SPX4 Acts on PHR1-Dependent and -Independent Regulation of Shoot Phosphorus Status in Arabidopsis

Marina Borges Osorio, Sophia Ng, Oliver Berkowitz, Inge De Clercq, Chuanzao Mao, Huixia Shou, James Whelan, Ricarda Jost

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Phosphorus (P) is an essential macronutrient for all living organisms and limits plant growth. Four proteins comprising a single SYG1/Pho81/XPR1 (SPX) domain, SPX1 to SPX4, are putative phosphate-dependent inhibitors of Arabidopsis (Arabidopsis thaliana) PHOSPHATE STARVATION RESPONSE1 (PHR1), the master transcriptional activator of phosphate starvation responses. This work demonstrated that SPX4 functions as a negative regulator not only of PHR1-dependent but also of PHR1-independent responses in P-replete plants. Transcriptomes of P-limited spx4 revealed that, unlike SPX1 and SPX2, SPX4 modulates the shoot phosphate starvation response but not short-term recovery after phosphate resupply. In roots, transcriptional regulation of P status is SPX4 independent. Genes misregulated in spx4 shoots intersect with both PHR1-dependent and PHOSPHATE2-dependent signaling networks associated with plant development, senescence, and ion/metabolite transport. Gene regulatory network analyses suggested that SPX4 interacts with transcription factors other than PHR1, such as SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 and ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN55, known regulators of shoot development. Transient expression studies in protoplasts indicated that PHR1 retention in the cytosol by SPX4 occurs in a dose- and P-status-dependent manner. Using a luciferase reporter in vivo, SPX4 expression kinetics and stability revealed that SPX4 is a short-lived protein with P-status-dependent turnover. SPX4 protein levels were quickly restored by phosphate resupply to P-limited plants. Unlike its monocot ortholog, AtSPX4 was not stabilized by the phosphate analog phosphite, implying that intracellular P status is sensed by its SPX domain via phosphate-rich metabolite signals.

Original languageEnglish
Pages (from-to)332-352
Number of pages21
JournalPlant Physiology
Volume181
Issue number1
DOIs
Publication statusPublished - 1 Sep 2019

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Starvation
Arabidopsis
Phosphorus
starvation
Phosphates
phosphates
phosphorus
shoots
metabolites
Phosphites
Proteins
Plant Development
proteins
Protoplasts
Gene Regulatory Networks
Ion Transport
luciferase
Liliopsida
Luciferases
Transcriptome

Cite this

Osorio, M. B., Ng, S., Berkowitz, O., De Clercq, I., Mao, C., Shou, H., ... Jost, R. (2019). SPX4 Acts on PHR1-Dependent and -Independent Regulation of Shoot Phosphorus Status in Arabidopsis. Plant Physiology, 181(1), 332-352. https://doi.org/10.1104/pp.18.00594
Osorio, Marina Borges ; Ng, Sophia ; Berkowitz, Oliver ; De Clercq, Inge ; Mao, Chuanzao ; Shou, Huixia ; Whelan, James ; Jost, Ricarda. / SPX4 Acts on PHR1-Dependent and -Independent Regulation of Shoot Phosphorus Status in Arabidopsis. In: Plant Physiology. 2019 ; Vol. 181, No. 1. pp. 332-352.
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Osorio, MB, Ng, S, Berkowitz, O, De Clercq, I, Mao, C, Shou, H, Whelan, J & Jost, R 2019, 'SPX4 Acts on PHR1-Dependent and -Independent Regulation of Shoot Phosphorus Status in Arabidopsis' Plant Physiology, vol. 181, no. 1, pp. 332-352. https://doi.org/10.1104/pp.18.00594

SPX4 Acts on PHR1-Dependent and -Independent Regulation of Shoot Phosphorus Status in Arabidopsis. / Osorio, Marina Borges; Ng, Sophia; Berkowitz, Oliver; De Clercq, Inge; Mao, Chuanzao; Shou, Huixia; Whelan, James; Jost, Ricarda.

In: Plant Physiology, Vol. 181, No. 1, 01.09.2019, p. 332-352.

Research output: Contribution to journalArticle

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AU - Osorio, Marina Borges

AU - Ng, Sophia

AU - Berkowitz, Oliver

AU - De Clercq, Inge

AU - Mao, Chuanzao

AU - Shou, Huixia

AU - Whelan, James

AU - Jost, Ricarda

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