Arabidopsis NUCLEOSTEMIN-LIKE 1 (NSN1) regulates cell cycling potentially by cooperating with nucleosome assembly protein AtNAP1;1

Zhen Wang,Qingchuan Yang,Bo Xie,Zonglie Hong,Xiaomin Wang

doi:10.1186/s12870-018-1289-2

Zhen Wang, Qingchuan Yang + Show 3 more

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https://doi.org/10.1186/s12870-018-1289-2

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Abstract

BackgroundIn mammals, nucleostemin (NS), a nucleolar GTPase, is involved in stem cell proliferation, embryogenesis and ribosome biogenesis. Arabidopsis NUCLEOSTEMIN-LIKE 1 (NSN1) has previously been shown to be essential for plant growth and development. However, the role of NSN1 in cell proliferation is largely unknown.ResultsUsing nsn1, a loss-of-function mutant of Arabidopsis NSN1, we investigated the function of NSN1 in plant cell proliferation and cell cycle regulation. Morphologically, nsn1 exhibited developmental defects in both leaves and roots, producing severely reduced vegetative organs with a much smaller number of cells than those in the wild type. Dynamic analysis of leaf and root growth revealed a lower cell proliferation rate and slower cell division in nsn1. Consistently, the transcriptional levels of key cell cycle genes, including those regulating the transition of G1-S and G2-M, were reduced drastically in nsn1. The introduction of CYCLIN B1::GUS into nsn1 resulted in confined expression of GUS in both the leaf primordia and root meristem, indicating that cell proliferation was hampered by the mutation of NSN1. Upon subjection to treatment with bleomycin and methyl methanesulfonate (MMS), nsn1 plants exhibited hypersensitivity to the genotoxic agents. In the nucleus, NSN1 interacted with nucleosome assembly protein1 (AtNAP1;1), a highly conserved histone chaperone functioning in cell proliferation. Notably, the N-terminal conserved domains of Arabidopsis NSN1 were critical for the physical interaction.ConclusionsAs a conserved homolog of mammalian nucleostemin, Arabidopsis NSN1 plays pivotal roles in embryogenesis and ribosome biogenesis. In this study, NSN1 was found to function as a positive regulator in cell cycle progression. The interaction between NSN1 and histone chaperone AtNAP1;1, and the high resemblance in sensitivity to genotoxics between nsn1 and atnap1;1 imply the indispensability of the two nuclear proteins for cell cycle regulation. This work provides an insight into the delicate control of cell proliferation through the cooperation of a GTP-binding protein with a nucleosome assembly/disassembly protein in Arabidopsis.

Highlights

In mammals, nucleostemin (NS), a nucleolar GTPase, is involved in stem cell proliferation, embryogenesis and ribosome biogenesis
This work provides an insight into the delicate control of cell proliferation through the cooperation of a GTP-binding protein with a nucleosome assembly/disassembly protein in Arabidopsis
Three biological replicates were performed with at least 15 plants measured for each experiment cotyledons of nsn1, a loss-of-function mutant of NUCLEOSTEMIN-LIKE 1 (NSN1), are initiated late at the embryo stage [15, 16], delayed emergence of the first leaf in nsn1 dwarf plant was observed (Fig. 1a) with the first leaf emerging at 9th day after germination (DAG), compared with the 5th DAG in the wild type plants (Table 1)

Summary

Introduction

Nucleostemin (NS), a nucleolar GTPase, is involved in stem cell proliferation, embryogenesis and ribosome biogenesis. NS contains an acidic amino acid (AAA) domain at the C-terminus, and a basic amino acid (BAA) domain and a coiled-coil (CC) domain at the Nterminus [1]. The latter two domains contribute predominantly to its biological functions as a nucleolar protein in cell cycle progression of both animals and plants [1, 7, 12,13,14]

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