SUB1A-1 anchors a regulatory cascade for epigenetic and transcriptional controls of submergence tolerance in rice

Abstract

Most rice (Oryza sativa) cultivars cannot survive under prolonged submergence. However, some O. sativa ssp. indica cultivars, such as FR13A, are highly tolerant owing to the SUBMERGENCE 1A-1 (SUB1A-1) allele, which encodes a Group VII ethylene-responsive factor (ERFVII) protein; other submergence-intolerant cultivars contain a SUB1A-2 allele. The two alleles differ only by a single substitution at the 186th amino acid position from serine in SUB1A-1 to proline in SUB1A-2 resulting in only SUB1A-1 being able to be phosphorylated. Two other ERFVIIs, ERF66 and ERF67, function downstream of SUB1A-1 to form a regulatory cascade in response to submergence stress. Here we show that SUB1A-1, but not SUB1A-2, interacts with ADA2b of the ADA2b-GCN5 acetyltransferase complex, in which GCN5 functions as a histone acetyltransferase. Phosphorylation of SUB1A-1 at serine 186 enhances the interaction of SUB1A-1 with ADA2b. ADA2b and GCN5 expression was induced under submergence, suggesting that these two genes might play roles in response to submergence stress. In transient assays, binding of SUB1A-1 to the ERF67 promoter and ERF67 transcription were highly induced when SUB1A-1 was expressed together with the ADA2b-GCN5 acetyltransferase complex. Taken together, these results suggest that phospho-SUB1A-1 recruits the ADA2-GCN5 acetyltransferase complex to modify the chromatin structure of the ERF66/ERF67 promoter regions and activate gene expression, which in turn enhances rice submergence tolerance.

Flooding Tolerance of Rice: Regulatory Pathways and Adaptive Mechanisms

“…Populations carrying SUB1A have two alleles, SUB1A-1 and SUB1A-2. The only difference between the two alleles is the presence of a proline residue at position 186 in SUB1A-2, instead of a serine residue in SUB1A-1 [15,17,19,58]. SUB1A-1 is specifically identified in submergence-tolerant cultivars, such as FR13A, and it can be strongly induced upon submergence to exert a determinant role in submergence stress responses, whereas the SUB1A-2 allele, which is only found in submergence-sensitive cultivars, such as IR29, is poorly induced during submergence [15,58].…”

“…SUB1A-1 also activates the transcription of other Group VII ERF transcription factors, such as ERF66 and ERF67, and enhances submergence tolerance by regulating various hypoxia-responsive genes [60]. Recently, one report showed that SUB1A-1 can interact with ADA2b (ALTER-ATION/DEFICIENCY IN AC-TIVATION 2) of the ADA2b-GCN5 (GENERAL CONTROL NON-REPRESSIBLE 5) acetyltransferase complex and recruits this complex to modify the chromatin structure of the ERF66/ERF67 promoter region and activate gene expression, which in turn enhances rice submergence tolerance [58]. In addition, the expression of DWARF1 (DWF1) and DWARF4 (DWF4), two key genes involved in the biosynthesis of brassinosteroids (BRs), is significantly higher in M202-Sub1 (tolerant variety) than in M202 (intolerant variety) during submergence, suggesting that SUB1A-1 can activate BR signaling.…”