Membralin is required for maize development and defines a branch of the endoplasmic reticulum–associated degradation pathway in plants

Author:

Liu Baiyu1ORCID,Xu Changzheng2ORCID,He Qiuxia3ORCID,Zhang Ke1ORCID,Qi Shoumei1ORCID,Jin Zhe1ORCID,Cheng Wen4ORCID,Ding Zhaohua4ORCID,Chen Donghua1ORCID,Zhao Xiangyu5ORCID,Zhang Wei1ORCID,Zhang Kewei1ORCID,Li Kunpeng1ORCID

Affiliation:

1. The Key Laboratory of Plant Development and Environment Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao 266237, China

2. School of Life Sciences, Southwest University, Chongqing 400715, China

3. Science and Technology Service Platform, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250103, China

4. Maize Institute of Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China

5. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, Shandong 271018, China

Abstract

Endoplasmic reticulum (ER)–associated degradation (ERAD) plays key roles in controlling protein levels and quality in eukaryotes. The Ring Finger Protein 185 (RNF185)/membralin ubiquitin ligase complex was recently identified as a branch in mammals and is essential for neuronal function, but its function in plant development is unknown. Here, we report the map-based cloning and characterization of Narrow Leaf and Dwarfism 1 ( NLD1 ), which encodes the ER membrane–localized protein membralin and specifically interacts with maize homologs of RNF185 and related components. The nld1 mutant shows defective leaf and root development due to reduced cell number. The defects of nld1 were largely restored by expressing membralin genes from Arabidopsis thaliana and mice, highlighting the conserved roles of membralin proteins in animals and plants. The excessive accumulation of β-hydroxy β-methylglutaryl-CoA reductase in nld1 indicates that the enzyme is a membralin-mediated ERAD target. The activation of bZIP60 mRNA splicing–related unfolded protein response signaling and marker gene expression in nld1 , as well as DNA fragment and cell viability assays, indicate that membralin deficiency induces ER stress and cell death in maize, thereby affecting organogenesis. Our findings uncover the conserved, indispensable role of the membralin-mediated branch of the ERAD pathway in plants. In addition, ZmNLD1 contributes to plant architecture in a dose-dependent manner, which can serve as a potential target for genetic engineering to shape ideal plant architecture, thereby enhancing high-density maize yields.

Funder

MOST | National Natural Science Foundation of China

Key R&D Program of Shandong Province, China

Shandong Zhongnong Tiantai Seeds Co., Ltd

Publisher

Proceedings of the National Academy of Sciences

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