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. 2018 Mar;176(3):2441-2455.
doi: 10.1104/pp.17.01525. Epub 2018 Jan 4.

The Deubiquitinase OTU5 Regulates Root Responses to Phosphate Starvation

Der-Fen Suen  1 , Yi-Hsiu Tsai  1 , Ya-Tan Cheng  1 , Ramalingam Radjacommare  2   3 , Ram Nivas Ahirwar  2   3 , Hongyong Fu  4   5 , Wolfgang Schmidt  4   5   6
Affiliations

The Deubiquitinase OTU5 Regulates Root Responses to Phosphate Starvation

Der-Fen Suen et al. Plant Physiol. 2018 Mar.

Abstract

Phosphorus, taken up by plants as inorganic phosphate (Pi), is an essential but often growth-limiting mineral nutrient for plants. As part of an orchestrated response to improve its acquisition, insufficient Pi supply triggers alterations in root architecture and epidermal cell morphogenesis. Arabidopsis (Arabidopsis thaliana) mutants defective in the expression of the OVARIAN TUMOR DOMAIN-CONTAINING DEUBIQUITINATING ENZYME5 (OTU5) exhibited a constitutive Pi deficiency root phenotype, comprising the formation of long and dense root hairs and attenuated primary root growth. Quantitative protein profiling of otu5 and wild-type roots using the isobaric tag for relative and absolute quantification methodology revealed genotype- and Pi-dependent alterations in protein profiles. In otu5 plants, Pi starvation caused a short-root-hair phenotype and decreased abundance of a suite of Pi-responsive root hair-related proteins. Mutant plants also showed the accumulation of proteins involved in chromatin remodeling and altered distribution of reactive oxygen species along the root, which may be causative for the alterations in root hair morphogenesis. The root hair phenotype of otu5 was synergistic to that of actin-related protein6 (arp6), harboring a mutation in the SWR1 chromatin-remodeling complex. Genetic analysis of otu5/arp6 double mutants suggests independent but functionally related roles of the two proteins in chromatin organization. The root hair phenotype of otu5 is not caused by a general up-regulation of the Pi starvation response, indicating that OTU5 acts downstream of or interacts with Pi signaling. It is concluded that OTU5 is involved in the interpretation of environmental information, probably by altering chromatin organization and maintaining redox homeostasis.

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Figures

Figure 1.
Figure 1.
Root phenotypes under Pi-replete conditions. A, Micrographs of the root hair zone. B, Root hair density. C, Root hair length. D, Primary root length, E, Lateral root number. Black lines in the box plots indicate the median, and red lines indicate the mean. The 5th/95th percentiles of outliers are shown. A minimum of 100 root hairs from five roots were measured for each genotype and growth type. Different letters show significant differences at P < 0.001 inferred from one-way ANOVA on ranks analysis followed by Dunn’s test. wt, Wild type.
Figure 2.
Figure 2.
Protein identification in roots of otu5 and the wild type (WT) under Pi-replete conditions. A, Venn diagram of the number of expressed proteins in three experimental runs (Bio1–Bio3). B, Distribution of protein abundance changes (iTRAQ counts) identified with false discovery rate (FDR) < 1%. C, Quantified differentially expressed proteins.
Figure 3.
Figure 3.
Protein identification in roots of otu5 and the wild type under Pi-deficient conditions. A and D, Venn diagrams of the number of expressed proteins in three experimental runs (Bio1–Bio3) in the wild type (A) and otu5 (D). B and E, Distribution of protein abundance changes (iTRAQ counts) identified with FDR < 1% in the wild type (B) and otu5 (E). C and F, Quantified differentially expressed proteins in the wild type (C) and otu5 plants (F).
Figure 4.
Figure 4.
Integrated PPI and coexpression network of chromatin-related proteins. Proteins with functions in chromatin remodeling that accumulated differentially between otu5 and wild-type plants were taken as bait to construct a network of interacting proteins and genes that are coexpressed with these proteins. The weight of the edges indicates the strength of the interactions. Yellow nodes indicate proteins with increased abundance, blue nodes denote proteins with decreased abundance, and purple nodes represent proteins that accumulate differentially under conditions of Pi deficiency. The smaller green nodes indicate genes that are coexpressed with these proteins. Letters in parentheses indicate the predominant location of the gene product: N, nucleus; C, cytoplasm. The network was constructed with GeneMANIA (http://genemania.org).
Figure 5.
Figure 5.
Root phenotypes under Pi-deficient conditions. A, Micrographs of the root hair zone. B, Root hair density. C, Root hair length. D, Primary root length. E, Lateral root number. Black lines in the box plots indicate the median, and red lines indicate the mean. The 5th/95th percentiles of outliers are shown. A minimum of 100 root hairs from five roots were measured for each genotype and growth type. Different letters show significant differences at P < 0.001 inferred from one-way ANOVA on ranks analysis followed by Dunn’s test. wt, Wild type.
Figure 6.
Figure 6.
Integrated PPI and coexpression network of proteins that were Pi responsive in otu5 but not in wild-type plants. Proteins that accumulated differentially between Pi-deficient and Pi-replete otu5 plants were taken as bait to construct a network of interacting proteins and genes that are coexpressed with these proteins (yellow nodes). Blue nodes indicate genes that are coexpressed with these proteins. The weight of the edges indicates the strength of the interactions. Numbers indicate induction level (n-fold) by Pi starvation. The network was constructed with GeneMANIA (http://genemania.org).
Figure 7.
Figure 7.
PPI network of root hair-related proteins with decreased abundance in otu5 plants. The first number indicates the otu5 low-Pi/wild-type low-Pi ratio of protein abundance, and the second number denotes the induction by Pi starvation in wild-type roots. Numbers in italics indicate nonsignificant changes. The weight of the edges indicates the strength of the interactions. The network was constructed with STRING (http://string-db.org).
Figure 8.
Figure 8.
Distribution of ROS along the roots. A and B, Roots stained with HPF for H2O2 in the meristem (A) and elongation zone (B). Plants were stained for 2 min in 0.1 m phosphate buffer (pH 6.1) containing 5 µm HPF. C, Quantification of HPF fluorescence intensity. D and E, Roots of 14-d-old Arabidopsis plants stained with NBT for superoxide in the meristem (D) and differentiation zone (E). Roots were stained for 25 min in 20 mm phosphate buffer (pH 6.1) containing 2 mm NBT and subsequently destained for 40 min. F, Quantification of NBT staining intensity. Error bars represent se; n = 20. Different letters indicate significant differences (P > 0.05) between samples as determined by two-way ANOVA and Tukey’s (NBT) or Fisher’s lsd (HPF) test. Bars = 100 µm; NBT differentiation zone = 200 µm.
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