PLATINUM SENSITIVE 2 LIKE Impacts Growth, Root Morphology, Seed Set, and Stress Responses

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2017 Jul 6

PMID 28678890

Citations 6

Authors

Amr R A Kataya

Maria T Creighton

Toga P Napitupulu

Christine Saetre

Behzad Heidari

Peter Ruoff

Cathrine Lillo

Affiliations

Soon will be listed here.

Abstract

Eukaryotic protein phosphatase 4 (PP4) is a PP2A-type protein phosphatase that is part of a conserved complex with regulatory factors PSY2 and PP4R2. Various lines of Arabidopsis thaliana with mutated PP4 subunit genes were constructed to study the so far completely unknown functions of PP4 in plants. Mutants with knocked out putative functional homolog of the PSY2 LIKE (PSY2L) gene were dwarf and bushy, while plants with knocked out PP4R2 LIKE (PP4R2L) looked very similar to WT. The psy2l seedlings had short roots with disorganized morphology and impaired meristem. Seedling growth was sensitive to the genotoxin cisplatin. Global transcript analysis (RNA-seq) of seedlings and rosette leaves revealed several groups of genes, shared between both types of tissues, strongly influenced by knocked out PSY2L. Receptor kinases, CRINKLY3 and WAG1, important for growth and development, were down-regulated 3-7 times. EUKARYOTIC ELONGATION FACTOR5A1 was down-regulated 4-6 fold. Analysis of hormone sensitive genes indicated that abscisic acid levels were high, while auxin, cytokinin and gibberellic acid levels were low in psy2l. Expression of specific transcription factors involved in regulation of anthocyanin synthesis were strongly elevated, e.g. the master regulator PAP1, and intriguingly TT8, which is otherwise mainly expressed in seeds. The psy2l mutants accumulated anthocyanins under conditions where WT did not, pointing to PSY2L as a possible upstream negative regulator of PAP1 and TT8. Expression of the sugar-phosphate transporter GPT2, important for cellular sugar and phosphate homeostasis, was enhanced 7-8 times. Several DNA damage response genes, including the cell cycle inhibitor gene WEE1, were up-regulated in psy2l. The activation of DNA repair signaling genes, in combination with phenotypic traits showing aberrant root meristem and sensitivity to the genotoxic cisplatin, substantiate the involvement of Arabidopsis PSY2L in maintenance of genome integrity.

Citing Articles

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References

Helps N, Brewis N, Lineruth K, Davis T, Kaiser K, Cohen P . Protein phosphatase 4 is an essential enzyme required for organisation of microtubules at centrosomes in Drosophila embryos. J Cell Sci. 1998; 111 ( Pt 10):1331-40. DOI: 10.1242/jcs.111.10.1331. View

Huang J, Xue L . Loss of flfl Triggers JNK-Dependent Cell Death in Drosophila. Biomed Res Int. 2015; 2015:623573. PMC: 4637051. DOI: 10.1155/2015/623573. View

Uhrig R, Labandera A, Moorhead G . Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci. 2013; 18(9):505-13. DOI: 10.1016/j.tplants.2013.05.004. View

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

Feyissa D, Lovdal T, Olsen K, Slimestad R, Lillo C . The endogenous GL3, but not EGL3, gene is necessary for anthocyanin accumulation as induced by nitrogen depletion in Arabidopsis rosette stage leaves. Planta. 2009; 230(4):747-54. DOI: 10.1007/s00425-009-0978-3. View

Del Pozo J, Allona I, Rubio V, Leyva A, de la Pena A, Aragoncillo C . A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J. 1999; 19(5):579-89. DOI: 10.1046/j.1365-313x.1999.00562.x. View

Winter D, Vinegar B, Nahal H, Ammar R, Wilson G, Provart N . An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One. 2007; 2(8):e718. PMC: 1934936. DOI: 10.1371/journal.pone.0000718. View

Alonso J, Stepanova A, Leisse T, Kim C, Chen H, Shinn P . Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003; 301(5633):653-7. DOI: 10.1126/science.1086391. View

Yoo S, Cho Y, Sheen J . Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc. 2007; 2(7):1565-72. DOI: 10.1038/nprot.2007.199. View

10.

Aarts M, Keijzer C, Stiekema W, Pereira A . Molecular characterization of the CER1 gene of arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell. 1995; 7(12):2115-27. PMC: 161066. DOI: 10.1105/tpc.7.12.2115. View

11.

Wolff S, Ma H, Burch D, Maciel G, Hunter T, Dillin A . SMK-1, an essential regulator of DAF-16-mediated longevity. Cell. 2006; 124(5):1039-53. DOI: 10.1016/j.cell.2005.12.042. View

12.

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

13.

Wu H, Brown J, Dorie M, Lazzeroni L, Brown J . Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res. 2004; 64(11):3940-8. DOI: 10.1158/0008-5472.CAN-03-3113. View

14.

Ren H, Gray W . SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth. Mol Plant. 2015; 8(8):1153-64. PMC: 5124491. DOI: 10.1016/j.molp.2015.05.003. View

15.

Schwab R, Palatnik J, Riester M, Schommer C, Schmid M, Weigel D . Specific effects of microRNAs on the plant transcriptome. Dev Cell. 2005; 8(4):517-27. DOI: 10.1016/j.devcel.2005.01.018. View

16.

Otero S, Desvoyes B, Peiro R, Gutierrez C . Histone H3 Dynamics Reveal Domains with Distinct Proliferation Potential in the Arabidopsis Root. Plant Cell. 2016; 28(6):1361-71. PMC: 4944401. DOI: 10.1105/tpc.15.01003. View

17.

Hincha D, Thalhammer A . LEA proteins: IDPs with versatile functions in cellular dehydration tolerance. Biochem Soc Trans. 2012; 40(5):1000-3. DOI: 10.1042/BST20120109. View

18.

Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D . A high-throughput Arabidopsis reverse genetics system. Plant Cell. 2002; 14(12):2985-94. PMC: 151197. DOI: 10.1105/tpc.004630. View

19.

Sheen J . Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol. 2001; 127(4):1466-75. PMC: 1540179. View

20.

Yuan D, Lai J, Xu P, Zhang S, Zhang J, Li C . AtMMS21 regulates DNA damage response and homologous recombination repair in Arabidopsis. DNA Repair (Amst). 2014; 21:140-7. DOI: 10.1016/j.dnarep.2014.04.006. View