Diversity in the complexity of phosphate starvation transcriptomes among rice cultivars based on RNA-Seq profiles

Plant Molecular Biology

Volumn 83, Issue 6, 2013, Pages 523-537

  Oono, Youko ^a   Kawahara, Yoshihiro ^a   Yazawa, Takayuki ^a,b   Kanamori, Hiroyuki ^a   Kuramata, Masato ^c   Yamagata, Harumi ^a   Hosokawa, Satomi ^a   Minami, Hiroshi ^d   Ishikawa, Satoru ^c   Wu, Jianzhong ^a   Antonio, Baltazar ^a   Handa, Hirokazu ^a   Itoh, Takeshi ^a   Matsumoto, Takashi ^a,e  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b HITACHI LTD   (Japan)

^c NATIONAL INSTITUTE FOR AGRO ENVIRONMENTAL SCIENCES   (Japan)

^d MITSUBISHI SPACE SOFTWARE CO LTD   (Japan)

^e Agriculture Forestry and Fisheries Research Council   (Japan)

Author keywords

Abiotic stress; Phosphate starvation; Phosphorus; Rice; RNA Seq; Transcriptome

Indexed keywords

PHOSPHATE; PLANT RNA; TRANSCRIPTOME;

ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHODOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; PLANT ROOT; POLYMERASE CHAIN REACTION; RICE;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; ORYZA SATIVA; PHOSPHATES; PLANT ROOTS; PLANT SHOOTS; POLYMERASE CHAIN REACTION; RNA, PLANT; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84887993280     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0106-4     Document Type: Article

References (48)

1. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. In: Elizabeth F, Neufeld VG (eds) Methods in enzymology. Academic, New York, pp 115-118.
2. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signalling pathway in plants. Plant Physiol 141: 988-999.
3. 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.
4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300.
5. Bennett T, van den Toorn A, Sanchez-Perez GF, Campilho A, Willemsen V, Snel B, Scheres B (2010) SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 22: 640-654.
6. 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 Genet 6: e1001102.
7. Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21: 3554-3566.
8. Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P (2011) OsPHF1 regulates the plasma membrane localization of low- and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol 157: 269-278.
9. Chin JH, Gamuyao R, Dalid C, Bustamam M, Prasetiyono J, Moeljopawiro S, Wissuwa M, Heuer S (2011) Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol 156: 1202-1216.
10. Dai XY, Wang YY, Yang A, Zhang WH (2012) OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol 159: 169-183.
11. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143: 1789-1801.
12. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488: 535-539.
13. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signalling pathways, is involved in salt stress response and lateral root development. Plant J 44: 903-916.
14. He GM, Zhu XP, Elling AA, Chen LB, Wang XF, Guo L, Liang MZ, He H, Zhang HY, Chen FF, Qi YJ, Chen RS, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22: 17-33.
15. Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19: 2156-2168.
16. 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 signalling and hormones. Plant Cell Environ 28: 353-364.
17. Huang CY, Shirley N, Genc Y, Shi B, Langridge P (2011) Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and noncoding RNA, IPS1, in barley. Plant Physiol 156: 1217-1229.
18. Huang X, Kurata N, Wei X, Wang ZX, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan X, Xu Q, Dong G, Zhan Q, Li C, Fujiyama A, Toyoda A, Lu T, Feng Q, Qian Q, Li J, Han B (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490: 497-501.
19. Hur YJ, Jin BR, Nam J, Chung YS, Lee JH, Choi HK, Yun DJ, Yi G, Kim YH, Kim DH (2010) Molecular characterization of OsPAP2: transgenic expression of a purple acid phosphatase up-regulated in phosphate-deprived rice suspension cells. Biotechnol Lett 32: 163-170.
20. Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signalling pathway in Arabidopsis. Plant Physiol 145: 1460-1470.
21. Kong ZS, Li MN, Yang WQ, Xu WY, Xue YB (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141: 1376-1388.
22. Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science 312: 1392-1396.
23. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
24. Li LH, Liu C, Lian XM (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72: 423-432.
25. Meireles-Filho AC, Stark A (2009) Comparative genomics of gene regulation-conservation and divergence of cis-regulatory information. Curr Opin Genet Dev 19: 565-570.
26. 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 Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934-11939.
27. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102: 7760-7765.
28. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461: 1130-1134.
29. Oono Y, Kawahara Y, Kanamori H, Mizuno H, Yamagata H, Yamamoto M, Hosokawa S, Ikawa H, Akahane I, Zhu Z, Wu J, Itoh T, Matsumoto T (2011) mRNA-Seq reveals a comprehensive transcriptome profile of rice under phosphate stress. Rice 4: 50-65.
30. Pariasca-Tanaka J, Satoh K, Rose T, Mauleon R, Wissuwa M (2009) Stress response versus stress tolerance: a transcriptome analysis of two rice lines contrasting in tolerance to phosphorus deficiency. Rice 2: 167-185.
31. Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99: 13324-13329.
32. Raghothama KG (1999) Phosphate Acquisition. Annu Rev Plant Physiol Plant Mol Biol 50: 665-693.
33. 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 signalling both in vascular plants and in unicellular algae. Gene Dev 15: 2122-2133.
34. Scarpella E, Simons EJ, Meijer AH (2005) Multiple regulatory elements contribute to the vascular-specific expression of the rice HD-Zip gene Oshox1 in Arabidopsis. Plant Cell Physiol 46: 1400-1410.
35. Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, Raghothama KG, Meagher RB (2010) Histone H2A. Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol 152: 217-225.
36. Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, McCouch SR (2007) Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet 3: e133.
37. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
38. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
39. Wang Z, Hu H, Huang H, Duan K, Wu Z, Wu P (2009) Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and Pi-starvation signalling in rice. J Integr Plant Biol 51: 663-674.
40. Wang L, Li Z, Qian W, Guo W, Gao X, Huang L, Wang H, Zhu H, Wu JW, Wang D, Liu D (2011) The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. Plant Physiol 157: 1283-1299.
41. 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 (2003a) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26: 1515-1523.
42. Wasaki J, Yonetani R, Shinano T, Kai M, Osaki M (2003b) Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status. New Phytol 158: 239-248.
43. Wissuwa M, Ae N (2001) Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breeding 120: 43-48.
44. Wu P, Shou H, Xu G, Lian X (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signalling and homeostasis. Curr Opin Plant Biol 16: 205-212.
45. Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Gene Dev 14: 3024-3036.
46. 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 Physiol 138: 2087-2096.
47. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Manila, pp 61-67.
48. Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, Zhong W, Wu P (2008) OsPHR2 is involved in phosphate-starvation signalling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146: 1673-1686.