Getting to the roots of it: Genetic and hormonal control of root architecture

Frontiers in Plant Science

Volumn 4, Issue JUN, 2013, Pages

  Jung, Janelle K H ^a   McCouch, Susan ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Genetics; Hormone interactions; O. sativa; Rice; Root development; Root growth; Root system architecture

Indexed keywords

EID: 84888417322     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00186     Document Type: Review

References (422)

1. Abel, S. (1994). Early auxin-induced genes encode short-lived nuclear proteins. Proc. Natl. Acad. Sci. U.S.A. 91, 326-330. doi: 10.1073/pnas.91.1.326
2. Ahn, S. J., Sivaguru, M., Osawa, H., Chung, G. C., and Matsumoto, H. (2001). Aluminum inhibits the H(+)-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiol. 126, 1381-1390. doi: 10.1104/pp.126.4.1381
3. Aida, M., Beis, D., Heidstra, R., Willemsen, V. A., Blilou, I., Reis Galinha, C. I., et al. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109-120. doi: 10.1016/j.cell.2004.09.018
4. Aida, M., Vernoux, T., Furutani, M., Traas, J., and Tasaka, M. (2002). Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129, 3965.
5. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827. doi: 10.1038/nature03608
6. Akiyama, K., Ogasawara, S., Ito, S., and Hayashi, H. (2010). Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol. 51, 1104-1117. doi: 10.1093/pcp/pcq058
7. Aloni, R., Aloni, E., Langhans, M., and Ullrich, C. I. (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. doi: 10.1093/aob/mcl027
8. Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J. R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148-2152. doi: 10.1126/science.284.5423.2148
9. Ané, J., Kiss, G., and Riely, B. (2004). Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364-1367. doi: 10.1126/science.1092986
10. Apse, M. P., Aharon, G. S., Snedden, W. A., and Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256-1258. doi: 10.1126/science.285.5431.1256
11. Ariel, F., Diet, A., Verdenaud, M., Gruber, V., Frugier, F., Chan, R., et al. (2010). Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. Plant Cell 22, 2171-2183. doi: 10.1105/tpc.110.074823
12. Arite, T., Kameoka, H., and Kyozuka, J. (2012). Strigolactone positively controls crown root elongation in rice. J. Plant Growth Regul. 31, 165-172. doi: 10.1007/s00344-011-9228-6
13. Armengaud, P., Zambaux, K., Hills, A., Sulpice, R., Pattison, R. J., Blatt, M. R., et al. (2009). EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. Plant J. 57, 945-956. doi: 10.1111/j.1365-313X.2008.03739.x
14. Arora, N., Skoog, F., and Allen, O. N. (1959). Kinetin-induced pseudonodules on tobacco roots. Am. J. Bot. 46, 610-613. doi: 10.2307/2439306
15. Badescu, G. O., and Napier, R. M. (2006). Receptors for auxin: will it all end in TIRs? Trends Plant Sci. 11, 217-223. doi: 10.1016/j.tplants.2006.03.001
16. Bai, H., Murali, B., Barber, K., and Wolverton, C. (2013). Low phosphate alters lateral root setpoint angle and gravitropism. Am. J. Bot. 100, 175-182. doi: 10.3732/ajb.1200285
17. Band, L., Wells, D., and Larrieu, A. (2012). Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc. Natl. Acad. Sci. U.S.A. 109, 4668-4673. doi: 10.1073/pnas.1201498109
18. Bano, A. (2010). Root-to-shoot signal transduction in rice under salt stress. Pak. J. Bot. 42, 329-339.
19. Bao, F., Shen, J., Brady, S. R., Muday, G. K., Asami, T., and Yang, Z. (2004). Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134, 1624-1631. doi: 10.1104/pp.103.036897
20. Bari, R., Pant, B. D., Stitt, M., and Scheible, W.-R. (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988-999. doi: 10.1104/pp.106.079707
21. Barker, S. J., and Tagu, D. (2000). The roles of auxins and cytokinins in mycorrhizal symbioses. J. Plant Growth Regul. 19, 144-154. doi: 10.1007/s003440000021
22. Bates, T. R., and Lynch, J. P. (1996). Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ. 19, 529-538. doi: 10.1111/j.1365-3040.1996.tb00386.x
23. Bates, T. R., and Lynch, J. P. (2000). Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 87, 958-963. doi: 10.2307/2656994
24. Bauer, P., Ratet, P., Crespi, M. D., Schultze, M., and Kondorosi, A. (1996). Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsEnod12A expression patterns in alfalfa roots. Plant J. 10, 91-105. doi: 10.1046/j.1365-313X.1996.10010091.x
25. Beeckman, T., Burssens, S., and Inze, D. (2001). The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 52, 403-411. doi: 10.1093/jexbot/52.suppl_1.403
26. Benkova, E., and Hejatko, J. (2009). Hormone interactions at the root apical meristem. Plant Mol. Biol. 69, 383-396. doi: 10.1007/s11103-008-9393-6
27. Bennett, M. J., Marchant, A., Green, H. G., May, S. T., Millner, P. A., Walker, A. R., et al. (1996). Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948-950. doi: 10.1126/science.273.5277.948
28. Berta, G., Fusconi, A., and Hooker, J. E. (2002). "Arbuscular mycorrhizal modifications to plant root systems: scale, mechanisms and consequences, " in Mycorrhizal Technology in Agriculture: from Genes to Bioproducts, eds S. Gianinazzi, H. Schüepp, J. M. Barea, and K. Haselwandter (Basel: Birkhäuser Verlag), 71-85.
29. Berta, G., Fusconi, A., Trotta, A., and Scannerini, S. (1990). Morphogenetic modifications induced by the mycorrhizal fungus glomus strain E3 in the root system of Allium porrum L. New Phytol. 114, 207-215. doi: 10.1111/j.1469-8137.1990.tb00392.x
30. Berta, G., Trotta, A., Fusconi, A., Hooker, J. E., Munro, M., Atkinson, D., et al. (1995). Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiol. 15, 281-293. doi: 10.1093/treephys/15.5.281
31. Bhalerao, R. P., Eklof, J., Ljung, K., Marchant, A., Bennett, M., and Sandberg, G. (2002). Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 29, 325-332. doi: 10.1046/j.0960-7412.2001.01217.x
32. Bhuja, P., McLachlan, K., Stephens, J., and Taylor, G. (2004). Accumulation of 1, 3-beta-D-glucans, in response to aluminum and cytosolic calcium in Triticum aestivum. Plant Cell Physiol. 45, 543-549. doi: 10.1093/pcp/pch068
33. Bishopp, A., Help, H., and Helariutta, Y. (2009). Cytokinin signaling during root development. Int. Rev. Cell Mol. Biol. 276, 1-48. doi: 10.1016/S1937-6448(09)76001-0
34. Blancaflor, E. B., and Masson, P. H. (2003). Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiol. 133, 1677-1690. doi: 10.1104/pp.103.032169
35. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., et al. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44. doi: 10.1038/nature03184
36. Boniotti, M. B., and Gutierrez, C. (2001). A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J. 28, 341-350. doi: 10.1046/j.1365-313X.2001.01160.x
37. Bonser, A. M., Lynch, J., and Snapp, S. (1996). Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol. 132, 281-288. doi: 10.1111/j.1469-8137.1996.tb01847.x
38. Boonsirichai, K., Sedbrook, J. C., Chen, R., Gilroy, S., and Masson, P. H. (2003). ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 15, 2612-2625. doi: 10.1105/tpc.015560
39. Borisov, A. Y., Madsen, L. H., Tsyganov, V. E., Umehara, Y., Voroshilova, V. A., Batagov, A. O., et al. (2003). The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol. 131, 1009-1017. doi: 10.1104/pp.102.016071
40. Bouranis, D., Buchner, P., Chorianopoulou, S. N., Hopkins, L., Protonotarios, V. E., Siyiannis, V. F., et al. (2008). "Responses to sulfur limitation in maize, " in Sulfur Assimilation and Abiotic Stress in Plants, eds N. A. Khan, S. Singh, and S. Umar (Berlin: Springer), 1-19. doi: 10.1007/978-3-540-76326-0_1
41. Brady, S. M., Sarkar, S. F., Bonetta, D., and McCourt, P. (2003). The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J. 34, 67-75. doi: 10.1046/j.1365-313X.2003.01707.x
42. Braga, R. A., Dupuy, L., Pasqual, M., and Cardoso, R. R. (2009). Live biospeckle laser imaging of root tissues. Eur. Biophys. J. 38, 679-686. doi: 10.1007/s00249-009-0426-0
43. Brunoud, G., Wells, D. M., Oliva, M., Larrieu, A., Mirabet, V., Burrow, A. H., et al. (2012). A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103-106. doi: 10.1038/nature10791
44. Buchner, P., Takahashi, H., and Hawkesford, M. J. (2004). Plant sulfate transporters: co-ordination of uptake, intracellular and long-distance transport. J. Exp. Bot. 55, 1765-1773. doi: 10.1093/jxb/erh206
45. Budíková, S. (1999). Structural changes and aluminium distribution in maize root tissues. Biol. Plant. 42, 259-266. doi: 10.1023/A:1002116803679
46. Buer, C. S., Sukumar, P., and Muday, G. K. (2006). Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol. 140, 1384-1396. doi: 10.1104/pp.105.075671
47. Campanoni, P., and Nick, P. (2005). Auxin-dependent cell division and cell elongation. 1-naphthaleneacetic acid and 2, 4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol. 137, 939-948. doi: 10.1104/pp.104.053843
48. Caniato, F. F., Guimaraes, C. T., Schaffert, R. E., Alves, V. C. M., Kochian, L. V., Borem, A., et al. (2007). Genetic diversity for aluminum tolerance in sorghum. Theor. Appl. Genet. 114, 863-876. doi: 10.1007/s00122-006-0485-x
49. Cao, Y. R., Chen, S.-Y., and Zhang, J.-S. (2008). Ethylene signaling regulates salt stress response: an overview. Plant. Signal. Behav. 3, 761-763. doi: 10.4161/psb.3.10.5934
50. Carraro, N., Forestan, C., Canova, S., Traas, J., and Varotto, S. (2006). ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol. 142, 254-264. doi: 10.1104/pp.106.080119
51. Casimiro, I., Marchant, A., Bhalerao, R. P., Beeckman, T., Dhooge, S., Swarup, R., et al. (2001). Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13, 843-852. doi: 10.1105/tpc.13.4.843
52. Catoira, R. (2000). Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12, 1647-1666. doi: 10.1105/tpc.12.9.1647
53. Celenza, J. L., Grisafi, P. L., and Fink, G. R. (1995). A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev. 9, 2131-2142. doi: 10.1101/gad.9.17.2131
54. Cervantes, E. (2001). ROS in root gravitropism: the auxin messengers? Trends Plant Sci. 6, 556-556. doi: 10.1016/S1360-1385(01)02197-5
55. Chandler, P. M., Marion-Poll, A., Ellis, M., and Gubler, F. (2002). Mutants at the slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol. 129, 181-190. doi: 10.1104/pp.010917
56. Chang, S., Kim, Y., and Lee, J. (2004). Brassinolide interacts with auxin and ethylene in the root gravitropic response of maize (Zea mays). Physiol. Plant. 121, 666-673. doi: 10.1111/j.0031-9317.2004.00356.x
57. 2+ spiking and specific ENOD gene expression. Plant Physiol. 136, 3582-3593. doi: 10.1104/pp.104.051110
58. Chen, C., DeClerck, G., Tian, F., Spooner, W., McCouch, S., and Buckler, E. (2012). PICARA, an analytical pipeline providing probabilistic inference about a priori candidates genes underlying genome-wide association QTL in plants. PLoS ONE 7:e46596. doi: 10.1371/journal.pone.0046596
59. Christie, J. M., Reymond, P., Powell, G. K., Bernasconi, P., Raibekas, A. A., Liscum, E., et al. (1998). ArabidopsisNPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282, 1698-1701. doi: 10.1126/science.282.5394.1698
60. Clark, R. T., Famoso, A. N., Zhao, K., Shaff, J. E., Craft, E. J., Bustamante, C. D., et al. (2013). High-throughput two-dimensional root system phenotyping platform facilitates genetic analysis of root growth and development. Plant Cell Environ. 36, 454-466. doi: 10.1111/j.1365-3040.2012.02587.x
61. Clark, R. T., MacCurdy, R. B., Jung, J. K., Shaff, J. E., McCouch, S. R., Aneshansley, D. J., et al. (2011). Three-dimensional root phenotyping with a novel imaging and software platform. Plant Physiol. 156, 455-465. doi: 10.1104/pp.110.169102
62. Correll, M. J., Coveney, K. M., Raines, S. V., Mullen, J. L., Hangarter, R. P., and Kiss, J. Z. (2003). Phytochromes play a role in phototropism and gravitropism in Arabidopsis roots. Adv. Space Res. 31, 2203-2210. doi: 10.1016/S0273-1177(03)00245-X
63. Cosgrove, D. J. (2000). Loosening of plant cell walls by expansins. Nature 407, 321-326. doi: 10.1038/35030000
64. Costigan, S. E., Warnasooriya, S. N., Humphries, B. A., and Montgomery, B. L. (2011). Root-localized phytochrome chromophore synthesis is required for photoregulation of root elongation and impacts root sensitivity to jasmonic acid in Arabidopsis. Plant Physiol. 157, 1138-1150. doi: 10.1104/pp.111.184689
65. Coudert, Y., Perin, C., Courtois, B., Khong, N. G., and Gantet, P. (2010). Genetic control of root development in rice, the model cereal. Trends Plant Sci. 15, 219-226. doi: 10.1016/j.tplants.2010.01.008
66. Cui, H., Levesque, M. P., Vernoux, T., Jung, J. W., Paquette, A. J., Gallagher, K. L., et al. (2007). An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421-425. doi: 10.1126/science.1139531
67. Dan, H., Yang, G., and Zheng, A.-L. (2007). A negative regulatory role for auxin in sulfate deficiency response in Arabidopsis thaliana. Plant Mol. Biol. 63, 221-235. doi: 10.1007/s11103-006-9084-0
68. Danjon, F., and Reubens, B. (2007). Assessing and analyzing 3D architecture of woody root systems, a review of methods and applications in tree and soil stability, resource acquisition and allocation. Plant Soil 303, 1-34. doi: 10.1007/s11104-007-9470-7
69. Deak, K. I., and Malamy, J. (2005). Osmotic regulation of root system architecture. Plant J. 43, 17-28. doi: 10.1111/j.1365-313X.2005.02425.x
70. De Kroon, H., Visser, E. J. W., Huber, H., Mommer, L., and Hutchings, M. J. (2009). A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ. 32, 704-712. doi: 10.1111/j.1365-3040.2009.01936.x
71. Delhaize, E., Ryan, P. R., and Randall, P. J. (1993). Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices). Plant Physiol. 103, 695-702. doi: 10.1104/pp.103.3.695
72. Dello Ioio, R., Linhares, F. S., and Sabatini, S. (2008). Emerging role of cytokinin as a regulator of cellular differentiation. Curr. Opin. Plant Biol. 11, 23-27. doi: 10.1016/j.pbi.2007.10.006
73. Demidchik, V., Cuin, T. A., Svistunenko, D., Smith, S. J., Miller, A. J., Shabala, S., et al. (2010). Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J. Cell Sci. 123, 1468-1479. doi: 10.1242/jcs.064352
74. De Rybel, B., Vassileva, V., Grunewald, W., Naudts, M., Levesque, M. P., Ehrismann, J. S., et al. (2010). Bimodular auxin response controls organogenesis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 107, 2705-2710. doi: 10.1073/pnas.0915001107
75. De Smet, I., Lau, S., Voss, U., Vanneste, S., Benjamins, R., Rademacher, E. H., et al. (2010). Bimodular auxin response controls organogenesis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 107, 2705-2710. doi: 10.1073/pnas.0915001107
76. De Smet, I., Signora, L., Beeckman, T., Inze, D., Foyer, C., and Zhang, H. (2003). An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 33, 543-555. doi: 10.1046/j.1365-313X.2003.01652.x
77. De Smet, I., Tetsumura, T., De Rybel, B., Freidit Frey, N., Laplaze, L., Casimiro, I., et al. (2007). Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134, 681-690. doi: 10.1242/dev.02753
78. De Smet, I., Zhang, H., Inzé, D., and Beeckman, T. (2006). A novel role for abscisic acid emerges from underground. Trends Plant Sci. 11, 434-439. doi: 10.1016/j.tplants.2006.07.003
79. Devaiah, B. N., Karthikeya, A. S., and Raghothama, K. G. (2007). WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143, 1789-1801. doi: 10.1104/pp.106.093971
80. Devaiah, B. N., and Raghothama, K. G. (2007). Transcriptional regulation of Pi starvation responses by WRKY75. Plant Signal. Behav. 2, 424-425. doi: 10.4161/psb.2.5.4418
81. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005). The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445. doi: 10.1038/nature03543
82. DiDonato, R. J., Arbuckle, E., Buker, S., Sheets, J., Tobar, J., Totong, T., et al. (2004). Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. Plant J. 37, 340-353. doi: 10.1046/j.1365-313X.2003.01964.x
83. Digby, J., and Firn, R. D. (1995). The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant Cell Environ. 18, 1434-1440. doi: 10.1111/j.1365-3040.1995.tb00205.x
84. Digby, J., and Firn, R. D. (2002). Light modulation of the gravitropic set-point angle (GSA). J. Exp. Bot. 53, 377-381. doi: 10.1093/jexbot/53.367.377
85. Di Laurenzio, L., Wysocka-Diller, J., Malamy, J. E., Pysh, L., Helariutta, Y., Freshour, G., et al. (1996). The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423-433. doi: 10.1016/S0092-8674(00)80115-4
86. Dill, A., and Sun, T. (2001). Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159, 777-785.
87. Dimkpa, C., Weinand, T., and Asch, F. (2009). Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32, 1682-1694. doi: 10.1111/j.1365-3040.2009.02028.x
88. Ding, Y., Kalo, P., Yendrek, C., Sun, J., Liang, Y., Marsh, J. F., et al. (2008). Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20, 2681-2695. doi: 10.1105/tpc.108.061739
89. Ding, Y., and Oldroyd, G. E. (2009). Positioning the nodule, the hormone dictum. Plant Signal. Behav. 4, 89-93. doi: 10.4161/psb.4.2.7693
90. Dixon, R. K. (1990). Cytokinin activity in citrus jambhiri seedlings colonized by mycorrhizal fungi. Agric. Ecosyst. Environ. 29, 103-106. doi: 10.1016/0167-8809(90)90262-C
91. Dokken, K. M., and Davis, L. C. (2007). Infrared imaging of sunflower and maize root anatomy. J. Agric. Food Chem. 55, 10517-10530. doi: 10.1021/jf072052e
92. Dubrovsky, J. G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M. G., Friml, J., Shishkova, S., et al. (2008). Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl. Acad. Sci. U.S.A. 105, 8790-8794. doi: 10.3410/f.1115286.571292
93. Edelmann, H. G., and Roth, U. (2006). Gravitropic plant growth regulation and ethylene: an unsought cardinal coordinate for a disused model. Protoplasma 229, 183-191. doi: 10.1007/s00709-006-0205-z
94. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., and Kiss, G. B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962-966. doi: 10.1038/nature00842
95. Eticha, D., Stass, A., and Horst, W. J. (2005). Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ. 28, 1410-1420. doi: 10.1111/j.1365-3040.2005.01375.x
96. Evelin, H., Kapoor, R., and Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 104, 1263-1280. doi: 10.1093/aob/mcp251
97. Fahn, A. (1990). Plant Anatomy, 4th Edn. New York: Pergamon.
98. Famoso, A. N., Clark, R. T., Shaff, J. E., Craft, E., McCouch, S. R., and Kochian, L. V. (2010). Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol. 153, 1678-1691. doi: 10.1104/pp.110.156794
99. Fang, S., Yan, X., and Liao, H. (2009). 3D reconstruction and dynamic modeling of root architecture in situ and its application to crop phosphorus research. Plant J. 60, 1096-1108. doi: 10.1111/j.1365-313X.2009.04009.x
100. Fang, Y., and Hirsch, A. M. (1998). Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol. 116, 53-68. doi: 10.1104/pp.116.1.53
101. Farrás, R., Ferrando, A., Jásik, J., Kleinow, T., Okrész, L., Tiburcio, A., et al. (2001). SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J. 20, 2742-2756. doi: 10.1093/emboj/20.11.2742
102. Ferguson, B. J., Indrasumunar, A., Hayashi, S., Lin, M.-H., Lin, Y.-H., Reid, D. E., et al. (2010). Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61-76. doi: 10.1111/j.1744-7909.2010.00899.x
103. Fiers, M., Golemiec, E., Van der Schors, R., Van der Geest, L., Li, K. W., Stiekema, W. J., et al. (2006). The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol. 141, 1284-1292. doi: 10.1104/pp.106.080671
104. Fiers, M., Hause, G., Boutilier, K., Casamitjana-Martinez, E., Weijers, D., Offringa, R., et al. (2004). Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene 327, 37-49. doi: 10.1016/j.gene.2003.11.014
105. Fitter, A. H. (1991). "The ecological significance of root system architecture: an economic approach, " in Plant Root Growth: An Ecological Perspective, ed. D. Atkinson (Oxford: Blackwell Scientific Publications), 229-243.
106. Fitze, D., Wiepning, A., Kaldorf, M., and Lidwig-Muller, J. (2005). Auxins in the development of an arbuscular mycorrhizal symbiosis in maize. J. Plant Physiol. 162, 1210-1219. doi: 10.1016/j.jplph.2005.01.014
107. Fleet, C. M., and Sun, T. (2005). A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr. Opin. Plant Biol. 8, 77-85. doi: 10.1016/j.pbi.2004.11.015
108. Flowers, T. J., and Yeo, A. R. (1995). Breeding for salinity resistance in crop plants: where next? Aust. J. Plant Physiol. 22, 875-884. doi: 10.1071/PP9950875
109. Foo, E., Yoneyama, K., Hugill, C. J., Quittenden, L. J., and Reid, J. B. (2012). Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol. Plant 6, 76-87. doi: 10.1093/mp/sss115
110. Foy, C. D. (1984). Adaptation of plants to mineral stress in problem soils. Ciba Found. Symp. 102, 20-39. doi: 10.1002/9780470720837.ch3
111. Franco-Zorrilla, J. M., Martin, A. C., Solano, R., Rubio, V., Leyva, A., and Paz-Ares, J. (2002). Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J. 32, 353-360. doi: 10.1046/j.1365-313X.2002.01431.x
112. French, A., Ubeda-Tomas, S., Holman, T. J., Bennett, M. J., and Pridmore, T. (2009). High-throughput quantification of root growth using a novel image-analysis tool. Plant Physiol. 150, 1784-1795. doi: 10.1104/pp.109.140558
113. Frigerio, M., Alabadi, D., Perez-Gomez, J., Garica-Carcel, L., Phillips, A. L., Hedden, P., et al. (2006). Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol. 142, 553-563. doi: 10.1104/pp.106.084871
114. Frugier, F., Kosuta, S., Murray, J. D., Crespi, M., and Szczyglowshi, K. (2008). Cytokinin: secret agent of symbiosis. Trends Plant Sci. 13, 115-120. doi: 10.1016/j.tplants.2008.01.003
115. Fu, X., and Harberd, N. P. (2003). Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740-743. doi: 10.1038/nature01387
116. Fukaki, H., Okushima, Y., and Tasaka, M. (2007). Auxin-mediated lateral root formation in higher plants. Int. Rev. Cytol. 256, 111-137. doi: 10.1016/S0074-7696(07)56004-3
117. Fukaki, H., and Tasaka, M. (2009). Hormone interactions during lateral root formation. Plant Mol. Biol. 69, 437-449. doi: 10.1007/s11103-008-9417-2
118. Fukao, T., Yeung, E., and Bailey-Serres, J. (2011). The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23, 412-427. doi: 10.1105/tpc.110.080325
119. Gagne, J. M., Downes, B. P., Shiu, S.-H., Durski, A. M., and Vierstra, R. D. (2002). The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 99, 11519-11524. doi: 10.1073/pnas.162339999
120. Galen, C., Rabenold, J. J., and Liscum, E. (2007). Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. New Phytol. 173, 91-99. doi: 10.1111/j.1469-8137.2006.01893.x
121. Gao, Q., Zhao, M., Li, F., Guo, Q., Xing, S., and Wang, W. (2008). Expansins and coleoptile elongation in wheat. Protoplasma 233, 73-81. doi: 10.1007/s00709-008-0303-1
122. Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P., Alper, S. L., and Fink, G. R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. U.S.A. 96, 1480-1485. doi: 10.1073/pnas.96.4.1480
123. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., et al. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230. doi: 10.1016/S0092-8674(03)00003-5
124. Gil, P., Dewey, E., Friml, J., Zhao, Y., Snowden, K. C., Putterill, J., et al. (2001). BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985-1997. doi: 10.1101/gad.905201
125. Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.-C., et al. (2007). Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316, 1307-1312. doi: 10.1126/science.1139548
126. Goh, T., Joi, S., Mimura, T., and Fukaki, H. (2012a). The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins. Development 139, 883-893. doi: 10.1242/dev.071928
127. Goh, T., Kasahara, H., Mimura, T., Kamiya, Y., and Fukaki, H. (2012b). Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1461-1468. doi: 10.1098/rstb.2011.0232
128. Gonzalez-Rizzo, S., Crespi, M., and Frugier, F. (2006). The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18, 2680-2693. doi: 10.1105/tpc.106.043778
129. Gou, J., Strauss, S. H., Tsai, C. J., Fang, K., Chen, Y., Jiang, X., et al. (2010). Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22, 623-639. doi: 10.1105/tpc.109.073239
130. Gowda, V. R. P. V., Henry, A., Yamauchi, A., Shashidhar, H. E., and Serraj, R. (2011). Root biology and genetic improvement for drought avoidance in rice. Field Crops Res. 122, 1-13. doi: 10.1016/j.fcr.2011.03.001
131. Gray, W. M., Kepinski, S., Rouse, D., Leyser, O., and Estelle, M. (2001). Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414, 271-276. doi: 10.1038/35104500
132. Gregory, P. J., Bengough, A. G., Grinev, D., Schmidt, S., Thomas, W. T. B., Wojciechowski, T., et al. (2009). Root phenomics of crops: opportunities and challenges. Funct. Plant Biol. 36, 922-929. doi: 10.1071/FP09150
133. Groth, P., Kalev, I., Kirov, I., Traikov, B., Leser, U., and Weiss, B. (2010). Phenoclustering: online mining of cross-species phenotypes. Bioinformatics 26, 1924-1925. doi: 10.1093/bioinformatics/btq311
134. Guo, F. Q., Wang, R., and Crawford, N. M. (2002). The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. J. Exp. Bot. 53, 835-844. doi: 10.1093/jexbot/53.370.835
135. Guo, H.-S., Xie, Q., Fei, J.-F., and Chua, N.-H. (2005). MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17, 1376-1386. doi: 10.1105/tpc.105.030841
136. Gutjahr, C., Casieri, L., and Paszkowski, U. (2009). Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytol. 184, 829-837. doi: 10.1111/j.1469-8137.2009.02839.x
137. Harrison, B., and Masson, P. H. (2008a). ARG1 and ARL2 form an actin-based gravity-signaling chaperone complex in root statocytes? Plant Signal. Behav. 3, 650-653. doi: 10.4161/psb.3.9.5749
138. Harrison, B. R., and Masson, P. H. (2008b). ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J. 53, 380-392. doi: 10.1111/j.1365-313X.2007.03351.x
139. He, X. J., Mu, R.-L., Cao, W.-H., Zhang, Z.-G., Zhang, J.-S., and Chen, S.-Y. (2005). AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J. 44, 903-916. doi: 10.1111/j.1365-313X.2005.02575.x
140. Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., et al. (2000). The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555-567. doi: 10.1016/S0092-8674(00)80865-X
141. Henrissat, B., and Davies, G. (1997). Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644. doi: 10.1016/S0959-440X(97)80072-3
142. Herrera-Medina, M. J., Steinkellner, S., Vierheilig, H., Bote, J. A. O., and Garrido, J. M. G. (2007). Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol. 175, 554-564. doi: 10.1111/j.1469-8137.2007.02107.x
143. Hetrick, B. A. D. (1991). Mycorrhizas and root architecture. Cell. Mol. Life Sci. 47, 355-362. doi: 10.1007/BF01972077
144. Hetrick, B. A. D., Leslie, J. F., Thompson Wilson, G., and Gerschefske Kitt, D. (1988). Physical and topological assessment of effects of a vesicular-arbuscular mycorrhizal fungus on root architecture of big bluestem. New Phytol. 110, 85-96. doi: 10.1111/j.1469-8137.1988.tb00240.x
145. Hetz, W., Hochholdinger, F., Schwall, M., and Feix, G. (1996). Isolation and characterization of rtcs, a maize mutant deficient in the formation of nodal roots. Plant J. 10, 845-857. doi: 10.1046/j.1365-313X.1996.10050845.x
146. Himanen, K., Boucheron, E., Vanneste, S., De Almeida Engler, J., Inze, D., and Beechmann, T. (2002). Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14, 2339-2351. doi: 10.1105/tpc.004960
147. Hirai, M. Y., Fujiwara, T., Awazuhara, M., Kimura, T., Noji, M., and Siato, K. (2003). Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33, 651-663. doi: 10.1046/j.1365-313X.2003.01658.x
148. Hirose, N., Makita, N., Kojima, M., Kamada-Nobusada, T., and Sakakibara, H. (2007). Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol. 48, 523-539. doi: 10.1093/pcp/pcm022
149. Hochholdinger, F. (2009). "The maize root system: morphology, anatomy and genetics, " in Handbook of Maize: Its Biology, eds J. L. Bennetzen and S. C. Hake (New York: Springer), 145-160. doi: 10.1007/978-0-387-79418-1_8
150. Hochholdinger, F., and Feix, G. (1998). Early post-embryonic root formation is specifically affected in the maize mutant Irt1. Plant J. 16, 247-255. doi: 10.1046/j.1365-313x.1998.00280.x
151. Hochholdinger, F., Park, W. J., and Feix, F. H. (2001). Cooperative action of SLR1 and SLR2 is required for lateral root-specific cell elongation in maize. Plant Physiol. 125, 1529-1539. doi: 10.1104/pp.125.3.1529
152. Hochholdinger, F., Park, W. J., Sauer, M., and Woll, K. (2004). From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci. 9, 42-48. doi: 10.1016/j.tplants.2003.11.003
153. Hochholdinger, F., and Tuberosa, R. (2009). Genetic and genomic dissection of maize root development and architecture. Curr. Opin. Plant Biol. 12, 172-177. doi: 10.1016/j.pbi.2008.12.002
154. Hochholdinger, F., and Zimmermann, R. (2008). Conserved and diverse mechanisms in root development. Curr. Opin. Plant Biol. 11, 70-74. doi: 10.1016/j.pbi.2007.10.002
155. Hoefgen, R., and Nikiforova, V. J. (2008). Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol. Plant. 132, 190-198. doi: 10.1111/j.1399-3054.2007.01012.x
156. Hogg, B. V., Cullimore, J. V., Ranjeva, R., and Bono, J.-J. (2006). The DMI1 and DMI2 early symbiotic genes of Medicago truncatula are required for a high-affinity nodulation factor-binding site associated to a particulate fraction of roots. Plant Physiol. 140, 365-373. doi: 10.1104/pp.105.068981
157. Horie, T., Costa, A., Kim, T. H., Han, M. J., Horie, R., Leung, H.-Y., et al. (2007). Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J. 26, 3003-3014. doi: 10.1038/sj.emboj.7601732
158. Horie, T., Hauser, F., and Schroeder, J. I. (2009). HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci. 14, 660-668. doi: 10.1016/j.tplants.2009.08.009
159. Horst, W. J., Wang, Y., and Eticha, D. (2010). The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann. Bot. 106, 185-197. doi: 10.1093/aob/mcq053
160. Horváth, B., Yeun, L. H., Domonkos, A., Halász, G., Gobbato, E., Ayaydin, F., et al. (2011). Medicago truncatulaIPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol. Plant Microbe Interact. 24, 1345-1358. doi: 10.1094/MPMI-01-11-0015
161. Huala, E., Oeller, P. W., Liscum, E., Han, I.-S., Larsen, E., and Briggs, W. R. (1997). Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278, 2120-2123. doi: 10.1126/science.278.5346.2120
162. Huang, C. F., Yamaji, N., Mitani, N., Yano, M., Nagamura, Y., and Ma, F. (2009a). A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21, 655-667. doi: 10.1105/tpc.108.064543
163. Huang, J., Xia, H., Li, Z., Xiong, Y., and Kong, G. (2009b). Soil aluminum uptake and accumulation by Paspalum notatum. Waste Manag. Res. 27, 668-675. doi: 10.1177/0734242X09103835
164. Huang, X., Wei, X., Sang, T., Zhao, Q., Feng, Q., Zhao, Y., et al. (2010). Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961-967. doi: 10.1038/ng.695
165. Ikeda, A., Sonoda, Y., Vernieri, P., Perata, P., Hirochika, H., and Yamaguchi, J. (2002). The slender rice mutant, with constitutively activated gibberellin signal transduction, has enhanced capacity for abscisic acid level. Plant Cell Physiol. 43, 974-979. doi: 10.1093/pcp/pcf115
166. Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., Koshioka, M., Futsuhara, Y., et al. (2001). Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13, 999-1010. doi: 10.1105/tpc.13.5.999
167. Imaizumi-Anraku, H., Takeda, N., and Charpentier, M. (2004). Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527-531. doi: 10.1038/nature03237
168. Inukai, Y., Miwa, M., Nagato, Y., Kitano, H., and Yamauchi, A. (2001). Characterization of rice mutants deficient in the formation of crown roots. Breed. Sci. 51, 123-129. doi: 10.1270/jsbbs.51.123
169. Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Shibata, Y., Gomi, K., Umemura, I., et al. (2005). Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17, 1387-1396. doi: 10.1105/tpc.105.030981
170. Itoh, J., Nonomura, K.-I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagushi, H., et al. (2005). Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46, 23-47. doi: 10.1093/pcp/pci501
171. Iwama, A., Yamashino, T., Tanaka, Y., Sakakibara, H., Kakimoto, T., Sato, S., et al. (2007). AHK5 histidine kinase regulates root elongation through an ETR1-dependent abscisic acid and ethylene signaling pathway in Arabidopsisthaliana. Plant Cell Physiol. 48, 375-380. doi: 10.1093/pcp/pcl065
172. Iyer-Pascuzzi, A. S., Symonova, O., Mileyko, Y., Hao, Y., Belcher, H., Harer, J., et al. (2010). Imaging and analysis platform for automatic phenotyping and trait ranking of plant root systems. Plant Physiol. 152, 1148-1157. doi: 10.1104/pp.109.150748
173. Jain, M., Tyagi, A. K., and Khurana, J. P. (2006). Molecular characterization and differential expression of cytokinin-responsive type-A response regulators in rice (Oryza sativa). Plant Biol. 6, 1. doi: 10.1146/annurev.arplant.52.1.89
174. Jebanathirajah, J. A., Peri, S., and Pandey, A. (2002). Toll and interleukin-1 receptor (TIR) domain-containing proteins in plants: a genomic perspective. Trends Plant Sci. 7, 388-391. doi: 10.1016/S1360-1385(02)02309-9
175. Jiang, C., Gao, X., Liao, L., Harberd, N. P., and Fu, X. (2007). Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol. 145, 1460-1470. doi: 10.1104/pp.107.103788
176. Jones, D. L., Blancaflor, E. B., Kochian, L. V., and Gilroy, S. (2006). Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ. 29, 1309-1318. doi: 10.1111/j.1365-3040.2006.01509.x
177. Joo, J. H., Bae, Y. S., and Lee, J. S. (2001). Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126, 1055. doi: 10.1104/pp.126.3.1055
178. Journet, E. P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., et al. (2001). Medicago truncatulaENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol. Plant Microbe Interact. 14, 737-748. doi: 10.1094/MPMI.2001.14.6.737
179. Kalo, P., Gleason, C., Edwards, A., Marsh, J. M., Mitra, R. M., Hirsch, S., et al. (2005). Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786-1789. doi: 10.1126/science.1110951
180. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 103, 359-364. doi: 10.1073/pnas.0508883103
181. Kapulnik, Y., Delaux, P. P.-M., Resnick, N., Mayzlish-Gati, E., Wininger, S., Bhattacharya, C., et al. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233, 209-216. doi: 10.1007/s00425-010-1310-y
182. Kartal, G., Temel, A., Arican, E., and Gozukirmizi, N. (2009). Effects of brassinosteroids on barley root growth, antioxidant system and cell division. Plant Growth Regul. 58, 261-267. doi: 10.1007/s10725-009-9374-z
183. Kepinski, S., and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451. doi: 10.1038/nature03542
184. Khadri, M., Tejera, N. A., and Lluch, C. (2006). Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J. Plant Growth Regul. 25, 110-119. doi: 10.1007/s00344-005-0004-3
185. Khan, G., Declerck, M., and Sorin, C. (2011). MicroRNAs as regulators of root development and architecture. Plant Mol. Biol. 77, 47-58. doi: 10.1007/s11103-011-9793-x
186. Kim, T.-W., Lee, S. M., Joo, S.-H., Yun, H. S., Lee, Y., Kaufman, P. B., et al. (2007). Elongation and gravitropic responses of Arabidopsis roots are regulated by brassinolide and IAA. Plant Cell Environ. 30, 679-689. doi: 10.1111/j.1365-3040.2007.01659.x
187. Kinoshita, A., Nakamura, Y., Sasaki, E., Kyozuka, J., Fukuda, H., and Sawa, S. (2007). Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. 48, 1821-1825. doi: 10.1093/pcp/pcm154
188. Kiss, J. Z., Mullen, J. L., Correll, M. J., and Hangarter, R. P. (2003). Phytochromes A and B mediate red-light-induced positive phototropism in roots. Plant Physiol. 131, 1411-1417. doi: 10.1104/pp.013847
189. Kistner, C., Winzer, T., Pitzschke, A., Mulder, L., Sato, S., Kaneko, T., et al. (2005). Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17, 2217-2229. doi: 10.1105/tpc.105.032714
190. Klug, B., and Horst, W. J. (2010). Spatial characteristics of aluminum uptake and translocation in roots of buckwheat (Fagopyrum esculentum). Physiol. Plant. 139, 181-191. doi: 10.1111/j.1399-3054.2010.01355.x
191. Kochian, L. V. (1995). Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 237. doi: 10.1146/annurev.pp.46.060195.001321
192. Kohlen, W., Charnikhova, T., and Liu, Q. (2011). Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host. Plant Physiol. 155, 974-987. doi: 10.1104/pp.110.164640
193. Kollmeier, M., Felle, H. H., and Horst, W. J. (2000). Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol. 122, 945-956. doi: 10.1104/pp.122.3.945
194. Koltai, H., Dor, E., Hershenhorn, J., Joel, D. M., Weininger, S., Lekalla, S., et al. (2010). Strigolactones' effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J. Plant Growth Regul. 29, 129-136. doi: 10.1007/s00344-009-9122-7
195. Kopittke, P., Blamey, F. P. C., and Menzies, N. W. (2008). Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root cortical cells of cowpea. Plant Soil 303, 217-227. doi: 10.1007/s11104-007-9500-5
196. Kosuta, S., Chabaud, M., Lougnon, G., Cough, C., Denarie, J., Barker, D. G., et al. (2003). A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol. 131, 952-962. doi: 10.1104/pp.011882
197. Kosuta, S., Hazledine, S., Sun, J., Miwa, H., Morris, R. J., Downie, J. A., et al. (2008). Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc. Natl. Acad. Sci. U.S.A. 105, 9823-9828. doi: 10.1073/pnas.0803499105
198. Kramer, E. M. (2004). PIN and AUX/LAX proteins: their role in auxin accumulation. Trends Plant Sci. 9, 578-582. doi: 10.1016/j.tplants.2004.10.010
199. Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E., et al. (2010). Nitrate-regulated Auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18, 927-937. doi: 10.1016/j.devcel.2010.05.008
200. Kuderová, A., Urbánková, I., Válková, M., Malbeck, J., Brzobohaty, B., Némethová, D., et al. (2008). Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant Cell Physiol. 49, 570-582. doi: 10.1093/pcp/pcn073
201. Kuiper, D., Schuit, J., and Kuiper, P. J. C. (1990). Actual cytokinin concentrations in plant tissue as an indicator for salt resistance in cereals. Plant Soil 123, 243-250. doi: 10.1007/BF00011276
202. Kurata, T., and Yamamoto, K. T. (1997). Light-stimulated root elongation in Arabidopsis thaliana. J. Plant Physiol. 151, 346-351. doi: 10.1016/S0176-1617(97)80263-5
203. Kurth, E., Cramer, G. R., Lauchli, A., and Epstein, E. (1986). Effects of NaCl and CaCl(2) on cell enlargement and cell production in cotton roots. Plant Physiol. 82, 1102-1106. doi: 10.1104/pp.82.4.1102
204. Kutz, A., Muller, A., Hennig, P., Kaiser, W. M., Piotrowski, M., and Weiler, E. W. (2002). A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J. 30, 95-106. doi: 10.1046/j.1365-313X.2002.01271.x
205. Kwon, H.-K., Yokoyama, R., and Nishitani, K. (2005). A proteomic approach to apoplastic proteins involved in cell wall regeneration in protoplasts of Arabidopsis suspension-cultured cells. Plant Cell Physiol. 46, 843-857. doi: 10.1093/pcp/pci089
206. Lamesch, P., Berardini, T. Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., et al. (2012). The Arabidopsisinformation resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40, D1202-D1210. doi: 10.1093/nar/gkr1090
207. Laplaze, L., Benkova, E., Casimiro, I., Maes, L., Vanneste, S., Swarup, R., et al. (2007). Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19, 3889-3900. doi: 10.1105/tpc.107.055863
208. Larsen, P. B., Cancel, J., Rounds, M., and Ochoa, V. (2007). Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225, 1447-1458. doi: 10.1007/s00425-006-0452-4
209. Laskowski, M., Biller, S., Stanley, K., Kajstura, T., and Prusty, R. (2006). Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol. 47, 788-792. doi: 10.1093/pcp/pcj043
210. Laskowski, M. J., Williams, M. E., Nusbaum, H. C., and Sussex, I. E. (1995). Formation of lateral root meristems is a two-stage process. Development 121, 3303-3310.
211. Lawrence, C., and Harper, L. (2008). MaizeGDB: the maize model organism database for basic, translational, and applied research. Int. J. Plant Genomics 2008, 496957. doi: 10.1155/2008/496957
212. Laxmi, A., Pan, J., Morsy, M., and Chen, R. (2008). Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS ONE 3:e1510. doi: 10.1371/journal.pone.0001510
213. Lee, H. W., Kim, N. Y., Lee, D. J., and Kim, J. (2009). LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol. 151, 1377-1389. doi: 10.1104/pp.109.143685
214. Lee, Y., and Kende, H. (2002). Expression of alpha-expansin and expansin-like genes in deepwater rice. Plant Physiol. 130, 1396-1405. doi: 10.1104/pp.008888
215. Lelandais-Briere, C., Jovanovic, M., Torres, G. M., Perrin, Y., Lemoine, R., Corre-Menguy, F., et al. (2007). Disruption of AtOCT1, an organic cation transporter gene, affects root development and carnitine-related responses in Arabidopsis. Plant J. 51, 154-164. doi: 10.1111/j.1365-313X.2007.03131.x
216. Leng, Q., Mercier, R. W., Hua, B.-G., Fromm, H., and Berkowitz, G. A. (2002). Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol. 128, 400-410. doi: 10.1104/pp.010832
217. Leustek, T., Martin, M. N., Bick, J.-A., and Davies, J. P. (2000). Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 141-165. doi: 10.1146/annurev.arplant.51.1.141
218. Lévy, J., Bres, C., and Geurts, R. (2004). A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361-1364. doi: 10.1126/science.1093038
219. Lewandowska, M., and Sirko, A. (2008). Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim. Pol. 55, 457-471.
220. Li, J., Zhu, S., Song, X., Shen, Y., Chen, H., Yu, J., et al. (2006). A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18, 340-349. doi: 10.1105/tpc.105.037713
221. Li, J.-Y., Jiang, A.-L., and Zhang, W. (2007). Salt stress-induced programmed cell death in rice root tip cells. J. Integr. Plant Biol. 49, 481-486. doi: 10.1111/j.1744-7909.2007.00445.x
222. Linkohr, B. I., Williamson, L. C., Fitter, A. H., and Leyser, O. (2002). Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J. 29, 751-760. doi: 10.1046/j.1365-313X.2002.01251.x
223. Little, D. Y., Rao, H., Oliva, S., Daniel-Vedele, F., Krapp, A., and Malamy, J. E. (2005). The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc. Natl. Acad. Sci. U.S.A. 102, 13693-13698. doi: 10.1073/pnas.0504219102
224. Liu, H., Wang, S., Yu, X., Yu, J., He, X., Zhang, S., et al. (2005). ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J. 43, 47-56. doi: 10.1111/j.1365-313X.2005.02434.x
225. Liu, J., and Zhu, J. K. (1998). A calcium sensor homolog required for plant salt tolerance. Science 280, 1943-1945. doi: 10.1126/science.280.5371.1943
226. Liu, K.-H., Huang, C.-Y., and Tsay, Y.-F. (1999). CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11, 865-874. doi: 10.1105/tpc.11.5.865
227. Liu, S., Wang, J., Wang, L., Wang, X., Xue, Y., Wu, P., et al. (2009). Adventitious root formation in rice requires OsGNOM1 and is mediated by the OsPINs family. Cell Res. 19, 1110-1119. doi: 10.1038/cr.2009.70
228. Lohar, D. P., Schaff, J. E., Laskey, J. G., Kieber, J. J., Bilyeu, K. D., and Bird, D. M. (2004). Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J. 38, 203-214. doi: 10.1111/j.1365-313X.2004.02038.x
229. Lohar, D. P., Sharopova, N., Endre, G., Penuela, S., Samac, D., Town, C., et al. (2006). Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol. 140, 221-234. doi: 10.1104/pp.105.070326
230. Lontoc-Roy, M., Dutilleul, P., Prasher, S. O., Han, L., Brouillet, T., and Smith, D. L. (2006). Advances in the acquisition and analysis of CT scan data to isolate a crop root system from the soil medium and quantify root system complexity in 3-D space. Geoderma 137, 231-241. doi: 10.1016/j.geoderma.2006.08.025
231. López-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Nieto-Jacobo, M. F., Simpson, J., and Herrera-Estrella, L. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129, 244-256. doi: 10.1104/pp.010934
232. López-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Perez-Torres, A., Rampey, R. A., Bartel, B., et al. (2005). An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol. 137, 681-691. doi: 10.1104/pp.104.049577
233. López-Ráez, J. A., and Bouwmeester, H. (2008). Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal. Behav. 3, 963-965. doi: 10.1111/j.1469-8137.2008.02406
234. Lorbiecke, R., and Sauter, M. (1999). Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiol. 119, 21-30. doi: 10.1104/pp.119.1.21
235. Lucas, M., Godin, C., Jay-Allemand, C., and Laplaze, L. (2008). Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J. Exp. Bot. 59, 55-66. doi: 10.1093/jxb/erm171
236. Lucas, M., Swarup, R., and Paponov, I. (2011). Short-root regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol. 155, 384-398. doi: 10.1104/pp.110.165126
237. Ludwig-Muller, J., and Guther, M. (2007). Auxins as signals in arbuscular mycorrhiza formation. Plant Signal. Behav. 2, 194-196. doi: 10.4161/psb.2.3.4152
238. Luo, Z. B., Janz, D., Jiang, X., Gobel, C., Wildhagen, H., Tan, Y., et al. (2009). Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol. 151, 1902-1917. doi: 10.1104/pp.109.143735
239. Luschnig, C. (2002). Auxin transport: ABC proteins join the club. Trends Plant Sci. 7, 329-332. doi: 10.1016/S1360-1385(02)02292-6
240. Lynch, J. P., and Brown, K. M. (2001). Topsoil foraging-an architectural adaptation of plants to low phosphorus availability. Plant Soil 237, 225-237. doi: 10.1023/A:1013324727040
241. Lynch, J. P., and Brown, K. M. (2012). New roots for agriculture: exploiting the root phenome. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1598-1604. doi: 10.1098/rstb.2011.0243
242. Ma, J. F., and Furukawa, J. (2003). Recent progress in the research of external Al detoxification in higher plants: a minireview. J. Inorg. Biochem. 97, 46-51. doi: 10.1016/S0162-0134(03)00245-9
243. Ma, J. F., Ryan, P. R., and Delaize, E. (2001). Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273-278. doi: 10.1016/S1360-1385(01)01961-6
244. Ma, J. F., Shen, R., Zhao, Z., Wissuwa, M., Takeuchi, Y., Ebitani, T., et al. (2002). Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol. 43, 652-659. doi: 10.1093/pcp/pcf081
245. Ma, Z., Baskin, T. I., Brown, K. M., and Lynch, J. P. (2003). Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol. 131, 1381-1390. doi: 10.1104/pp.012161
246. Macgregor, D. R., Deak, K. I., Ingram, P. A., and Malamy, J. E. (2008). Root system architecture in Arabidopsisgrown in culture is regulated by sucrose uptake in the aerial tissues. Plant Cell 20, 2643-2660. doi: 10.1105/tpc.107.055475
247. Magalhaes, J. V., Garvin, D. F., Wang, Y., Sorrells, M. E., Klein, P. E., Schaffert, R. E., et al. (2004). Comparative mapping of a major aluminum tolerance gene in Sorghum and other species in the Poaceae. Genetics 167, 1905-1914. doi: 10.1534/genetics.103.023580
248. Mahajan, S., and Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139-158. doi: 10.1016/j.abb.2005.10.018
249. Malamy, J. E. (2005). Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28, 67-77. doi: 10.1111/j.1365-3040.2005.01306.x
250. Malamy, J. E., and Benfey, P. N. (1997). Down and out in Arabidopsis: the formation of lateral roots. Trends Plant Sci. 2, 390-396. doi: 10.1016/S1360-1385(97)90054-6
251. Malamy, J. E., and Ryan, K. S. (2001). Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol. 127, 899-909. doi: 10.1104/pp.010406
252. Mao, C. Z., Yang, L., Zheng, B.-S., Wu, Y.-R., Liu, F.-Y., and Wu, P. (2004). Comparative mapping of QTLs for Al tolerance in rice and identification of positional Al-induced genes. J. Zhejiang Univ. Sci. 5, 634-643. doi: 10.1631/jzus.2004.0634
253. Maraschin, F. D. S., Memelink, J., and Offringa, R. (2009). Auxin-induced, SCF(TIR1)-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J. 59, 100-109. doi: 10.1111/j.1365-313X.2009.03854.x
254. Marin-Rodriguez, M. C., Orchard, J., and Seymour, G. B. (2002). Pectate lyases, cell wall degradation and fruit softening. J. Exp. Bot. 53, 2115-2119. doi: 10.1093/jxb/erf089
255. Markmann, K., and Parniske, M. (2009). Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci. 14, 77-86. doi: 10.1016/j.tplants.2008.11.009
256. Marsh, J. F., Rakocevic, A., Mitra, R. M., Brocard, L., Sun, J., Eschstruth, A., et al. (2007). Medicago truncatulaNIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol. 144, 324-335. doi: 10.1104/pp.106.093021
257. Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T., and Takahashi, H. (2003). Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132, 597-605. doi: 10.1104/pp.102.019802
258. Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T., and Takahashi, H. (2004). Regulation of high-affinity sulfate transporters in plants: towards systematic analysis of sulphur signaling and regulation. J. Exp. Bot. 55, 1843-1849. doi: 10.1093/jxb/erh175
259. Matsumoto, H. (2000). Cell biology of aluminum toxicity and tolerance in higher plants. Int. Rev. Cytol. 200, 1-46. doi: 10.1016/S0074-7696(00)00001-2
260. Matsumoto, H., Senoo, Y., Kasai, M., and Maeshima, M. (1996). Response of the plant root to aluminum stress: analysis of the inhibition of the root elongation and changes in membrane function. J. Plant Res. 109, 99-105. doi: 10.1007/BF02344294
261. Mayzlish-Gati, E., De-Cuyper, C., Goormachtig, S., Beeckman, T., Vuylsteke, M., Brewer, P. B., et al. (2012). Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol. 160, 1329-1341. doi: 10.1104/pp.112.202358
262. McNally, K. L., Bruskiewich, R., Mackill, D., Buell, C. R., Leach, J. E., and Leung, H. (2006). Sequencing multiple and diverse rice varieties. Connecting whole-genome variation with phenotypes. Plant Physiol. 141, 26-31. doi: 10.1104/pp.106.077313
263. Meijer, M., and Murray, J. (2000). The role and regulation of D-type cyclins in the plant cell cycle. Plant Mol. Biol. 43, 621-633. doi: 10.1023/A:1006482115915
264. Meng, Y., Ma, X., Chen, D., Wu, P., and Chen, M. (2010). MicroRNA-mediated signaling involved in plant root development. Biochem. Biophys. Res. Commun. 393, 345-349. doi: 10.1016/j.bbrc.2010.01.129
265. Menzel, M. I., Oros-Peusquens, A.-M., Pohlmeier, A., Shah, J., Schurr, U., and Schneider, H. U. (2007). Comparing 1H-NMR imaging and relaxation mapping of German white asparagus from five different cultivation sites. J. Plant Nutr. Soil Sci. 170, 24-38. doi: 10.1002/jpln.200625114
266. Mergemann, H., and Sauter, M. (2000). Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol. 124, 609-614. doi: 10.1104/pp.124.2.609
267. Messinese, E., Mun, J. H., Yeun, L. H., Jayaraman, D., Rouge, P., Barre, A., et al. (2007). A novel nuclear protein interacts with the symbiotic DMI3 calcium-and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant-Microbe Interact. 20, 912-921. doi:10.1094/MPMI-20-8-0912.
268. Middleton, P. H., Jakab, J., Penmetsa, R. V., Starker, C. G., Doll, J., Kalo, P., et al. (2007). An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19, 1221-1234. doi: 10.1105/tpc.106.048264
269. Mitra, R., Gleason, C., and Edwards, A. (2004). A Ca 2 calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. U.S.A. 101, 4701-4705. doi: 10.1073/pnas.0400595101
270. Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A. S., Raghothama, K. G., et al. (2005). The ArabidopsisSUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl. Acad. Sci. U.S.A. 102, 7760-7765. doi: 10.1073/pnas.0500778102
271. Miwa, H., Kinoshita, A., Fukuda, H., and Sawa, S. (2009). Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J. Plant Res. 122, 31-39. doi: 10.1007/s10265-008-0207-3
272. Miyasaka, S. C., Buta, G. J., Howell, R. K., and Foy, C. D. (1991). Mechanism of aluminum tolerance in snapbeans: root exudation of citric acid. Plant Physiol. 96, 737-743. doi: 10.1104/pp.96.3.737
273. Miyasaka, S. C., Kochian, L. V., Shaff, J. E., and Foy, C. D. (1989). Mechanisms of aluminum tolerance in wheat: an investigation of genotypic differences in rhizosphere pH, K, and H transport, and root-cell membrane potentials. Plant Physiol. 91, 1188-1196. doi: 10.1104/pp.91.3.1188
274. Molas, M. L., and Kiss, J. Z. (2008). PKS1 plays a role in red-light-based positive phototropism in roots. Plant Cell Environ. 31, 842-849. doi: 10.1111/j.1365-3040.2008.01797.x
275. Moreno-Risueno, M. A., Van Norman, J. M., Moreno, A., Zhang, J., Ahnert, S. E., and Benfey, P. N. (2010). Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329, 1306-1311. doi: 10.1126/science.1191937
276. Morita, M. T. (2010). Directional gravity sensing in gravitropism. Annu. Rev. Plant Biol. 61, 705-720. doi: 10.1146/annurev.arplant.043008.092042
277. Moubayidin, L., Di Mambro, R., and Sabatini, S. (2009). Cytokinin-auxin crosstalk. Trends Plant Sci. 14, 557-562. doi: 10.1016/j.tplants.2009.06.010
278. Mullen, J. L., and Hangarter, R. P. (2003). Genetic analysis of the gravitropic set-point angle in lateral roots of Arabidopsis. Adv. Space Res. 31, 2229-2236. doi: 10.1016/S0273-1177(03)00249-7
279. Mullen, J. L., Wolverton, C., Ishikawa, H., Hangarter, R. P., and Evans, M. L. (2002). Spatial separation of light perception and growth response in maize root phototropism. Plant Cell Environ. 25, 1191-1196. doi: 10.1046/j.1365-3040.2002.00899.x
280. Muller, B., and Sheen, J. (2008). Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453, 1094-1097. doi: 10.1038/nature06943
281. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681. doi: 10.1146/annurev.arplant.59.032607.092911
282. Munos, S., Cazettes, C., Fizames, C., Gaymard, F., Tillard, P., Lepetit, M., et al. (2004). Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell 16, 2433-2447. doi: 10.1105/tpc.104.024380
283. Nacry, P., Canivenc, G., and Muller, B. (2005). A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol. 138, 2061-2074. doi: 10.1104/pp.105.060061
284. Nap, J., and Bisseling, T. (1990). The roots of nodulins. Physiol. Plant. 79, 407-414. doi: 10.1111/j.1399-3054.1990.tb06760.x
285. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., and Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633-650. doi: 10.1046/j.1365-313X.2003.01657.x
286. Nishimura, T., Nakano, H., Hayashi, K.-I., Niwa, C., and Koshiba, T. (2009). Differential downward stream of auxin synthesized at the tip has a key role in gravitropic curvature via TIR1/AFBs-mediated auxin signaling pathways. Plant Cell Physiol. 50, 1874-1885. doi: 10.1093/pcp/pcp129
287. Noh, B., Bandyopadhyay, A., Peer, W. A., Spalding, E. P., and Murphy, A. S. (2003). Enhanced gravi-and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature 423, 999-1002. doi: 10.1038/nature01716
288. Noh, B., Murphy, A. S., and Spalding, E. P. (2001). Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13, 2441-2454. doi: 10.1105/tpc.010350
289. Nutman, P. S. (1948). Physiological studies on nodule formation: I. The relation between nodulation and lateral root formation in red clover. Ann. Bot. 12, 81-96.
290. Ogawa, M., Kay, P., Wilson, S., and Swain, S. M. (2009). ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21, 216-233. doi: 10.1105/tpc.108.063768
291. Ohkama, N., Takei, K., Sakakibara, H., Hayashi, H., Yoneyama, T., and Fujiwara, T. (2002). Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol. 43, 1493-1501. doi: 10.1093/pcp/pcf183
292. Okushima, Y., Overvoorde, P. J., Arima, K., Alonso, J. M., Chan, A., Chang, C., et al. (2005). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17, 444-463. doi: 10.1105/tpc.104.028316
293. Olah, B., Briere, C., Becard, G., Denarie, J., and Gough, C. (2005). Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signaling pathway. Plant J. 44, 195-207. doi: 10.1111/j.1365-313X.2005.02522.x
294. O'Malley, R. C., Rodriguez, F. I., Esch, J. J., Binder, B. M., O'Donnell, P., Klee, H. J., et al. (2005). Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. Plant J. 41, 651-659. doi: 10.1111/j.1365-313X.2004.02331.x
295. Osmont, K. S., Sibout, R., and Hardtke, C. S. (2007). Hidden branches: developments in root system architecture. Annu. Rev. Plant Biol. 58, 93-113. doi: 10.1146/annurev.arplant.58.032806.104006
296. Overvoorde, P., Fukaki, H., and Beeckman, T. (2010). Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2, a001537. doi: 10.1101/cshperspect.a001537
297. Pacheco-Villalobos, D., and Hardtke, C. S. (2012). Natural genetic variation of root system architecture from Arabidopsis to Brachypodium: towards adaptive value. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1552-1558. doi: 10.1098/rstb.2011.0237
298. Paquette, A. J., and Benfey, P. N. (2005). Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol. 138, 636-640. doi: 10.1104/pp.104.058362
299. Pareek, A., Singla-Pareek, S. L., Sopory, S. K., and Grover, A. (2007). "Analysis of salt stress-related transcriptome fingerprints from diverse plant species, " in Genomics-Assisted Crop Improvement, Vol. 1, eds R. Varshney and R. Tuberosa (Berlin: Springer), 267-287.
300. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat. Rev. Microbiol. 6, 763-775. doi: 10.1038/nrmicro1987
301. Parry, G., Marchant, A., May, S., Swarup, R., Swarup, K., James, N., et al. (2001). Quick on the uptake: characterization of a family of plant auxin influx carriers. J. Plant Growth Regul. 20, 217-225. doi: 10.1007/s003440010030
302. Paszkowski, U., and Boller, T. (2002). The growth defect of lrt1, a maize mutant lacking lateral roots, can be complemented by symbiotic fungi or high phosphate nutrition. Planta 214, 584-590. doi: 10.1007/s004250100642
303. Péret, B., De Rybel, B., Casimiro, I., Benková, E., Swarup, R., Laplaze, L., et al. (2009a). Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14, 399-408. doi: 10.1016/j.tplants.2009.05.002
304. Péret, B., Larrieu, A., and Bennett, M. J. (2009b). Lateral root emergence: a difficult birth. J. Exp. Bot. 60, 3637-3643. doi: 10.1093/jxb/erp232
305. Perez-Perez, J. M. (2007). Hormone signaling and root development: an update on the latest Arabidopsis thalianaresearch. Funct. Plant Biol. 34, 163-171. doi: 10.1071/FP06341
306. Perez-Torres, C.-A., Lopez-Bucio, J., Cruz-Ramirez, A., Ibarra-Laclette, E., Dharmasiri, W., Estelle, M., et al. (2008). Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20, 3258-3272. doi: 10.1105/tpc.108.058719
307. Pernisova, M., Klima, P., Horak, J., Valkova, M., Malbeck, J., Soucek, P., et al. (2009). Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc. Natl. Acad. Sci. U.S.A. 106, 3609-3614. doi: 10.1073/pnas.0811539106
308. Perret, J. S., Al-Belushi, M. E., and Deadman, M. (2007). Non-destructive visualization and quantification of roots using computed tomography. Soil Biol. Biochem. 39, 391-399. doi: 10.1016/j.soilbio.2006.07.018
309. Perrin, R. M., Young, L.-S., Murthy, U. M. N., Harrison, B. R., Wang, Y., Will, J. L., et al. (2005). Gravity signal transduction in primary roots. Ann. Bot. 96, 737-743. doi: 10.1093/aob/mci227
310. Petrásek, J., and Friml, J. (2009). Auxin transport routes in plant development. Development 136, 2675-2688. doi: 10.1242/dev.030353
311. Pirozynski, K. A., and Malloch, D. W. (1975). The origin of land plants: a matter of mycotrophism. Biosystems 6, 153. doi: 10.1016/0303-2647(75)90023-4
312. Provorov, N. A. (2000). The population genetics of nodule bacteria. Zh. Obshch. Biol. 61, 229-257.
313. Puig, J., Pauluzzi, G., Guiderdoni, E., and Gantet, P. (2012). Regulation of shoot and root development through mutual signaling. Mol. Plant 5, 974-983. doi: 10.1093/mp/sss047
314. + homeostasis. Proc. Natl. Acad. Sci. U.S.A. 99, 9061-9066. doi: 10.1073/pnas.132092099
315. Rani Debi, B., Chhun, T., Taketa, S., Tsurumi, S., Xia, K., Miyao, A., et al. (2005). Defects in root development and gravity response in the aem1 mutant of rice are associated with reduced auxin efflux. J. Plant Physiol. 162, 678-685. doi: 10.1016/j.jplph.2004.09.012
316. Rebouillat, J., Dievart, A., Verdeil, J. L., Escoute, J., Giese, G., Breitler, J. C., et al. (2009). Molecular genetics of rice root development. Rice 2, 15-34. doi: 10.1007/s12284-008-9016-5
317. Reed, J. W. (2001). Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420-425. doi: 10.1016/S1360-1385(01)02042-8
318. Relic, B., Talmont, F., Kopcinska, J., Golinowski, W., Prome, J. C., and Broughton, W. J. (1993). Biological activity of Rhizobium sp. NGR 234 nod-factors on Macroptilium atropurpureum. Mol. Plant Microbe Interact. 6, 764-774. doi: 10.1094/MPMI-6-764
319. Remans, T., Nacry, P., Pervent, M., Filleur, S., Diatloff, E., Mounier, E., et al. (2006a). The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc. Natl. Acad. Sci. U.S.A. 103, 19206-19211. doi: 10.1073/pnas.0605275103
320. Remans, T., Nacry, P., Prevent, M., Girin, T., Tillard, P., Lepetit, M., et al. (2006b). A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol. 140, 909-921. doi: 10.1104/pp.105.075721
321. Reymond, M., Svistoonoff, S., Loudet, O., Nussaume, L., and Desnos, T. (2006). Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ. 29, 115-125. doi: 10.1111/j.1365-3040.2005.01405.x
322. Richter, S., Anders, N., Wolters, H., Beckmann, H., Thomann, A., Heinrich, R., et al. (2010). Role of the GNOM gene in Arabidopsis apical-basal patterning-from mutant phenotype to cellular mechanism of protein action. Eur. J. Cell Biol. 89, 138-144. doi: 10.1016/j.ejcb.2009.11.020
323. Rodriguez-Barrueco, C., and De Castro, F. B. (1973). Cytokinin-induced pseudonodules on Alnus glutinosa. Physiol. Plant. 29, 277-280. doi: 10.1111/j.1399-3054.1973.tb03107.x
324. Ruppel, N. J., Hangarter, R. P., and Kiss, J. Z. (2001). Red-light-induced positive phototropism in Arabidopsisroots. Planta 212, 424-430. doi: 10.1007/s004250000410
325. Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B.-H., Matsumoto, T. K., et al. (2001). AtHKT1 is a salt tolerance determinant that controls Na(+) entry into plant roots. Proc. Natl. Acad. Sci. U.S.A. 98, 14150-14155. doi: 10.1073/pnas.241501798
326. Ruyter-Spira, C., Kohlen, W., Charnikhova, T., Van Zeijl, A., Van Bezouwen, L., De Ruijter, N., et al. (2011). Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol. 155, 721-734. doi: 10.1104/pp.110.166645
327. Ruzicka, K., Simaskova, M., Duclercq, J., Petrasek, J., Zazimalova, E., Simon, S., et al. (2009). Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl. Acad. Sci. U.S.A. 106, 4284-4289. doi: 10.1073/pnas.0900060106
328. Ryan, P. R., Ditomaso, J. M., and Kochian, L. V. (1993). Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44, 437-446. doi: 10.1093/jxb/44.2.437
329. Saab, I. N., Sharp, R. E., Pritchard, J., and Voetberg, G. S. (1990). Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol. 93, 1329-1336. doi: 10.1104/pp.93.4.1329
330. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., et al. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472. doi: 10.1016/S0092-8674(00)81535-4
331. Sabatini, S., Heidstra, R., Wildwater, M., and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354. doi: 10.1101/gad.252503
332. Saito, K. (2000). Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3, 188-195. doi: 10.1016/S1369-5266(00)80064-3
333. Saito, K., Yoshikawa, M., Yano, K., Miwa, H., Uchida, H., Asamizu, E., et al. (2007). NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19, 610-624. doi: 10.1105/tpc.106.046938
334. Sanchez-Calderon, L., Lopez-Bucio, J., Chacon-Lopez, A., Cruz-Ramirez, A., Nieto-Jacobo, F., Dubrovsky, J. G., et al. (2005). Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol. 46, 174-184. doi: 10.1093/pcp/pci011
335. Sano, T., and Nagata, T. (2002). The possible involvement of a phosphate-induced transcription factor encoded by Phi-2 gene from Tobacco in ABA-signaling pathways. Plant Cell Physiol. 43, 12-20. doi: 10.1093/pcp/pcf002
336. Scheres, B., McKhann, H. I., and Van Den Berg, C. (1996). Roots redefined: anatomical and genetic analysis of root development. Plant Physiol. 111, 959-964.
337. Schmidt, W., and Schikora, A. (2001). Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol. 125, 2078-2084. doi: 10.1104/pp.125.4.2078
338. Schmohl, N., Pilling, J., Fisahn, J., and Horst, W. J. (2000). Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol. Plant. 109, 419-427. doi: 10.1034/j.1399-3054.2000.100408.x
339. Schüßler, A., Schwarzott, D., and Walker, C. (2001). A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 1413. doi: 10.1017/S0953756201005196
340. Schulze, J., Temple, G., Temple, S. J., Beschow, H., and Vance, C. P. (2006). Nitrogen fixation by white lupin under phosphorus deficiency. Ann. Bot. 98, 731-740. doi: 10.1093/aob/mcl154
341. Shane, M., and Lambers, H. (2005). Cluster roots: a curiosity in context. Plant Soil 274, 101-125. doi: 10.1007/s11104-004-2725-7
342. Sharp, R. E., Silk, W. K., and Hsiao, T. C. (1988). Growth of the maize primary root at low water potentials: I. Spatial distribution of expansive growth. Plant Physiol. 87, 50-57. doi: 10.1104/pp.87.1.50
343. Shashidhar, H. E., Henry, A., and Hardy, B. (2012). Methodologies for Root Drought Studies in Rice. Los Baños: International Rice Research Institute, 65 p.
344. Sheng, M., Tang, M., Chen, H., Yang, B., Zhang, F., and Huang, Y. (2008). Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18, 287-296. doi: 10.1007/s00572-008-0180-7
345. Shilev, S., Sancho, E. D., and Benlloch-Gonzalez, M. (2010). Rhizospheric bacteria alleviate salt-produced stress in sunflower. J. Environ. Manage. 95, S37-S41. doi: 10.1016/j.jenvman.2010.07.019
346. Shimizu, A., Yanagihara, S., Kawasaki, S., and Ikehashi, H. (2004). Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor. Appl. Genet. 109, 1361-1368. doi: 10.1007/s00122-004-1751-4
347. Signora, L., De Smet, I., Foyer, C. H., and Zhang, H. (2001). ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J. 28, 655-662. doi: 10.1046/j.1365-313x.2001.01185.x
348. Simon, L., Bousquet, J., Levesque, R. C., and Lalonde, M. (1993). Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67-69. doi: 10.1038/363067a0
349. Sivaguru, M., Ezaki, B., He, Z.-H., Tong, H., Osawa, H., Baluska, F., et al. (2000). Aluminum-induced 1 3-beta-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol. 124, 991-1006. doi: 10.1104/pp.124.3.991
350. Sivaguru, M., and Horst, W. J. (1998). The distal part of the transition zone is the most aluminum-sensitive apical root zone of Maize. Plant Physiol. 116, 155-163. doi: 10.1104/pp.116.1.155
351. Sivaguru, M., Horst, W. J., Eticha, D., and Matsumoto, H. (2006). Aluminum inhibits apoplastic flow of high-molecular weight solutes in root apices of Zea mays L. J. Plant Nutr. Soil Sci. 169, 679-690. doi: 10.1002/jpln.200620603
352. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T., et al. (2005). NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789-1791. doi: 10.1126/science.1111025
353. Snapp, S. S., and Shennan, C. (1992). Effects of salinity on root growth and death dynamics of tomato, Lycopersiconesculentum Mill. New Phytol. 121, 71-79. doi: 10.1111/j.1469-8137.1992.tb01094.x
354. Soni, R. (1995). A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7, 85-103. doi: 10.1105/tpc.7.1.85
355. Sreevidya, V. S., Hernandez-Oane, R. J., Gyaneshwar, P., Lara-Flores, M., Ladha, J. K., and Reddy, P. M. (2010). Changes in auxin distribution patterns during lateral root development in rice. Plant Sci. 178, 531-538. doi: 10.1016/j.plantsci.2010.03.004
356. Steffens, B., and Sauter, M. (2005). Epidermal cell death in rice is regulated by ethylene, gibberellin, and abscisic acid. Plant Physiol. 139, 713-721. doi: 10.1104/pp.105.064469
357. 2 through an autoamplified signal pathway. Plant Cell 21, 184-196. doi: 10.1105/tpc.108.061887
358. Steffens, B., Wang, J., and Sauter, M. (2006). Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223, 604-612. doi: 10.1007/s00425-005-0111-1
359. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C. L., Paris, S., et al. (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316-318. doi: 10.1126/science.286.5438.316
360. Strabala, T., and O'Donnell, P. (2006). Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR. Plant Physiol. 140, 1331-1344. doi: 10.1104/pp.105.075515
361. Strack, D., Fester, T., Hause, B., Schliemann, W., and Walter, M. H. (2003). Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J. Chem. Ecol. 29, 1955-1979. doi: 10.1023/A:1025695032113
362. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., et al. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959-962. doi: 10.1038/nature00841
363. Sun, J., Xu, Y., Ye, S., Jiang, H., Chen, Q., Liu, F., et al. (2009). Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21, 1495-1511. doi: 10.1105/tpc.108.064303
364. Sun, P., Tian, Q.-Y., Chen, J., and Zhang, W.-H. (2010). Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J. Exp. Bot. 61, 347-356. doi: 10.1093/jxb/erp306
365. Suralta, R. R., Inukai, Y., and Yamauchi, A. (2008). Genotypic variations in responses of lateral root development to transient moisture stresses in rice cultivars. Plant Prod. Sci. 11, 324-335. doi: 10.1626/pps.11.324
366. Svistoonoff, S., Sy, M.-O., Diagne, N., Barker, D. G., Bogusz, D., and Franche, C. (2010). Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation. Mol. Plant Microbe Interact. 23, 740-747. doi: 10.1094/MPMI-23-6-0740
367. Swarup, K., Benkova, E., Swarup, R., Casimiro, I., Péret, B., Yang, Y., et al. (2008). The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946-954. doi: 10.1038/ncb1754
368. Swarup, R., Kramer, E. M., Perry, P., Knox, K., Ottoline Leyser, H. M., Haseloff, J., et al. (2005). Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057-1065. doi: 10.1038/ncb1316
369. Swensen, S. M. (1996). The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. Am. J. Bot. 83, 1503-1512. doi: 10.2307/2446104
370. Takahashi, H. (2010). Regulation of sulfate transport and assimilation in plants. Int. Rev. Cell Mol. Biol. 281, 129-159. doi: 10.1016/S1937-6448(10)81004-4
371. Takahashi, H., Noji, M., and Saito, K. (1999). Molecular regulation and engineering of sulfur transport and assimilation. Tanpakushitsu Kakusan Koso 44, 2291-2298.
372. Takahashi, H., Watanabe-Takahashi, A., Smith, F. W., Blake-Kalff, M., Hawkesford, M. J., and Saito, K. (2000). The roles of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J. 23, 171-182. doi: 10.1046/j.1365-313x.2000.00768.x
373. Taramino, G., Sauer, M., Stauffer, J. L., Multani, D., Niu, X., Sakai, H., et al. (2007). The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation. Plant J. 50, 649-659. doi: 10.1111/j.1365-313X.2007.03075.x
374. + transport in higher plants. Ann. Bot. 91, 503-527. doi: 10.1093/aob/mcg058
375. Ticconi, C. A., Delatorre, C. A., Lahner, B., Salt, D. E., and Abel, S. (2004). Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J. 37, 801-814. doi: 10.1111/j.1365-313X.2004.02005.x
376. Ticconi, C. A., Lucero, R. D., Sakhonwasee, S., Adamson, A. W., Creff, A., Nussaume, L., et al. (2009). ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc. Natl. Acad. Sci. U.S.A. 106, 14174-14179. doi: 10.1073/pnas.0901778106
377. Tillich, H. (1977). Vergleichend morphologische Untersuchungen zur Identität der Gramineen-Primärwurzel. Flora 166, 415-421.
378. Tirichine, L., Sandal, N., Madsen, L. H., Radutoiu, S., Albrektsen, A. S., Sato, S., et al. (2007). A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315, 104-107. doi: 10.1126/science.1132397
379. Tirlapur, U. K., and Konig, K. (1999). Technical advance: near-infrared femtosecond laser pulses as a novel non-invasive means for dye-permeation and 3D imaging of localised dye-coupling in the Arabidopsis root meristem. Plant J. 20, 363-370. doi: 10.1046/j.1365-313X.1999.t01-1-00603.x
380. Tracy, S. R., Roberts, J. A., Black, C. R., McNeill, A., Davidson, R., and Mooney, S. J. (2010). The X-factor: visualizing undisturbed root architecture in soils using X-ray computed tomography. J. Exp. Bot. 61, 311-313. doi: 10.1093/jxb/erp386
381. Tsuchisaka, A., and Theologis, A. (2004). Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 136, 2982-3000. doi: 10.1104/pp.104.049999
382. Tung, C.-W., Zhao, K., Wright, M. H., Ali, M. L., Jung, J., Kimball, J., et al. (2010). Development of a research platform for dissecting phenotype-genotype associations in rice (Oryza spp.). Rice 3, 205-217. doi: 10.1007/s12284-010-9056-5
383. Ueda, M., Koshino-Kimura, Y., and Okada, K. (2005). Stepwise understanding of root development. Curr. Opin. Plant Biol. 8, 71-76. doi: 10.1016/j.pbi.2004.11.014
384. Uexküll, H. R., and Mutert, E. (1995). Global extent, development and economic impact of acid soils. Plant Soil 171, 1-15. doi: 10.1007/BF00009558
385. Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N., and Yamaguchi, S. (2010). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 51, 1118-1126. doi: 10.1093/pcp/pcq084
386. Uozumi, N., Kim, E. J., Rubio, G., Yamaguchi, T., Muto, S., Tsuboi, A., et al. (2000). The Arabidopsis HKT1 gene homolog mediates inward Na(+) currents in Xenopus laevis oocytes and Na(+) uptake in Saccharomyces cerevisiae. Plant Physiol. 122, 1249-1259. doi: 10.1104/pp.122.4.1249
387. Verma, D. P. S., Hu, C.-A., and Zhang, M. (1992). Root nodule development: origin, function and regulation of nodulin genes. Physiol. Plant. 85, 253-265. doi: 10.1111/j.1399-3054.1992.tb04730.x
388. Vernie, T., Moreau, S., de Billy, F., Plet, J., Combier, J.-P., Rogers, C., et al. (2008). EFD is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20, 2696-2713. doi: 10.1105/tpc.108.059857
389. Vierheilig, H., Bago, B., Lerat, S., and Piche, Y. (2002). Shoot-produced, light-dependent factors are partially involved in the expression of the arbuscular mycorrhizal (AM) status of AM host and non-host plants. J. Plant Nutr. 165, 21-25. doi: 10.1002/1522-2624(200202)165:1
390. Vilella, A. J., Severin, J., Ureta-Vidal, A., Heng, L., Durbin, R., and Birney, E. (2009). EnsemblCompara genetrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327-335. doi: 10.1101/gr.073585.107
391. Walch-Liu, P., Ivanov, I. I., Filleur, S., Gan, Y., Remans, T., and Forde, B. G. (2006). Nitrogen regulation of root branching. Ann. Bot. 97, 875-881. doi: 10.1093/aob/mcj601
392. Wang, J. R., Hu, H., Wand, G.-H., Li, J., Chen, J.-Y., and Wu, P. (2009). Expression of PIN genes in rice (Oryza sativaL.): tissue specificity and regulation by hormones. Mol. Plant 2, 823-831. doi: 10.1093/mp/ssp023
393. Wang, J.-W., Wang, L.-J., Mao, Y.-B., Cai, W.-J., Xue, H.-W., and Chen, X.-Y. (2005). Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17, 2204-2216. doi: 10.1105/tpc.105.033076
394. Wiegers, B. S., Cheer, A. Y., and Silk, W. K. (2009). Modeling the hydraulics of root growth in three dimensions with phloem water sources. Plant Physiol. 150, 2092-103. doi: 10.1104/pp.109.138198
395. Williamson, L. C., Ribrioux, S. P. C. P., Fitter, A. H., and Leyser, H. M. O. (2001). Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol. 126, 875-882. doi: 10.1104/pp.126.2.875
396. Woll, K., Borsuk, L. A., Stransky, H., Nettleton, D., Schnable, P. S., and Hochholdinger, F. (2005). Isolation, characterization, and pericycle-specific transcriptome analyses of the novel maize lateral and seminal root initiation mutant rum1. Plant Physiol. 139, 1255-1267. doi: 10.1104/pp.105.067330
397. Wu, G., Lewis, D. R., and Spalding, E. P. (2007). Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell 19, 1826-1837. doi: 10.1105/tpc.106.048777
398. Xie, Q. (2000). Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14, 3024-3036. doi: 10.1101/gad.852200
399. Xu, K., Xu, X., Fukao, T., Canlas, P., Maghirang-Rodriguez, R., Heuer, S., et al. (2006). Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705-708. doi: 10.1038/nature04920
400. Xu, M., Zhu, L., Shou, H., and Wu, P. (2005). A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674-1681. doi: 10.1093/pcp/pci183
401. Xue, R., and Zhang, B. (2007). Increased endogenous methyl jasmonate altered leaf and root development in transgenic soybean plants. J. Genet. Genomics 34, 339-346. doi: 10.1016/S1673-8527(07)60036-8
402. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., et al. (2001). The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017-1023. doi: 10.1093/pcp/pce127
403. Yamaji, N., Huang, C. F., Nagao, S., Yano, M., Sato, Y., Nagamura, Y., et al. (2009). A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21, 3339-3349. doi: 10.1105/tpc.109.070771
404. Yan, J., Shah, T., Warburton, M., Buckler, E. S., McMullen, M. D., and Crouch, J. (2009). Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4:e8451. doi: 10.1371/journal.pone.0008451
405. Yano, K., Yoshida, S., Müller, J., Singh, S., Banba, M., Vickers, K., et al. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. 105, 20540-20545. doi: 10.1073/pnas.0811417106
406. Yi, K., Wu, Z., Zhou, J., Du, L., Guo, L., Wu, Y., et al. (2005). OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol. 138, 2087-2096. doi: 10.1104/pp.105.063115
407. Yokoyama, R., and Nishitani, K. (2004). Genomic basis for cell-wall diversity in plants. A comparative approach to gene families in rice and Arabidopsis. Plant Cell Physiol. 45, 1111-1121. doi: 10.1093/pcp/pch151
408. Yoneyama, K., Takeuchi, Y., and Sekimoto, H. (2007a). Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225, 1031-1038. doi: 10.1007/s00425-006-0410-1
409. Yoneyama, K., Xie, X., and Kusumoto, D. (2007b). Nitrogen deficiency as well as phosphorus deficiency in Sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular. Planta 227, 125-132. doi: 10.1007/s00425-007-0600-5
410. Yoneyama, K., Xie, X., and Sekimoto, H. (2008). Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol. 179, 484-494. doi: 10.1111/j.1469-8137.2008.02462.x
411. Yoshida, S., and Parniske, M. (2005). Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J. Biol. Chem. 280, 9203-9209. doi: 10.1074/jbc.M411665200
412. Yoshimoto, N., Takahashi, H., Smith, F. W., Yamaya, T., and Saito, K. (2002). Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 29, 465-473. doi: 10.1046/j.0960-7412.2001.01231.x
413. Young, L. M., and Evans, M. L. (1996). Patterns of auxin and abscisic acid movement in the tips of gravistimulated primary roots of maize. Plant Growth Regul. 20, 253-258. doi: 10.1007/BF00043315
414. Yun, H., Joo, S., Park, C., and Kim, S. (2009). Effects of brassinolide and IAA on ethylene production and elongation in maize primary roots. J. Plant Biol. 52, 268-274. doi: 10.1007/s12374-009-9032-z
415. Zeng, H.-Q., Zhu, Y.-Y., Bao, Y., Shen, Q.-R., Guo, K., Huang, S.-Q., et al. (2010). Relationship between the development of tomato lateral roots and expression of miR164, NAC1 under P deficiency. Acta Metall. Sin. 16, 166-171.
416. Zhang, H., and Forde, B. G. (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409. doi: 10.1126/science.279.5349.407
417. Zhang, H., Jennings, A., Barlow, P. W., and Forde, B. (1999). Dual pathways for regulation of root branching by nitrate. Proc. Natl. Acad. Sci. U.S.A. 96, 6529-6534. doi: 10.1073/pnas.96.11.6529
418. Zhang, Z., Ersoz, E., Lai, C.-Q., Todhunter, R. J., Tiwari, H. K., Gore, M. A., et al. (2010). Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355-360. doi: 10.1038/ng.546
419. Zhao, Y., Hu, Y., Dai, M., Huang, L., and Zhou, D.-X. (2009). The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21, 736-748. doi: 10.1105/tpc.108.061655
420. Zhu, J. K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant. Biol. 53, 247-273. doi: 10.1146/annurev.arplant.53.091401.143329
421. Zhu, J. K., Liu, J., and Xiong, L. (1998). Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10, 1181-1191. doi: 10.1105/tpc.10.7.1181
422. Zidan, I., Azaizeh, H., and Neumann, P. M. (1990). Does salinity reduce growth in maize root epidermal cells by inhibiting their capacity for cell wall acidification? Plant Physiol. 93, 7-11. doi: 10.1104/pp.93.1.7