Arabidopsis plasma membrane intrinsic protein (AtPIP2;1) is implicated in a salinity conditional influence on seed germination
Phan Thi Thanh Hoai
A B C * , Jiaen Qiu A B , Michael Groszmann D , Annamaria De Rosa D , Stephen D. Tyerman A B and Caitlin S. Byrt A B D *
+ Author Affiliations
- Author Affiliations
A Australian Research Council Centre of Excellence in Plant Energy Biology, Waite Research Precinct, University of Adelaide, Glen Osmond, SA, Australia.
B School of Agriculture, Food and Wine, and Waite Research Institute, Waite Research Precinct, University of Adelaide, Glen Osmond, SA, Australia.
C Faculty of Agriculture and Forestry, Tay Nguyen University, 567 Le Duan, BMT, Dak Lak, Vietnam.
D Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Sciences, Research School of Biology, The Australian National University, Acton, ACT 2601, Australia.
* Correspondence to: hoaiphan.agsc@gmail.com, Caitlin.Byrt@anu.edu.au
Handling Editor: Frans Maathuis
Functional Plant Biology 50(8) 633-648 https://doi.org/10.1071/FP22260
Submitted: 9 November 2022 Accepted: 15 May 2023 Published: 6 June 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Dynamic changes in aquaporin gene expression occur during seed germination. One example is the ~30-fold increase in Arabidopsis thaliana PIP2;1 transcripts within 24 h of seed imbibition. To investigate whether AtPIP2;1 can influence seed germination wild-type Columbia-0, single (Atpip2;1) and double (Atpip2;1-Atpip2;2) loss-of-function mutants, along with transgenic 2x35S::AtPIP2;1 over-expressing (OE) lines and null-segregant controls, were examined. The various genotypes were germinated in control and saline (75 mM NaCl treatment) conditions and tested for germination efficiency, imbibed seed maximum cross sectional (MCS) area, imbibed seed mass, and seed Na+ and K+ content. Seed lacking functional AtPIP2;1 and/or AtPIP2;2 proteins or constitutively over-expressing AtPIP2;1, had delayed germination in saline conditions relative to wild-type and null-segregant seed, respectively. Exposure to saline germination conditions resulted in Atpip2;1 mutants having greater imbibed seed mass and less accumulated Na+ than wild-type, whereas lines over-expressing AtPIP2;1 had reduced imbibed seed mass and greater seed K+ content than null-segregant control seed. The results imply a role for AtPIP2;1 in seed germination processes, whether directly through its capacity for water and ion transport or H2O2 signalling, or indirectly through potentially triggering dynamic differential regulation of other aquaporins expressed during germination. Future research will aid in dissecting the aquaporin functions influencing germination and may lead to novel solutions for optimising germination in sub-optimal conditions, such as saline soils.
Keywords: aquaporins, Arabidopsis spp., hydraulic conductivity, ion channel, ion transport, physiology, salinity, seed viability, signalling, sodium transport, sucrose, transporter proteins.
References
Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochimica et Biophysica Acta – General subjects 1840, 1468–1481.| Diversity and evolution of membrane intrinsic proteins.Crossref | GoogleScholarGoogle Scholar |
Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Frontiers in Plant Science 4, 63
| ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination.Crossref | GoogleScholarGoogle Scholar |
Ayers AD, Hayward HE (1949) A method for measuring the effects of soil salinity on seed germination with observations on several crop plants. Soil Science Society of America Journal 13, 224–226.
| A method for measuring the effects of soil salinity on seed germination with observations on several crop plants.Crossref | GoogleScholarGoogle Scholar |
Bafoil M, Le Ru A, Merbahi N, Eichwald O, Dunand C, Yousfi M (2019) New insights of low-temperature plasma effects on germination of three genotypes of Arabidopsis thaliana seeds under osmotic and saline stresses. Scientific Reports 9, 8649
| New insights of low-temperature plasma effects on germination of three genotypes of Arabidopsis thaliana seeds under osmotic and saline stresses.Crossref | GoogleScholarGoogle Scholar |
Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G, Maurel C, Santoni V (2016) Novel aquaporin regulatory mechanisms revealed by interactomics. Molecular & Cellular Proteomics 15, 3473–3487.
| Novel aquaporin regulatory mechanisms revealed by interactomics.Crossref | GoogleScholarGoogle Scholar |
Belmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, Hashimoto M, Fei J, Harada CM, Munoz MD, Le BH, Drews GN, Brady SM, Goldberg RB, Harada JJ (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proceedings of the National Academy of Sciences 110, E435–E444.
| Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed.Crossref | GoogleScholarGoogle Scholar |
Bewley JD (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066.
| Seed germination and dormancy.Crossref | GoogleScholarGoogle Scholar |
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) ‘Seeds: physiology of development, germination and dormancy.’ 3rd edn. (Springer: New York, NY, USA) https://doi.org/10.1007/978-1-4614-4693-4
Bienert GP, Chaumont F (2014) Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochimica et Biophysica Acta (BBA) – General Subjects 1840, 1596–1604.
| Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar |
Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW, Qiu J, Gilliham M, Schultz C, Schwarz M, Ramesh SA, Yool A, Tyerman S (2017) Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant, Cell & Environment 40, 802–815.
| Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH.Crossref | GoogleScholarGoogle Scholar |
Ceciliato PHO, Zhang J, Liu Q, Shen X, Hu H, Liu C, Schäffner AR, Schroeder JI (2019) Intact leaf gas exchange provides a robust method for measuring the kinetics of stomatal conductance responses to abscisic acid and other small molecules in Arabidopsis and grasses. Plant Methods 15, 38
| Intact leaf gas exchange provides a robust method for measuring the kinetics of stomatal conductance responses to abscisic acid and other small molecules in Arabidopsis and grasses.Crossref | GoogleScholarGoogle Scholar |
Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiology 125, 1206–1215.
| Aquaporins constitute a large and highly divergent protein family in maize.Crossref | GoogleScholarGoogle Scholar |
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
| Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Coolbear P, Francis A, Grierson D (1984) The effect of low temperature pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds. Journal of Experimental Botany 35, 1609–1617.
| The effect of low temperature pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds.Crossref | GoogleScholarGoogle Scholar |
Crowe JH, Crowe LM (1992) Membrane integrity in an hydrobiotic organisms: toward a mechanism for stabilizing dry seeds. In ‘Water and life’. (Eds GN Somero, CB Osmond, CL Bolis) pp. 87–103. (Springer: Berlin, Heidelberg, Germany)
Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133, 462–469.
| A gateway cloning vector set for high-throughput functional analysis of genes in planta.Crossref | GoogleScholarGoogle Scholar |
Czechowski T, Stitt M, Altmann T, Udvardi M, Scheible W-R̈ (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139, 5–17.
| Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Da Ines O (2008) Functional analysis of PIP2 aquaporins in Arabidopsis thaliana. PhD thesis, Ludwig-Maximilians University, Munich, Germany.
Da Ines O, Graf W, Franck KI, Albert A, Winkler JB, Scherb H, Stichler W, Schaffner AR (2010) Kinetic analyses of plant water relocation using deuterium as tracer – reduced water flux of Arabidopsis pip2 aquaporin knockout mutants. Plant Biology 12, 129–139.
| Kinetic analyses of plant water relocation using deuterium as tracer – reduced water flux of Arabidopsis pip2 aquaporin knockout mutants.Crossref | GoogleScholarGoogle Scholar |
Daszkowska-Golec A (2011) Arabidopsis seed germination under abiotic stress as a concert of action of phytohormones. OMICS: A Journal of Integrative Biology 15, 763–774.
| Arabidopsis seed germination under abiotic stress as a concert of action of phytohormones.Crossref | GoogleScholarGoogle Scholar |
do Espirito Santo Pereira A, Caixeta Oliveira H, Fernandes Fraceto L, Santaella C (2021) Nanotechnology potential in seed priming for sustainable agriculture. Nanomaterials 11, 267
| Nanotechnology potential in seed priming for sustainable agriculture.Crossref | GoogleScholarGoogle Scholar |
Duan L, Dietrich D, Ng CH, Chan PMY, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. The Plant Cell 25, 324–341.
| Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar |
Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochemical Journal 414, 53–61.
| Plant plasma membrane water channels conduct the signalling molecule H2O2.Crossref | GoogleScholarGoogle Scholar |
Fenner M, Thompson K (2005) ‘The ecology of seeds.’ (Cambridge University Press: Cambridge, UK) https://doi.org/10.1017/CBO9780511614101.007
Footitt S, Clewes R, Feeney M, Finch-Savage WE, Frigerio L (2019) Aquaporins influence seed dormancy and germination in response to stress. Plant, Cell & Environment 42, 2325–2339.
| Aquaporins influence seed dormancy and germination in response to stress.Crossref | GoogleScholarGoogle Scholar |
Gattolin S, Sorieul M, Frigerio L (2011) Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane. Molecular Plant 4, 180–189.
| Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane.Crossref | GoogleScholarGoogle Scholar |
Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C (2015) Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. The Plant Cell 27, 1945–1954.
| Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation.Crossref | GoogleScholarGoogle Scholar |
Groszmann M, Osborn HL, Evans JR (2017) Carbon dioxide and water transport through plant aquaporins. Plant, Cell & Environment 40, 938–961.
| Carbon dioxide and water transport through plant aquaporins.Crossref | GoogleScholarGoogle Scholar |
Groszmann M, De Rosa A, Chen W, Qiu J, McGaughey SA, Byrt CS, Evans JR (2021) Permeability profiling of all 13 Arabidopsis PIP aquaporins using a high throughput yeast approach [Preprint]. bioRxiv
| Permeability profiling of all 13 Arabidopsis PIP aquaporins using a high throughput yeast approach [Preprint].Crossref | GoogleScholarGoogle Scholar |
Guha T, Das H, Mukherjee A, Kundu R (2021) Elucidating ROS signaling networks and physiological changes involved in nanoscale zero valent iron primed rice seed germination sensu stricto. Free Radical Biology and Medicine 171, 11–25.
| Elucidating ROS signaling networks and physiological changes involved in nanoscale zero valent iron primed rice seed germination sensu stricto.Crossref | GoogleScholarGoogle Scholar |
Han C-s, Kim S, Lee S-e, Choi S, Kim S-h, Yoon Is, Hwang Y-s (2018) Cross-talk between ABA and sugar signaling is mediated by the ACGT core and CE1 element reciprocally in OsTIP3;1 promoter. Journal of Plant Physiology 224-225, 103–111.
| Cross-talk between ABA and sugar signaling is mediated by the ACGT core and CE1 element reciprocally in OsTIP3;1 promoter.Crossref | GoogleScholarGoogle Scholar |
Harrison SJ, Mott EK, Parsley K, Aspinall S, Gray JC, Cottage A (2006) A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2, 19
| A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation.Crossref | GoogleScholarGoogle Scholar |
Hoai PTT, Tyerman SD, Schnell N, Tucker M, McGaughey SA, Qiu J, Groszmann M, Byrt CS (2020) Deciphering aquaporin regulation and roles in seed biology. Journal of Experimental Botany 71, 1763–1773.
| Deciphering aquaporin regulation and roles in seed biology.Crossref | GoogleScholarGoogle Scholar |
Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, Kang H (2012) Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. Journal of Plant Research 125, 147–153.
| Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Hu Y, Omary M, Hu Y, Doron O, Hoermayer L, Chen Q, Megides O, Chekli O, Ding Z, Friml J, Zhao Y, Tsarfaty I, Shani E (2021) Cell kinetics of auxin transport and activity in Arabidopsis root growth and skewing. Nature Communications 12, 1657
| Cell kinetics of auxin transport and activity in Arabidopsis root growth and skewing.Crossref | GoogleScholarGoogle Scholar |
Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiology 126, 1358–1369.
| The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants.Crossref | GoogleScholarGoogle Scholar |
Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA (2016) A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. The Plant Journal : for Cell and Molecular Biology 88, 1058–1070.
| A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling.Crossref | GoogleScholarGoogle Scholar |
Kourghi M, Nourmohammadi S, Pei JV, Qiu J, McGaughey S, Tyerman SD, Byrt CS, Yool AJ (2017) Divalent cations regulate the ion conductance properties of diverse classes of aquaporins. International Journal of Molecular Sciences 18, 2323
| Divalent cations regulate the ion conductance properties of diverse classes of aquaporins.Crossref | GoogleScholarGoogle Scholar |
Li X, Pan Y, Chang B, Wang Y, Tang Z (2016) NO promotes seed germination and seedling growth under high salt may depend on EIN3 protein in Arabidopsis. Frontiers in Plant Science 6, 1203
| NO promotes seed germination and seedling growth under high salt may depend on EIN3 protein in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Liu C (2015) The PIP1 protein expression is positively regulated by PIP2;1 and PIP2;2 in Arabidopsis thaliana. Dissertation, Ludwig-Maximilians-Universität München. Available at https://edoc.ub.uni-muenchen.de/18857/1/Liu_Chen.pdf
Liu H-Y, Yu X, Cui D-Y, Sun M-H, Sun W-N, Tang Z-C, Kwak S-S, Su W-A (2007) The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Research 17, 638–649.
| The role of water channel proteins and nitric oxide signaling in rice seed germination.Crossref | GoogleScholarGoogle Scholar |
Liu C, Fukumoto T, Matsumoto T, Gena P, Frascaria D, Kaneko T, Katsuhara M, Zhong S, Sun X, Zhu Y, Iwasaki I, Ding X, Calamita G, Kitagawa Y (2013a) Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiology and Biochemistry 63, 151–158.
| Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination.Crossref | GoogleScholarGoogle Scholar |
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang H-Q, Luan S, Li J, He Z-H (2013b) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proceedings of the National Academy of Sciences 110, 15485–15490.
| Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Liu X-M, Nguyen XC, Kim KE, Han HJ, Yoo J, Lee K, Kim MC, Yun D-J, Chung WS (2013c) Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress. Biochemical and Biophysical Research Communications 430, 1054–1059.
| Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress.Crossref | GoogleScholarGoogle Scholar |
Lutts S, Benincasa P, Wojtyla L, Szymon Kubala S, Pace R, Lechowska K, Quinet M, Garnczarska M (2016) Seed priming: new comprehensive approaches for an old empirical technique. In ‘New challenges in seed biology – basic and translational research driving seed technology’. (Eds S Araujo, A Balestrazzi) (pp. 1–30). (InTech: London, UK) https://doi.org/10.5772/64420
Mahdieh M, Mostajeran A, Horie T, Katsuhara M (2008) Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant and Cell Physiology 49, 801–813.
| Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants.Crossref | GoogleScholarGoogle Scholar |
Manz B, Muller K, Kucera B, Volke F, Leubner-Metzger G (2005) Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant Physiology 138, 1538–1551.
| Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging.Crossref | GoogleScholarGoogle Scholar |
Matsunami M, Hayashi H, Murai-Hatano M, Ishikawa-Sakurai J (2022) Effect of hydropriming on germination and aquaporin gene expression in rice. Plant Growth Regulation 97, 263–270.
| Effect of hydropriming on germination and aquaporin gene expression in rice.Crossref | GoogleScholarGoogle Scholar |
Maurel C, Chrispeels M, Lurin C, Tacnet F, Geelen D, Ripoche P, Guern J (1997) Function and regulation of seed aquaporins. Journal of Experimental Botany 48, 421–430.
| Function and regulation of seed aquaporins.Crossref | GoogleScholarGoogle Scholar |
McDowell SC, Akmakjian G, Sladek C, Mendoza-Cozatl D, Morrissey JB, Saini N, Mittler R, Baxter I, Salt DE, Ward JM, Schroeder JI, Guerinot ML, Harper JF (2013) Elemental concentrations in the seed of mutants and natural variants of Arabidopsis thaliana grown under varying soil conditions. PLoS ONE 8, e63014
| Elemental concentrations in the seed of mutants and natural variants of Arabidopsis thaliana grown under varying soil conditions.Crossref | GoogleScholarGoogle Scholar |
McGaughey SA, Qiu J, Tyerman SD, Byrt CS (2018) Regulating root aquaporin function in response to changes in salinity. Annual Plant Reviews online 1, 1–36.
| Regulating root aquaporin function in response to changes in salinity.Crossref | GoogleScholarGoogle Scholar |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
| Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar |
Narsai R, Gouil Q, Secco D, Srivastava A, Karpievitch YV, Liew LC, Lister R, Lewsey MG, Whelan J (2017) Extensive transcriptomic and epigenomic remodelling occurs during Arabidopsis thaliana germination. Genome Biology 18, 172
| Extensive transcriptomic and epigenomic remodelling occurs during Arabidopsis thaliana germination.Crossref | GoogleScholarGoogle Scholar |
Nasri N, Maatallah S, Kaddour R, Lachaal M (2016) Effect of salinity on Arabidopsis thaliana seed germination and acid phosphatase activity. Archives of Biological Sciences 68, 17–23.
| Effect of salinity on Arabidopsis thaliana seed germination and acid phosphatase activity.Crossref | GoogleScholarGoogle Scholar |
Niemann S, Burghardt M, Popp C, Riederer M (2013) Aqueous pathways dominate permeation of solutes across Pisum sativum seed coats and mediate solute transport via diffusion and bulk flow of water. Plant, Cell & Environment 36, 1027–1036.
| Aqueous pathways dominate permeation of solutes across Pisum sativum seed coats and mediate solute transport via diffusion and bulk flow of water.Crossref | GoogleScholarGoogle Scholar |
Obroucheva NV (2013) Aquaporins in seeds. Seed Science Research 23, 213–216.
| Aquaporins in seeds.Crossref | GoogleScholarGoogle Scholar |
Pachchigar KP, Dharajiya DT, Jani SN, Songara JN, Dave GS (2022) Mechanisms and applications of nanopriming: new vista for seed germination. In ‘Miniaturized analytical devices: materials and technology’. (Eds SK Kailasa, CM Hussain) pp. 261–277. (Wiley-VCH: Weinheim, Germany)
Paul S, Dey S, Kundu R (2022) Seed priming: an emerging tool towards sustainable agriculture. Plant Growth Regulation 97, 215–234.
| Seed priming: an emerging tool towards sustainable agriculture.Crossref | GoogleScholarGoogle Scholar |
Péret B, Li G, Zhao J, Band LR, Voß U, Postaire O, Luu D-T, Da Ines O, Casimiro I, Lucas M (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology 14, 991–998.
| Auxin regulates aquaporin function to facilitate lateral root emergence.Crossref | GoogleScholarGoogle Scholar |
Prado K, Cotelle V, Li G, Bellati J, Tang N, Tournaire-Roux C, Martinière A, Santoni V, Maurel C (2019) Oscillating aquaporin phosphorylation and 14-3-3 proteins mediate the circadian regulation of leaf hydraulics. The Plant Cell 31, 417–429.
| Oscillating aquaporin phosphorylation and 14-3-3 proteins mediate the circadian regulation of leaf hydraulics.Crossref | GoogleScholarGoogle Scholar |
Qing D, Yang Z, Li M, Wong WS, Guo G, Liu S, Guo H, Li N (2016) Quantitative and functional phosphoproteomic analysis reveals that ethylene regulates water transport via the C-terminal phosphorylation of aquaporin PIP2;1 in Arabidopsis. Molecular Plant 9, 158–174.
| Quantitative and functional phosphoproteomic analysis reveals that ethylene regulates water transport via the C-terminal phosphorylation of aquaporin PIP2;1 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Qiu J, McGaughey SA, Groszmann M, Tyerman SD, Byrt CS (2020) Phosphorylation influences water and ion channel function of AtPIP2;1. Plant, Cell & Environment 43, 2428–2442.
| Phosphorylation influences water and ion channel function of AtPIP2;1.Crossref | GoogleScholarGoogle Scholar |
Ravindran P, Yong SY, Mohanty B, Kumar PP (2020) An LRR-only protein regulates abscisic acid-mediated abiotic stress responses during Arabidopsis seed germination. Plant Cell Reports 39, 909–920.
| An LRR-only protein regulates abscisic acid-mediated abiotic stress responses during Arabidopsis seed germination.Crossref | GoogleScholarGoogle Scholar |
Reid DA, Lott JNA, Attree SM, Fowke LC (1999) Imbibition of white spruce seeds and somatic embryos: a study of morphological changes in an environmental scanning electron microscope and potassium leakage. In Vitro Cellular & Developmental Biology – Plant 35, 303–308.
| Imbibition of white spruce seeds and somatic embryos: a study of morphological changes in an environmental scanning electron microscope and potassium leakage.Crossref | GoogleScholarGoogle Scholar |
Rodrigues O, Reshetnyak G, Grondin A, Saijo Y, Leonhardt N, Maurel C, Verdoucq L (2017) Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proceedings of the National Academy of Sciences 114, 9200–9205.
| Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure.Crossref | GoogleScholarGoogle Scholar |
Rosental L, Nonogaki H, Fait A (2014) Activation and regulation of primary metabolism during seed germination. Seed Science Research 24, 1–15.
| Activation and regulation of primary metabolism during seed germination.Crossref | GoogleScholarGoogle Scholar |
Shabala S, Shabala L, Volkenburgh EV (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Functional Plant Biology 30, 507–514.
| Effect of calcium on root development and root ion fluxes in salinised barley seedlings.Crossref | GoogleScholarGoogle Scholar |
Simon EW, Harun RMR (1972) Leakage during Seed Imbibition. Journal of Experimental Botany 23, 1076–1085.
| Leakage during Seed Imbibition.Crossref | GoogleScholarGoogle Scholar |
Simon EW, Mills LK (1983) Imbibition, leakage and membranes. In ‘Mobilization of reserves in germination’. (Eds C Nozzolillo, PJ Lea, FA Loewus) pp. 9–27. (Springer: Boston, MA, USA)
Su Y, Liu Z, Sun J, Wu C, Li Y, Zhang C, Zhao L (2022) Genome-wide identification of maize aquaporin and functional analysis during seed germination and seedling establishment. Frontiers in Plant Science 13, 831916
| Genome-wide identification of maize aquaporin and functional analysis during seed germination and seedling establishment.Crossref | GoogleScholarGoogle Scholar |
Takahashi H, Rai M, Kitagawa T, Morita S, Masumura T, Tanaka K (2004) Differential localization of tonoplast intrinsic proteins on the membrane of protein body type II and aleurone grain in rice seeds. Bioscience, Biotechnology, and Biochemistry 68, 1728–1736.
| Differential localization of tonoplast intrinsic proteins on the membrane of protein body type II and aleurone grain in rice seeds.Crossref | GoogleScholarGoogle Scholar |
Tian S, Wang X, Li P, Wang H, Ji H, Xie J, Qiu Q, Shen D, Dong H (2016) Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiology 171, 1635–1650.
| Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways.Crossref | GoogleScholarGoogle Scholar |
Tuan PA, Nguyen T-N, Jordan MC, Ayele BT (2021) A shift in abscisic acid/gibberellin balance underlies retention of dormancy induced by seed development temperature. Plant, Cell & Environment 44, 2230–2244.
| A shift in abscisic acid/gibberellin balance underlies retention of dormancy induced by seed development temperature.Crossref | GoogleScholarGoogle Scholar |
Tyerman SD, McGaughey SA, Qiu J, Yool AJ, Byrt CS (2021) Adaptable and multifunctional ion-conducting aquaporins. Annual Review of Plant Biology 72, 703–736.
| Adaptable and multifunctional ion-conducting aquaporins.Crossref | GoogleScholarGoogle Scholar |
Utsugi S, Shibasaka M, Maekawa M, Katsuhara M (2015) Control of the water transport activity of barley HvTIP3;1 specifically expressed in seeds. Plant and Cell Physiology 56, 1831–1840.
| Control of the water transport activity of barley HvTIP3;1 specifically expressed in seeds.Crossref | GoogleScholarGoogle Scholar |
Vander Willigen C, Postaire O, Tournaire-Roux C, Boursiac Y, Maurel C (2006) Expression and inhibition of aquaporins in germinating Arabidopsis seeds. Plant and Cell Physiology 47, 1241–1250.
| Expression and inhibition of aquaporins in germinating Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar |
Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136, 1005–1016.
| Auxin: a trigger for change in plant development.Crossref | GoogleScholarGoogle Scholar |
Van Steveninck J, Ledeboer AM (1974) Phase transitions in the yeast cell membrane the influence of temperature on the reconstitution of active dry yeast. Biochimica et Biophysica Acta (BBA) – Biomembranes 352, 64–70.
| Phase transitions in the yeast cell membrane the influence of temperature on the reconstitution of active dry yeast.Crossref | GoogleScholarGoogle Scholar |
Verdoucq L, Rodrigues O, Martiniere A, Luu DT, Maurel C (2014) Plant aquaporins on the move: reversible phosphorylation, lateral motion and cycling. Current Opinion in Plant Biology 22, 101–107.
| Plant aquaporins on the move: reversible phosphorylation, lateral motion and cycling.Crossref | GoogleScholarGoogle Scholar |
Wang Y, Tajkhorshid E (2010) Nitric oxide conduction by the brain aquaporin AQP4. Proteins: Structure, Function, and Bioinformatics 78, 661–670.
| Nitric oxide conduction by the brain aquaporin AQP4.Crossref | GoogleScholarGoogle Scholar |
Wang C, Hu H, Qin X, Zeise B, Xu D, Rappel W-J, Boron WF, Schroeder JI (2016) Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. The Plant Cell 28, 568–582.
| Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor.Crossref | GoogleScholarGoogle Scholar |
Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. Journal of Experimental Botany 62, 3289–3309.
| First off the mark: early seed germination.Crossref | GoogleScholarGoogle Scholar |
Wilson RL, Kim H, Bakshi A, Binder BM (2014) The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiology 165, 1353–1366.
| The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress.Crossref | GoogleScholarGoogle Scholar |
Wojtyla L, Lechowska K, Kubala S, Garnczarska M (2016) Different modes of hydrogen peroxide action during seed germination. Frontiers in Plant Science 7, 66
| Different modes of hydrogen peroxide action during seed germination.Crossref | GoogleScholarGoogle Scholar |
Zhang W-H, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW (2007) Review: Nutrient loading of developing seeds. Functional Plant Biology 34, 314–331.
| Review: Nutrient loading of developing seeds.Crossref | GoogleScholarGoogle Scholar |
Zhang S, Feng M, Chen W, Zhou X, Lu J, Wang Y, Li Y, Jiang C-Z, Gan S-S, Ma N, Gao J (2019) In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin. Nature Plants 5, 290–299.
| In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin.Crossref | GoogleScholarGoogle Scholar |
Zhou Y, Setz N, Niemietz C, Qu H, Offler CE, Tyerman SD, Patrick JW (2007) Aquaporins and unloading of phloem-imported water in coats of developing bean seeds. Plant, Cell & Environment 30, 1566–1577.
| Aquaporins and unloading of phloem-imported water in coats of developing bean seeds.Crossref | GoogleScholarGoogle Scholar |
