf yellowing phenotype under dark- and ABA-induced senescence conditions. Like other TMD-containing NAC TFs reported previously, ONAC054 activity is regulated by the proteolytic processing of TMD. We found that nuclear import of ONAC054 requires cleavage of the putative C-terminal TMD caused in the presence of ABA. Furthermore, the ONAC054 transcript (termed ONAC054α) has an alternatively spliced form (ONAC054β), with seven nucleotides inserted between intron 5 and exon 6, truncating ONAC054α protein at a premature stop codon. ONAC054β lacks the TMD and thus localizes to the nucleus. These findings demonstrate that the activity of ONAC054, which is important for ABA-induced leaf senescence in rice, is precisely controlled by multilayered regulatory processes.

Next steps: Although we revealed that ONAC054 activates ABI5, an ABA signaling-associated gene, and NYC1, a senescence-associated gene, by directly binding to their promoters, other downstream genes of ONAC054 are yet to be identified. Thus, one interesting direction for future exploration is to identify other downstream target genes of ONAC054 to gain a further understanding of the role of ONAC054.

Yasuhito Sakuraba, Dami Kim, Su-Hyun Han, Suk-Hwan Kim, Weilan Piao, Shuichi Yanagisawa, Gynheung An, and Nam-Chon Paek. (2019). Multilayered regulation of membrane-bound ONAC054 is essential for abscisic acid-induced leaf senescence in rice. Plant Cell.

Key words: senescence, transcription factor, rice