Growing out of stress: The role of cell- and organ-scale growth control in plant water-stress responses

Plant Cell

Volumn 28, Issue 8, 2016, Pages 1769-1782

  Feng, Wei ^a   Lindner, Heike ^a   Robbins Ii, Neil E ^b   Dinneny, José R ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

WATER;

CELL WALL; DEHYDRATION; DESICCATION; DROUGHT; METABOLISM; PLANT;

CELL WALL; DEHYDRATION; DESICCATION; DROUGHTS; PLANTS; WATER;

EID: 84984820371     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.16.00182     Document Type: Review

References (148)

1. Akashi, T., Kawasaki, S., and Shibaoka, H. (1990). Stabilization of cortical microtubules by the cell wall in cultured tobacco cells: Effects of extensin on the cold-stability of cortical microtubules. Planta 182: 363–369.
2. Arai-Sanoh, Y., Takai, T., Yoshinaga, S., Nakano, H., Kojima, M., Sakakibara, H., Kondo, M., and Uga, Y. (2014). Deep rooting conferred by DEEPER ROOTING 1 enhances rice yield in paddy fields. Sci. Rep. 4: 5563.
3. Bailey, P.H.J., Currey, J.D., and Fitter, A.H. (2002). The role of root system architecture and root hairs in promoting anchorage against uprooting forces in Allium cepa and root mutants of Arabidopsis thaliana. J.Exp.Bot.53: 333–340.
4. Baluska, F., Samaj, J., Wojtaszek, P., Volkmann, D., and Menzel, D. (2003). Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol. 133: 482–491.
5. Bao, Y., et al. (2014). Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc. Natl. Acad. Sci. USA 111: 9319–9324.
6. Beauzamy, L., Nakayama, N., and Boudaoud, A. (2014). Flowers under pressure: ins and outs of turgor regulation in development. Ann. Bot. (Lond.) 114: 1517–1533.
7. Bernier, J., Serraj, R., Kumar, A., Venuprasad, R., Impa, S., Veeresh Gowda, R.P., Oane, R., and Atlin, G. (2009). The large-effect drought-resistance QTL qtl12.1 increases water uptake in upland rice. Field Crops Res. 110: 139–146.
8. Blancaflor, E.B., Fasano, J.M., and Gilroy, S. (1998). Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol. 116: 213–222.
9. Boisson-Dernier, A., Kessler, S.A., and Grossniklaus, U. (2011). The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J. Exp. Bot. 62: 1581–1591.
10. Boisson-Dernier, A., Lituiev, D.S., Nestorova, A., Franck, C.M., Thirugnanarajah, S., and Grossniklaus, U. (2013). ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol. 11: e1001719.
11. Boisson-Dernier, A., Roy, S., Kritsas, K., Grobei, M.A., Jaciubek, M., Schroeder, J.I., and Grossniklaus, U. (2009). Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136: 3279–3288.
12. Borsa, A.A., Agnew, D.C., and Cayan, D.R. (2014). Remote hydrology. Ongoing drought-induced uplift in the western United States. Science 345: 1587–1590.
13. Brutnell, T.P., Bennetzen, J.L., and Vogel, J.P. (2015). Brachypodium distachyon and Setaria viridis: Model genetic systems for the grasses. Annu. Rev. Plant Biol. 66: 465–485.
14. Burk, D.H., and Ye, Z.-H. (2002). Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14: 2145–2160.
15. Burton, R.A., Gidley, M.J., and Fincher, G.B. (2010). Heterogeneity in the chemistry, structure and function of plant cell walls. Nat. Chem. Biol. 6: 724–732.
16. Cassab, G.I., Eapen, D., and Campos, M.E. (2013). Root hydrotro-pism:anupdate.Am.J.Bot.100: 14–24.
17. Christmann, A., Grill, E., and Huang, J. (2013). Hydraulic signals in long-distance signaling. Curr. Opin. Plant Biol. 16: 293–300.
18. Cosgrove, D.J. (2016a). Catalysts of plant cell wall loosening. F1000 Res. 5: 5.
19. Cosgrove, D.J. (2016b). Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J. Exp. Bot. 67: 463–476.
20. Cosgrove, D.J. (2014). Re-constructing our models of cellulose and primary cell wall assembly. Curr. Opin. Plant Biol. 22: 122–131.
21. Cosgrove, D.J., and Green, P.B. (1981). Rapid suppression of growth by blue light: Biophysical mechanism of action. Plant Physiol. 68: 1447–1453.
22. Courtois, B., Ahmadi, N., Khowaja, F., Price, A.H., Rami, J.-F., Frouin, J., Hamelin, C., and Ruiz, M. (2009). Rice root genetic architecture: Meta-analysis from a drought QTL database. Rice (N.Y.) 2: 115–128.
23. Dai, F., Zhang, C., Jiang, X., Kang, M., Yin, X., Lü, P., Zhang, X., Zheng, Y., and Gao, J. (2012). RhNAC2 and RhEXPA4 are involved in the regulation of dehydration tolerance during the expansion of rose petals. Plant Physiol. 160: 2064–2082.
24. Deak, K.I., and Malamy, J. (2005). Osmotic regulation of root system architecture. Plant J. 43: 17–28.
25. Dinneny, J.R. (2014). A gateway with a guard: how the endodermis regulates growth through hormone signaling. Plant Sci. 214: 14–19.
26. Dinneny, J.R. (2015). A developmental biologist’s journey to rediscover the Zen of plant physiology. F1000Research 2015 4: 264.
27. Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J., and Benfey, P.N. (2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320: 942–945.
28. Do Amaral, S.H., De Assis, S.A., de Faria Oliveira, O., and Mascarenhas, M. (2005). Partial purification and characterization of pectin methylesterase from orange (Citrus sinensis) cv.Pera-rio. J. Food Biochem. 29: 367–380.
29. Duan, L., Dietrich, D., Ng, C.H., Chan, P.M.Y., Bhalerao, R., Bennett, M.J., and Dinneny, J.R. (2013). Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25: 324–341.
30. Duan, Q., Kita, D., Li, C., Cheung, A.Y., and Wu, H.-M. (2010). FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl. Acad. Sci. USA 107: 17821–17826.
31. Eapen, D., Barroso, M.L., Campos, M.E., Ponce, G., Corkidi, G., Dubrovsky, J.G., and Cassab, G.I. (2003). A no hydrotropic response root mutant that responds positively to gravitropism in Arabidopsis. Plant Physiol. 131: 536–546.
32. Eghball, B., and Maranville, J.W. (1993). Root development and nitrogen influx of corn genotypes grown under combined drought and nitrogen stresses. Agron. J. 85: 147–152.
33. Endler, A., Kesten, C., Schneider, R., Zhang, Y., Ivakov, A., Froehlich, A., Funke, N., and Persson, S. (2015). A mechanism for sustained cellulose synthesis during salt stress. Cell 162: 1353–1364.
34. Erickson, R.O. (1976). Modeling of plant growth. Annu. Rev. Plant Physiol. 27: 407–434.
35. Erickson, R.O., and Silk, W.K. (1980). The kinematics of plant growth. Sci. Am. 242: 134–151.
36. Esau, K. (1953). Plant Anatomy, (New York: John Wiley & Sons).
37. Escobar-Restrepo, J.-M., Huck, N., Kessler, S., Gagliardini, V., Gheyselinck, J., Yang, W.-C., and Grossniklaus, U. (2007). The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317: 656–660.
38. Ferrari, S., Savatin, D.V., Sicilia, F., Gramegna, G., Cervone, F., and Lorenzo, G.D. (2013). Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4: 49.
39. Furuichi, T., Iida, H., Sokabe, M., and Tatsumi, H.(2012). Expression of Arabidopsis MCA1 enhanced mechanosensitive channel activity in the Xenopus laevis oocyte plasma membrane. Plant Signal. Behav. 7: 1022–1026.
40. Galvan-Ampudia, C.S., Julkowska, M.M., Darwish, E., Gandullo, J., Korver, R.A., Brunoud, G., Haring, M.A., Munnik, T., Vernoux, T., and Testerink, C. (2013). Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23: 2044–2050.
41. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jürgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219–230.
42. Geng, Y., Wu, R., Wee, C.W., Xie, F., Wei, X., Chan, P.M.Y., Tham, C., Duan, L., and Dinneny, J.R. (2013). A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25: 2132–2154.
43. Giarola, V., Krey, S., von den Driesch, B., and Bartels, D. (2016). The Craterostigma plantagineum glycine-rich protein CpGRP1 interacts with a cell wall-associated protein kinase 1 (CpWAK1) and accumulates in leaf cell walls during dehydration. New Phytol. 210: 535–550.
44. Grant, G.T., Morris, E.R., Rees, D.A., Smith, P.J.C., and Thom, D. (1973). Biological interactions between polysaccharides and divalent cations: The egg-box model. FEBS Lett. 32: 195–198.
45. Guo, H., Li, L., Ye, H., Yu, X., Algreen, A., and Yin, Y. (2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 106: 7648–7653.
46. Guo, W., Zhao, J., Li, X., Qin, L., Yan, X., and Liao, H. (2011). A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J. 66: 541–552.
47. Gutierrez, R., Lindeboom, J.J., Paredez, A.R., Emons, A.M.C., and Ehrhardt, D.W. (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11: 797–806.
48. Haberlandt, G. (1900). Über die Perception des geotropischen Reizes. Berichte der Deutschen Botanischen Gesellschaft 18: 261–272.
49. Hamilton, E.S., Jensen, G.S., Maksaev, G., Katims, A., Sherp, A.M., and Haswell, E.S. (2015). Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350: 438–441.
50. Harb, A., Krishnan, A., Ambavaram, M.M.R., and Pereira, A. (2010). Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol. 154: 1254–1271.
51. Haruta, M., Sabat, G., Stecker, K., Minkoff, B.B., and Sussman, M.R. (2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343: 408–411.
52. Haswell, E.S., and Meyerowitz, E.M. (2006). MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol. 16: 1–11.
53. Haswell, E.S., and Verslues, P.E. (2015). The ongoing search for the molecular basis of plant osmosensing. J. Gen. Physiol. 145: 389–394.
54. Hématy, K., Sado, P.-E., Van Tuinen, A., Rochange, S., Desnos, T., Balzergue, S., Pelletier, S., Renou, J.-P., and Höfte, H. (2007). A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17: 922–931.
55. 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.
56. Hou, C., Tian, W., Kleist, T., He, K., Garcia, V., Bai, F., Hao, Y., Luan, S., and Li, L. (2014). DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res. 24: 632–635.
57. Huck, N., Moore, J.M., Federer, M., and Grossniklaus, U. (2003). The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130: 2149–2159.
58. Jaffe, M.J., Takahashi, H., and Biro, R.L.(1985). A pea mutant for the study of hydrotropism in roots. Science 230: 445–447.
59. Julkowska, M.M., Hoefsloot, H.C.J., Mol, S., Feron, R., deBoer, G.-J., Haring, M.A., and Testerink, C. (2014). Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiol. 166: 1387–1402.
60. Julkowska, M.M., and Testerink, C. (2015). Tuning plant signaling and growth to survive salt. Trends Plant Sci. 20: 586–594.
61. Kang, J.S., et al. (2008). Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc.Natl.Acad.Sci.USA105: 5933–5938.
62. Kaplan, D.R. (1992). The relationship of cells to organisms in plants: Problem and implications of an organismal perspective. Int. J. Plant Sci. 153: S28–S37.
63. Kobayashi, A., Takahashi, A., Kakimoto, Y., Miyazawa, Y., Fujii, N., Higashitani, A., and Takahashi, H. (2007). A gene essential for hydrotropisminroots.Proc.Natl.Acad.Sci.USA 104: 4724–4729.
64. Kohorn, B.D. (2016). Cell wall-associated kinases and pectin perception. J. Exp. Bot. 67: 489–494.
65. Kohorn, B.D., Johansen, S., Shishido, A., Todorova, T., Martinez, R., Defeo, E., and Obregon, P. (2009). Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J. 60: 974–982.
66. Kohorn, B.D., Kobayashi, M., Johansen, S., Riese, J., Huang, L.-F., Koch, K., Fu, S., Dotson, A., and Byers, N. (2006). An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J. 46: 307–316.
67. Kohorn, B.D., and Kohorn, S.L. (2012). The cell wall-associated kinases, WAKs, as pectin receptors. Front. Plant Sci. 3: 88.
68. Komis, G., Apostolakos, P., and Galatis, B. (2001). Altered patterns of tubulin polymerization in dividing leaf cells of Chlorophyton co-mosum after a hyperosmotic treatment. New Phytol. 149: 193–207.
69. Komis, G., Apostolakos, P., and Galatis, B. (2002). Hyperosmotic stress induces formation of tubulin macrotubules in root-tip cells of Triticum turgidum: their probable involvement in protoplast volume control. Plant Cell Physiol. 43: 911–922.
70. Kramer, P.J., and Boyer, J.S. (1995). Water Relations of Plants and Soils. (San Diego, CA: Elsevier Science).
71. Kung, C. (2005). A possible unifying principle for mechanosensation. Nature 436: 647–654.
72. Lally, D., Ingmire, P., Tong, H.Y., and He, Z.H.(2001). Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. Plant Cell 13: 1317–1331.
73. Lavenus, J., Goh, T., Roberts, I., Guyomarc’h, S., Lucas, M., De Smet, I., Fukaki, H., Beeckman, T., Bennett, M., and Laplaze, L. (2013). Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18: 450–458.
74. LeNoble, M.E., Spollen, W.G., and Sharp, R.E. (2004). Maintenance of shoot growth by endogenous ABA: genetic assessment of the involvement of ethylene suppression. J. Exp. Bot. 55: 237–245.
75. Leung, J., Merlot, S., and Giraudat, J. (1997). The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759–771.
76. Li, C., et al. (2015). Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife 4: 4.
77. Lindner, H., Müller, L.M., Boisson-Dernier, A., and Grossniklaus, U. (2012). CrRLK1L receptor-like kinases: not just another brick in the wall. Curr. Opin. Plant Biol. 15: 659–669.
78. Lou, Q., Chen, L., Mei, H., Wei, H., Feng, F., Wang, P., Xia, H., Li, T., and Luo, L. (2015). Quantitative trait locus mapping of deep rooting by linkage and association analysis in rice. J. Exp. Bot. 66: 4749–4757.
79. Lü, P., Kang, M., Jiang, X., Dai, F., Gao, J., and Zhang, C. (2013). RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis. Planta 237: 1547–1559.
80. Lynch, J.P. (2013). Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann. Bot. (Lond.) 112: 347–357.
81. Lynch, J.P., Chimungu, J.G., and Brown, K.M. (2014). Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. J. Exp. Bot. 65: 6155–6166.
82. Maurel, C., Verdoucq, L., Luu, D.-T., and Santoni, V. (2008). Plant aquaporins: membrane channels with multiple integrated functions. Annu.Rev.PlantBiol.59: 595–624.
83. Mauseth, J.D. (2008). An Introduction to Plant Biology, 4th ed. (Burlington, MA: Jones and Bartlett Learning).
84. McFarlane, H.E., Döring, A., and Persson, S. (2014). The cell biology of cellulose synthesis. Annu. Rev. Plant Biol. 65: 69–94.
85. Miyazaki, S., Murata, T., Sakurai-Ozato, N., Kubo, M., Demura, T., Fukuda, H., and Hasebe, M. (2009). ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19: 1327–1331.
86. Miyazawa, Y., Takahashi, A., Kobayashi, A., Kaneyasu, T., Fujii, N., and Takahashi, H. (2009). GNOM-mediated vesicular trafficking plays an essential role in hydrotropism of Arabidopsis roots. Plant Physiol. 149: 835–840.
87. Monshausen, G.B., and Gilroy, S. (2009). Feeling green: mechano-sensing in plants. Trends Cell Biol. 19: 228–235.
88. Moore, J.P., Vicré-Gibouin, M., Farrant, J.M., and Driouich, A. (2008). Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol. Plant. 134: 237–245.
89. 2+ influx and touch sensing in roots. Proc. Natl. Acad. Sci. USA 104: 3639–3644.
90. Nakayama, M., Kaneko, Y., Miyazawa, Y., Fujii, N., Higashitani, N., Wada, S., Ishida, H., Yoshimoto, K., Shirasu, K., Yamada, K., Nishimura, M., and Takahashi, H. (2012). A possible involvement of autophagy in amyloplast degradation in columella cells during hydrotropic response of Arabidopsis roots. Planta 236: 999–1012.
91. Nari, J., Noat, G., and Ricard, J. (1991). Pectin methylesterase, metal ions and plant cell-wall extension. Hydrolysis of pectin by plant cell-wall pectin methylesterase. Biochem. J. 279: 343–350.
92. Nèmec, B. (1900). Über die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Berichte der Deutschen Botanischen Gesellschaft 18: 241.
93. Nick, P. (2013). Microtubules, signalling and abiotic stress. Plant J. 75: 309–323.
94. Nobel, P.S., and Sanderson, J. (1984). Rectifier-like activities of roots of two desert succulents. J. Exp. Bot. 35: 727–737.
95. Nord, E.A., and Lynch, J.P. (2009). Plant phenology: a critical controller of soil resource acquisition.J.Exp.Bot.60: 1927–1937.
96. Oparka, K.J. (1994). Plasmolysis: new insights into an old process. New Phytol. 126: 571–591.
97. Orman-Ligeza, B., Parizot, B., Gantet, P.P., Beeckman, T., Bennett, M.J., and Draye, X. (2013). Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci. 18: 459–467.
98. Paredez, A.R., Somerville, C.R., and Ehrhardt, D.W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312: 1491–1495.
99. Park, A.R., Cho, S.K., Yun, U.J., Jin, M.Y., Lee, S.H., Sachetto-Martins, G., and Park, O.K.(2001). Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine-rich protein, AtGRP-3. J. Biol. Chem. 276: 26688–26693.
100. Passioura, J.B. (1979). Accountability, philosophy and plant physiology. Search 10: 347–350.
101. Peaucelle, A., Braybrook, S., and Höfte, H. (2012). Cell wall mechanics and growth control in plants: the role of pectins revisited. Front. Plant Sci. 3: 121.
102. Pelloux, J., Rustérucci, C., and Mellerowicz, E.J. (2007). New insights into pectin methylesterase structure and function. Trends Plant Sci. 12: 267–277.
103. Plieth, C., and Trewavas, A.J. (2002). Reorientation of seedlings in the earth’s gravitationalfield induces cytosolic calcium transients. Plant Physiol. 129: 786–796.
104. Rellán-Álvarez, R., et al. (2015). GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. eLife 4: 393.
105. Rellán-Álvarez, R., Lobet, G., and Dinneny, J.R. (2016). Environmental control of root system biology. Annu. Rev. Plant Biol. 67: 619–642.
106. Robbins II, N.E., and Dinneny, J.R. (2015). The divining root: moisture-driven responses of roots at the micro- and macro-scale. J. Exp. Bot. 66: 2145–2154.
107. Rogers, E.D., and Benfey, P.N. (2015). Regulation of plant root system architecture: implications for crop advancement. Curr. Opin. Biotechnol. 32: 93–98.
108. Rosquete, M.R., von Wangenheim, D., Marhavý, P., Barbez, E., Stelzer, E.H.K., Benková, E., Maizel, A., and Kleine-Vehn, J. (2013). An auxin transport mechanism restricts positive orthogra-vitropism in lateral roots. Curr. Biol. 23: 817–822.
109. Rotman, N., Rozier, F., Boavida, L., Dumas, C., Berger, F., and Faure, J.-E. (2003). Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr.Biol.13: 432–436.
110. Rundel, P.W., Nobel, P.S., and Atkinson, D. (1991). Structure and function in desert root systems. In Plant Root Growth: An Ecological Perspective, D. Atkinson, ed (Oxford, UK: Blackwell Scientific Pub-lications), pp. 349-378.
111. 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.
112. Salguero-Gómez, R., and Casper, B.B. (2011). Introducing short roots in a desert perennial: anatomy and spatiotemporal foraging responses to increased precipitation. New Phytol. 191: 173–183.
113. Sato, E.M., Hijazi, H., Bennett, M.J., Vissenberg, K., and Swarup, R. (2015). New insights into root gravitropic signalling. J. Exp. Bot. 66: 2155–2165.
114. Saucedo, M., Ponce, G., Campos, M.E., Eapen, D., García, E., Luján, R., Sánchez, Y., and Cassab, G.I. (2012). An altered hydrotropic response (ahr1) mutant of Arabidopsis recovers root hydrotropism with cytokinin. J. Exp. Bot. 63: 3587–3601.
115. Schallus, T., Fehér, K., Sternberg, U., Rybin, V., and Muhle-Goll, C. (2010). Analysis of the specific interactions between the lectin domain of malectin and diglucosides. Glycobiology 20: 1010–1020.
116. Sebastian, J., et al. (2016). Grasses suppress shoot-borne roots to conserve water during drought. Proc. Natl. Acad. Sci. USA 113: 8861–8866.
117. Shabala, S.N., and Lew, R.R. (2002). Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol. 129: 290–299.
118. Sharp, R.E., and Davies, W.J. (1979). Solute regulation and growth by roots and shoots of water-stressed maize plants. Planta 147: 43– 49.
119. Sharp, R.E., Hsiao, T.C., and Silk, W.K. (1990). Growth of the maize primary root at low water potentials: II. Role of growth and deposition of hexose and potassium in osmotic adjustment. Plant Physiol. 93: 1337–1346.
120. 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.
121. Shih, H.-W., Miller, N.D., Dai, C., Spalding, E.P., and Monshausen, G.B. (2014). The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24: 1887–1892.
122. Smith, L.G., Hake, S., and Sylvester, A.W. (1996). The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122: 481–489.
123. Spollen, W.G., LeNoble, M.E., Samuels, T.D., Bernstein, N., and Sharp, R.E. (2000). Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol. 122: 967–976.
124. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Gälweiler, L., Palme, K., and Jürgens, G. (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286: 316–318.
125. Steudle, E., and Peterson, C.a. (1998). How does water get through roots? J. Exp. Bot. 49: 775–788.
126. Sun, F., Zhang, W., Hu, H., Li, B., Wang, Y., Zhao, Y., Li, K., Liu, M., and Li, X. (2008). Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol. 146: 178–188.
127. Swarup, R., Kramer, E.M., Perry, P., Knox, K., Leyser, H.M.O., Haseloff, J., Beemster, G.T.S., Bhalerao, R., and Bennett, M.J. (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.
128. Takahashi, N., Yamazaki, Y., Kobayashi, A., Higashitani, A., and Takahashi, H. (2003). Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of Arabidopsis and radish. Plant Physiol. 132: 805–810.
129. Takano, M., Takahashi, H., and Suge, H. (1997). Calcium requirement for the induction of hydrotropism and enhancement of calcium-induced curvature by water stress in primary roots of pea, Pisum sativum L. Plant Cell Physiol. 38: 385–391.
130. Taramino, G., Sauer, M., Stauffer, J.L., Jr., Multani, D., Niu, X., Sakai, H., and Hochholdinger, F. (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.
131. Tron, S., Bodner, G., Laio, F., Ridolfi, L., and Leitner, D. (2015). Can diversity in root architecture explain plant water use efficiency? A modeling study. Ecol. Modell. 312: 200–210.
132. Uga, Y., et al. (2013). Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 45: 1097–1102.
133. Uga, Y., Kitomi, Y., Yamamoto, E., Kanno, N., Kawai, S., Mizubayashi, T., and Fukuoka, S. (2015). A QTL for root growth angle on rice chromosome 7 is involved in the genetic pathway of DEEPER ROOTING 1. Rice (N. Y.) 8: 8.
134. Van Norman, J.M., Xuan, W., Beeckman, T., and Benfey, P.N. (2013). To branch or not to branch: the role of pre-patterning in lateral root formation. Development 140: 4301–4310.
135. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., and Zhu, J.-K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45: 523–539.
136. Voetberg, G.S., and Sharp, R.E. (1991). Growth of the maize primary root at low water potentials: III. Role ofincreasedprolinedeposition in osmotic adjustment. Plant Physiol. 96: 1125–1130.
137. Wade, L.J., et al. (2015). Environmental response and genomic regions correlated with rice root growth and yield under drought in the OryzaSNP panel across multiple study systems. PLoS One 10: e0124127.
138. Wilson, M.E., Jensen, G.S., and Haswell, E.S. (2011). Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23: 2939–2949.
139. Wu, Y., Thorne, E.T., Sharp, R.E., and Cosgrove, D.J. (2001). Modification of expansin transcript levels in the maize primary root at low water potentials. Plant Physiol. 126: 1471–1479.
140. Xiong, L., Wang, R.-G., Mao, G., and Koczan, J.M. (2006). Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol. 142: 1065–1074.
141. Xu, P., Cai, X.-T., Wang, Y., Xing, L., Chen, Q., and Xiang,C.-B. (2014). HDG11 upregulates cell-wall-loosening protein genes to promote root elongation in Arabidopsis. J. Exp. Bot. 65: 4285–4295.
142. Yang, L., Zheng, B., Mao, C., Qi, X., Liu, F., and Wu, P.(2004). Analysis of transcripts that are differentially expressed in three sectors of the rice root system under water deficit. Mol. Genet. Genomics 272: 433–442.
143. Yoo, S.-H., Fishman, M.L., Savary, B.J., and Hotchkiss, A.T., Jr. (2003). Monovalent salt-induced gelation of enzymatically dees-terified pectin. J. Agric. Food Chem. 51: 7410–7417.
144. 2+ increases vital for osmosensing in Arabidopsis. Nature 514: 367– 371.
145. Zhong, R., Burk, D.H., Morrison III, W.H., and Ye, Z.-H. (2002). A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14: 3101–3117.
146. Zhu, J., Lee, B.-H., Dellinger, M., Cui, X., Zhang, C., Wu, S., Nothnagel, E.A., and Zhu, J.-K. (2010). A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J. 63: 128–140.
147. Zolla, G., Heimer, Y.M., and Barak, S. (2010). Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J. Exp. Bot. 61: 211–224.
148. Zwicke, M., Picon-Cochard, C., Morvan-Bertrand, A., Prud’homme, M.-P., and Volaire, F. (2015). What functional strategies drive drought survival and recovery of perennial species from upland grassland? Ann. Bot. (Lond.) 116: 1001–1015.