Arabidopsis Seedling Lethal 1 Interacting With Plastid-Encoded RNA Polymerase Complex Proteins Is Essential for Chloroplast Development.

Deyuan Jiang,Yafei Shi,Renjie Tang,Sheng Luan,Yetao Wang,Xiangsheng Ke,Xin Hou,Yufen Che

doi:10.3389/fpls.2020.602782

Deyuan Jiang, Yafei Shi + Show 6 more

Open Access

https://doi.org/10.3389/fpls.2020.602782

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Abstract

Mitochondrial transcription termination factors (mTERFs) are highly conserved proteins in metazoans. Plants have many more mTERF proteins than animals. The functions and the underlying mechanisms of plants’ mTERFs remain largely unknown. In plants, mTERF family proteins are present in both mitochondria and plastids and are involved in gene expression in these organelles through different mechanisms. In this study, we screened Arabidopsis mutants with pigment-defective phenotypes and isolated a T-DNA insertion mutant exhibiting seedling-lethal and albino phenotypes [seedling lethal 1 (sl1)]. The SL1 gene encodes an mTERF protein localized in the chloroplast stroma. The sl1 mutant showed severe defects in chloroplast development, photosystem assembly, and the accumulation of photosynthetic proteins. Furthermore, the transcript levels of some plastid-encoded proteins were significantly reduced in the mutant, suggesting that SL1/mTERF3 may function in the chloroplast gene expression. Indeed, SL1/mTERF3 interacted with PAP12/PTAC7, PAP5/PTAC12, and PAP7/PTAC14 in the subgroup of DNA/RNA metabolism in the plastid-encoded RNA polymerase (PEP) complex. Taken together, the characterization of the plant chloroplast mTERF protein, SL1/mTERF3, that associated with PEP complex proteins provided new insights into RNA transcription in the chloroplast.

Highlights

Plant plastids contain their own genomes that evolved through endosymbiosis as a relic of their cyanobacterial origins
We provided evidence that SL1/mTERF3 interacts directly with the plastid-encoded RNA polymerase (PEP) complex (Figure 6), suggesting that SL1/mTERF3 is an important protein associated with PEP complex proteins that participate in chloroplast gene transcription
polymerase-associated proteins (PAPs) can be divided into four groups depending on their potential function: involvement in DNA/RNA metabolism (Group 1), finetuning of the redox regulation of chloroplast gene transcription (Group 2), protection of the PEP complex against reactive oxygen species (ROS) (Group 3), and unclear function (Group 4; Kindgren and Strand, 2015; Chang et al, 2017)

Summary

Introduction

Plant plastids contain their own genomes that evolved through endosymbiosis as a relic of their cyanobacterial origins. Proper expression and functioning of plastid-encoded genes are essential for plant growth and development (Pfannschmidt et al, 2015). Studies have revealed high coordination in the expression of chloroplast proteins encoded by the plastid and nuclear genomes, establishing a concept called genome-coupling (Zhao et al, 2020). Plastid genes are transcribed by two types of RNA polymerases: the single-subunit, nucleus-encoded plastid RNA polymerase (NEP), and the multi-subunit, plastid-encoded RNA polymerase (PEP; Pfalz and Pfannschmidt, 2013). NEP is responsible for the expression of house-keeping genes, such as RNA polymerase subunits (rpo) genes, as well as several genes that are involved in gene expression and other basic plastid functions. The rpo transcripts are translated into plastid ribosomes and assembled into PEP. PEP drives the mass production of photosynthesisrelated gene transcripts that are necessary for generating functional chloroplasts. Plastid genes can be divided into three classes whose transcription depends solely on PEP (Class I), PEP and NEP (Class II), or NEP alone (Class III; Yu et al, 2014)

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