Involvement of lignin and hormones in the response of woody poplar taproots to mechanical stress

Physiologia Plantarum

Volumn 146, Issue 1, 2012, Pages 39-52

  Trupiano, Dalila ^a   Di Iorio, Antonino ^b   Montagnoli, Antonio ^b   Lasserre, Bruno ^a   Rocco, Mariapina ^c   Grosso, Alessandro ^d   Scaloni, Andrea ^e   Marra, Mauro ^d   Chiatante, Donato ^b   Scippa, Gabriella S ^a  

^a UNIVERSITY OF MOLISE   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

^c UNIVERSITY OF SANNIO   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

LIGNIN; PHYTOHORMONE;

ADAPTATION; ARTICLE; MECHANICAL STRESS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT ROOT; POPULUS;

ADAPTATION, PHYSIOLOGICAL; LIGNIN; PLANT GROWTH REGULATORS; PLANT ROOTS; POPULUS; STRESS, MECHANICAL; STRESS, PHYSIOLOGICAL;

POPULUS; POPULUS NIGRA;

EID: 84865075873     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2012.01601.x     Document Type: Article

References (97)

1. Aloni R, Tollier T, Monties B (1990) The role of auxin and gibberellin in controlling lignin formation in primary phloem fibers and in xylem of Coleus blumei stems. Plant Physiol 94: 1743-1747
2. Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 97: 883-893
3. Anten NPR, Casado-Garcia R, Nagashima H (2005) Effects of mechanical stress and plant density on mechanical characteristics, growth and lifetime reproduction of tobacco plants. Am Naturalist 166: 650-660
4. Aubert D, Chevillard M, Dorne AM, Arlaud G, Herzog M (1998) Expression patterns of GASA genes in Arabidopsis thaliana: the GASA4 gene is up-regulated by gibberellins in meristematic regions. Plant Mol Biol 36: 871-883
5. Azri W, Chambonc C, Herbettea S, Brunela N, Coutand C, Leplee JH, Rejebb IB, Ammarb S, Juliena JL, Roeckel- Reveta P (2009) Proteome analysis of apical and basal regions of poplar stems under gravitropic stimulation. Physiol Plant 136: 193-208
6. Baba K, Karlberg A, Schmidt J, Schrader J, Hvidsten TR, Bako L, Bhalerao RP (2011) Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen. Proc Natl Acad Sci USA 108: 3418-3423
7. Barnett JR (1981) Secondary xylem cell development. In: Barnett JR(ed) Xylem Cell Development. Castle House Publications, Tunbridge Wells, UK, pp 47-95
8. Ben-Nissan G, Lee JY, Borohov A, Weiss D (2004) GIP, a Petunia hybrida GA-induced cysteine-rich protein: a possible role in shoot elongation and transition to flowering. Plant J 37: 229-238
9. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545-580
10. Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165: 373-389
11. Braam J, Davis RW (1990) Rain-, wind-, and touch- induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60: 357-364
12. 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: 65-171
13. Chen THH, Howe GT, Bradshaw HD (2002) Molecular genetic analysis of dormancy related traits in poplars. Weed Sci 50: 232-240
14. Chiatante D, Scippa GS (2006) Root architecture: influence of metameric organization and emission of lateral roots. Plant Biosyst 140: 307-320
15. Chiatante D, Scippa GS, Di Iorio A, Sarnataro M (2001) Root architecture modified by mechanical stress in seedlings of Fraxinus ornus L. and Spartium junceum L. growing on slopes. In: Radoglou K (ed) Proceedings of the International Conference on Forest Research: A Challenge for an Integrated European approach. NAGEF - Forest Research Institute, Thessaloniki, Greece, pp 477-482
16. Chiatante D, Scippa GS, Di Iorio A, Sarnataro M (2003a) The influence of steep slopes on root system development. J Plant Growth Regul 21: 247-260
17. Chiatante D, Sarnataro M, Fusco S, Di Iorio A, Scippa GS(2003b) Modification of root morphological parameters and root architecture in seedlings of Fraxinus ornus L. and Spartium junceum L. growing on slopes. Plant Biosyst 1: 47-55
18. Chiatante D, Beltotto E, Onelli E, Di Iorio A, Montagnoli A, Scippa GS (2010) New branch roots produced by vascular cambium derivatives in woody parental roots of Populus nigra L. Plant Biosyst 144: 420-433
19. Cucchi V, Meredieu C, Stokes A, Berthier S, Bert D, Najar M, Denis A, Lastennet R (2004) Root anchorage of inner and edge trees in stands of Maritime pine (Pinus pinaster Ait.) growing in different podzolic soil conditions. Trees Struct Funct 18: 460-466
20. Danjon F, Bert D, Godin C, Trichet P (1999) Structural root architecture of 5-year-old Pinus pinaster measured by 3D digitising and analysed with AMAPmod. Plant Soil 217: 49-63
21. De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33: 543-555
22. De Smet I, Zhang H, Inzé D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11: 1360-1385
23. De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inzé D, Bennett MJ, Beeckman T (2007) Auxin dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681-690
24. Di Iorio A, Lasserre B, Scippa GS, Chiatante D (2005) Root system architecture of Quercus pubescens trees growing on different sloping conditions. Ann Bot 95: 351-361
25. Di Michele M, Chiatante D, Plomion C, Scippa GS (2006) A proteomic analysis of Spanish broom (Spartium junceum L.) root growing on a slope condition. Plant Sci 170: 926-935
26. Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I, van der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R, Laux T, Palme K (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci USA 105: 18818-18823
27. Doster MA, Bostock RM (1988) Quantification of lignin formation in almond bark in response to wounding and infection by Phytophthora species. Phytopathology 78: 473-477
28. Druart N, Johansson A, Baba K, Schrader J, Sjödin A, Bhalerao RR, Resman L, Trygg J, Moritz T, Bhalerao RP (2007) Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage specific modulation of transcriptional and metabolic networks. Plant J 50: 557-573
29. Dupuy L, Fourcaud T, Stokes A (2005) A numerical investigation into the influence of soil type and root architecture on tree anchorage. Plant Soil 278: 119-134
30. Dupuy L, Fourcaud T, Lac P, Stokes A (2007) A generic 3D finite element model of tree anchorage integrating soil mechanics and real root system architecture. Am J Bot 94: 1506-1514
31. Fourcaud T, Ji JN, Zhang ZQ, Stokes A (2008) Understanding the impact of root morphology on overturning mechanisms: a modelling approach. Ann Bot 101: 1267-1280
32. Fredericksen TS, Hedden RL, Williams SA (1994) The effect of stem bending on hydraulic conductivity and wood strength of loblolly pine. Can J For Res 24: 442-446
33. Frigerio M, Alabadi D, Perez-Gomez J, Gracia-Cacel L, Phillips AL, Hedden P, Blazquez A (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142: 553-563
34. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi KS, Shinozak K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signalling networks. Curr Opin Plant Bio l9: 436-442
35. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69: 437-449
36. Furukawa T, Sakaguchi N, Shimada H (2006) Two OsGASR genes, rice GAST homologue genes that are abundant in proliferating tissues, show different expression patterns in developing panicles. Genes Genet Syst 81: 171-180
37. Godin C, Costes E, Caraglio Y (1997) Exploring plant topological structure with the AMAPmod software: an outline. Silva Fenn 31: 355-366
38. Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones.Plant Cell 22: 623-639
39. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Van Montagu M, Inzé D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proc Natl Acad Sci USA 101: 5146-5151
40. Howe GT, Hackett WP, Furnier GR, Klevorn RE (1995) Photoperiodic responses of a northern and southern ecotype of black cottonwood. Physiol Plant 93: 695-708
41. Hu WJ, Lung J, Harding SA, Popko JL, Ralph J, Stokke DD, Tsai CJ, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotech 17: 808-812
42. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55: 335-347
43. Jaffe MJ (1973) Thigmomorphogenesis: the response of plant growth and development to mechanical stimulation. Planta 114: 143-157
44. Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44: 283-307
45. Ko JH, Han KH, Park S, Yang J (2004) Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol 135: 1069-1083
46. Kovach WL (1994) Oriana for Windows, Version 2.01. Kovach Computing Services, Pentraeth, Wales, UK
47. Kus JV, Zaton K, Sarkar R, Cameron RK (2002) Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell 14: 479-490
48. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Maree AF, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6: e307
49. Li C, Puhakainen T, Welling A, Vihera-Aarnio A, Ernstsen A, Junttila O, Heino P, Palva ET (2002) Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiol Plant 116: 478-488
50. Lindstrom A, Rune G (1999) Root deformation in plantations of container grown Scots pine trees: effects on root growth, tree stability and stem straightness. Plant Soil 217: 29-37
51. Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280-287
52. Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17: 2186-2203
53. Lucas M, Godin C, Jay-Allemand C, Laplaze L (2008a) Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J Exp Bot 59: 55-66
54. Lucas M, Guedon Y, Jay-Allemand C, Godin C, Laplaze L (2008b) An auxin transport-based model of root branching in Arabidopsis thaliana. PLoS One 3: e3673
55. Malamy J (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67-77
56. Mardia KV, Jupp PE (2000) Directional Statistics. Wiley, Chichester, UK
57. Masle J (2002) High soil strength: mechanical forces at play on root morphogenesis and in root:shoot signaling. In Waisel Y, Eshel A, Kafkafi U (eds) Plant Roots, The Hidden Half, 3rd Edn. Marcel Dekker, New York, NY, pp 807-819
58. Mitchell CA (1977) Influence of mechanical stress on auxin-stimulated growth on excised pea stem sections. Physiol Plant 41: 412-424
59. Okada K, Shimura Y (1994) Modulation of root growth by physical stimuli. In Meyerowitz EM, Somerville CR (eds) Arabidopsis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 665-668
60. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58: 93-113
61. Pearson K (1957) The Grammar of Science. The Meridian Library, New York, NY
62. Peltola H, Kellomski S, Hassinen A, Granander M (2000) Mechanical stability of Scots pine, Norway spruce and birch: an analysis of tree-pulling experiments in Finland. Forest Ecol Manag 135: 145-153
63. Peret B, de Rybel B, Casimiro I, Benkova I, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14: 399-408
64. Rees DJ, Grace J (1980a) The effect of wind on the extension growth of Pinus contorta Douglas. Forestry 53: 145-153
65. Rees DJ, Grace J (1980b) The effects of shaking on extension growth of Pinus contorta Douglas. Forestry 53: 155-166
66. Richter GL, Monshausen GB, Krol A, Gilroy S (2009) Mechanical stimuli modulate lateral root organogenesis. Plant Physiol 151: 1855-1866
67. Rinne P, Hänninen H, Kaikuranta P, Jalonen JE, Repo T (1997) Freezing exposure releases bud dormancy in Betula pubescens and B. pendula. Plant Cell Environ 20: 1199-1204
68. Rinne P, Welling A, Kaikuranta P (1998) Onset of freezing tolerance in birch (Betula pubescens Ehrh.) involves LEA proteins and osmoregulation and is impaired in an ABA-deficient genotype. Plant Cell Environ 21: 601-611
69. Ruonala R, Rinne PLH, Baghour M, Moritz T, Tuominen H, Kangasjarvi J (2006) Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J 46: 628-640
70. Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100: 10096-101014
71. Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40: 173-187
72. Scippa GS, Di Michele M, Di Iorio A, Costa A, Lasserre B, Chiatante D (2006) The response of Spartium junceum root to slope: anchorage and gene factors. Ann Bot 97: 857-866
73. Scippa GS, Trupiano D, Rocco M, Di Iorio A, Chiatante D (2008) Unravelling the response of poplar (Populus nigra) roots to mechanical stress imposed by bending. Plant Biosyst 142: 401-413
74. Shi L, Olszewski NE (1998) Gibberellin and abscisic acid regulate GAST1 expression at the level of transcription. Plant Mol Biol 38: 1053-1060
75. Sinnott EW (1952) Reaction wood and the regulation of tree form. Am J Bot 39: 69-78
76. Sinoquet H, Rivet P (1997) Measurement and visualisation of the architecture of an adult tree based on a three-dimensional digitising device. Trees 11: 265-270
77. 2+ binding protein and shown environmentally induced and tissue-specific regulation. Plant Cell 6: 1553-1565
78. Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19: 2169-2185
79. Stokes A, Guitard D (1997) Tree root response to mechanical stress. In: Altman A, Waisel Y (eds) Biology of Root Formation and Development. Plenum Press, New York, NY. pp 227-236
80. Stokes A, Nicoll BC, Coutts MP, Fitter AM (1997) Responses of young Sitka spruce clones to mechanical perturbation and nutrition: effects on biomass allocation, root development, and resistance to bending. Can J Forest Res 27: 1049-1057
81. Sundberg B, Uggla C, Tuominen H (2000) Cambial growth and auxin gradients. In: Savidge R, Barnett J, Napier R (eds) Cell and Molecular Biology of Wood Formation. BIOS, Oxford, UK, pp 169-188
82. Taiz L, Zeiger E (2006) Plant Physiology, 4th Edn. Sinauer Associates Inc, Sunderland, MA, pp 764
83. Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. J Exp Bot 51: 1563-1574
84. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific indication of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132: 68-76
85. Telewski FW (1995) Wind induced physiological and developmental responses in trees. In: Coutts MP, Grace J (eds) Wind and Trees. Cambridge University Press, Cambridge, UK, pp 237-263
86. Telewski FW (2006) A unified hypothesis of mechanoperception in plants. Am J Bot 93: 1466-1476
87. Timell TE (1986) Compression Wood in Gymnosperms. Springer-Verlag, Heidelberg, Germany
88. Valinger E, Lundqvist L, Sundberg B (1995) Mechanical bending stress applied during dormancy and (or) growth stimulates stem diameter growth of Scots pine seedlings. Can J Forest Res 25: 886-890
89. Vanneste S, De Rybel B, Beemster GTS, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inzé D, Fukaki H, Beeckman T (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17: 3035-3050
90. Watson AJ (2000) Wind-induced forces in the near-surface lateral roots of Radiata pine. For Ecol Manag 135: 133-142
91. Wareing PF (1969). The control of bud dormancy in seed plants. In: Wareing PF (ed) Dormancy and Survival. Symposia of the Society for Experimental Biology, no. XXIII, pp 241-262
92. Welling A, Kaikuranta P, Rinne P (1997) Photoperiodic induction of dormancy and freezing tolerance in Betula pubescens. Involvement of ABA and dehydrins. Physiol Plant 100: 119-125
93. Welling A, Moritz T, Palva ET, Junttila O (2002) Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiol 129: 1633-1641
94. Wu L, Joshi CP, Chiang VL (2000) A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J 22: 495-502
95. Xu W, Purugganan MM, Polisensky DH, Antosiewicz DM, Fry SC, Braam J (1995) Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7: 1555-1567
96. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35: 155-189
97. Zimmermann R, Sakai H, Hochholdinger F (2010) The gibberellic acid stimulated-like gene family in maize and its role in lateral root development. Plant Physiol 152: 356-365