Transcriptome response to phosphorus starvation in rice

Acta Physiologiae Plantarum

Volumn 34, Issue 1, 2012, Pages 327-341

  Cai, Hongmei ^a   Xie, Weibo ^a   Zhu, Tong ^b   Lian, Xingming ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

Affymetrix GeneChip; MicroRNAs; Phosphorus; Rice; Transcription profile

Indexed keywords

ARABIDOPSIS; DICOTYLEDONEAE;

EID: 84855227053     PISSN: 01375881     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11738-011-0832-7     Document Type: Article

References (120)

1. Abel S, Nurnberger T, Ahnert V, Krauss GJ, Glund K (2000) Induction of an extracellular cyclic nucleotide phosphodiesterase as an accessory ribonucleolytic activity during phosphate starvation of cultured tomato cells. Plant Physiol 122: 543-552.
2. Alexa A, Rahnenfuhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600-1607.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141: 1000-1011.
5. Bachmair A, Novatchkova M, Potuschak T, Eisenhaber F (2001) Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci 6: 463-470.
6. Barabote RD, Tamang DG, Abeywardena SN, Fallah NS, Fu JYC, Lio JK, Mirhosseini P, Pezeshk R, Podell S, Salampessy ML, Thever MD, Saier MH (2006) Extra domains in secondary transport carriers and channel proteins. Biochim Biophys Acta 1758: 1557-1579.
7. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141: 988-999.
8. Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6: 673-685.
9. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
10. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 21: 529-538.
11. Berglund AC, Sjolund E, Ostlund G, Sonnhammer EL (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36: D263-D266.
12. Bi YM, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8: 281-297.
13. Bonnet E, Peer YV, Rouze P (2006) The small RNA world of plants. New Phytol 171: 451-468.
14. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53: 739-749.
15. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301: 336-338.
16. Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559-574.
17. Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30: 323-332.
18. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412-421.
19. Combier JP, Frugier F, Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20: 3084-3088.
20. Combier JP, Billy F, Gamas P, Biebel A, Rivas S (2008) Trans-regulating of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev 22: 1549-1559.
21. Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172.
22. Doerner P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11: 1-5.
23. 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. Plant J 54: 965-975.
24. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90: 791-800.
25. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8: 155-168.
26. Fang Z, Shao C, Meng Y, Wu P, Chen M (2009) Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci 176(2): 170-180.
27. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14: 675-1690.
28. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15: 2038-2043.
29. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12: 393-404.
30. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130: 1319-1334.
31. Goldstein AH, Beartlein DA, McDaniel RG (1988) Phosphate starvation inducible metabolism in Lycopersicon esculentum: I. Excretion of acid phosphatase by tomato plants and suspension cultured cells. Plant Physiol 87: 711-715.
32. Green PJ (1994) The ribonucleases of higher plants. Annu Rev, Plant Physiol, Plant Mol Biol 45: 421-445.
33. Griffiths-Jones S (2006) miRBase: the microRNA sequence database. Methods Mol Biol 342: 129-138.
34. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopericum. Physiol Plantarum 138: 226-237.
35. Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17: 1376-1386.
36. Hamburger D, Rezzonico E, MacDonald-Comber Petétot 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.
37. Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May TM, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132: 578-596.
38. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113.
39. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Montagu MV, Inze D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proc Natl Acad Sci USA 101: 5146-5151.
40. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827.
41. Hou XL, Wu P, Jiao FC, Jia QJ, Chen HM, Yu J, Song XW, Yi KK (2005) Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signaling and hormones. Plant, Cell and Environment 28: 353-364.
42. Hsieh L-C, Lin S-I, Shih AC-C, Chen J-W, Lin W-Y, Tseng C-Y, Li W-H, Chiou T-J (2009) Uncoveringsmall RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151: 2120-2132.
43. Hubner N, Caroline AW, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, Musilova A, Kren V, Causton H, Game L, Born G, Schmidt S, Müller A, Cook SA, Kurtz TW, Whittaker J, Pravenec M, Aitman TJ (2005) Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet 37: 243-253.
44. Jofuku KD, Boer BG, Montagu MV, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6: 1211-1225.
45. Jones-Rhoades MJ, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799.
46. Jones-Rhoades MJ, Bartel B, Bartel DP (2006) MicroRNAs and their regulatory targets in plants. Annu Rev Plant Biol 57: 19-53.
47. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert H (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13: 889-905.
48. Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14: 2481-2494.
49. Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8: 137-153.
50. Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW, Callis J (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 139: 1597-1611.
51. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141.
52. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20: 2238-2251.
53. Li L, Liu C, Lian X (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72: 423-432.
54. Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, Li X, Yuan D, Han B, Zhang Q (2006) Expression profiles of 10, 422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Mol Biol 60: 617-631.
55. Lin S-I, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil J-L, Breitler JC, Périn C, Ko S-S, Guiderdoni E, Chiou T-J, Echeverria M (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51: 2119-2131.
56. Liu F, Wang Z, Ren H, Shen C, Li Y, Ling H-Q, 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. Plant J 62: 508-517.
57. Lundmark M, Kner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in esponse to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plantarum 140: 57-68.
58. Ma L, Gao Y, Qu L, Chen Z, Li J, Zhao H, Deng XW (2002) Genomic evidence for COP1 as repressor of light regulated gene expression and development in Arabidopsis. Plant Cell 14: 2383-2398.
59. Mahalingam R, Gomez-Buitrago AM, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4: R20.
60. Malboobi MA, Lefebvre DD (1997) A phosphate-starvation inducible-glucosidase (psr3. 2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol Biol 34: 57-68.
61. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410.
62. Mallory A, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet S31-36.
63. Mallory AC, Dugas DV, Bartel DB, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14: 1035-1046.
64. Marschner H (1995) Mineral Nutrition of Higher Plants. Academic Press, SanDiego, CA.
65. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsisthaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934-11939.
66. Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, Spielman RS, Cheung VG (2004) Genetic analysis of genome-wide variation in human gene expression. Nature 430: 743-747.
67. Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143: 156-171.
68. Nakanishi H, Okumura N, Umehara Y, Nishizawa NK, Chino M, Mori S (1993) Expression of a gene specific for iron deficiency (Ids3) in the roots of Hordeum vulgare. Plant Cell Physiol 34: 401-410.
69. Nover L, Scharf KD, Gagliardi D, Vergne P, Czarnecka-Verner E, Gurley WB (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones 1: 215-223.
70. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173-182.
71. Olczak M, Morawiecka B, Watorek W (2003) Plant purple acid phosphatases-genes, structures and biological function. Acta Biochim Pol 50: 1245-1256.
72. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35: D883-D887.
73. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible W (2009) Identification of nutrient-responsive Arabidopsis and Rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150: 1541-1555.
74. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts Arabidopsis adaptability to nitrogen limitation. Plant J 50: 320-337.
75. Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97: 1087-1093.
76. Pozo JC, Allona I, Rubio V, Leyva A, Pena A, Aragoncillo C, Paz-Ares J (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilizing/oxidative stress conditions. Plant J 19: 579-589.
77. Pré M, Atallah M, Champion A, Vos MD, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147: 1347-1357.
78. Raghothama KG (1999) Phosphate acquisition. Ann Rev, Plant Physiol, Plant Mol Biol 50: 665-693.
79. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditiselegans. Nature 403: 901-906.
80. Remm M, Storm CE, Sonnhammer EL (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 314: 1041-1052.
81. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707-719.
82. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110: 513-520.
83. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379: 633-646.
84. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110.
85. Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130: 1109-1120.
86. Rubio V, Francisco L, Roberto S, Ana C, Martin JI, Antonio L, Javier Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular. Gene Dev 15: 2122-2133.
87. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290: 998-1009.
88. Schachtman DP, Shin R (2007) Nutrient Sensing and Signaling: NPKS. Annu Rev Plant Biol 58: 47-69.
89. Secco D, Baumann A, Poirier (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 Physiol 152: 1693-1704.
90. Seki M, Narusaka M, Abe H, Kasuko M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1, 300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13: 61-72.
91. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7, 000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
92. Shen YG, Zhang WK, He SJ, Zhang JS, Liu Q, Chen SY (2003) An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet 106: 923-930.
93. Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101: 8827-8832.
94. 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. Plant J 50: 982-994.
95. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019.
96. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18: 2051-2065.
97. Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Sci 12: 301-309.
98. Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH (2001) Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci USA 98: 9437-9442.
99. Theodoru ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101: 339-344.
100. Thibaud M-C, Arrighi J-F, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64: 775-789.
101. Trull MC, Deikman J (1998) An Arabidopsis mutant missing one acid phosphatase isoform. Planta 206: 544-550.
102. Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172: 47-62.
103. Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248: 99-116.
104. Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18: 1187-1197.
105. Wang YH, Garvin DF, Kochian LV (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots: evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol 130: 1361-1370.
106. Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the ArabidopsisPHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135: 400-411.
107. Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009a) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57: 895-904.
108. Wang Z, Hu H, Huang H, Duan K, Wu Z, Wu P (2009b) Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and Pi-starvation signaling in rice. J Integr Plant Biol 51: 663-674.
109. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S, Yamagishi M, Osaki M (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26: 1515-1523.
110. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132: 1260-1271.
111. Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99: 909-917.
112. Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Bio Chem 282: 16369-16378.
113. Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory Manual for Physiological Studies of Rice, 3rd ed. International Rice Research Institute, Manila.
114. Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50: 849-859.
115. Zhang Y (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33: W701-W704.
116. Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006a) Conservation and divergence of plant microRNA genes. Plant J 46: 243-259.
117. Zhang B, Pan X, Cobb GP, Anderson TA (2006b) Plant microRNA: A small regulatory molecule with big impact. Dev Bio 289: 3-16.
118. Zhu T (2003) Global analysis of gene expression using Gene Chip microarrays. Curr Opin Plant Biol 6: 1-8.
119. Zhu T, Budworth P, Han B, Brown D, Chang HS, Zou G, Wang X (2001) Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8, 300 gene by a high-density oligonucleotide probe array. Plant Physiol Biochem 39: 221-242.
120. Zhu YY, Zeng HQ, Dong CX, Yin XM, Shen QR, Yang ZM (2010) MicroRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Sci 178: 23-29.