Interaction between glucose and brassinosteroid during the regulation of lateral root development in arabidopsis

Plant Physiology

Volumn 168, Issue 1, 2015, Pages 307-320

  Gupta, Aditi ^a   Singh, Manjul ^a   Laxmi, Ashverya ^a  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; ATHXK1 PROTEIN, ARABIDOPSIS; BRASSINOSTEROID; GLUCOSE; HEXOKINASE; INDOLEACETIC ACID DERIVATIVE;

ARABIDOPSIS; BIOLOGICAL MODEL; DRUG EFFECTS; EPISTASIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMOZYGOTE; METABOLISM; MUTATION; PHENOTYPE; PHOTOSYNTHESIS; PLANT ROOT; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; BRASSINOSTEROIDS; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GLUCOSE; HEXOKINASE; HOMOZYGOTE; INDOLEACETIC ACIDS; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PHOTOSYNTHESIS; PLANT ROOTS; SIGNAL TRANSDUCTION;

EID: 84930624345     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.256313     Document Type: Article

References (63)

1. Baena-González E (2010) Energy signaling in the regulation of gene expression during stress. Mol Plant 3: 300–313
2. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938–942
3. Bajguz A (2009) Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. J Plant Physiol 166: 882–886
4. Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol 134: 1624–1631
5. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a commonmodule for plant organ formation. Cell 115: 591–602
6. Booker KS, Schwarz J, Garrett MB, Jones AM (2010) Glucose attenuation of auxin-mediated bimodality in lateral root formation is partly coupled by the heterotrimeric G protein complex. PLoS ONE 5: e12833
7. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8: 165–171
8. Chen JG, Jones AM (2004) AtRGS1 function in Arabidopsis thaliana. Methods Enzymol 389: 338–350
9. Chen JG, Willard FS, Huang J, Liang J, Chasse SA, Jones AM, Siderovski DP (2003) A seven-transmembrane RGS protein that modulates plant cell proliferation. Science 301: 1728–1731
10. Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, Park J, Han S, Beeckman T, Bennett MJ, et al (2014) A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat Cell Biol 16: 66–76
11. Cuesta C, Wabnik K, Benková E (2013) Systems approaches to study root architecture dynamics. Front Plant Sci 4: 537
12. Den Herder G, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15: 600–607
13. De Smet I (2012) Lateral root initiation: one step at a time. New Phytol 193: 867–873
14. Duan L, Dietrich D, Ng CH, Chan PM, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25: 324–341
15. Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63: 3367–3377
16. Freixes S, Thibaud MC, Tardieu F, Muller B (2002) Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings. Plant Cell Environ 25: 1357–1366
17. Fu Y, Lim S, Urano D, Tunc-Ozdemir M, Phan NG, Elston TC, Jones AM (2014) Reciprocal encoding of signal intensity and duration in a glucosesensing circuit. Cell 156: 1084–1095
18. 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
19. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69: 437–449
20. Garay-Arroyo A, De La Paz Sánchez M, García-Ponce B, Azpeitia E, Alvarez-Buylla ER (2012) Hormone symphony during root growth and development. Dev Dyn 241: 1867–1885
21. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. J Exp Bot 55: 253–264
22. Goetz M, Godt DE, Roitsch T (2000) Tissue-specific induction of the mRNA for an extracellular invertase isoenzyme of tomato by brassinosteroids suggests a role for steroid hormones in assimilate partitioning. Plant J 22: 515–522
23. Gonzali S, Novi G, Loreti E, Paolicchi F, Poggi A, Alpi A, Perata P (2005) A turanose-insensitive mutant suggests a role for WOX5 in auxin homeostasis in Arabidopsis thaliana. Plant J 44: 633–645
24. Gupta A, Singh M, Jones AM, Laxmi A (2012) Hypocotyl directional growth in Arabidopsis: a complex trait. Plant Physiol 159: 1463–1476
25. Hardtke CS, Dorcey E, Osmont KS, Sibout R (2007) Phytohormone collaboration: zooming in on auxin-brassinosteroid interactions. Trends Cell Biol 17: 485–492
26. Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugarsignaling mechanism in Arabidopsis. Plant Cell 18: 1226–1238
27. Jung JK, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4: 186
28. Kircher S, Schopfer P (2012) Photosynthetic sucrose acts as cotyledonderived long-distance signal to control root growth during early seedling development in Arabidopsis. Proc Natl Acad Sci USA 109: 11217–11221
29. Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, et al (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19: 3889–3900
30. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47: 788–792
31. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Marée AFM, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6: e307
32. 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
33. Laxmi A, Paul LK, Peters JL, Khurana JP (2004) Arabidopsis constitutive photomorphogenic mutant, bls1, displays altered brassinosteroid response and sugar sensitivity. Plant Mol Biol 56: 185–201
34. Lewis DR, Negi S, Sukumar P, Muday GK (2011) Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138: 3485–3495
35. Li L, Xu J, Xu ZH, Xue HW (2005) Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17: 2738–2753
36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402–408
37. Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67–77
38. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33–44
39. Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32: 149–158
40. Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 4: e4502
41. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332–336
42. Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443: 458–461
43. Mudgil Y, Uhrig JF, Zhou J, Temple B, Jiang K, Jones AM (2009) Arabidopsis N-MYC DOWNREGULATED-LIKE1, a positive regulator of auxin transport in a G protein-mediated pathway. Plant Cell 21: 3591–3609
44. Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2: E258
45. Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13: 2441–2454
46. Ohto MA, Hayashi S, Sawa S, Hashimoto-Ohta A, Nakamura K (2006) Involvement of HLS1 in sugar and auxin signaling in Arabidopsis leaves. Plant Cell Physiol 47: 1603–1611
47. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ ASL genes in Arabidopsis. Plant Cell 19: 118–130
48. Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. The Arabidopsis Book 6: e0117, doi/10.1199/tab.0117
49. Rognoni S, Teng S, Arru L, Smeekens SCM, Perata P (2007) Sugar effects on early seedling development in Arabidopsis. Plant Growth Regul 52: 217–228
50. Sairanen I, Novák O, Pénćík A, Ikeda Y, Jones B, Sandberg G, Ljung K (2012) Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24: 4907–4916
51. Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57: 67–79
52. Singh M, Gupta A, Laxmi A (2014a) Glucose control of root growth direction in Arabidopsis thaliana. J Exp Bot 65: 2981–2993
53. Singh M, Gupta A, Laxmi A (2014b) Glucose and phytohormone interplay in controlling root directional growth in Arabidopsis. Plant Signal Behav 9: e29219
54. Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10: 946–954
55. Swarup R, Péret B (2012) AUX/LAX family of auxin influx carriers: an overview. Front Plant Sci 3: 225
56. Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171–182
57. Urano D, Chen JG, Botella JR, Jones AM (2013) Heterotrimeric G protein signalling in the plant kingdom. Open Biol 3: 120186
58. Urano D, Phan N, Jones JC, Yang J, Huang J, Grigston J, Taylor JP, Jones AM (2012) Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nat Cell Biol 14: 1079–1088
59. Vandenbussche F, Suslov D, De Grauwe L, Leroux O, Vissenberg K, Van der Straeten D (2011) The role of brassinosteroids in shoot gravitropism. Plant Physiol 156: 1331–1336
60. Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci USA 105: 9829–9834
61. Vicentini R, Felix JdeM, Dornelas MC, Menossi M (2009) Characterization of a sugarcane (Saccharum spp.) gene homolog to the brassinosteroid insensitive1-associated receptor kinase 1 that is associated to sugar content. Plant Cell Rep 28: 481–491
62. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496: 181–186
63. Yuan TT, Xu HH, Zhang KX, Guo TT, Lu YT (2014) Glucose inhibits root meristemgrowth via ABA INSENSITIVE 5, which represses PIN1 accumulation and auxin activity in Arabidopsis. Plant Cell Environ 37: 1338–1350