Crucial roles of sucrose and microRNA399 in systemic signaling of P deficiency: A tale of two team players?

Plant Signaling and Behavior

Volumn 5, Issue 12, 2010, Pages

  Liu, Junqi ^a,b   Vance, Carroll P ^a,c  

^a Dep of Agronomy and Plant Genetics   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

MicroRNA399; P deficiency; Sucrose; Systemic signaling

Indexed keywords

MICRORNA; PHOSPHORUS; SUCROSE;

GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHLOEM; REVIEW; SIGNAL TRANSDUCTION;

GENE EXPRESSION REGULATION, PLANT; MICRORNAS; PHLOEM; PHOSPHORUS; SIGNAL TRANSDUCTION; SUCROSE;

EID: 79551675071     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.5.12.13293     Document Type: Review

References (58)

1. Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytol 2003; 157:423-447.
2. Gilbert N. The disappearing nutrient. Nature 2009; 461:716-718.
3. Hammond JP, White PJ. Sucrose transport in the phloem: integrating root response to phosphorus starvation. J Exp Bot 2008; 59:93-109.
4. Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP. Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 2005; 41:257-268.
5. Müller R, Morant M, Jarmer H, Nilsson L, Nielsen TH. Genome-wide analysis of Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 2007; 143:156-171.
6. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG. Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 2007; 225:907-918.
7. Bari R, Pant BD, Stitt M, Scheible WR. PHO2, microRNA399 and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 2006; 141:988-999.
8. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 2006; 18:412-421.
9. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. A miRNA involved in phosphate-starvation responses in Arabidopsis. Curr Biol 2005; 15:2038-2043.
10. Chiou TJ, Bush DR. Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci USA 1998; 95:4784-4788.
11. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 2008; 53:739-749.
12. Pant BD, Buhtz A, Kehr J, Scheible WR. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 2008; 53:731-738.
13. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, et al. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 2008; 147:732-746.
14. Liu TY, Chang CY, Chiou TJ. The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 2009; 12:312-319.
15. Chiou TJ. The role of microRNAs in sensing nutrient stress. Plant Cell Environ 2007; 30:323-332.
16. Doerner P. Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 2008; 11:536-540.
17. Tesfaye M, Liu J, Allan DL, Vance CP. Genomic and genetic control of phosphate stress in legumes. Plant Physiol 2007; 144:594-603.
18. Vance CP. QTLs, epigenetics, sugars and miRNAs: Quatern In phosphate acquisition and use. Plant Physiol 2010; In Press.
19. Ford BG. The role of long-distance signaling in plant responses to nitrate and other nutrients. J Exp Bot 2002; 53:39-43.
20. Smeekens S. Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 2000; 51:49-81.
21. Cakmak I, Hengeler C, Marschner H. Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium-deficiency in bean plants. J Exp Bot 1994; 45:1251-1257.
22. Hermans C, Hammond JP, White PJ, Verbruggen N. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 2006; 11:610-617.
23. Hernández G, Ramirez M, Valdés-Lopez O, Tesfaye M, Graham MA, Czechowski T, et al. Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 2007; 144:752-767.
24. Fredeen AL, Rao IM, Terry N. Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol 1989; 89:225-230.
25. Ciereszko I, Gniazdowska A, Mikulska M, Rychter AM. Assimilate translocation in bean plants (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 1996; 149:343-348.
26. Ciereszko I, Barbachowska A. Sucrose metabolism in leaves and roots of bean (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 2000; 156:640-644.
27. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, et al. Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signaling. Plant Cell Environ 2003; 26:1053-1066.
28. Ciereszko I, Johabsson H, Kleczkowski LA. Interactive effects of phosphate deficiency, sucrose and light/dark conditions on gene expression of UDP-glucose pyrophosphorylase in Arabidopsis. J Plant Physiol 2005; 162:343-353.
29. Nacry P, Canivene 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; 138:2061-2074.
30. Zhou K, Yamagishi M, Osaki M, Masuda K. Sugar signaling mediates cluster root formation and phosphorus starvation-induced gene expression in white lupin. J Exp Bot 2008; 59:2749-2756.
31. Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, et al. Differential effects of sucrose and auxin on localized phosphate deficiencyinduced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 2007; 144:232-247.
32. Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J. Interaction between phosphate-starvation, sugar and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 2005; 138:847-857.
33. Lejay L, Gansel X, Cerezo M, Tilland P, Muller C, Krap A, et al. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 2003; 15:2218-2232.
34. Lejay L, Wirth J, Pervent M, Cross JMF, Tillard P, Gojon A. Oxidative pentose phosphate pathwaydependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol 2008; 146:2036-2053.
35. Zakhleniuk OV, Raines CA, Lloyd JC. pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta 2001; 212:529-534.
36. Lloyd JC, Zakhleniuk OV. Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 2004; 55:1221-1230.
37. Klein D, Morcuende R, Stitt M, Krapp A. Regulation of nitrate reductase expression in leaves by nitrate and nitrogen metabolism is completely overridden when sugars fall below a critical level. Plant Cell Environ 2000; 23:863-871.
38. Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, et al. Steps towards an integrated view of nitrogen metabolism. J Exp Bot 2002; 53:959-970.
39. Burleigh SH, Harrison M. The downregulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 1999; 119:241-248.
40. López-Bucio J, Cruiz-Ramirez A, Herrera-Estrella L. The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 2003; 6:280-287.
41. 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; 39:792-796.
42. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S. Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 2004; 37:801-814.
43. Ticconi C, Lucero R, Sakhonwasee S, Adamson A, Creff A, Nussaume L, et al. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci USA 2009; 106:14174-14179.
44. Liu J, Allan DL, Vance CP. Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Mol Plant 2010; 3:428-437.
45. Chen X. Small RNAs-secrets and surprises of the genome. Plant J 2010; 61:941-958.
46. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 2006; 57:19-53.
47. Mallory AC, Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nat Genet 2006; 38:31-36.
48. Sunkar R, Chinnusamy V, Zhu JK. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 2007; 12:301-309.
49. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, et al. Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 2009; 57:313-321.
50. Sunkar R, Zhu JK. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 2004; 16:2001-2019.
51. Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M. Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 2007; 282:16369-16378.
52. Valdés-Lopez O, Yang SS, Aparicio-Fabre R, Graham P, Reyes JL, Vance CP, et al. MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 2010; 187:805-818.
53. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, et al. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 2009; 151:2120-2132.
54. 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; 141:1000-1011.
55. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 2007; 39:1033-1037.
56. Pasquinelli AE. Paring miRNAs through pairing. Science 2010; 328:1494-1495.
57. Ameres SL, Horwich MD, Hung JH, Xu J, Ghildiyal M, Weng Z, et al. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010; 328:1534-1539.
58. Cazalla D, Yario T, Steitz J. Downregulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 2010; 328:1563-1566.