Mutation in a putative glycosyltransferase-like gene causes programmed cell death and early leaf senescence in rice

Shanwen Ke,Xin-Ming Xie,Xin Luan,Tzung-Fu Hsieh,Xiang-Qian Zhang,Shuchun Liu

doi:10.1186/s12284-019-0266-1

Abstract

Leaf senescence is a genetically regulated, highly complex and ordered process. Although it has been extensively studied, the mechanism of leaf senescence is not well understood. In this study, we isolated a rice mutant, designated as premature senescence leaf (psl), which exhibits early senescence and spontaneous lesion mimic phenotype after flowering. The psl mutant displays programmed cell death with elevated accumulation of reactive oxygen species (ROS). Molecular and genetic analyses revealed that the phenotypes were caused by a phenylalanine deletion in the OsPSL (LOC_Os12g42420) that encode a putative core 2/I branching beta-1,6-N-acetylglucosaminyl transferase predicted to be involved in protein glycosylation modification. OsPSL mRNA levels increased as senescence progressed, with maximum accumulation of transcripts at late senescence stages in WT plants. Moreover, remarkedly down-regulated transcriptional levels of O-linked N-acetylglucosamine (O-GlcNAc) transferases (OGTs) genes were observed in psl mutant, supporting the occurrence of impaired O-glycosylation modification. Proteomic analysis showed that ethylene-related metabolic enzymes including S-adenosyl methionine (SAM) synthetase (SAMS) were significantly upregulated in the psl mutant compared with WT. Consistent with the proteomic results, ethylene concentration is higher in psl mutant than in wild-type plants, and transcript levels of ethylene synthesis and signal transduction genes were induced in psl mutant. The early leaf senescence of psl can be partially rescued by ethylene biosynthesis inhibitor aminoethoxyvinylglycine treatment. These results highlight the importance of protein O-glycosylation in PCD and leaf senescence, and suggest a possible role of OsPSL in ethylene signaling.

Highlights

Leaf senescence is a highly complex and programmed process and involves a series of cytological and biochemical changes
For core1-core4 mucin-type O-glycans, the carbohydrate chain is initiated with an N-acetylgalactosamine (GalNAc) residue linked to Ser or Thr
Unlike the yellowing of leaves due to naturally senescence, small yellow lesions appeared on the leaves of psl mutant plants, whereas the leaves of wild-type plants at the same stage exhibited no such abnormal symptoms (Fig. 1b)

Summary

Introduction

Leaf senescence is a highly complex and programmed process and involves a series of cytological and biochemical changes. The onset of leaf senescence depends on developmental programs and environmental signals; i.e., it occurs in an age-dependent manner. For core1-core mucin-type O-glycans, the carbohydrate chain is initiated with an N-acetylgalactosamine (GalNAc) residue linked to Ser or Thr. For example, core mucin-type of O-glycosylation starts with the addition of a GalNAc residue onto the hydroxyl groups of Ser or Thr. Core 2 β-1,6-N-acetylglucosaminyltransferase-1 (C2GNT) catalyzes the transfer of N-acetylglucosamine from uridine diphosphate-N-acetylglucosamine with a β1,6-linkage to α-N-acetylgalactosamine of a core 1 O-glycan (Kojima et al, 2015). O-GlcNAcylated proteins consist of a single O-linked N-acetylglucosamine on serine and threonine residues belong to core mucin-type glycosylated protein (Xu et al, 2017)

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Results

Discussion

Conclusion