The Arabidopsis Nucleoporin NUP1 is Essential for Megasporogenesis and Early Stages of Pollen Development

Overview

Journal Plant Cell Rep

Publisher Springer

Date 2018 Oct 21

PMID 30341574

Citations 8

Authors

Shuguang Bao

Guangshuang Shen

Guichen Li

Zhikang Liu

Muhammad Arif

Qingqing Wei

Shuzhen Men

Affiliations

Soon will be listed here.

Abstract

Loss-of-function of nucleoporin NUP1 in Arabidopsis causes defect in both male and female gametogenesis. Its ovules are arrested during meiosis, and its pollen grains are aborted at mitosis I. Nuclear pore complex (NPC) plays crucial roles in nucleocytoplasmic trafficking of proteins and RNAs. The NPC contains approximately 30 different proteins termed nucleoporins (NUPs). So far, only a few of plant NUPs have been characterized. The Arabidopsis NUP1 was identified as an ortholog of the yeast NUP1 and animal NUP153. Loss-of-function of NUP1 in Arabidopsis caused fertility defect; however, the molecular mechanism of this defect remains unknown. Here, we found that both male and female gametogenesis of the nup1 mutants were defective. nup1 ovules were arrested from the meiosis stage onward; only approximately 6.7% and 3% ovules of the nup1-1 and nup1-4 mutants developed up to the FG7 stage, respectively. Pollen development of the nup1 mutants was arrested during the first mitotic division. In addition, enlarged pollen grains with increased DNA content were observed in the nup1 mutant. RNA-sequencing showed that expression levels of genes involved in pollen development or regulation of cell size were reduced dramatically in nup1 compared with wild type. These results suggest that NUP1 plays an important role in gametogenesis.

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References

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

Johnson-Brousseau S, McCormick S . A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J. 2004; 39(5):761-75. DOI: 10.1111/j.1365-313X.2004.02147.x. View

Zhang Y, Li X . A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1. Plant Cell. 2005; 17(4):1306-16. PMC: 1088004. DOI: 10.1105/tpc.104.029926. View

Barow M . Endopolyploidy in seed plants. Bioessays. 2006; 28(3):271-81. DOI: 10.1002/bies.20371. View

Parry G, Ward S, Cernac A, Dharmasiri S, Estelle M . The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE proteins are nucleoporins with an important role in hormone signaling and development. Plant Cell. 2006; 18(7):1590-603. PMC: 1488926. DOI: 10.1105/tpc.106.041566. View

Dong C, Hu X, Tang W, Zheng X, Kim Y, Lee B . A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol. 2006; 26(24):9533-43. PMC: 1698518. DOI: 10.1128/MCB.01063-06. View

Galbraith D, Harkins K, Maddox J, Ayres N, Sharma D, Firoozabady E . Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science. 1983; 220(4601):1049-51. DOI: 10.1126/science.220.4601.1049. View

Harper N, Al-Greene N, Basrai M, Belanger K . Mutations affecting spindle pole body and mitotic exit network function are synthetically lethal with a deletion of the nucleoporin NUP1 in S. cerevisiae. Curr Genet. 2007; 53(2):95-105. PMC: 6296230. DOI: 10.1007/s00294-007-0168-4. View

Xu X, Meier I . The nuclear pore comes to the fore. Trends Plant Sci. 2007; 13(1):20-7. DOI: 10.1016/j.tplants.2007.12.001. View

10.

Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof Y . Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol. 2008; 10(2):237-44. DOI: 10.1038/ncb1686. View

11.

Meier I, Brkljacic J . The nuclear pore and plant development. Curr Opin Plant Biol. 2008; 12(1):87-95. DOI: 10.1016/j.pbi.2008.09.001. View

12.

Fiserova J, Kiseleva E, Goldberg M . Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. Plant J. 2009; 59(2):243-55. DOI: 10.1111/j.1365-313X.2009.03865.x. View

13.

Neumann N, Jeffares D, Poole A . Outsourcing the nucleus: nuclear pore complex genes are no longer encoded in nucleomorph genomes. Evol Bioinform Online. 2009; 2:23-34. PMC: 2674657. View

14.

Cheng Y, Germain H, Wiermer M, Bi D, Xu F, Garcia A . Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell. 2009; 21(8):2503-16. PMC: 2751965. DOI: 10.1105/tpc.108.064519. View

15.

Lu Q, Tang X, Tian G, Wang F, Liu K, Nguyen V . Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J. 2009; 61(2):259-70. DOI: 10.1111/j.1365-313X.2009.04048.x. View

16.

Lee H, Davidson J, Duronio R . Endoreplication: polyploidy with purpose. Genes Dev. 2009; 23(21):2461-77. PMC: 2779750. DOI: 10.1101/gad.1829209. View

17.

Du Z, Zhou X, Ling Y, Zhang Z, Su Z . agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010; 38(Web Server issue):W64-70. PMC: 2896167. DOI: 10.1093/nar/gkq310. View

18.

Dieppois G, Stutz F . Connecting the transcription site to the nuclear pore: a multi-tether process that regulates gene expression. J Cell Sci. 2010; 123(Pt 12):1989-99. DOI: 10.1242/jcs.053694. View

19.

Walde S, Kehlenbach R . The Part and the Whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol. 2010; 20(8):461-9. DOI: 10.1016/j.tcb.2010.05.001. View

20.

Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I . Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell. 2010; 22(12):4084-97. PMC: 3027183. DOI: 10.1105/tpc.110.079947. View