The root cap at the forefront

Comptes Rendus - Biologies

Volumn 333, Issue 4, 2010, Pages 335-343

  Arnaud, Carole ^a   Bonnot, Clémence ^a   Desnos, Thierry ^a   Nussaume, Laurent ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Arabidopsis thaliana; Environment; Root; Root cap; Sensing

Indexed keywords

WATER;

ANGIOSPERM; ENVIRONMENTAL CHANGE; ROOT; SOIL PROPERTY; STEM;

ARABIDOPSIS; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; EMBRYO DEVELOPMENT; ENVIRONMENTAL CHANGE; GRAVITROPISM; HEREDITY; MOLECULAR MECHANICS; NONHUMAN; NUTRIENT UPTAKE; PHOTOTROPISM; PLANT ENVIRONMENT INTERACTION; PLANT GROWTH; PLANT ROOT; PLANT ROOT CAP; REGULATORY MECHANISM; RHIZOSPHERE; ROOT GROWTH; STEM CELL; WATER TRANSPORT;

ARABIDOPSIS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PLANT PHYSIOLOGICAL PHENOMENA; PLANT ROOTS; SOIL; WATER;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77950371027     PISSN: 16310691     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.crvi.2010.01.011     Document Type: Article

References (121)

1. Drew M.C. Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New phytologist 75 (1975) 479-490
2. Gregory P. Plant roots: growth, activity, and interaction with soils (2006), Wiley-Blackwell, Oxford
3. Barlow P.W. The root cap: cell dynamics, cell differentiation and cap function. Journal of plant growth regulation 21 (2003) 261-286
4. Beeckman T. Root Development (2009), Wiley-Blackwell, Oxford Annual Plant Reviews, volume 37
5. Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K., et al. Cellular organisation of the Arabidopsis thaliana root. Development (1993) 71-84
6. Rost T.L., and Bryant J.A. Root organization and gene expression patterns. Journal of experimental botany 47 (1996) 1613-1628
7. Dolan L., Duckett C.M., Grierson C., Linstead P., Schneider K., Lawson E., et al. Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development (Cambridge) 120 (1994) 2465
8. van den Berg C., Willemsen V., Hage W., Weisbeek P., and Scheres B. Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378 (1995) 62-65
9. Van den Berg C., Willemsen V., Hendriks G., Weisbeek P., and Scheres B. Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390 (1997) 287
10. Clowes F.A.L. Localization of nucleic acid synthesis in root meristems. Journal of experimental botany 7 (1956) 307-312
11. Popham R.A. Zonation of primary and lateral root apices of Pisum sativum. American journal of botany 42 (1955) 267-273
12. Clowes F.A.L. Duration of the mitotic cycle in a meristem. Journal of experimental botany 12 (1961) 283-293
13. Scheres B., Wolkenfelt H., Willemsen V., Terlouw M., Lawson E., Dean C., et al. Embryonic origin of the Arabidopsis primary root and root meristem initials. Development (1994) 2475-2487
14. Rost T.L., Baum S.F., and Nichol S. Root apical organization in Arabidopsis thaliana ecotype ëWSí and a comment on root cap structure. Plant and soil 187 (1996) 91-95
15. Baum S.F., and Rost T.L. Root apical organization in Arabidopsis thaliana 1. Root cap and protoderm. Protoplasma 192 (1996) 178-188
16. Baum S.F., Dubrovsky J.G., and Rost T.L. Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots 1, American Journal of Botany. Botanical Society of America (2002) 908-920
17. Moore R., and McClelen C.E. Ultrastructural aspects of cellular differentiation in the root cap of Zea mays. Canadian journal of botany 61 (1983) 1566-1572
18. Bengough A.G., and McKenzie B.M. Sloughing of root cap cells decreases the frictional resistance to maize (Zea mays L.) root growth. Journal of experimental botany 48 (1997) 885
19. Iijima M., Griffiths B., and Bengough A.G. Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New phytologist 145 (2000) 477-482
20. Iijima M., Higuchi T., Barlow P.W., and Bengough A.G. Root cap removal increases root penetration resistance in maize (Zea mays L.). Journal of experimental botany 54 (2003) 2105
21. Iijima M., Barlow P.W., and Bengough A.G. Root cap structure and cell production rates of maize (Zea mays) roots in compacted sand. New phytologist 160 (2003) 127-134
22. Iijima M., Morita S., and Barlow P.W. Structure and function of the root cap. Plant production science 11 (2008) 17-27
23. Noriega A., Cervantes E., and Tocino. Ethylene responses in Arabidopsis seedlings include the reduction of curvature values in the root cap. Journal of Plant Physiology 165 (2007) 960-966
24. Sievers A., Braun M., Monshausen G.B., Waisel Y., Eshel A., and Kafkafi U. The root cap: structure and function. Plant roots: The hidden half. 3rd ed. (2002), Marcel Dekker, New York 33-47
25. Williams B.C. The structure of the meristematic root tip and origin of the primary tissues in the roots of vascular plants. American journal of botany 34 (1947) 455-462
26. Barlow P.W., Hawes C.R., and Horne J.C. Structure of amyloplasts and endoplasmic reticulum in the root caps of Lepidium sativum and Zea mays observed after selective membrane staining and by high-voltage electron microscopy. Planta 160 (1984) 363-371
27. B.E. Juniper, F.A.L. Clowes, Cytoplasmic organelles and cell growth in root caps, Nature 208 (1965); 864-865.
28. Rougier M. Secretory activity of the root cap. Encyclopedia of plant physiology New series 13 (1981) 542-574
29. Hawes M.C. Living plant cells released from the root cap: A regulator of microbial populations in the rhizosphere?. Plant and Soil 129 (1990) 19-27
30. Vermeer J., and McCully M.E. The rhizosphere in Zea: new insight into its structure and development. Planta 156 (1982) 45
31. Hawes M.C., and Pueppke S.G. Sloughed peripheral root cap cells: yield from different species and callus formation from single cells. American Journal of Botany 73 (1986) 1466-1473
32. Knudson L. Viability of detached root-cap cells. American Journal of Botany (1919) 309-310
33. Brigham L.A., Woo H.H., Nicoll S.M., and Hawes M.C. Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiology 109 (1995) 457
34. Hawes M.C., and Lin H.J. Correlation of pectolytic enzyme activity with the programmed release of cells from root caps of pea (Pisum sativum). Plant Physiology 94 (1990) 1855
35. Hawes M.C., Brigham L.A., Wen F., Woo H.H., and Zhu Y. Function of Root Border Cells in Plant Health: Pioneers 1 in the Rhizosphere. Annual review of phytopathology 36 (1998) 311-327
36. Hawes M., Bengough G., Cassab G., and Ponce G. Root caps and rhizosphere. Journal of plant growth regulation 21 (2003) 352-367
37. Driouich A., Durand C., and VicrÈ-Gibouin M. Formation and separation of root border cells. Trends in plant science 12 (2007) 14-19
38. Stephenson M.B., and Hawes M.C. Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant physiology 106 (1994) 739
39. Wen F., Zhu Y., and Hawes M.C. Effect of pectin methylesterase gene expression on pea root development. The Plant cell online 11 (1999) 1129
40. Campillo E., Abdel-Aziz A., Crawford D., and Patterson S.E. Root cap specific expression of an endo-1, 4-glucanase (cellulase): a new marker to study root development in Arabidopsis. Plant molecular biology 56 (2004) 309-323
41. Miller I., and Moore R. Defective secretion of mucilage is the cellular basis for agravitropism in primary roots of Zea mays cv. Ageotropic. Annals of botany 66 (1990) 169
42. Vicre M., Santaella C., Blanchet S., Gateau A., and Driouich A. Root border-like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria. Plant physiology 138 (2005) 998-1008
43. Durand C., Vicre-Gibouin M., Follet-Gueye M.L., Duponchel L., Moreau M., Lerouge P., et al. The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant physiology 150 (2009) 1411
44. Hamamoto L., Hawes M.C., and Rost T.L. The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Annals of botany 97 (2006) 917
45. Brigham L.A., Woo H.H., Wen F., and Hawes M.C. Meristem-specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals. Plant physiology 118 (1998) 1223
46. Clowes F.A.L. The cytogenerative centre in roots with broad columellas. New phytologist 52 (1953) 48-57
47. Clowes F.A.L. The promeristem and the minimal constructional centre in grass root apices. New phytologist (1954) 108-116
48. Barlow P. Regeneration of the cap of primary roots of Zea mays. New phytologist (1974) 937-954
49. Feldman L.J. The de novo origin of the quiescent center regenerating root apices of Zea mays. Planta 128 (1976) 207-212
50. R. Benjamins, B. Scheres, Auxin: the looping star in plant development, Annual Review of Biology 59 (2008) 443-465.
51. Friml J., Wisniewska J., Benkova E., Mendgen K., and Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415 (2002) 806-809
52. Blilou I., Xu J., Wildwater M., Willemsen V., and Paponov I. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433 (2005) 39-44
53. Wisniewska J., Xu J., Seifertova D., Brewer P.B., Ruzicka K., Blilou I., et al. Polar PIN localization directs auxin flow in plants. Science 312 (2006) 883
54. Sabatini S., Beis D., Wolkenfelt H., Murfett J., Guilfoyle T., Malamy J., et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell (Cambridge MA) 99 (1999) 463-472
55. Kleine-Vehn J.r., Dhonukshe P., Sauer M., Brewer P.B., Wisniewska J., Paciorek T., et al. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Current biology 18 (2008) 526-531
56. Aida M., Beis D., Heidstra R., Willemsen V., Blilou I., Galinha C., et al. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119 (2004) 109-120
57. Boutilier K., Offringa R., Sharma V.K., Kieft H., Ouellet T., Zhang L., et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. The Plant cell online 14 (2002) 1737
58. Galinha C., Hofhuis H., Luijten M., Willemsen V., Blilou I., Heidstra R., et al. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449 (2007) 1053-1057
59. Wang J.W., Wang L.J., Mao Y.B., Cai W.J., Xue H.W., and Chen X.Y. Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. The Plant cell online 17 (2005) 2204
60. Willemsen V., Bauch M., Bennett T., Campilho A., Wolkenfelt H., Xu J., et al. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Developmental cell 15 (2008) 913-922
61. Benkova E., and Hejtko J. Hormone interactions at the root apical meristem. Plant molecular biology 69 (2009) 383-396
62. Mouchel C.F., Osmont K.S., and Hardtke C.S. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443 (2006) 458-461
63. Achard P., Gusti A., Cheminant S., Alioua M., Dhondt S., Coppens F., et al. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Current biology 19 (2009) 1188-1193
64. Ponce G., Barlow P.W., Feldman L.J., and Cassab G.I. Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant, cell & environment 28 (2005) 719-732
65. Jiang K., Meng Y.L., and Feldman L.J. Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130 (2003) 1429
66. Morgan P.W., and Gausman H.W. Effects of ethylene on auxin transport. Plant physiology 41 (1966) 45
67. Iijima M., and Kono Y. Development of Golgi apparatus in the root cap cells of maize (Zea mays L.) as affected by compacted soil. Annals of botany 70 (1992) 207
68. Tsugeki R., and Fedoroff N.V. Genetic ablation of root cap cells in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America (1999) 12941 96
69. Scheres B., McKhann H.I., and Van Den Berg C. Roots redefined: Anatomical and genetic analysis of root development. Plant physiology 111 (1996) 959
70. Hawes M.C., Gunawardena U., Miyasaka S., and Zhao X. The role of root border cells in plant defense. Trends in plant science 5 (2000) 128-133
71. Wen F., White G.J., VanEtten H.D., Xiong Z., and Hawes M.C. Extracellular DNA is required for root tip resistance to fungal infection. Plant physiology 151 (2009) 820-829
72. Wen F., VanEtten H.D., Tsaprailis G., and Hawes M.C. Extracellular proteins in pea root tip and border cell exudates. Plant physiology 143 (2007) 773-783
73. Chen R., Rosen E., and Masson P.H. Gravitropism in higher plants. Plant physiology 120 (1999) 343-350
74. Wolverton C., Mullen J., Ishikawa H., and Evans M. Root gravitropism in response to a signal originating outside of the cap. Planta 215 (2002) 153-157
75. Blancaflor E.B., Fasano J.M., and Gilroy S. Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant physiology 116 (1998) 213-222
76. Caspar T., and Pickard B.G. Gravitropism in a starchless mutant of Arabidopsis. Planta 177 (1989) 185-197
77. Vitha S., Yang M., Sack F.D., and Kiss J.Z. Gravitropism in the starch excess mutant of Arabidopsis thaliana. American journal of botany 94 (2007) 590-598
78. Leitz G., Kang B.H., Schoenwaelder M.E.A., and Staehelin L.A. Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing arabidopsis columella cells. The Plant cell 21 (2009) 843-860
79. Harrison B.R., Masson P., and ARL2 H. ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. The Plant journal 53 (2008) 380-392
80. Stanga J.P., Boonsirichai K., Sedbrook J.C., Otegui M.S., and Masson P.H. A role for the TOC complex in arabidopsis root gravitropism. Plant physiology 149 (2009) 1896-1905
81. Jarvis P. Targeting of nucleus-encoded proteins to chloroplasts in plants. New phytologist 179 (2008) 257-285
82. Holland J.J., Roberts D., and Liscum E. Understanding phototropism: from Darwin to today. Journal of experimental botany 60 (2009) 1969-1978
83. Galen C., Jessica J.R., and Emmanuel L. Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in "Arabidopsis thaliana". New phytologist 173 (2007) 91-99
84. Correll M.J., and Kiss J.Z. Interactions between gravitropism and phototropism in plants. Journal of plant growth regulation 21 (2002) 89-101
85. Liscum E., and Briggs W.R. Mutations in the NPH1 locus of arabidopsis disrupt the perception of phototropic stimuli. The Plant cell 7 (1995) 473-485
86. Briggs W.R., and Christie J.M. Phototropins 1 and 2: versatile plant blue-light receptors. Trends in plant science 7 (2002) 204-210
87. Sakamoto K., and Briggs W.R. Cellular and subcellular localization of phototropin 1. The Plant cell 14 (2002) 1723-1735
88. Mullen J.L., Wolverton C., Ishikawa H., Hangarter R.P., and Evans M.L. Spatial separation of light perception and growth response in maize root phototropism. Plant, cell & environment 25 (2002) 1191-1196
89. Lin C. Plant blue-light receptors. Trends in plant science 5 (2000) 337-342
90. Ruppel N.J., Hangarter R.P., and Kiss J.Z. Red-light-induced positive phototropism in Arabidopsis roots. Planta 212 (2001) 424-430
91. Hall A., Kozma-Bognar L., Toth R., Nagy F., and Millar A.J. Conditional circadian regulation of PHYTOCHROME a gene expression. Plant physiology 127 (2001) 1808-1818
92. Kiss J.Z., Mullen J.L., Correll M.J., and Hangarter R.P. Phytochromes A and B mediate red-light-induced positive phototropism in roots. Plant physiology 131 (2003) 1411-1417
93. Correll M.J., and Kiss J.Z. The roles of phytochromes in elongation and gravitropism of roots. Plant & cell physiology 46 (2005) 317-323
94. Lariguet P., Schepens I., Hodgson D., Pedmale U.V., Trevisan M., Kami C., et al. Phytochrome Kinase Substrate 1 is a phototropin 1 binding protein required for phototropism. Proceedings of the National Academy of Sciences (2006) 10134-10139 103
95. Fankhauser C., Yeh K.-C., Clark J., Lagarias H., Zhang T.D., Elich J., et al. PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in arabidopsis. Science 284 (1999) 1539-1541
96. Boccalandro H.E., De Simone S.N., Bergmann-Honsberger A., Schepens I., Fankhauser C., and Casal J.J. Phytochrome Kinase Substrate1 regulates root phototropism and gravitropism. Plant physiology 146 (2008) 108-115
97. Takahashi H. Hydrotropism: The current state of our knowledge. Journal of plant research 110 (1997) 163-169
98. Takahashi N., Yamazaki Y., Kobayashi A., Higashitani A., and Takahashi H. Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of arabidopsis and radish. Plant physiology 132 (2003) 805-810
99. Eapen D., Barroso M.L., Campos M.E., Ponce G., Corkidi G., Dubrovsky J.G., et al. A no hydrotropic response root mutant that responds positively to gravitropism in arabidopsis. Plant physiology 131 (2003) 536-546
100. Ponce G., F¡Tima R.A., and Gladys C.I. Roles of amyloplasts and water deficit in root tropisms. Plant, cell & environment 31 (2008) 205-217
101. Kobayashi A., Takahashi A., Kakimoto Y., Miyazawa Y., Fujii N., Higashitani A., et al. A gene essential for hydrotropism in roots. Proceedings of the National Academy of Sciences (2007) 4724-4729 104
102. Geldner N., Anders N., Wolters H., Keicher J., Kornberger W., Muller P., et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112 (2003) 219-230
103. Miyazawa Y., Takahashi A., Kobayashi A., Kaneyasu T., Fujii N., and Takahashi H. GNOM-mediated vesicular trafficking plays an essential role in hydrotropism of arabidopsis roots. Plant physiology 149 (2009) 835-840
104. Kaneyasu T., Kobayashi A., Nakayama M., Fujii N., Takahashi H., and Miyazawa Y. Auxin response, but not its polar transport, plays a role in hydrotropism of Arabidopsis roots. Journal of experimental botany 58 (2007) 1143-1150
105. LÛpez-Bucio J., Cruz-RamÌrez A., and Herrera-Estrella L. The role of nutrient availability in regulating root architecture. Current opinion in plant biology 6 (2003) 280-287
106. Ticconi C.A., and Abel S. Short on phosphate: plant surveillance and countermeasures. Trends in plant science 9 (2004) 548-555
107. Desnos T. Root branching responses to phosphate and nitrate. Current opinion in plant biology 11 (2008) 82-87
108. 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. Nature genetics 39 (2007) 792-796
109. Sanchez-Calderon L., Lopez-Bucio J., Chacon-Lopez A., Gutierrez-Ortega A., Hernandez-Abreu E., and Herrera-Estrella L. Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of arabidopsis to phosphorus deficiency. Plant physiology 140 (2006) 879-889
110. Ticconi C.A., Delatorre C.A., Lahner B., Salt D.E., and Abel S. Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. The Plant journal 37 (2004) 801-814
111. Reymond M., Svistoonoff S., Loudet O., Nussaume L., and Desnos T. Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant, cell & environment 29 (2006) 115-125
112. Ticconi C.A., Lucero R.D., Sakhonwasee S., Adamson A.W., Creff A., Nussaume L., et al. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proceedings of the National Academy of Sciences (2009) 14174-14179 106
113. Camacho-Cristóbal J., Rexach J., Conéjéro G., Al-Ghazi Y., Nacry P., and Doumas P. PRD, an Arabidopsis AINTEGUMENTA -like gene, is involved in root architectural changes in response to phosphate starvation. Planta 228 (2008) 511-522
114. Zhang H., and Forde B.G. Regulation of Arabidopsis root development by nitrate availability. Journal of experimental botany 51 (2000) 51-59
115. Forde B.G., and Walch-Liu P. Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant, Cell & Environment 32 (2009) 682-693
116. Zhang H., and Forde B.G. An arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279 (1998) 407-409
117. Remans T., Nacry P., Pervent M., Filleur S., Diatloff E., Mounier E., et al. The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences (2006) 19206-19211 103
118. Liu K.H., and Tsay Y.F. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. The EMBO journal 22 (2003) 1005-1013
119. Ho C.H., Lin S.H., Hu H.C., and Tsay Y.F. CHL1 functions as a nitrate sensor in plants. Cell 138 (2009) 1184-1194
120. Guo F.Q., Wang R., Chen M., and Crawford N.M. The Arabidopsis Dual-Affinity Nitrate Transporter Gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. The Plant cell 13 (2001) 1761-1777
121. Esmon A.C., Pedmale U.V., and Liscum E. Plant tropisms: providing the power of movement to a sessile organism. The international journal of developmental biology 49 (2005) 665-674