Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand

Dmitry S. Veselov A , Guzel V. Sharipova A , Stanislav Yu. Veselov B , Ian C. Dodd C , Igor Ivanov A and Guzel R. Kudoyarova A D
+ Author Affiliations
- Author Affiliations

A Ufa Institute of Biology of Russian Academy of Sciences, pr. Octyabrya, 69, Ufa 450 054, Russia.

B Biological Faculty of Bashkir State University, Validi, 32, Ufa 450 073, Russia.

C Lancaster Environment Centre, Lancaster University, Bailrigg, Lancashire LA1 4YQ, UK.

D Corresponding author. Email: guzel@anrb.ru

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanic Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 19–23 June 2016.

Functional Plant Biology - https://doi.org/10.1071/FP16242
Submitted: 13 July 2016  Accepted: 23 September 2016   Published online: 9 November 2016

Abstract

To address the involvement of abscisic acid (ABA) in regulating transpiration and root hydraulic conductivity (LpRoot) and their relative importance for maintaining leaf hydration, the ABA-deficient barley mutant Az34 and its parental wild-type (WT) genotype (cv. Steptoe) were grown in hydroponics and exposed to changes in atmospheric vapour pressure deficit (VPD) imposed by air warming. WT plants were capable of maintaining leaf water potential (ψL) that was likely due to increased LpRoot enabling higher water flow from the roots, which increased in response to air warming. The increased LpRoot and immunostaining for HvPIP2;2 aquaporins (AQPs) correlated with increased root ABA content of WT plants when exposed to increased air temperature. The failure of Az34 to maintain ψL during air warming may be due to lower LpRoot than WT plants, and an inability to respond to changes in air temperature. The correlation between root ABA content and LpRoot was further supported by increased root hydraulic conductivity in both genotypes when treated with exogenous ABA (10-5 M). Thus the ability of the root system to rapidly regulate ABA levels (and thence aquaporin abundance and hydraulic conductivity) seems important to maintain leaf hydration.

Additional keywords: absicisic acid, Hordeum vulgare, tissue hydration, water relations.


References

Blum A (2015) Towards a conceptual ABA ideotype in plant breeding for water limited environments. Functional Plant Biology 42, 502–513.
Towards a conceptual ABA ideotype in plant breeding for water limited environments.CrossRef | 1:CAS:528:DC%2BC2MXosFGltbg%3D&md5=df93c3f98d431e366dd23298f419f025CAS |

Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrition deprivation may involve the regulation of water-channel function. Planta 199, 372–381.
Responses of wheat plants to nutrition deprivation may involve the regulation of water-channel function.CrossRef | 1:CAS:528:DyaK28XksFGlsLw%3D&md5=a0e059eec69e61960b1551f87db4009dCAS |

Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology 164, 1600–1618.
Aquaporins: highly regulated channels controlling plant water relations.CrossRef | 1:CAS:528:DC%2BC2cXmsV2jsr4%3D&md5=9280679c4bdf33a07e273d0c68e480d4CAS |

Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiology 147, 469–486.
Quantitative trait loci and crop performance under abiotic stress: where do we stand?CrossRef | 1:CAS:528:DC%2BD1cXnsVyhsbw%3D&md5=091e0657835bbc82b320b0aab219ee95CAS |

Dodd IC (2005) Root-to-shoot signalling: assessing the roles of ‘up’ in the up and down world of long-distance signalling in planta. Plant and Soil 274, 251–270.
Root-to-shoot signalling: assessing the roles of ‘up’ in the up and down world of long-distance signalling in planta.CrossRef | 1:CAS:528:DC%2BD2MXhtVWiurfM&md5=dabb2fb6a51f2eb8deff44d2fae6d32eCAS |

Dodd IC (2013) Abscisic acid and stomatal closure: a hydraulic conductance conundrum? New Phytologist 197, 6–8.
Abscisic acid and stomatal closure: a hydraulic conductance conundrum?CrossRef | 1:CAS:528:DC%2BC38XhslelsLzM&md5=dfdb647f3a93c2e05812cddc8cd3e7dfCAS |

Horie T, Kaneko T, Sugimoto G, Sasano S, Panda SK, Shibasaka M, Katsuhara M (2011) Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant & Cell Physiology 52, 663–675.
Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots.CrossRef | 1:CAS:528:DC%2BC3MXksFKju7s%3D&md5=b129bc944c2821c7590ba9961700c72cCAS |

Hose E, Steudle E, Hartung W (2000) Abscisic acid and hydraulic conductance of maize roots: a study using cell- and root-pressure probes. Planta 211, 874–882.
Abscisic acid and hydraulic conductance of maize roots: a study using cell- and root-pressure probes.CrossRef | 1:CAS:528:DC%2BD3cXotVKnt7k%3D&md5=620e7d3e64c9b8c968aff6662a99fa4eCAS |

Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant & Cell Physiology 43, 885–893.
Functional analysis of water channels in barley roots.CrossRef | 1:CAS:528:DC%2BD38XmsFOkurw%3D&md5=1f4cbfd2f54aea94b5b7e8de83aa6e0dCAS |

Knipfer T, Fricke W (2011) Water uptake by seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.). Journal of Experimental Botany 62, 717–733.
Water uptake by seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.).CrossRef | 1:CAS:528:DC%2BC3cXhsFyrsb%2FJ&md5=cab8d0f3557a641f162369169ca7bb95CAS |

Kudoyarova G, Veselova S, Hartung W, Farhutdinov R, Veselov D, Sharipova G (2011) Involvement of root ABA and hydraulic conductance in the control of water relations in wheat plants exposed to increased evaporative demand. Planta 233, 87–94.
Involvement of root ABA and hydraulic conductance in the control of water relations in wheat plants exposed to increased evaporative demand.CrossRef | 1:CAS:528:DC%2BC3MXjs1yq&md5=1a8d9218230ce781cad40aaf71b8fd7dCAS |

Makela P, Munns R, Colmer TD, Peltonen-Sainio P (2003) Growth of tomato and an ABA-deficient mutant (sitiens) under saline conditions. Physiologia Plantarum 117, 58–63.
Growth of tomato and an ABA-deficient mutant (sitiens) under saline conditions.CrossRef | 1:CAS:528:DC%2BD3sXhtlOltbk%3D&md5=320267db848c170029ce76d80bab447fCAS |

Martin-Vertedor AI, Dodd IC (2011) Root-to-shoot signalling when soil moisture is heterogeneous: increasing the proportion of root biomass in drying soil inhibits leaf growth and increases leaf abscisic acid concentration. Plant, Cell & Environment 34, 1164–1175.
Root-to-shoot signalling when soil moisture is heterogeneous: increasing the proportion of root biomass in drying soil inhibits leaf growth and increases leaf abscisic acid concentration.CrossRef | 1:CAS:528:DC%2BC3MXpsVKhtb0%3D&md5=7916e9359655628a41de47db7a9d0e9eCAS |

Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology 59, 595–624.
Plant aquaporins: membrane channels with multiple integrated functions.CrossRef | 1:CAS:528:DC%2BD1cXntFaqtr4%3D&md5=97d8106a11545dbd3e6210d3e54da2cdCAS |

McAdam SAM, Sussmilch FC, Brodribb TJ (2016) Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant, Cell & Environment 39, 485–491.
Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms.CrossRef | 1:CAS:528:DC%2BC28Xit1Krur0%3D&md5=a48382f29856a076f7453dc748413c40CAS |

Meinzer FG (2002) Co-ordination of vapour and liquid phase water transport properties in plants. Plant, Cell & Environment 25, 265–274.
Co-ordination of vapour and liquid phase water transport properties in plants.CrossRef |

Mulholland BJ, Taylor B, Black CR, Roberts JA (1996) Effect of soil compaction on barley (Hordeum vulgare L.) growth II. Are increased xylem sap ABA concentrations involved in maintaining leaf expansion in compacted soils? Journal of Experimental Botany 47, 551–556.
Effect of soil compaction on barley (Hordeum vulgare L.) growth II. Are increased xylem sap ABA concentrations involved in maintaining leaf expansion in compacted soils?CrossRef | 1:CAS:528:DyaK28XivFequrg%3D&md5=0388008911e5f4e9ce499c39930db909CAS |

Neill SJ, Horgan R (1985) Abscisic acid production and water relations in wilty tomato mutants subjected to water deficiency. Journal of Experimental Botany 36, 1222–1231.
Abscisic acid production and water relations in wilty tomato mutants subjected to water deficiency.CrossRef | 1:CAS:528:DyaL2MXlsFOlsL0%3D&md5=00dab3b1c14b48876885dcd442134a8bCAS |

Pantin F, Monnet F, Jannaud D, Costa JM, Renaud J, Muller B, Simonneau T, Genty B (2013) The dual effect of abscisic acid on stomata. New Phytologist 197, 65–72.
The dual effect of abscisic acid on stomata.CrossRef | 1:CAS:528:DC%2BC38XhslelsL%2FP&md5=af75ae1154f2111d486a5f42317a8604CAS |

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 conductance and leaf growth rate: a trans-scale approach. Plant Physiology 149, 2000–2012.
Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductance and leaf growth rate: a trans-scale approach.CrossRef | 1:CAS:528:DC%2BD1MXks1Wnsrg%3D&md5=c82d9ef52fd8ea8edd63b731a59f6b4eCAS |

Reynolds MP, Singh RP, Ibrahim A, Ageeb OA, Larque-Saavedra A, Quick JS (1998) Evaluating physiological traits to complement empirical selection for wheat in warm environments. Euphytica 100, 85–94.
Evaluating physiological traits to complement empirical selection for wheat in warm environments.CrossRef |

Sharipova G, Veselov D, Kudoyarova G, Fricke W, Dodd IC, Katsuhara M, Furuichi T, Ivanov I, Veselov S (2016) Exogenous application of abscisic acid (ABA) increases root and cell hydraulic conductivity and abundance of some aquaporin isoforms in the ABA-deficient barley mutant Az34. Annals of Botany
Exogenous application of abscisic acid (ABA) increases root and cell hydraulic conductivity and abundance of some aquaporin isoforms in the ABA-deficient barley mutant Az34.CrossRef |

Tardieu F, Lafarge T, Simonneau T (1996) Stomatal control by fed or endogenous xylem ABA in sunflower: Interpretation of correlations between leaf water potential and stomatal conductance in anisohydric species. Plant, Cell & Environment 19, 75–84.

Tardieu F, Parent B, Simonneau T (2010) Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? Plant, Cell & Environment 33, 636–647.
Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes?CrossRef |

Thompson AJ, Andrews J, Mulholland BJ, McKee JMT, Hilton HW, Horridge JS, Farquhar GR, Smeeton RC, Smillie IRA, Black CR, Taylor IB (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductance and influences leaf expansion. Plant Physiology 143, 1905–1917.
Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductance and influences leaf expansion.CrossRef | 1:CAS:528:DC%2BD2sXksFWjuro%3D&md5=3d9ee773fa9b82c177ba2c833c76fbb4CAS |

Vandeleur RK, Sullivan W, Athman A, Jordans C, Gilliham M, Kaiser BN, Tyerman SD (2014) Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant, Cell & Environment 37, 520–538.
Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins.CrossRef | 1:CAS:528:DC%2BC2cXlsF2itA%3D%3D&md5=992796f05c1d0d0358ed93d45a652ed1CAS |

Veselov S, Kudoyarova G, Egutkin N, Gyuli-Zade V, Mustafina A, Kof E (1992) Modified solvent partitioning scheme providing increased specificity and rapidity of immunoassay for indole 3-acetic acid. Physiologia Plantarum 86, 93–96.
Modified solvent partitioning scheme providing increased specificity and rapidity of immunoassay for indole 3-acetic acid.CrossRef | 1:CAS:528:DyaK3sXhvVOmug%3D%3D&md5=78a3c59a9571d2266bd2ee9043d19e07CAS |

Veselov DS, Sharipova GV, Veselov SU, Kudoyarova GR (2008) The effects of NaCl treatment on water relations, growth and ABA content in barley cultivars differing in drought tolerance. Journal of Plant Growth Regulation 27, 380–386.
The effects of NaCl treatment on water relations, growth and ABA content in barley cultivars differing in drought tolerance.CrossRef | 1:CAS:528:DC%2BD1cXhtlGrt7zJ&md5=075846aa0912addab3ed9903fd9c8e71CAS |

Vysotskaya LB, Arkhipova TN, Timergalina LN, Dedov AV, Veselov SY, Kudoyarova GR (2004) Effect of partial root excision on transpiration, root hydraulic conductance and leaf growth in wheat seedlings. Plant Physiology and Biochemistry 42, 251–255.
Effect of partial root excision on transpiration, root hydraulic conductance and leaf growth in wheat seedlings.CrossRef | 1:CAS:528:DC%2BD2cXis1Wnt70%3D&md5=017d32ad4b93c7a976b50e5f9796e9f9CAS |

Vysotskaya LB, Korobova AV, Veselov SY, Dodd IC, Kudoyarova GR (2009) ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient deprived durum wheat. Functional Plant Biology 36, 66–72.
ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient deprived durum wheat.CrossRef | 1:CAS:528:DC%2BD1MXhs1Ggsg%3D%3D&md5=14497ef2ff8e98450b29f09b2599c72aCAS |

Zhang J, Davies WJ (1990) Changes in the concentration of ABA in xylem sap as a function of changing soil water status can account for changes in leaf conductance and growth. Plant, Cell & Environment 13, 277–285.



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