Soybean SPX1 is an important component of the response to phosphate deficiency for phosphorus homeostasis

doi:10.1016/j.plantsci.2016.04.010

Plant Science

Volume 248, July 2016, Pages 82-91

https://doi.org/10.1016/j.plantsci.2016.04.010 Get rights and content

Highlights

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GmSPX1 could negative controls transcription of Pi starvation responsive genes indirectly.
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The elongation and number of root hairs was suppressed by overexpression of GmSPX1.
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The yeast two-hybrid assays and BiFC assays demonstrated that GmSPX1 could interact with GmMYB48.
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GmMYB48 is a new phosphate starvation induced transcription factor, and the interaction of GmSPX1/GmMYB48 can be considered a potential candidate suppressor.

Abstract

Phosphate (Pi) homeostasis is required for plant growth and development, but the Pi-signaling pathways in plants still remain largely unknown. Proteins only containing the SPX domain are very important in phosphate (Pi) homeostasis and signaling transduction. In the T-DNA insertion Arabidopsis mutant spx3, AtPHT1-4, AtPHT1-5, AtACP5, AtRNS, and AtAT4 expression levels were increased under Pi-sufficient condition and low Pi condition compared with WT. Meanwhile, the expression levels of these phosphate starvation genes was inhibited in OXSPX1 and spx3/OXSPX1 compared with WT, only under Pi-sufficient condition. These imply that GmSPX1 may negatively control the transcription of Pi starvation responsive genes indirectly. However, there were no differences between expression levels of these PSI genes in spx3 and those in WT under −Pi conditions. These facts imply that the negative regulation of GmSPX1 and AtSPX3 on PSI genes is depending on Pi concentration. Consistent with this, GmSPX1 overexpression in the WT and spx3 decreased the total Pi concentration in plants and changed root hair morphology, suppressing the elongation and number of root hairs compared with the WT and spx3. The yeast two-hybrid assays and BiFC assays demonstrated that GmSPX1 could interact with GmMYB48.The qRT-PCR analysis showed that GmMYB48 is a new phosphate starvation induced transcription factor in soybean. Also, GmSPX1 overexpression led to decreased transcripts of AtMYB4, an ortholog of GmMYB48, in OXSPX1. Together, these results suggest that GmSPX1 is a negative regulator in the Pi signaling network of soybean, and the interaction of GmSPX1/GmMYB48 can be considered a potential candidate suppressor.

Introduction

As a major constituent of plant cell components, including nucleic acids, membranes and ATP, phosphorus (P) is a macronutrient and plays a crucial role in energy transformation and protein activation. Although P is abundant in many soils, most of the P in the soil is converted to organic compounds or becomes insoluble [1], [2], [3]. As a result, very little P is present in ionic forms that are available to plants. Intensive application of chemical fertilizers containing phosphate (Pi) has therefore become a standard agricultural practice to ensure crop productivity [4]. To cope with low nutritional Pi availability, plants have developed a wide spectrum of mechanisms to improve Pi-use efficiency, such as altered morphology, physiology, and biochemical processes [5], [6].

At the molecular level, our knowledge of the plant response to Pi starvation has greatly improved with the identification of several key players involved in Pi signaling, which have been well reviewed in recent years [4], [7], [8], [9]. Using forward and reverse genetics, several important transcription factors in Pi signaling pathways have been identified, including MYB, WRKY, and bHLH family members [10], [11], [12], [13]. MYB transcription factors are defined by a highly conserved MYB DNA-binding domain at the N-terminus, and constitute one of the largest transcription factor (TF) families in the plant kingdom [14]. Among MYB TFs, PHR1, MYB62, MYB2 and MYB82 have already been confirmed to be involved in phosphate starvation responses [10], [13], [15], [16]. PHR1, a R2R3-MYB protein, is the central integrator in the transcriptional regulation of phosphate starvation responses [15]. PHR1 plays a crucial role in regulating genes involved in Pi transport and remobilization, anthocyanin biosynthesis, carbohydrate metabolism, and root system architecture (RSA) [15], [17], [18], [19]. Recent studies have shown that OsSPX1, OsSPX2 and OsSPX4 can interact with OsPHR2 and inhibit its binding activity with the cis-element P1BS. The SPX/PHR2 interaction is highly Pi-dependent in planta [20], [21]. A similar interaction, SPX1/PHR1, was also confirmed in Arabidopsis and could negatively regulate Pi signaling [22].

Proteins containing the SPX domain are key players controlling a set of processes involved in maintaining an internal steady state of phosphate ions at the cell level, defined as Pi homeostasis [23], [24], [25]. The SPX domain is named after the yeast SYG1 and Pho81 proteins and human XPR1 protein, which contain a conserved domain in their N-terminal peptides [26], [27], [28], [29]. In plants, SPX-domain-containing proteins can be divided into four families based on the presence of additional domains in their structure, SPX-EXS, SPX-MFS, SPX-RING and SPX, among which only those containing the SPX domain are referred to as SPX proteins [30], [31], [32], [33], [34], [35]. Four members of the SPX family have been found in Arabidopsis, named AtSPX1, AtSPX2, AtSPX3, and AtSPX4. AtSPX1 is a positive regulator of some phosphate-starvation-inducible (PSI) genes while AtSPX3 plays a negative role. Repression of AtSPX3 by RNA interference led to aggravated Pi-deficiency symptoms, altered P allocation and enhanced expression of a subset of phosphate-responsive genes including AtSPX1 [23]. However, according to the newest publication, AtSPX1 could inhibit AtPHR1 activity through interaction and then act as negative regulator of some phosphate starvation induced (PSI) genes. Similarly, there are six members of the SPX family in rice, named OsSPX1, OsSPX2, OsSPX3, OsSPX4, OsSPX5 and OsSPX6 [25], [36], [37].

In this paper, we cloned the full-length cDNA of GmSPX1. Subsequently, analysis of GmSPX1’s function showed that it is a negative regulator in the feedback network of Pi signaling. The results of further experimental studies suggested that GmSPX1 might be involved in phosphate starvation responses through interaction with GmMYB48.

Section snippets

Phylogenetic and gene structure analysis

SPX sequences from Arabidopsis (Arabidopsis thaliana (L.)) and soybean were identified through a BLAST search of The Arabidopsis Information Resource (TAIR, http://www.Arabidopsis.org) and National Center for Biotechnology Information (NCBI, http://www.ncbi.nlm.nih.gov/) databases, using AtSPX genes as queries [23]. Multiple alignments were prepared using ClustalX 2.0.11. Neighbor-joining phylogenetic trees were generated using the MEGA 5.1 program.

Plant material and growth conditions

Seeds of soybean genotype Williams 82 were

Structure and homology characterization of SPX domain genes

Based on their sequence homology to Arabidopsis SPX, 10 GmSPX genes were identified from the soybean genome (NCBI, http://www.ncbi.nlm.nih.gov and Phytozome 9.1, http://www.phytozome.net). Of the 10 genes, 9 had been described in a previous report and named GmSPX1–9 [44]. Therefore, we named the tenth GmSPX gene GmSPX10 (Glyma03g03820). Phylogenetic analysis demonstrated that the GmSPX family could be classified into three groups, and group I could be further subdivided into two subgroups as

Discussion

SPX proteins are highly homologous to each other in structure and sequence in plants. In recent years, the role and importance of the SPX gene family in the regulation of Pi homeostasis has become increasingly clear. Four SPX proteins in Arabidopsis and six in rice have been identified, named AtSPX1–AtSPX4 and OsSPX1–OsSPX6 [23], [37]. In legumes, there have been nine genes reported in soybean [44] and three in common bean [49]. In this report, a 10th SPX family gene was found in soybean, named

Acknowledgements

This work was supported by the National Transgene Science and Technology Major Program of China (2011ZX08004-005, 2013ZX08004-005, 2014ZX08004-005), the National Hightech R & D Program of China (2011AA10A105), the National Key Basic Research Program of China (2011CB109301), and the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT13073), and Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP). We thank Shanghai OE Biotech Company

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Similarly to the components of the local Pi-sensing mechanism, at least one ortholog for each main component of the systemic Pi-sensing mechanism was found, including orthologs for PHR1 in all species analyzed and at least two SPX and two PHL representants. Members of SPX families have been studied to a significant degree in Arabidopsis (Duan et al., 2008; Puga et al., 2014) and in rice (Lv et al., 2014; Zhong et al., 2018), and relatively well documented in soybean (Xue et al., 2018; Yao et al., 2014b; Zhang et al., 2016) and in common bean (Phaseolus vulgaris L.; Yao et al., 2014a). The evolutionary aspects of the SPX family in plants, as well as its specific role in responses to phosphorus stress, have been recently explored (see Liu et al., 2018).
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Soybean SPX1 is an important component of the response to phosphate deficiency for phosphorus homeostasis

Highlights

Abstract

Introduction

Section snippets

Phylogenetic and gene structure analysis

Plant material and growth conditions

Structure and homology characterization of SPX domain genes

Discussion

Acknowledgements

Trends Plant Sci.

Biochim. Biophys. Acta

Mol. Plant

Trends Biochem. Sci.

J. Biol. Chem.

J. Mol. Biol.

Biochim. Biophys. Acta

Curr. Opin. Plant Biol.

Mol. Plant

Trends Plant Sci.

Phosphorus in the global environment

Mineral nutrition of higher plants

Plant Cell Environ.

Phosphate acquisition

Annu. Rev. Plant Biol.

Signaling network in sensing phosphate availability in plants

Annu. Rev. Plant Biol.

Molecular and biochemical mechanisms of phosphorus uptake into plants

J. Plant Nutrit. Soil Sci.

Phosphate acquisition

Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation

Physiol. Plant.

Regulation of phosphate starvation responses in plants: signaling players and cross-talks

Mol. Plant

Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis

Plant Physiol.

BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis

Biochem. J.

MYB82 functions in regulation of trichome development in Arabidopsis

J. Exp. Bot.

One billion years of Myb

Oncogene

A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis

PLoS Genet.

Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis

Plant J.

Phospholi-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana

Plant Cell Environ.

A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae

Genes Dev.

SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice

Plant Cell

Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner

Proc. Natl. Acad. Sci. U.S.A.

SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis

Proc. Natl. Acad. Sci. U.S.A.