A re-assessment of sucrose signaling involved in cluster-root formation and function in phosphate-deficient white lupin (Lupinus albus)

Physiologia Plantarum

Volumn 154, Issue 3, 2015, Pages 407-419

  Wang, Zhengrui ^a   Shen, Jianbo ^b   Ludewig, Uwe ^a   Neumann, Günter ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LUPINUS ALBUS; PROTEACEAE;

ACID PHOSPHATASE; CITRIC ACID; PHOSPHATE; PHOSPHOENOLPYRUVATE CARBOXYLASE; PLANT PROTEIN; SUCROSE;

DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROPONICS; LUPIN; METABOLISM; PH; PLANT ROOT; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTOR;

ACID PHOSPHATASE; CITRATES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, PLANT; HYDROGEN-ION CONCENTRATION; HYDROPONICS; LUPINUS; PHOSPHATES; PHOSPHOENOLPYRUVATE CARBOXYLASE; PLANT PROTEINS; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SUCROSE; TIME FACTORS;

EID: 84922458336     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12311     Document Type: Article

References (63)

1. Barrett-Lennard EG, Dracup M (1988) A porous agar medium for improving the growth of plants under sterile conditions. Plant Soil 108: 294-298
2. Blakeney AB, Mutton LL (1980) A simple colorimetric method for the determination of sugars in fruit and vegetables. J Sci Food Agric 31: 889-897
3. Chincinska I, Gier K, Krügel U, Liesche J, He H, Grimm B, Harren FJM, Cristescu SM, Kühn C (2013) Photoperiodic regulation of the sucrose transporter StSUT4 affects the expression of circadian-regulated genes and ethylene production. Front Plant Sci 4: 26
4. Chiou T, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci USA 95: 4784-4788
5. Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12: 285-292
6. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108: 183-200
7. Dinkelaker B, Hengeler C, Neumann G, Eltrop L, Marschner H (1997) Root exudates and mobilization of nutrients. In: Rennenberg H, Eschrich W, Ziegler H (eds) Trees: Contributions to Modern Tree Physiology. Backhuys Publishers, Leiden, pp 441-452
8. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69: 437-449
9. Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70: 107-124
10. Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8: 93-102
11. Gilbert GA, Knight JD, Vance CP, Allan DL (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ 22: 801-810
12. Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot 85: 921-928
13. Hagström J, James WM, Skene KR (2001) A comparison of structure, development and function in cluster roots of Lupinus albus L. under phosphate and iron stress. Plant Soil 232: 81-90
14. Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59: 93-109
15. Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156: 1033-1040
16. Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144: 232-247
17. Jeong S, Das PK, Jeoung SC, Song J, Lee HK, Kim Y, Kim WJ, Park YI, Yoo S, Choi S, Choi G, Park Y (2010) Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. Plant Physiol 154: 1514-1531
18. Johnson JF, Vance CP, Allan DL (1996) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol 112: 31-41
19. Kania A, Langlade N, Martinoia E, Neumann G (2003) Phosphorus deficiency-induced modifications in citrate catabolism and in cytosolic pH as related to citrate exudation in cluster-roots of white lupin. Plant Soil 248: 117-127
20. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225: 907-918
21. Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant Cell Environ 21: 467-478
22. Kobayashi H, Saka H (2000) Relationship between ethylene evolution and sucrose content in excised leaf blades of rice. Plant Prod Sci 3: 398-403
23. Lambers H, Bishop JG, Hopper SD, Laliberté E, Zúñiga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Ann Bot 110: 329-348
24. Lei M, Liu Y, Zhang B, Zhao Y, Wang X, Zhou Y, Raghothama KG, Liu D (2011) Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol 156: 1116-1130
25. Li H, Shen J, Zhang F, Lambers H (2010) Localized application of soil organic matter shifts distribution of cluster-roots of white lupin in the soil profile due to localized release of phosphorus. Ann Bot 105: 585-593
26. Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41: 257-268
27. 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
28. Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd Edn. Academic Press, London, pp 131-183
29. Marschner H, Römheld V, Cakmak I (1987) Root-induced changes of nutrient availability in the rhizosphere. J Plant Nutr 10: 1175-1184
30. Massonneau A, Langlade N, Léon S, Smutny J, Vogt E, Neumann G, Martinoia E (2001) Metabolic changes associated with cluster-root development in white lupin (Lupinus albus L.): relationship between organic acid excretion, sucrose metabolism and energy status. Planta 213: 534-542
31. Meir S, Riov J, Philosoph-Hadas S, Aharoni N (1989) Carbohydrates stimulate ethylene production in tobacco leaf discs. III. Stimulation of enzymic hydrolysis of indole-3-acetyl-L-alanine. Plant Physiol 90: 1246-1248
32. Meng ZB, Chen LQ, Suo D, Li GX, Tang CX, Zheng SJ (2012) Nitric oxide is the shared signaling molecule in phosphorus- and iron-deficiency-induced formation of cluster-roots in white lupin (Lupinus albus). Ann Bot 109: 1055-1064
33. Meng ZB, You XD, Suo D, Chen YL, Tang C, Yang JL, Zheng SJ (2013) Root-derived auxin contributes to the phosphorus-deficiency-induced cluster-root formation in white lupin (Lupinus albus). Physiol Plant 148: 481-489
34. Neumann G, Martinoia E (2002) Cluster-roots - an underground adaptation for survival in extreme environments. Trends Plant Sci 7: 162-167
35. Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211: 121-130
36. Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface, 2nd Edn. CRC Press, Boca Raton, FL, pp 23-72
37. Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208: 373-382
38. Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Römheld V, Martinoia E (2000) Physiological aspects of cluster-root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann Bot 85: 909-919
39. O'Rourke JA, Yang SS, Miller SS, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu ZJ, Allan D, Gronwald JW, Vance CP (2013) An RNA-seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161: 705-724
40. Philosoph-Hadas S, Meir S, Aharoni N (1985) Carbohydrates stimulate ethylene production in tobacco leaf discs: II. Sites of stimulation in the ethylene biosynthesis pathway. Plant Physiol 78: 139-143
41. Purnell H (1960) Studies of the family Proteaceae. I. Anatomy and morphology of the roots of some Victorian species. Aust J Bot 8: 38-50
42. Qin L, He J, Lee SK, Dodd IC (2007) An assessment of the role of ethylene in mediating lettuce (Lactuca sativa) root growth at high temperatures. J Exp Bot 58: 3017-3024
43. Rodriguez-Medina C, Atkins CA, Mann AJ, Jordan ME, Smith PMC (2011) Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.). BMC Plant Biol 11: 36
44. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709
45. Shane MW, De Vos M, De Roock S, Lambers H (2003) 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
46. Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2: 410-418
47. Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster-root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Sci 168: 837-845
48. Sinha AK, Hofmann MG, Römer U, Köckenberger W, Elling L, Roitsch T (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiol 128: 1480-1489
49. Skene KR (1998) Cluster-roots: some ecological considerations. J Ecol 86: 1060-1064
50. Skene KR (2000) Pattern formation in cluster-roots: some developmental and evolutionary considerations. Ann Bot 85: 901-908
51. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13: 273-278
52. Straub D, Yang H, Liu Y, Tsap T, Ludewig U (2013) Root ethylene signaling is involved in Miscanthus sinensis growth promotion by the bacterial endophyte Herbaspirillum frisingense GSF30T. J Exp Bot 64: 4603-4615
53. Torrey JG (1976) Root hormones and plant growth. Annu Rev Plant Physiol 27: 435-459
54. Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003a) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248: 99-116
55. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003b) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131: 1064-1079
56. von Wirén N, Römheld V, Shioiri T, Marschner H (1995) Competition between microorganisms and roots of barley and sorghum for iron accumulated in the root apoplasm. New Phytol 130: 511-521
57. Wang BL, Tang XY, Cheng LY, Zhang AZ, Zhang WH, Zhang FS, Liu JQ, Cao Y, Allan DL, Vance CP, Shen JB (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187: 1112-1123
58. Wang Z, Rahman ABMM, Wang G, Ludewig U, Shen J, Neumann G (2014a) Hormonal interactions during cluster-root development in phosphate-deficient white lupin (Lupinus albus L.) J Plant Physiol published online http://dx.doi.org/10.1016/j.jplph.2014.10.022.
59. Wang Z, Straub D, Yang H, Kania A, Shen J, Ludewig U, Neumann G (2014b) The regulatory network of cluster-root function and development in phosphate-deficient white lupin (Lupinus albus) identified by transcriptome sequencing. Physiol Plant 151: 323-338
60. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126: 875-882
61. Wind J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71: 1610-1614
62. Zhou K, Yamagishi M, Osaki M, Masuda K (2008) Sugar signaling mediates cluster-root formation and phosphorus starvation-induced gene expression in white lupin. J Exp Bot 59: 2749-2756
63. Zhu Y, Yan F, Zörb C, Schubert S (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46: 892-901