Functional characterization of the rice SPX-MFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves

New Phytologist

Volumn 196, Issue 1, 2012, Pages 139-148

  Wang, Chuang ^a   Huang, Wei ^a   Ying, Yinghui ^a   Li, Shuai ^a   Secco, David ^a,b   Tyerman, Steve ^c   Whelan, James ^a,b   Shou, Huixia ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Homeostasis; MiRNA; OsPHR2; Phosphate; Rice; SPX; Transporter

Indexed keywords

BETA GLUCURONIDASE; MICRORNA; PHOSPHATE; VEGETABLE PROTEIN;

FUNCTIONAL CHANGE; GENE EXPRESSION; HOMEOSTASIS; LEAF; MUTATION; RICE; SIGNAL; YEAST;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; MUTATION; PLANT GENE; PLANT LEAF; PLANT ROOT; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; RICE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; GLUCURONIDASE; HOMEOSTASIS; MICRORNAS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; ORYZA SATIVA; PHOSPHATES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

OSA;

EID: 84865569878     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04227.x     Document Type: Article

References (49)

1. Abramson J, Kaback HR, Iwata S. 2004. Structural comparison of lactose permease and the glycerol-3-phosphate antiporter: members of the major facilitator superfamily. Current Opinion Structure Biology 14: 413-419.
2. Bari R, Datt Pant B, Stitt M, Scheible WR. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141: 988-999.
3. Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Perez-Perez J, Solano R, Leyva A, Paz-Ares J. 2010. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genetics 6: 9.
4. Chen Y-F, Li L-Q, Xu Q, Kong Y-H, Wang H, Wu W-H. 2009. The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21: 3554-3566.
5. Chen ZH, Nimmo GA, Jenkins GI, Nimmo HG. 2007. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochemistry Journal 405: 191-198.
6. Chiou TJ, Lin SI. 2011. Signaling network in sensing phosphate availability in plants. Annual Review Plant Biology 62: 185-206.
7. Dai X, Wang Y, Yang A, Zhang WH. 2012. OsMYB2P-1, a R2R3 MYB transcription factor, is involved in regulation of phosphate-starvation responses and root architecture in rice. Plant Physiology 159: 169-183.
8. Devaiah BN, Karthikeyan AS, Raghothama KG. 2007a. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiology 143: 1789-1801.
9. Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG. 2009. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Molecular Plant 2: 43-58.
10. Devaiah BN, Nagarajan VK, Raghothama KG. 2007b. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiology 145: 147-159.
11. Duan K, Yi K, Dang L, Huang H, Wu W, Wu P. 2008. Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. The Plant Journal 54: 965-975.
12. Filippelli GM. 2008. The global phosphorus cycle: past, present, and future. Elements 4: 89-95.
13. Ghillebert R, Swinnen E, De Snijder P, Smets B, Winderickx J. 2011. Differential roles for the low-affinity phosphate transporters Pho87 and Pho90 in Saccharomyces cerevisiae. Biochemistry Journal 434: 243-251.
14. Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Somerville C, Poirier Y. 2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14: 889-902.
15. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ. 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151: 2120-2132.
16. Hurlimann HC, Pinson B, Stadler-Waibel M, Zeeman SC, Freimoser FM. 2009. The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity. EMBO Report 10: 1003-1008.
17. Hurlimann HC, Stadler-Waibel M, Werner TP, Freimoser FM. 2007. Pho91 Is a vacuolar phosphate transporter that regulates phosphate and polyphosphate metabolism in Saccharomyces cerevisiae. Molecular Biology Cell 18: 4438-4445.
18. Jefferson RA, Kavanagh TA, Bevan MW. 1987. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6: 3901-3907.
19. Kant S, Peng M, Rothstein SJ. 2011. Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genetics 7: e1002021.
20. Lemieux MJ, Huang Y, Wang DN. 2004. The structural basis of substrate translocation by the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily. Current Opinion Structure Biology 14: 405-412.
21. Lin SI, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil JL, Breitler JC, Perin C, Ko SS et al. 2010. Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiology 51: 2119-2131.
22. Liu F, Wang Z, Ren H, Shen C, Li Y, Ling HQ, Wu C, Lian X, Wu P. 2010. OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. The Plant Journal 62: 508-517.
23. Lu S, Sun YH, Chiang VL. 2008. Stress-responsive microRNAs in Populus. The Plant Journal 55: 131-151.
24. +-coupled phosphate transporter in Saccharomyces cerevisiae. Molecular Genomic Genetics 258: 628-638.
25. Nilsson L, Muller R, Nielsen TH. 2007. Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell & Environment 30: 1499-1512.
26. Nishimura A, Aichi I, Matsuoka M. 2006. A protocol for Agrobacterium-mediated transformation in rice. Nature Protocol 1: 2796-2802.
27. Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen X, Triplett BA, Stelly DM, Chen ZJ. 2009. Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biology 10: R122.
28. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR. 2009. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150: 1541-1555.
29. Pao SS, Paulsen IT, Saier MH Jr. 1998. Major facilitator superfamily. Microbiology Molecular Biology Review 62: 1-34.
30. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ. 2007. A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. The Plant Journal 50: 320-337.
31. Pinson B, Merle M, Franconi JM, Daignan-Fornier B. 2004. Low affinity orthophosphate carriers regulate PHO gene expression independently of internal orthophosphate concentration in Saccharomyces cerevisiae. Journal Biology Chemistry 279: 35273-35280.
32. Pratt J, Boisson A-M, Gout E, Bligny R, Douce R, Aubert S. 2009. Phosphate (Pi) starvation effect on the cytosolic Pi concentration and Pi exchanges across the tonoplast in plant cells: an in vivo 31P-nuclear magnetic resonance study using methylphosphonate as a Pi analog. Plant Physiology 151: 1646-1657.
33. Rouached H, Arpat AB, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: signaling players and cross-Ttlks. Molecular Plant 3: 288-299.
34. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Development 15: 2122-2133.
35. Schachtman DP, Shin R. 2007. Nutrient sensing and signaling: NPKS. Annual Review Plant Biology 58: 47-69.
36. Secco D, Baumann A, Poirier Y. 2010. Characterization of the Rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiology 152: 1693-1704.
37. Secco D, Wang C, Arpat BA, Wang Z, Poirier Y, Tyerman SD, Wu P, Shou H, Whelan J. 2012a. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytologist 193: 842-851.
38. Secco D, Wang C, Shou H, Whelan J. 2012b. Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins. FEBS Letters 586: 289-295.
39. Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, Delessert S, Poirier Y. 2007. Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. The Plant Journal 50: 982-994.
40. Ticconi CA, Abel S. 2004. Short on phosphate: plant surveillance and countermeasures. Trends in Plant Science 9: 548-555.
41. Wang C, Ying S, Huang H, Li K, Wu P, Shou H. 2009. Involvement of OsSPX1 in phosphate homeostasis in rice. The Plant Journal 57: 895-904.
42. Wykoff DD, Rizvi AH, Raser JM, Margolin B, O'Shea EK. 2007. Positive feedback regulates switching of phosphate transporters in S. cerevisiae. Molecular Cell 27: 1005-1013.
43. Xue LJ, Zhang JJ, Xue HW. 2009. Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Research 37: 916-930.
44. Yaeno T, Iba K. 2008. BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiology 148: 1032-1041.
45. Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P. 2005. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiology 138: 2087-2096.
46. Yoshida S, Forno DA, Cock JH, KA G. 1976. Laboratory manual for physiological studies of rice, 3rd edn . Manila, The Philippines: The International Rice Research Institute.
47. Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D. 2009. A genome-wide characterization of microRNA genes in maize. PLoS Genetics 5: e1000716.
48. Zheng L, Cheng Z, Ai C, Jiang X, Bei X, Zheng Y, Glahn RP, Welch RM, Miller DD, Lei XG et al. 2010. Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5: e10190.
49. Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, Zhong W, Wu P. 2008. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiology 146: 1673-1686.