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

Shi J, Hu H, Zhang K, Zhang W, Yu Y, Wu Z, Wu P - J. Exp. Bot. (2013)

Bottom Line: In vitro and in vivo protein-protein interaction analyses indicated that these two proteins can form homodimers and heterodimers, also implying their functional redundancy.Genetic interaction analysis indicated that SPX3/5 are functional repressors of OsPHR2 (PHR2), the rice orthologue of the central regulator AtPHR1 for Pi homeostasis and Pi signalling.These results suggest that the evolution of the additional redundant paralogous SPX genes is beneficial to plants recovering Pi homeostasis after Pi starvation by PHR2 pathway.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou 310058, China.

ABSTRACT
The importance of SPX-domain-containing proteins to phosphate (Pi) homeostasis and signalling transduction has been established in plants. In this study, phylogenetic analysis revealed that OsSPX3 and OsSPX5 (SPX3/5) are paralogous SPX genes ( SYG1/Pho81/XPR1) in cereal crops. SPX3/5 are specifically responsive to Pi starvation at both the transcriptional and post-transcriptional levels. Similar tissue expression patterns of the two genes and proteins were identified by in situ hybridization and the transgenic plants harbouring SPX3pro-SPX3-GUS or SPX5pro-SPX5-GUS fusions, respectively. Both SPX3/5 are localized in the nucleus and cytoplasm in rice protoplasts and plants. SPX3/5 negatively regulate root-to-shoot Pi translocation with redundant function. The data showed that the Pi-starvation-accumulated SPX3/5 proteins are players in restoring phosphate balance following phosphate starvation. In vitro and in vivo protein-protein interaction analyses indicated that these two proteins can form homodimers and heterodimers, also implying their functional redundancy. Genetic interaction analysis indicated that SPX3/5 are functional repressors of OsPHR2 (PHR2), the rice orthologue of the central regulator AtPHR1 for Pi homeostasis and Pi signalling. These results suggest that the evolution of the additional redundant paralogous SPX genes is beneficial to plants recovering Pi homeostasis after Pi starvation by PHR2 pathway.

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Expression patterns of SPX3/5 in roots and leaf blades indicated by in situ hybridization. (A–F) In situ hybridization on cross-sections of primary roots with SPX3 or SPX5 antisense probes (B and E); negative control with sense probes (A and D); and detailed antisense signals (C and F). (G–L) In situ hybridization on cross-sections of leaf blades with SPX3 or SPX5 antisense probes (H and K); negative control with sense probes (G and J); and detailed antisense (I and L). Roots and leaves were sampled from 20-d-old seedlings treated with Pi starvation for 7 d. Ab, abaxial; Ad, adaxial; Co, cortex; Ep, epidermis; Ex, exodermis; Mes, mesophyll; Mtx, metaxylem; Ph, phloem; Sc, sclerenchyma layer; St, stele; Xy, xylem. Bars, 100 µm.
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Figure 2: Expression patterns of SPX3/5 in roots and leaf blades indicated by in situ hybridization. (A–F) In situ hybridization on cross-sections of primary roots with SPX3 or SPX5 antisense probes (B and E); negative control with sense probes (A and D); and detailed antisense signals (C and F). (G–L) In situ hybridization on cross-sections of leaf blades with SPX3 or SPX5 antisense probes (H and K); negative control with sense probes (G and J); and detailed antisense (I and L). Roots and leaves were sampled from 20-d-old seedlings treated with Pi starvation for 7 d. Ab, abaxial; Ad, adaxial; Co, cortex; Ep, epidermis; Ex, exodermis; Mes, mesophyll; Mtx, metaxylem; Ph, phloem; Sc, sclerenchyma layer; St, stele; Xy, xylem. Bars, 100 µm.

Mentions: The tissue expression patterns of SPX3/5 were investigated using in situ hybridization with probes specific to SPX3 or SPX5 (Supplementary Table S1). The roots of 15-d-old plants treated with Pi starvation for 7 d had an overlapped hybridization signal of SPX3/5 in root epidermis, exodermis, and the sclerenchymal layer. The hybridization signal was also detected for SPX3 in cortex and endosperm (Fig. 2A–F). Under Pi starvation, the specific hybridization signals of SPX3/5 were present in mesophyll and phloem in the vascular bundles (Fig. 2G–L). The signal was highly specific and did not appear in leaf and root tissues when using control sense probes.


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

Shi J, Hu H, Zhang K, Zhang W, Yu Y, Wu Z, Wu P - J. Exp. Bot. (2013)

Expression patterns of SPX3/5 in roots and leaf blades indicated by in situ hybridization. (A–F) In situ hybridization on cross-sections of primary roots with SPX3 or SPX5 antisense probes (B and E); negative control with sense probes (A and D); and detailed antisense signals (C and F). (G–L) In situ hybridization on cross-sections of leaf blades with SPX3 or SPX5 antisense probes (H and K); negative control with sense probes (G and J); and detailed antisense (I and L). Roots and leaves were sampled from 20-d-old seedlings treated with Pi starvation for 7 d. Ab, abaxial; Ad, adaxial; Co, cortex; Ep, epidermis; Ex, exodermis; Mes, mesophyll; Mtx, metaxylem; Ph, phloem; Sc, sclerenchyma layer; St, stele; Xy, xylem. Bars, 100 µm.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3924727&req=5

Figure 2: Expression patterns of SPX3/5 in roots and leaf blades indicated by in situ hybridization. (A–F) In situ hybridization on cross-sections of primary roots with SPX3 or SPX5 antisense probes (B and E); negative control with sense probes (A and D); and detailed antisense signals (C and F). (G–L) In situ hybridization on cross-sections of leaf blades with SPX3 or SPX5 antisense probes (H and K); negative control with sense probes (G and J); and detailed antisense (I and L). Roots and leaves were sampled from 20-d-old seedlings treated with Pi starvation for 7 d. Ab, abaxial; Ad, adaxial; Co, cortex; Ep, epidermis; Ex, exodermis; Mes, mesophyll; Mtx, metaxylem; Ph, phloem; Sc, sclerenchyma layer; St, stele; Xy, xylem. Bars, 100 µm.
Mentions: The tissue expression patterns of SPX3/5 were investigated using in situ hybridization with probes specific to SPX3 or SPX5 (Supplementary Table S1). The roots of 15-d-old plants treated with Pi starvation for 7 d had an overlapped hybridization signal of SPX3/5 in root epidermis, exodermis, and the sclerenchymal layer. The hybridization signal was also detected for SPX3 in cortex and endosperm (Fig. 2A–F). Under Pi starvation, the specific hybridization signals of SPX3/5 were present in mesophyll and phloem in the vascular bundles (Fig. 2G–L). The signal was highly specific and did not appear in leaf and root tissues when using control sense probes.

Bottom Line: In vitro and in vivo protein-protein interaction analyses indicated that these two proteins can form homodimers and heterodimers, also implying their functional redundancy.Genetic interaction analysis indicated that SPX3/5 are functional repressors of OsPHR2 (PHR2), the rice orthologue of the central regulator AtPHR1 for Pi homeostasis and Pi signalling.These results suggest that the evolution of the additional redundant paralogous SPX genes is beneficial to plants recovering Pi homeostasis after Pi starvation by PHR2 pathway.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou 310058, China.

ABSTRACT
The importance of SPX-domain-containing proteins to phosphate (Pi) homeostasis and signalling transduction has been established in plants. In this study, phylogenetic analysis revealed that OsSPX3 and OsSPX5 (SPX3/5) are paralogous SPX genes ( SYG1/Pho81/XPR1) in cereal crops. SPX3/5 are specifically responsive to Pi starvation at both the transcriptional and post-transcriptional levels. Similar tissue expression patterns of the two genes and proteins were identified by in situ hybridization and the transgenic plants harbouring SPX3pro-SPX3-GUS or SPX5pro-SPX5-GUS fusions, respectively. Both SPX3/5 are localized in the nucleus and cytoplasm in rice protoplasts and plants. SPX3/5 negatively regulate root-to-shoot Pi translocation with redundant function. The data showed that the Pi-starvation-accumulated SPX3/5 proteins are players in restoring phosphate balance following phosphate starvation. In vitro and in vivo protein-protein interaction analyses indicated that these two proteins can form homodimers and heterodimers, also implying their functional redundancy. Genetic interaction analysis indicated that SPX3/5 are functional repressors of OsPHR2 (PHR2), the rice orthologue of the central regulator AtPHR1 for Pi homeostasis and Pi signalling. These results suggest that the evolution of the additional redundant paralogous SPX genes is beneficial to plants recovering Pi homeostasis after Pi starvation by PHR2 pathway.

Show MeSH