Root architecture responses: In search of phosphate

Plant Physiology

Volumn 166, Issue 4, 2014, Pages 1713-1723

  Péret, Benjamin ^a,b,c   Desnos, Thierry ^a,b,c   Jost, Ricarda ^d   Kanno, Satomi ^e   Berkowitz, Oliver ^d   Nussaume, Laurent ^a,b,c  

^a University of Aix Marseille   (France)

^b Laboratoire de Biologie du Développement des Plantes ^*  (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE; PHOSPHORUS; SOIL;

CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT; PLANT DEVELOPMENT; PLANT ROOT; SOIL;

PHOSPHATES; PHOSPHORUS; PLANT DEVELOPMENT; PLANT ROOTS; PLANTS; SOIL;

EID: 84914164065     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.244541     Document Type: Article

References (99)

1. Abel S (2011) Phosphate sensing in root development. Curr Opin Plant Biol 14: 303-309.
2. Aeschbacher RA, Hauser MT, Feldmann KA, Benfey PN (1995) The SABRE gene is required for normal cell expansion in Arabidopsis. Genes Dev 9: 330-340.
3. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signaling. Plant Cell Environ 26: 1053-1066.
4. Arahou M, Diem HG (1997) Iron deficiency induces cluster (proteoid) root formation in Casuarina glauca. Plant Soil 196: 71-79.
5. Berkowitz O, Jost R, Kollehn DO, Fenske R, Finnegan PM, O'Brien PA, Hardy GE, Lambers H (2013) Acclimation responses of Arabidopsis thaliana to sustained phosphite treatments. J Exp Bot 64: 1731-1743.
6. Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132: 281-288.
7. Bournier M, Tissot N, Mari S, Boucherez J, Lacombe E, Briat JF, Gaymard F (2013) Arabidopsis ferritin 1 (AtFer1) gene regulation by the phosphate starvation response 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. J Biol Chem 288: 22670-22680.
8. Calderón-Vázquez C, Sawers RJ, Herrera-Estrella L (2011) Phosphate deprivation in maize: genetics and genomics. Plant Physiol 156: 1067-1077.
9. Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9: 2131-2142.
10. Cheng L, Bucciarelli B, Shen J, Allan D, Vance CP (2011) Update on lupin cluster roots: update on white lupin cluster root acclimation to phosphorus deficiency. Plant Physiol 156: 1025-1032.
11. Dai X, WangY, YangA, ZhangWH(2012) OsMYB2P-1, an R2R3MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol 159: 169-183.
12. Dasgupta K, Khadilkar AS, Sulpice R, Pant B, Scheible WR, Fisahn J, Stitt M, Ayre BG (2014) Expression of sucrose transporter cDNAs specifically in companion cells enhances phloem loading and long-distance transport of sucrose, but leads to an inhibition of growth and the perception of a phosphate limitation. Plant Physiol 165: 715-731.
13. Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107: 207-213.
14. 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.
15. Giehl RF, Gruber BD, von Wirén N (2014) It's time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65: 769-778.
16. González-Mendoza V, Zurita-Silva A, Sánchez-Calderón L, Sánchez-Sandoval ME, Oropeza-Aburto A, Gutiérrez-Alanís D, Alatorre-Cobos F, Herrera-Estrella L (2013) APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability. Plant Sci 205-206: 2-12.
17. Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163: 161-179.
18. Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156: 1033-1040.
19. Hochholdinger F, Zimmermann R (2008) Conserved and diverse mechanisms in root development. Curr Opin Plant Biol 11: 70-74.
20. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162: 9-24.
21. Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322: 49-86.
22. Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156: 1101-1115.
23. Igarashi D, Tsuda K, Katagiri F (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71: 194-204.
24. Kang J, Yu H, Tian C, Zhou W, Li C, Jiao Y, Liu D (2014) Suppression of photosynthetic gene expression in roots is required for sustained root growth under phosphate deficiency. Plant Physiol 165: 1156-1170.
25. Karthikeyan AS, Jain A, Nagarajan VK, Sinilal B, Sahi SV, Raghothama KG (2014) Arabidopsis thaliana mutant lpsi reveals impairment in the root responses to local phosphate availability. Plant Physiol Biochem 77: 60-72.
26. Kellermeier F, Armengaud P, Seditas TJ, Danku J, Salt DE, Amtmann A (2014) Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 26: 1480-1496.
27. Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106: 15067-15072.
28. Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible WR, Stitt M, Teste F, Turner BL (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol 196: 1098-1108.
29. Lambers H, Finnegan PM, Laliberté E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Update on phosphorus nutrition in Proteaceae: phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156: 1058-1066.
30. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrientacquisition strategies change with soil age. Trends Ecol Evol 23: 95-103.
31. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot (Lond) 98: 693-713.
32. Lamont B (1972) The morphology and anatomy of proteoid roots in the genus Hakea. Aust J Bot 20: 155-174.
33. Lamont BB (2003) Structure, ecology and physiology of root clusters-a review. Plant Soil 248: 1-19.
34. Lavenus J, Goh T, Roberts I, Guyomarc'h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18: 450-458.
35. Lei M, Liu Y, Zhang B, Zhao Y, Wang X, Zhou Y, Raghothama KG, Liu D (2011a) Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol 156: 1116-1130.
36. Lei M, Zhu C, Liu Y, Karthikeyan AS, Bressan RA, Raghothama KG, Liu D (2011b) Ethylene signalling is involved in regulation of phosphate starvationinduced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytol 189: 1084-1095.
37. Li H, Xia M, Wu P (2000) Effect of phosphorus deficiency stress on rice lateral root growth and nutrient absorption. Acta Bot Sin 43: 1154-1160.
38. Li Z, Xu C, Li K, Yan S, Qu X, Zhang J (2012) Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone. BMC Plant Biol 12: 89.
39. Lobet G, Draye X, Périlleux C (2013) An online database for plant image analysis software tools. Plant Methods 9: 38.
40. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129: 244-256.
41. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) 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 137: 681-691.
42. Lynch J, Brown M (2001) Topsoil foraging-an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225-237.
43. Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156: 1041-1049.
44. McCluskey J, Herdman L, Skene KR (2004) Iron deficiency induces changes in metabolism of citrate in lateral roots and cluster roots of Lupinus albus. Physiol Plant 121: 586-594.
45. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138: 2061-2074.
46. Nagarajan VK, Smith AP (2012) Ethylene's role in phosphate starvation signaling: more than just a root growth regulator. Plant Cell Physiol 53: 277-286.
47. Neumann G, Martinoia E (2002) Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci 7: 162-167.
48. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot (Lond) 112: 391-408.
49. Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi TM, Thibaud MC (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2: 83.
50. O'Rourke JA, Yang SS, Miller SS, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu ZJ, Allan D, et al (2013) An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161: 705-724.
51. Panigrahy M, Rao DN, Sarla N (2009) Molecular mechanisms in response to phosphate starvation in rice. Biotechnol Adv 27: 389-397.
52. ParniskeM(2008) Arbuscular mycorrhiza: themother of plant root endosymbioses. Nat Rev Microbiol 6: 763-775.
53. Péret B, Clément M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16: 442-450.
54. Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14: 399-408.
55. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20: 3258-3272.
56. Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stressinduced morphogenic responses: growing out of trouble? Trends Plant Sci 12: 98-105.
57. Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crops Res 117: 169-176.
58. Rath M, Salas J, Parhy B, Norton R, Menakuru H, Sommerhalter M, Hatlstad G, Kwon J, Allan DL, Vance CP (2010) Identification of genes induced in proteoid roots of white lupin under nitrogen and phosphorus deprivation, with functional characterization of a formamidase. Plant Soil 334: 137-150.
59. Remy E, Cabrito TR, Batista RA, Teixeira MC, Sá-Correia I, Duque P (2012) The Pht1; 9 and Pht1; 8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytol 195: 356-371.
60. Robinson WD, Park J, Tran HT, Del Vecchio HA, Ying S, Zins JL, Patel K, McKnight TD, Plaxton WC (2012) The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana. J Exp Bot 63: 6531-6542.
61. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46: 174-184.
62. Secco D, Shou H, Whelan J, Berkowitz O (2014) RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin. BMC Genomics 15: 230.
63. Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004a) Developmental physiology of clusterroot carboxylate synthesis and exudation in harsh hakea: expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135: 549-560.
64. Shane MW, De Vos M, de Roock S, Cawthray GR, Lambers H (2003a) Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R. Br. Plant Soil 209-219.
65. Shane MW, De Vos M, De Roock S, Lambers H (2003b) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26: 265-273.
66. Shane MW, Fedosejevs ET, Plaxton WC (2013) Reciprocal control of anaplerotic phosphoenolpyruvate carboxylase by in vivo monoubiquitination and phosphorylation in developing proteoid roots of phosphate-deficient harsh hakea. Plant Physiol 161: 1634-1644.
67. Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274: 101-125.
68. Shane MW, Szota C, Lambers H (2004b) A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae). Plant Cell Environ 27: 991-1004.
69. Shi L, Shi T, Broadley MR, White PJ, Long Y, Meng J, Xu F, Hammond JP (2013) High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities. Ann Bot (Lond) 112: 381-389.
70. Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1; 1 and Pht1; 4 play a major role in phosphate acquisition from both low-and high-phosphate environments. Plant J 39: 629-642.
71. Shu L, Shen J, Rengel Z, Tang C, Zhang F (2007) Cluster root formation by Lupinus albus is modified by stratified application of phosphorus in a split-root system. J Plant Nutr 30: 271-288.
72. Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86: 1060-1064.
73. Skene KR (2000) Pattern formation in cluster roots: some developmental and evolutionary considerations. Ann Bot (Lond) 85: 901-908.
74. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156: 1050-1057.
75. Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N, et al (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ 37: 1276-1298.
76. Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate-and nitrate-deficiencyinduced root development and auxin transport in rice. J Exp Bot (in press).
77. Svistoonoff S, Creff A, ReymondM, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39: 792-796.
78. Thibaud MC, Arrighi JF, 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.
79. Ticconi CA, Delatorre CA, Abel S (2001) Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol 127: 963-972.
80. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37: 801-814.
81. Ticconi CA, Lucero RD, Sakhonwasee S, AdamsonAW, Creff A, Nussaume L, Desnos T, Abel S (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci USA 106: 14174-14179.
82. Tran HT, Qian W, Hurley BA, She YM, Wang D, Plaxton WC (2010) Biochemical and molecular characterization of AtPAP12 and AtPAP26: the predominant purple acid phosphatase isozymes secreted by phosphatestarved Arabidopsis thaliana. Plant Cell Environ 33: 1789-1803.
83. Vandenbussche F, Vaseva I, Vissenberg K, Van Der Straeten D (2012) Ethylene in vegetative development: a tale with a riddle. New Phytol 194: 895-909.
84. Varadarajan DK, Karthikeyan AS, Matilda PD, Raghothama KG (2002) Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol 129: 1232-1240.
85. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, et al (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195: 306-320.
86. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79: 607-622.
87. Wang H, Xu Q, Kong YH, Chen Y, Duan JY, Wu WH, Chen YF (2014a) Arabidopsis WRKY45 transcription factor activates PHOSPHATE TRANSPORTER1; 1 expression in response to phosphate starvation. Plant Physiol 164: 2020-2029.
88. Wang L, Dong J, Gao Z, Liu D (2012) The Arabidopsis gene hypersensitive to phosphate starvation 3 encodes ethylene overproduction 1. Plant Cell Physiol 53: 1093-1105.
89. Wang L, Li Z, Qian W, Guo W, Gao X, Huang L, Wang H, Zhu H, Wu JW, Wang D, et al (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.
90. Wang S, Zhang S, Sun C, Xu Y, Chen Y, Yu C, Qian Q, Jiang DA, Qi Y (2014b) Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol 201: 91-103.
91. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147: 1181-1191.
92. 2 concentration. Plant Physiol 120: 705-716.
93. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126: 875-882.
94. Yang WT, Baek D, Yun DJ, Hwang WH, Park DS, Nam MH, Chung ES, Chung YS, Yi YB, Kim DH (2014) Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice. Plant Physiol Biochem 80: 259-267.
95. Yu H, Luo N, Sun L, Liu D (2012) HPS4/SABRE regulates plant responses to phosphate starvation through antagonistic interaction with ethylene signalling. J Exp Bot 63: 4527-4538.
96. Zaid H, El Morabet R, Diem HG, Arahou M (2003) Does ethylene mediate cluster root formation under iron deficiency? Ann Bot (Lond) 92: 673-677.
97. Zhang YM, Yan YS, Wang LN, Yang K, Xiao N, Liu YF, Fu YP, Sun ZX, Fang RX, Chen XY (2012) A novel rice gene, NRR responds to macronutrient deficiency and regulates root growth. Mol Plant 5: 63-72.
98. 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 Physiol 146: 1673-1686.
99. Zhou W, Wei L, Xu J, Zhai Q, Jiang H, Chen R, Chen Q, Sun J, Chu J, Zhu L, et al (2010) Arabidopsis Tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22: 3692-3709.