Root architecture remodeling induced by phosphate starvation

Plant Signaling and Behavior

Volumn 6, Issue 8, 2011, Pages 1122-1126

  Sato, Aiko ^a   Miura, Kenji ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Auxin; Phosphate deficiency; Root system architecture modulation

Indexed keywords

EID: 79961197939     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.6.8.15752     Document Type: Review

References (67)

1. Raghothama KG. Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 1999; 50:665-9.
2. Vence CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 2003; 157:423-47.
3. Berndt T, Kumar R. Phosphatonins and the regulation of phosphate homeostasis. Annu Rev Physiol 2007; 69:341-59.
4. Nielsson L, Müller R, Nielsen TH. Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol Plant 2010; 139:129-43.
5. Cordell D, Drangert JO, White S. The story of phosphorus: global food security and food for thought. Global Environ Change 2009; 19:292-305.
6. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T. Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 2006; 29:115-25.
7. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera- Estrella L. Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorusinduced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 2006; 140:879-89.
8. Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, et al. Differntial effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 2007; 144:232-47.
9. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, et al. Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 2007; 39:792-6.
10. Lai F, Thacker J, Li Y, Doerner P. Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 2007; 50:545-56.
11. Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, et al. SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 2011; 155:1000-12.
12. Linkohr BI, Williamson LC, Fitter AH, Leyser HMO. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 2002; 29:751-60.
13. Franco-Zorrilla JM, Martin AC, Solano R, Rubio V, Leyva A, Paz-Ares J. Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J 2002; 32:353-60.
14. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, et al. A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 2005; 138:2061-74.
15. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, et al. An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis: identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 2005; 137:681-91.
16. Cheng Y, Dai X, Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 2006; 20:1790-9.
17. Péret B, Rybel BD, Casimiro I, Benková E, Swarup R, Laplaze L, et al. Arabidopsis lateral root development: an emerging story. Trends Plant Sci 2009; 14:399-408.
18. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 2002; 129:244-56.
19. Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, et al. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev 2001; 15:1985-97.
20. Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, et al. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acd Sci USA 2009; 106:14174-9.
21. Chen DL, Delatorre CA, Bakker A, Abel S. Conditional identification of phosphate-starvationresponse mutants in Arabidopsis thaliana. Planta 2000; 211:13-22.
22. Ticconi CA, Delatorre CA, Lahner B, Salt D, Abel S. Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 2004; 37:801-14.
23. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, et al. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 1996; 86:423-33.
24. Gallagher KL, Benfey PN. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J 2009; 57:785-97.
25. Wang X, Du G, Wang X, Meng Y, Li Y, Wu P, Yi K. The function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana. Plant Cell Physiol 2010; 51:380-94.
26. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, et al. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 2005; 102:7760-5.
27. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, et al. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 2007; 19:1403-14.
28. Miura K, Jin JB, Hasegawa PM. Sumoylation, a posttranslational regulatory process in plants. Curr Opin Plant Biol 2007; 10:495-502.
29. Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM. Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA 2009; 106:5418-23.
30. Miura K, Lee J, Miura T, Hasegawa PM. SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol 2010; 51:103-13.
31. Miura K, Hasegawa PM. Regulation of cold signaling by sumoylation of ICE1. Plant Signal Behav 2008; 3:52-3.
32. Miura K, Hasegawa PM. Sumoylation and abscisic acid signaling. Plant Signal Behav 2009; 4:1176-8.
33. Miura K, Hasegawa PM. Sumoylation and other ubiquitin- like post-translational modifications in plants. Trends Cell Biol 2010; 223-32.
34. Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, et al. The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 2008; 53:530-40.
35. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 1999; 286:316-8.
36. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R. Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 2006; 47:788-92.
37. Sampedro J, Cosgrove DJ. The expansin superfamily. Genome Biol 2005; 6:242.
38. Lopez-Casado G, Urbanowicz BR, Damasceno CM, Rose JK. Plant glycosyl hydrolases and biofuels: a natural marriage. Curr Opin Plant Biol 2008; 11:329-37.
39. Devaiah BN, Karthikeyan AS, Raghothama KG. WRKY75 transcription factor is modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 2007; 143:1789-801.
40. Devaiah BN, Nagarajan VK, Raghothama KG. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 2007; 145:147-59.
41. Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2009; 2:43-58.
42. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 2005; 102:11934-9.
43. Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, de los Santos B, Romero F, Pliego-Alfaro F, et al. Evidence for a positive regulatory role of strawberry (Fragaria x ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. J Exp Bot 2009; 60:3043-65.
44. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, et al. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 2003; 132:1260-71.
45. Chen ZH, Nimmo GA, Jenkins GI, Nimmo HG. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J 2007; 405:191-8.
46. Camacho-Cristóbal JJ, Rexach J, Conéjéro G, Al-Ghazi Y, Nacry P, Doumas P. PRD, an Arabidopsis AINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation. Physiol Plant 2008; 132:272-82.
47. Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, Raghothama KG, et al. Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol 2010; 152:217-25.
48. Chacón-López A, Ibarra-Laclette E, Sánchez-Calderón L, Gutiérrez-Alanís D, Herrera-Estrella L. Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation. Plant Signal Behav 2011; 6:1-11.
49. Poirier Y, Thoma S, Somerville C, Schiefelbein J. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 1991; 97:1087-93.
50. Delhaize E, Randall PJ. Characterization of a phosphate- accumulator mutant of Arabidopsis thaliana. Plant Physiol 1995; 107:207-13.
51. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 2005; 15:2038-43.
52. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ. pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 2006; 141:1000-11.
53. Bari R, Datt Pant B, Stitt M, Scheible WR. PHO2, microRNA399 and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 2006; 141:989-99.
54. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 2001; 15:2122-33.
55. Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, et al. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 2001; 13:843-52.
56. Vanneste S, Friml J. Auxin: a trigger for change in plant development. Cell 2009; 136:1005-16.
57. Horgan JM, Wareing PF. Cytokinins and the growth responses of seedlings of Betula pendula Roth. And Acer pseudoplatanus L. to nitrogen and phosphorus deficiency. J Exp Bot 1980; 31:525-32.
58. Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Peña A, et al. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 2000; 24:559-67.
59. Franco-Zorrilla JM, González E, Bustos R, Linhares F, Leyva A, Paz-Ares J. The transcriptional control of plant responses to phosphate limitation. J Exp Bot 2004; 55:285-93.
60. Ma Z, Baskin TI, Brown KM, Lynch JP. Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 2003; 131:1381-90.
61. He Z, Ma Z, Brown KM, Lynch JP. Assessment of inequality of root hair density in Arabidopsis thaliana using the Gini coefficient: a close look at the effect of phosphorus and its interaction with ethylene. Ann Bot 2005; 95:287-93.
62. Richards DE, King KE, Ait-ali T, Harberd NP. How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 2001; 52:67-88.
63. Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M, et al. Identification and characterization of Arabidopsis gibberellin receptors. Plant J 2006; 46:880-9.
64. Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP. The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 2004; 16:1406-18.
65. Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, et al. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 2006; 18:3399-414.
66. Jiang C, Gao X, Liao L, Harberd NP, Fu X. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 2007; 145:1460-70.
67. Harrison MJ. Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 2005; 59:19-42.