Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: Crop water-use efficiency, growth and yield

Plant Cell and Environment

Volumn 38, Issue 9, 2015, Pages 1785-1793

  Moshelion, Menachem ^a   Halperin, Ofer ^a   Wallach, Rony ^a   Oren, Ram ^b,c   Way, Danielle A ^b,d  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b DUKE UNIVERSITY   (United States)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Anisohydric; Drought stress; Isohydric; Risk taking

Indexed keywords

AQUAPORIN; CARBON DIOXIDE; WATER;

ANATOMY AND HISTOLOGY; CARBON CYCLE; DEHYDRATION; EVAPOTRANSPIRATION; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; PLANT DEVELOPMENT; PLANT LEAF; PLANT ROOT; SHOOT;

AQUAPORINS; CARBON CYCLE; CARBON DIOXIDE; DEHYDRATION; PHOTOSYNTHESIS; PLANT DEVELOPMENT; PLANT LEAVES; PLANT ROOTS; PLANT SHOOTS; PLANT TRANSPIRATION; PLANTS; WATER;

EID: 84938637177     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12410     Document Type: Review

References (103)

1. Ache P., Bauer H., Kollist H., Al-Rasheid K.A.S., Lautner S., Hartung W. & Hedrich R. (2010) Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant Journal 62, 1072-1082.
2. Aharon R., Shahak Y., Wininger S., Bendov R., Kapulnik Y. & Galili G. (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. The Plant Cell Online 15, 439-447.
3. Alassimone J., Naseer S. & Geldner N. (2010) A developmental framework for endodermal differentiation and polarity. Proceedings of the National Academy of Sciences 107, 5214-5219.
4. Alexandersson E., Fraysse L., Sjövall-Larsen S., Gustavsson S., Fellert M., Karlsson M., ... Kjellbom P. (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Molecular Biology 59, 469-484.
5. Aloni R. (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany 97, 883-893.
6. Bauer H., Ache P., Lautner S., Fromm J., Hartung W., Al-Rasheid Khaled A.S., ... Hedrich R. (2013) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Current Biology 23, 53-57.
7. Birnbaum K., Shasha D.E., Wang J.Y., Jung J.W., Lambert G.M., Galbraith D.W. & Benfey P.N. (2003) A gene expression map of the Arabidopsis root. Science 302, 1956-1960.
8. Boursiac Y., Chen S., Luu D.T., Sorieul M., van den Dries N. & Maurel C. (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiology 139, 790-805.
9. Boyer J.S. (1982) Plant productivity and environment. Science 218, 443-448.
10. Bramley H., Turner N.C., Turner D.W. & Tyerman S.D. (2010) The contrasting influence of short-term hypoxia on the hydraulic properties of cells and roots of wheat and lupin. Functional Plant Biology 37, 183-193.
11. Brodribb T.J. & Jordan G.J. (2008) Internal coordination between hydraulics and stomatal control in leaves. Plant, Cell & Environment 31, 1557-1564.
12. Brodribb T.J. & McAdam S.A.M. (2013) Abscisic acid mediates a divergence in the drought response of two conifers. Plant Physiology 162, 1370-1377.
13. Cano F.J., Sanchez-Gomez D., Rodriguez-Calcerrada J., Warren C.R., Gil L. & Aranda I. (2013) Effects of drought on mesophyll conductance and photosynthetic limitations at different tree canopy layers. Plant, Cell & Environment 36, 1961-1980.
14. Carvajal M., Cooke D.T. & Clarkson D.T. (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199, 372-381.
15. Casimiro I., Beeckman T., Graham N., Bhalerao R., Zhang H., Casero P., ... Bennett M.J. (2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165-171.
16. Chaumont F., Moshelion M. & Daniels M.J. (2005) Regulation of plant aquaporin activity. Biology of the Cell 97, 749-764.
17. Christmann A., Hoffmann T., Teplova I. Grill E. & Muller A. (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant physiology 137, 209-219.
18. Christmann A., Weiler E.W., Steudle E. & Grill E. (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant Journal 52, 167-174.
19. Clarkson D.T., Carvajal M., Henzler T., Waterhouse R.N., Smyth A.J., Cooke D.T. & Steudle E. (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany 51, 61-70.
20. Cochard H., Venisse J.S., Barigah T.S., Brunel N., Herbette S., Guilliot A., ... Sakr S. (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiology 143, 122-133.
21. Cornic G., Le Gouallec J.L., Brintais J.M. & Hodges M. (1989) Effects of dehydration and high light on photosynthesis of two C3 plants (Phaseolus vulgaris L. and Elatostema repens (Lour.) Hall F.). Planta 177, 84-90.
22. De Smet I., Tetsumura T., De Rybel B., Frei dit Frey N., Laplaze L., Casimiro I., ... Beeckman T. (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development (Cambridge, England) 134, 681-690.
23. DeWitt C.T. (1958) Transpiration and crop yield. Institution of Biology and Chemistry Research on Field Crops and Herbage, Wageningen, The Netherlands. 64, 6-87.
24. Duan B., Li Y., Zhang X., Korpelainen H. & Li C. (2009) Water deficit affects mesophyll limitation of leaves more strongly in sun than in shade in two contrasting Picea asperata populations. Tree Physiology 29, 1551-1561.
25. Endo A., Sawada Y., Takahashi H., Okamoto M., Ikegami K., Koiwai H., ... Nambara E. (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiology 147, 1984-1993.
26. Epron D. (1997) Effects of drought on photosynthesis and the thermotolerance of photosystem II in seedlings of cedar (Cedrus atalntica and C.libani). Journal of Experimental Botany 48, 1835-1841.
27. 2 in vivo. Plant Journal 48, 427-439.
28. 2: an unappreciated central player in photosynthesis'. Plant Science 196, 70-84.
29. Frangne N., Maeshima M., Schaffner A.R., Mandel T., Martinoia E. & Bonnemain J.L. (2001) Expression and distribution of a vaculoar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta 212, 270-278.
30. Gallé Á., Csiszár J., Benyó D., Laskay G., Leviczky T., Erdei L. & Tari I. (2013) Isohydric and anisohydric strategies of wheat genotypes under osmotic stress: biosynthesis and function of ABA in stress responses. Journal of Plant Physiology 170, 1389-1399.
31. Galle A., Florez-Sarasa I., Tomas M., Pou A., Medrano H., Ribas-Carbo M. & Flexas J. (2009) Mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? Journal of Experimental Botany 60, 2379-2390.
32. Galvez-Valdivieso G., Fryer M.J., Lawson T., Slattery K., Truman W., Smirnoff N., ... Mullineaux P.M. (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. The Plant Cell 21, 2143-2162.
33. Gorska A., Zwieniecka A., Michele Holbrook N. & Zwieniecki M.A. (2008) Nitrate induction of root hydraulic conductivity in maize is not correlated with aquaporin expression. Planta 228, 989-998.
34. Hacke U.G., Sperry J.S., Ewers B.E., Ellsworth D.S., Schäfer K.V.R. & Oren R. (2000) Influence of soil porosity on water use in Pinus taeda. Oecologia 124, 495-505.
35. 2 assimilation in the leaves of transgenic rice plants. Plant and Cell Physiology 45, 521-529.
36. 2 transport facilitator. The Plant Journal 67, 795-804.
37. Hodge A. (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162, 9-24.
38. Holbrook N.M., Shashidhar V.R., James R.A. & Munns R. (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. Journal of Experimental Botany 53, 1503-1514.
39. Hose E., Steudle E. & Hartung W. (2000) Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes. Planta 211, 874-882.
40. Huebert R.C., Jagavelu K., Hendrickson H.I., Vasdev M.M., Arab J.P., Splinter P.L., ... Shah V.H. (2011) Aquaporin-1 promotes angiogenesis, fibrosis, and portal hypertension through mechanisms dependent on osmotically sensitive MicroRNAs. The American Journal of Pathology 179, 1851-1860.
41. Jang J.Y., Kim D.G., Kim Y.O., Kim J.S. & Kang H.S. (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Molecular Biology 54, 713-725.
42. Kaldenhoff R., Grote K., Zhu J.-J. & Zimmermann U. (1998) Significance of plasmalemma aquaporins for water-transport in Arabidopsis thaliana. The Plant Journal 14, 121-128.
43. Kaldenhoff R., Bertl A., Otto B., Moshelion M. & Uehlein N. (2007) Characterization of plant aquaporins. Methods in Enzymology 428, 505-531.
44. Kawase M., Hanba Y.T. & Katsuhara M. (2013) The photosynthetic response of tobacco plants overexpressing ice plant aquaporin McMIPB to a soil water deficit and high vapor pressure deficit. Journal of Plant Research 126, 517-527.
45. Kemanian A.R., Stöckle C.O. & Huggins D.R. (2005) Transpiration-use efficiency of barley. Agricultural and Forest Meteorology 130, 1-11.
46. Kinsman E.A. & Pyke K.A. (1998) Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development (Cambridge, England) 125, 1815-1822.
47. Lawlor D.W. & Tezara W. (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Annals of Botany 103, 561-579.
48. Levin M., Lemcoff J.H., Cohen S. & Kapulnik Y. (2007) Low air humidity increases leaf-specific hydraulic conductance of Arabidopsis thaliana (L.) Heynh (Brassicaceae). Journal of Experimental Botany 58, 3711.
49. Lin W., Peng Y., Li G., Arora R., Tang Z., Su W. & Cai W. (2007) Isolation and functional characterization of PgTIP1, a hormone-autotrophic cells-specific tonoplast aquaporin in ginseng. Journal of Experimental Botany 58, 947-956.
50. López-Bucio J., Hernández-Abreu E., Sánchez-Calderón L., Nieto-Jacobo M.F., Simpson J. & Herrera-Estrella L. (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiology 129, 244-256.
51. McDowell N., Pockman W.T., Allen C.D., Breshears D.D., Cobb N., Kolb T., ... Yepez E.A. (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178, 719-739.
52. Maggio A. & Joly R.J. (1995) Effects of mercuric-chloride on the hydraulic conductivity of tomato root systems - evidence for a channel-mediated water pathway. Plant Physiology 109, 331-335.
53. Mahdieh M. & Mostajeran A. (2009) Abscisic acid regulates root hydraulic conductance via aquaporin expression modulation in Nicotiana tabacum. Journal of Plant Physiology 166, 1993-2003.
54. Malamy J.E. (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell & Environment 28, 67-77.
55. Markhart A.H., Fiscus E.L., Nnaylor A.W. & Kramer P.J. (1979) Effect of abscisic acid on root hydraulic conductivity. Plant Physiology 64, 611-614.
56. Martre P., Morillon R., Barrieu F., North G.B., Nobel P.S. & Chrispeels M.J. (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology 130, 2101-2110.
57. Maurel C., Verdoucq L., Luu D.-T. & Santoni V. (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology 59, 595-624.
58. Maurel C., Santoni V., Luu D.-T., Wudick M.M. & Verdoucq L. (2009) The cellular dynamics of plant aquaporin expression and functions. Current Opinion in Plant Biology 12, 690-698.
59. Maurel C., Simonneau T. & Sutka M. (2010) The significance of roots as hydraulic rheostats. Journal of Experimental Botany 61, 3191-3198.
60. Monti A., Brugnoli E., Scartazza A. & Amaducci M. (2006) The effect of transient and continuous drought on yield, photosynthesis and carbon isotope discrimination in sugar beet (Beta vulgaris L.). Journal of Experimental Botany 57, 1253-1262.
61. Moon G.J., Clough B.F., Peterson C.A. & Allaway W.G. (1986) Apoplastic and symplastic pathways in Avicennia marina (Forsk.) Vierh. roots revealed by fluorescent tracer dyes. Australian Journal of Plant Physiology 13, 637-648.
62. Naor A., Schneider D., Ben-Gal A., Zipori I., Dag A., Kerem Z., ... Gal Y. (2013) The effects of crop load and irrigation rate in the oil accumulation stage on oil yield and water relations of 'Koroneiki' olives. Irrigation Science 31, 781-791.
63. Nardini A., Raimondo F., Lo Gullo M.A. & Salleo S. (2010) Leafminers help us understanding leaf hydraulic design. Plant, Cell & Environment 33, 1091-1100.
64. Oishi A.C., Oren R., Novick K.A., Palmroth S. & Katul G.G. (2010) Interannual invariability of forest evapotranspiration and its consequence to water flow downstream. Ecosystems 13, 421-436.
65. Otto B., Uehlein N., Sdorra S., Fischer M., Ayaz M., Belastegui-Macadam X., ... Kaldenhoff R. (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. Journal of Biological Chemistry 285, 31253-31260.
66. Pantin F., Monnet F., Jannaud D., Costa J.M., Renaud J., Muller B., ... Genty B. (2013) The dual effect of abscisic acid on stomata. New Phytologist 197, 65-72.
67. Parent B., Hachez C., Redondo E., Simonneau T., Chaumont F. & Tardieu F. (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiology 149, 2000-2012.
68. Parry M., Flexas J. & Medrano H. (2005) Prospects for crop production under drought: research priorities and future directions. Annals of Applied Biology 147, 211-226.
69. Peng Y., Lin W., Cai W. & Arora R. (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226, 729-740.
70. Perez-Martin A., Michelazzo C., Torres-Ruiz J.M., Flexas J., Fernandez J.E., Sebastiani L. & Diaz-Espejo A. (2014) Regulation of photosynthesis and stomatal and mesophyll conductance under water stress and recovery in olive trees: correlation with gene expression of carbonic anhydrase and aquaporins. Journal of Experimental Botany 65, 3143-3156.
71. Pou A., Medrano H., Flexas J. & Tyerman S.D. (2013) A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant, Cell & Environment 36, 828-843.
72. Prado K., Boursiac Y., Tournaire-Roux C., Monneuse J.M., Postaire O., Da Ines O., ... Maurel C. (2013) Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. The Plant Cell 25, 1029-1039.
73. Quintero J.M., Fournier J.M. & Benlloch M. (1999) Water transport in sunflower root systems: effects of ABA, Ca2+ status and HgCl2. Journal of Experimental Botany 50, 1607-1612.
74. Ranathunge K. & Schreiber L. (2011) Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. Journal of Experimental Botany 62, 1961-1974.
75. Reed R.C., Brady S.R. & Muday G.K. (1988) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiolgy 118, 1369-1378.
76. Sack L. & Holbrook N.M. (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361.
77. Sade N., Vinocur B.J., Diber A., Shatil A., Ronen G., Nissan H., ... Moshelion M. (2009) Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytologist 181, 651-661.
78. Sade N., Gebretsadik M., Seligmann R., Schwartz A., Wallach R. & Moshelion M. (2010) The role of tobacco aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiology 152, 245-254.
79. Sade N., Gebremedhin A. & Moshelion M. (2012) Risk-taking plants: anisohydric behavior as a stress-resistance trait. Plant Signaling & Behavior 7, 767-770.
80. 2 under standard and salt-stress conditions. Planta 239, 357-366.
81. Schiefelbein J.W. & Benfey P.N. (1991) The development of plant roots: new approaches to underground problems. The Plant Cell Online 3, 1147-1154.
82. Shapira O., Khadka S., Israeli Y., Shani U. & Schwartz A. (2009) Functional anatomy controls ion distribution in banana leaves: significance of Na+ seclusion at the leaf margins. Plant, Cell & Environment 32, 476-485.
83. Shatil-Cohen A., Attia Z. & Moshelion M. (2011) Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? The Plant Journal 67, 72-80.
84. Siefritz F., Tyree M.T., Lovisolo C., Schubert A. & Kaldenhoff R. (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. The Plant Cell Online 14, 869-876.
85. Sinclair T.R., Tanner C.B. & Bennett J.M. (1984) Water-use efficiency in crop production. American Institute of Biological Sciences 34, 36-40.
86. Steudle E. (2000) Water uptake by roots: effects of water deficit. Journal of Experimental Botany 51, 1531-1542.
87. Tardieu F. & Simonneau T. (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419-432.
88. 2 diffusion across the plasma membrane. Plant and Cell Physiology 43, 70-78.
89. Tournaire-Roux C., Sutka M., Javot H., Gout E., Gerbeau P., Luu D.T., ... Maurel C. (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393-397.
90. Tyerman S.D., Niemietz C.M. & Bramley H. (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant, Cell & Environment 25, 173-194.
91. 2 pore with physiological functions. Nature 425, 734-737.
92. 2 permeability. The Plant Cell 20, 648-657.
93. Vandeleur R.K., Mayo G., Shelden M.C., Gilliham M., Kaiser B.N. & Tyerman S.D. (2008) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiology 149, 445-460.
94. Vandeleur R.K., Sullivan W., Athman A., Jordans C., Gilliham M., Kaiser B.N. & Tyerman S.D. (2014) Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant, Cell & Environment 37, 520-525.
95. Wallach R., Da-Costa N., Raviv M. & Moshelion M. (2010) Development of synchronized, autonomous, and self-regulated oscillations in transpiration rate of a whole tomato plant under water stress. Journal of Experimental Botany 61, 3439-3449.
96. 2 transfer but atmospheric water deficits do not. Journal of Experimental Botany 59, 327-334.
97. Xiong L., Wang R.G., Mao G. & Koczan J.M. (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiology 142, 1065-1074.
98. Yamaji N. & Ma J.F. (2009) A transporter at the node responsible for intervascular transfer of silicon in rice. The Plant Cell Online 21, 2878-2883.
99. Yamori W. (2006) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant and Cell Physiology 47, 1069-1080.
100. Yaneff A., Sigaut L., Marquez M., Alleva K., Pietrasanta L.I. & Amodeo G. (2013) Heteromerization of PIP aquaporins affects their intrinsic permeability. Proceedings of the National Academy of Sciences 111, 231-236.
101. Zhang B., Wang Q., Wang K., Pan X., Liu F., Guo T., ... Anderson T.A. (2007) Identification of cotton microRNAs and their targets. Gene 397, 26-37.
102. Zhang Y., Oren R. & Kang S. (2011) Spatiotemporal variation of crown-scale stomatal conductance in an arid Vitis vinifera L. cv. Merlot vineyard: direct effects of hydraulic properties and indirect effects of canopy leaf area. Tree Physiology 32, 262-279.
103. Zimmermann M.H. (1983) Xylem Stracture and the Ascent of Sap, 1st edn, Berlin, Germany.