Deactivation of aquaporins decreases internal conductance to CO2 diffusion in tobacco leaves grown under long-term drought
Shin-Ichi Miyazawa A , Satomi Yoshimura A , Yuki Shinzaki A , Masayoshi Maeshima B and Chikahiro Miyake A C DA Research Institute of Innovative Technology for the Earth (RITE), 9-2 Kizugawadai, Kizugawa City, Kyoto 619-0292, Japan.
B Laboratory of Cell Dynamics, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan.
C Present address: Laboratory of Plant Nutrition, Department of Biological and Environmental Science, Faculty of Agriculture, Graduate School of Agricultural Science, Kobe University, Nada, Kobe 657-8501, Japan.
D Corresponding author. Email: cmiyake@hawk.kobe-u.ac.jp
Functional Plant Biology 35(7) 553-564 https://doi.org/10.1071/FP08117
Submitted: 10 April 2008 Accepted: 3 June 2008 Published: 21 August 2008
Abstract
We compared the diffusion conductance to CO2 from the intercellular air space to the chloroplasts (internal conductance (g i)) between tobacco leaves acclimated to long-term drought (drought-acclimated (DA)) and those grown under sufficient irrigation (well-watered (WW)), and analysed the changes in g i in relation to the leaf anatomical characteristics and a possible CO2 transporter, aquaporin. The g i, which was estimated by combined analyses of CO2 gas exchange with chlorophyll fluorescence, in the DA plants was approximately half of that in the WW plants. The mesophyll and chloroplast surface areas exposing the intercellular air space, which potentially affect g i, were not significantly different between the WW and DA plants. The amounts of plasma membrane aquaporins (PIP), immunochemically determined using radish PIP antibodies, were unrelated to g i. After treatment with HgCl2, an aquaporin inhibitor, the water permeability of the leaf tissues (measured as the weight loss of fully-turgid leaf disks without the abaxial epidermis in 1 m sorbitol) in WW plants decreased with an increase in HgCl2 concentration. The g i in the WW plants decreased to similar levels to the DA plants when the detached leaflets were fed with 0.5 mm HgCl2. In contrast, both water permeability and g i were insensitive to HgCl2 treatments in DA plants. These results suggest that deactivation of aquaporins is responsible for the significant reduction in g i observed in plants growing under long-term drought.
Additional keywords: acclimation, drought stress, leaf anatomy, mesophyll conductance.
Acknowledgements
S.-I. Miyazawa thanks Professor Ichiro Terashima for his constructive comments on early drafts of this manuscript and also Dr Hiroshi Yamamoto for his helpful suggestions. We also thank the anonymous reviewers for their advice. This work was supported by the Ministry of Economy, Trade and Industry (METI), Japan.
Atkin OK,
Evans JR, Siebke K
(1998) Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. Australian Journal of Plant Physiology 25, 437–443.
Bernacchi CJ,
Portis AR,
Nakano H,
von Caemmerer S, Long SP
(2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo.
Plant Physiology 130, 1992–1998.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Biela A,
Grote K,
Otto B,
Hoth S,
Hedrich R, Kaldenhoff R
(1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. The Plant Journal 18, 565–570.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chartzoulakis K,
Patakas A,
Kofidis G,
Bosabalidis A, Nastou A
(2002) Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars. Scientia Horticulturae 95, 39–50.
| Crossref | GoogleScholarGoogle Scholar |
Cooper GJ, Boron WF
(1998) Effects of PCMBS on CO2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant. The American Journal of Physiology 275, C1481–C1486.
| PubMed |
Epron D,
Godard D,
Cornic G, Genty B
(1995) Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant, Cell & Environment 18, 43–51.
| Crossref | GoogleScholarGoogle Scholar |
Ethier GJ, Livingston NJ
(2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant, Cell & Environment 27, 137–153.
| Crossref | GoogleScholarGoogle Scholar |
Evans JR,
von Caemmerer S,
Setchell BA, Hudson GS
(1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Australian Journal of Plant Physiology 21, 475–495.
Flexas J,
Ribas-Carbo M,
Hanson DT,
Bota J,
Otto B,
Cifre J,
McDowell N,
Medrano H, Kaldenhoff R
(2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2
in vivo.
The Plant Journal 48, 427–439.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Flexas J,
Ribas-Carbo M,
Diaz-Espejo A,
Galmes J, Medrano H
(2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fraysse LC,
Wells B,
McCann MC, Kjellbom P
(2005) Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biology of the Cell 97, 519–534.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fredeen AL,
Gamon JA, Field CB
(1991) Responses of photosynthesis and carbohydrate-partitioning to limitations in nitrogen and water availability in field-grown sunflower. Plant, Cell & Environment 14, 963–970.
| Crossref | GoogleScholarGoogle Scholar |
Galmes J,
Medrano H, Flexas J
(2006) Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. Journal of Experimental Botany 57, 3659–3667.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Genty B,
Briantais JM, Baker N
(1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
Hanba YT,
Miyazawa S-I, Terashima I
(1999) The Influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Functional Ecology 13, 632–639.
| Crossref | GoogleScholarGoogle Scholar |
Hanba YT,
Shibasaka M,
Hayashi Y,
Hayasaka T,
Kasamo K,
Terashima I, Katsuhara M
(2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant & Cell Physiology 45, 521–529.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Johanson U, Gustavsson S
(2002) A new subfamily of major intrinsic proteins in plants. Molecular Biology and Evolution 19, 456–461.
| PubMed |
Johansson I,
Larsson C,
Ek B, Kjellbom P
(1996) The major intrinsic proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. The Plant Cell 8, 1181–1191.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Johansson I,
Karlsson M,
Shukla VK,
Chrispeels MJ,
Larsson C, Kjellbom P
(1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. The Plant Cell 10, 451–459.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maeshima M
(1992) Characterization of the major integral protein of vacuolar membrane. Plant Physiology 98, 1248–1254.
| PubMed |
Makino A,
Mae T, Ohira K
(1986) Colorimetric measurement of protein stained with Coomassie Brilliant Blue R on sodium dodecyl sulfate–polyacrylamide gel electrophoresis by eluting with formamide. Agricultural and Biological Chemistry 50, 1911–1912.
Miyake C, Okamura M
(2003) Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid members from spinach chloroplasts. Plant & Cell Physiology 44, 457–462.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miyazawa S-I, Terashima I
(2001) Slow chloroplast development in the evergreen broad-leaved tree species: relationship between leaf anatomical characteristics and photosynthetic rate during leaf development. Plant, Cell & Environment 26, 745–755.
Monti A,
Brugnoli E,
Scartazza A, Amaducci MT
(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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nakhoul NL,
Davis BA,
Romero MF, Boron W
(1998) Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. The American Journal of Physiology 43, C543–C548.
North GB, Nobel PS
(2000) Heterogeneity in water availability alters cellular development and hydraulic conductivity along roots of a desert succulent. Annals of Botany 85, 247–255.
| Crossref | GoogleScholarGoogle Scholar |
Ohshima Y,
Iwasaki I,
Suga S,
Murakami M,
Inoue K, Maeshima M
(2001) Low aquaporin content and low osmotic water permeability of the plasma and vacuolar membranes of a CAM plant Graptopetalum paraguayense: comparison with radish. Plant & Cell Physiology 42, 1119–1129.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Otto B, Kaldenhoff R
(2000) Cell-specific expression of the mercury-insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum.
Planta 211, 167–172.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Parkhurst DF, Mott KA
(1990) Intercellular diffusion limits to CO2 uptake in leaves. Plant Physiology 94, 1024–1032.
| PubMed |
Porra RJ,
Thompson WA, Kriedemann PE
(1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
| Crossref | GoogleScholarGoogle Scholar |
Reich PB,
Walters MB, Tabone TJ
(1989) Response of Ulmus americana seedlings to varying nitrogen and water status. 2 Water and nitrogen use efficiency in photosynthesis. Tree Physiology 5, 173–184.
| PubMed |
Suga S, Maeshima M
(2004) Water channel activity of radish plasma membrane aquaporins heterologously expressed in yeast and their modification by site-directed mutagenesis. Plant & Cell Physiology 45, 823–830.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Suga S,
Imagawa S, Maeshima M
(2001) Specificity of the accumulation of mRNAs and proteins of the plasma membrane and tonoplast aquaporins in radish organs. Planta 212, 294–304.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Syvertsen JP,
Lloyd J,
McConchie C,
Kriedemann PE, Farquhar GD
(1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell & Environment 18, 149–157.
| Crossref | GoogleScholarGoogle Scholar |
Tazawa M,
Asai K, Iwasaki N
(1996) Characteristics of Hg- and Zn-sensitive water channels in the plasma membrane of Chara cells. Botanica Acta 109, 388–396.
Terashima I, Ono K
(2002) Effects of HgCl2 on CO2 dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant & Cell Physiology 43, 70–78.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Terashima I,
Miyazawa S-I, Hanba YT
(2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. Journal of Plant Research 114, 93–105.
| Crossref | GoogleScholarGoogle Scholar |
Terashima I,
Araya T,
Miyazawa S-I,
Sone K, Yano S
(2005) Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. Annals of Botany 95, 507–519.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thain JF
(1983) Curvature correction factors in the measurement of cell surface areas in plant tissues. Journal of Experimental Botany 34, 87–94.
| Crossref | GoogleScholarGoogle Scholar |
Uehlein N,
Lovisolo C,
Siefritz F, Kaldenhoff R
(2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425, 734–737.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Uehlein N,
Otto B,
Hanson DT,
Fischer M,
McDowell N, Kaldenhoff R
(2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. The Plant Cell 20, 648–657.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Warren CR
(2008) Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not. Journal of Experimental Botany 59, 327–334.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wegener AD, Jones LR
(1984) Phosphorylation-induced mobility shift in phospholamban in sodium-dodecyl-sulfate–polyacrylamide gels. Journal of Biological Chemistry 259, 1834–1841.
| PubMed |
Yamori W,
Noguchi K,
Hanba YT, Terashima I
(2006) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant & Cell Physiology 47, 1069–1080.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yang B,
Fukuda N,
van Hoek A,
Matthay MA,
Ma T, Verkman AS
(2000) Carbon dioxide permeability of aquaporin-1 measured in erythrocytes and lung of aquaporin-1 nul mice and in reconstituted proteoliposomes. Journal of Biological Chemistry 275, 2686–2692.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
