The S-domain receptor kinase arabidopsis receptor kinase2 and the U box/armadillo repeat-containing E3 ubiquitin ligase9 module mediates lateral root development under phosphate starvation in arabidopsis

Plant Physiology

Volumn 165, Issue 4, 2014, Pages 1647-1656

  Deb, Srijani ^a   Sankaranarayanan, Subramanian ^a   Wewala, Gayathri ^a   Widdup, Ellen ^a   Samuel, Marcus A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84905270268     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.244376     Document Type: Article

References (44)

1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophot Int 11: 36-42
2. 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 signalling. Plant Cell Environ 26: 1053-1066
3. Bassham DC (2007) Plant autophagy-more than a starvation response. Curr Opin Plant Biol 10: 587-593
4. Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2: 2-11
5. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602
6. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24: 225-252
7. Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9: 2131-2142
8. Chen ZH, Jenkins GI, Nimmo HG (2008) Identification of an F-box protein that negatively regulates P(i) starvation responses. Plant Cell Physiol 49: 1902-1906
9. Chung T, Phillips AR, Vierstra RD (2010) ATG8 lipidation and ATG8 mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci. Plant J 62: 483-493
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, Möller B, Wilson M, et al (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20: 1697-1706
12. Dröse S, Boddien C, Gassel M, Ingenhorst G, Zeeck A, Altendorf K (2001) Semisynthetic derivatives of concanamycin A and C, as inhibitors of V-and P-type ATPases: structure-activity investigations and developments of photoaffinity probes. Biochemistry 40: 2816-2825
13. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29: 153-168
14. Guiboileau A, Yoshimoto K, Soulay F, Bataillé MP, Avice JC, Masclaux-Daubresse C (2012) Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol 194: 732-740
15. Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156: 1033-1040
16. Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339-2351
17. Hobbie L, Estelle M (1995) The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J 7: 211-220
18. Hur YJ, Yi YB, Lee JH, Chung YS, Jung HW, Yun DJ, Kim KM, Park DS, Kim DH (2012) Molecular cloning and characterization of OsUPS, a U-box containing E3 ligase gene that respond to phosphate starvation in rice (Oryza sativa). Mol Biol Rep 39: 5883-5888
19. 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
20. 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
21. Lynch JP, Brown KM (2001) Topsoil foraging: an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225-237
22. Malamy JE, Ryan KS (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol 127: 899-909
23. Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24: 559-567
24. Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, et al (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108: 18512-18517
25. Mudgil Y, Shiu S-H, Stone SL, Salt JN, Goring DR (2004) A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiol 134: 59-66
26. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-497
27. 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
28. 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
29. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50: 665-693
30. Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3: 182-187
31. Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13: 465-480
32. Rojas-Triana M, Bustos R, Espinosa-Ruiz A, Prat S, Paz-Ares J, Rubio V (2013) Roles of ubiquitination in the control of phosphate starvation responses in plants(f). J Integr Plant Biol 55: 40-53
33. Sakhonwasee S, Abel S (2009) Autophagy sustains the Arabidopsis root meristem during phosphate starvation. Proceedings of the International Plant Nutrition Colloquium XVI. University of California, Davis, CA. http://www.escholarship.org/uc/item/50t6w37f (June 1, 2014)
34. Samuel MA, Mudgil Y, Salt JN, Delmas F, Ramachandran S, Chilelli A, Goring DR (2008) Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol 147: 2084-2095
35. Shiu SH, Bleecker AB (2001a) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001: re22
36. Shiu SH, Bleecker AB (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98: 10763-10768
37. Stone SL, Anderson EM, Mullen RT, Goring DR (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15: 885-898
38. Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10: 946-954
39. Tamura K, Shimada T, Ono E, Tanaka Y, Nagatani A, Higashi SI, Watanabe M, Nishimura M, Hara-Nishimura I (2003) Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J 35: 545-555
40. Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138: 2097-2110
41. Wang X, Yi K, Tao Y, Wang F, Wu Z, Jiang D, Chen X, Zhu L, Wu P (2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29: 1924-1935
42. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126: 875-882
43. Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42: 535-546
44. Yee D, Goring DR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60: 1109-1121