The paralogous SPX3 and SPX5 genes redundantly modulate Pi homeostasis in rice

Shi, Jing; Hu, Han; Zhang, Keming; Zhang, Wei; Yu, Yanan; Wu, Zhongchang; Wu, Ping

doi:10.1093/jxb/ert424

Cited by 82 publications

(81 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…While at a low cellular Pi concentration, SPX4 is degraded through the proteasome pathway, resulting in increased targeting of PHR2 to the nucleus and enhancing its PIBSbinding ability, which eventually leads to the up-regulation of PSI genes. Additionally, SPX3 and SPX5 were indicated to be repressors of PHR2, although the precise mechanism remains to be determined (33). We note that the induced transcript levels of PSI genes and the enrichment of PHR2 binding on the IPS1 promoter in spx1spx2 under +P conditions have not reached their induced levels under −P conditions in WT (Fig.…”

Section: Discussionmentioning

confidence: 85%

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

Wang

Ruan

Shi

et al. 2014

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

Self Cite

356

326

View full text Add to dashboard Cite

In plants, sensing the levels of external and internal nutrients is essential for reprogramming the transcriptome and adapting to the fluctuating environment. Phosphate (Pi) is a key plant nutrient, and a large proportion of Pi starvation-responsive genes are under the control of PHOSPHATE STARVATION RESPONSE REGULATOR 1 (PHR1) in Arabidopsis (AtPHR1) and its homologs, such as Oryza sativa (Os)PHR2 in rice. AtPHR1 and OsPHR2 expression is not very responsive to Pi starvation, raising the question as to how plants sense changes in cellular Pi levels to activate the central regulator. SPX [named after SYG1 (suppressor of yeast gpa1), Pho81 (CDK inhibitor in yeast PHO pathway), and XPR1 (xenotropic and polytropic retrovirus receptor)] proteins that harbor only the SPX domain are reported to be involved in the negative regulation of Pi starvation responses. Here, we show that the nuclear localized SPX proteins SPX1 and SPX2 are Pi-dependent inhibitors of the activity of OsPHR2 in rice. Indeed, SPX1 and SPX2 proteins interact with PHR2 through their SPX domain, inhibiting its binding to P1BS (the PHR1-binding sequence: GNATATNC). In vivo data, as well as results from in vitro experiments using purified SPX1, SPX2, and OsPHR2 proteins, showed that SPX1 and SPX2 inhibition of OsPHR2 activity is Pi-dependent. These data provide evidence to support the involvement of SPX1 and SPX2 in the Pi-sensing mechanism in plants.SPX-domain protein | PHR2 | Pi signaling | Pi-dependent inhibition P hosphorus (P) is an essential macroelement for plant growth and development. Because of high chemical fixation, slow diffusion, and substantial fractions of organic compounds by microorganisms, phosphate (Pi) limitation is usually a constraint for crop production in cultivated soils (1). However, intensive application of P fertilizer to increase agricultural production results in higher cost and environmental pollution and aggravates the shortage of nonrenewable resources worldwide for P fertilizer production (2). Therefore, improving effective Pi use by crops to reduce agricultural dependence on heavy Pi fertilizer application is an important challenge for sustainable agricultural production.The role of Arabidopsis PHOSPHATE STARVATION RESPONSE REGULATOR 1 (AtPHR1) and its orthologs as important regulators in Pi signaling and homeostasis through binding to the PHR1-binding sequence (P1BS) is well established in plants. AtPHR1 binds as a dimer to an imperfect palindromic sequence (GNATATNC), and this DNA-binding ability is dependent on the MYB and coiled-coil (CC) domains present in AtPHR1 and related proteins (3, 4). Orthologs of AtPHR1 have also been described in rice [Oryza sativa ( The SPX domain (Pfam PF03105) is named after the suppressor of yeast gpa1 (SYG1), the yeast cyclin-dependent kinase inhibitor (PHO81), and the human xenotropic and polytropic retrovirus receptor 1 (XPR1). In yeast (Saccharomyces cerevisiae), the SPX domain forms part of the competitive dual-transporter system that prolongs preparation for starvation and faci...

show abstract

Section: Discussionmentioning

confidence: 85%

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

Wang

Ruan

Shi

et al. 2014

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

Self Cite

356

326

View full text Add to dashboard Cite

show abstract

“…Additional evidence in support of this premise comes from a yeast 2-hybrid screen that identified ubiquitin conjugase protein 8 as an NLA-interacting protein, and bimolecular fluorescence complementation analysis revealed that these two proteins interacted specifically in nuclear speckles (Peng et al 2007a). Previous studies have shown also that there is an extensive transcriptome response in Arabidopsis that is triggered by nitrogen limitation and regulated by NLA (Peng et al 2007b), and given that other members of the plant SPX-domaincontaining protein family are known to function, at least in part, in the nucleus by interacting (via their SPX domains) with transcription factors that control the phosphate starvation pathway (Wang et al 2004b;Lv et al 2014;Shi et al 2014) Given the complex subcellular targeting of NLA, the aim of the current study was to conduct a detailed mutational assessment of the distinct functional/structural domains in NLA to determine their role(s) in the protein's function and/or subcellular localization. Each of the mutant proteins was assessed to determine its subcellular localization, as well as its ability to functionally complement the low-nitrogen phenotype of nla mutant plants.…”

Section: Mutants Harboring Disruptions In the Phosphate Transporter Tmentioning

confidence: 99%

Distinct domains within the NITROGEN LIMITATION ADAPTATION protein mediate its subcellular localization and function in the nitrate-dependent phosphate homeostasis pathway

Hannam

Gidda

Humbert

et al. 2018

Botany

View full text Add to dashboard Cite

The NITROGEN LIMITATION ADAPTATION (NLA) protein is a RING-type E3 ubiquitin ligase that plays an essential role in the regulation of nitrogen and phosphate homeostasis. NLA is localized to two different subcellular sites (the plasma membrane and the nucleus), and contains four distinct domains: (i) a RING domain that mediates degradation of phosphate transporters at the plasma membrane; (ii) an SPX domain that facilitates NLA’s interaction with the phosphate transporters, and also exists in other proteins that regulate the nuclear transcription factors that control the phosphate starvation response pathway; (iii) a linker domain that lies between the RING and SPX domains; and (iv) a C-terminal domain, which, like the linker region, is of unknown function. Here we carried out a mutational analysis of NLA, which indicated that all the domains are not only essential for proper functioning of the protein, but also mediate its localization to the plasma membrane and (or) nucleus, as well as to different subdomains within the nucleus. Overall, the results provide new insights to the distinct protein motifs within NLA and the role(s) that this protein serves at different subcellular sites with respect to the regulation of nitrogen-dependent phosphate homeostasis as well as other possible physiological functions.

show abstract

“…Wang et al, 2009;Liu et al, 2010). Recently, SPX3 and SPX5 were also demonstrated to be functional repressors of PHR2, although the precise mechanism remains to be determined (Shi et al, 2014).…”

Section: Spx4 Is a Key Component In The Regulation Of Phosphate Signamentioning

confidence: 99%

“…Wang et al, 2009). Although it has been genetically demonstrated that SPX1, SPX3, and SPX5 in rice are involved in the negative regulation of PHR2 (Liu et al, 2010;Shi et al, 2014), the mechanisms of the negative regulation and the different functions of these SPX proteins have not been discovered.…”

Section: Introductionmentioning

confidence: 99%

SPX4 Negatively Regulates Phosphate Signaling and Homeostasis through Its Interaction with PHR2 in Rice

et al. 2014

Self Cite

View full text Add to dashboard Cite

PHR2, a central regulator of phosphate signaling in rice, enhanced the expression of phosphate starvation-induced (PSI) genes and resulted in the enhancement of Pi acquisition under Pi deficiency stress. This occurred via PHR2 binding to a cis-element named the PHR1 binding sequences. However, the transcription level of PHR2 was not responsive to Pi starvation. So how is activity of transcription factor PHR2 adjusted to adapt diverse Pi status? Here, we identify an SPX family protein, Os-SPX4 (SPX4 hereafter), involving in Pi starvation signaling and acting as a negative regulator of PHR2. SPX4 is shown to be a fast turnover protein. When Pi is sufficient, through its interaction with PHR2, SPX4 inhibits the binding of PHR2 to its cis-element and reduces the targeting of PHR2 to the nucleus. However, when plants grow under Pi deficiency, the degradation of SPX4 is accelerated through the 26S proteasome pathway, thereby releasing PHR2 into the nucleus and activating the expression of PSI genes. Because the level of SPX4 is responsive to Pi concentration and SPX4 interacts with PHR2 and regulates its activity, this suggests that SPX4 senses the internal Pi concentration under diverse Pi conditions and regulates appropriate responses to maintain Pi homeostasis in plants.

show abstract

The paralogous SPX3 and SPX5 genes redundantly modulate Pi homeostasis in rice

Cited by 82 publications

References 38 publications

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

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

Distinct domains within the NITROGEN LIMITATION ADAPTATION protein mediate its subcellular localization and function in the nitrate-dependent phosphate homeostasis pathway

SPX4 Negatively Regulates Phosphate Signaling and Homeostasis through Its Interaction with PHR2 in Rice

Contact Info

Product

Resources

About