Portal de Periódicos da CAPES

Ion homeostasis: plants feel better with proper control

2007; Springer Nature; Volume: 8; Issue: 8 Linguagem: Inglês

10.1038/sj.embor.7401040

1469-3178

Bernd Mueller‐Roeber, Ingo Drèyer,

Legume Nitrogen Fixing Symbiosis

Review1 August 2007free access Ion homeostasis: plants feel better with proper control Bernd Mueller-Roeber Corresponding Author Bernd Mueller-Roeber Universität Potsdam, Institut für Biochemie und Biologie, Molekularbiologie, Karl-Liebknecht-Strasse 24-25, Haus 20, D-14476 Potsdam/Golm, Germany Search for more papers by this author Ingo Dreyer Ingo Dreyer Universität Potsdam, Institut für Biochemie und Biologie, Molekularbiologie, Karl-Liebknecht-Strasse 24-25, Haus 20, D-14476 Potsdam/Golm, Germany Search for more papers by this author Bernd Mueller-Roeber Corresponding Author Bernd Mueller-Roeber Universität Potsdam, Institut für Biochemie und Biologie, Molekularbiologie, Karl-Liebknecht-Strasse 24-25, Haus 20, D-14476 Potsdam/Golm, Germany Search for more papers by this author Ingo Dreyer Ingo Dreyer Universität Potsdam, Institut für Biochemie und Biologie, Molekularbiologie, Karl-Liebknecht-Strasse 24-25, Haus 20, D-14476 Potsdam/Golm, Germany Search for more papers by this author Author Information Bernd Mueller-Roeber 1 and Ingo Dreyer1 1Universität Potsdam, Institut für Biochemie und Biologie, Molekularbiologie, Karl-Liebknecht-Strasse 24-25, Haus 20, D-14476 Potsdam/Golm, Germany *Corresponding author. Tel: +49 331 977 2810; Fax: +49 331 977 2512; E-mail: [email protected] EMBO Reports (2007)8:735-736https://doi.org/10.1038/sj.embor.7401040 PDFDownload PDF of article text and main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info Plant growth and the ecologically and agriculturally important processes of biomass accumulation and seed production are affected by numerous environmental factors, including air temperature, illumination, water availability and infestation with pathogens. Inorganic ions also represent an integral part of the environmental cocktail that affects plant growth. Of the best bio-available alkali cations—Na+ and K+—plants have a strong preference for K+. K+, the most abundant cation in plant cells, is an essential macronutrient; by contrast, elevated concentrations of Na+ are generally toxic to plants. Therefore, it is not surprising that plants have evolved several strategies that enable them to keep the cytosolic concentration of Na+ low. Only a relatively small number of species can withstand saline environments, and plant researchers are keen to unravel the underlying mechanisms to improve the salt tolerance of crops (Yamaguchi & Blumwald, 2005). Despite the generally toxic effect of high concentrations of Na+, plants have transporters that allow the uptake of Na+ from the soil. Members of the HKT gene family of Na+ and Na+/K+ transporters seem to have a crucial role in controlling this process (Platten et al, 2006). Why do plants have such transporters, if Na+ uptake is so immensely harmful? Physiological studies from the early 1980s reported that at low concentrations Na+ can positively affect the growth of many species of plants. This indicates that, under these conditions, Na+acts as a nutrient rather than as a stress factor. Consequently, a model has been proposed claiming that Na+ can, to some extent, replace its ‘sibling’ K+ in carrying out crucial cellular functions. However, a transporter for Na+ uptake at low external concentrations of Na+ was not known in plants. In a recent article published in The EMBO Journal, Tomoaki Horie and co-workers from three laboratories in San Diego (USA), Pohang (Korea) and Tsukuba (Japan) report their findings on mutant rice plants that lack a functional Na+ transporter called OsHKT2;1 (Horie et al, 2007; Fig 1A). In such lines the OsHKT2;1 gene was disrupted through the insertion of a transposable element—Tos17—which undergoes local transposition events during tissue culture but remains non-mobile in regenerated rice plants. Under standard growth conditions, the knockout plants were indistinguishable from their wild-type counterparts; however, importantly, oshkt2;1 mutants grew to much smaller sizes than the control plants when challenged with low concentrations of Na+ under conditions of K+ starvation. They also accumulated considerably less Na+ in both shoots and roots. Thus, OsHKT2;1 functions in Na+ accumulation and favours plant biomass accumulation under such extreme conditions. Figure 1.Ion homeostasis. The model plant species, thale cress (Arabidopsis thaliana, right) and rice (Oryza sativa, left), are displayed as a chimera. (A) OsHKT2;1 functions as a transporter for Na+ uptake. (B) QSO2, a flavoprotein quiescin sulphydryl oxidase, is a new component in ion homeostasis at the root symplast–xylem interface. (C) Downregulation of OST2/AHA1 H+-ATPase activity is a prerequisite for ABA-induced stomatal closure. ABA, abscisic acid; OST2/AHA, OPEN STOMATA 2. Download figure Download PowerPoint These findings clearly show the nutritional aspect of Na+ and the involvement of a transporter in Na+ uptake. The rice genome contains nine HKT genes, two of which might be pseudogenes (Garciadeblás et al, 2003). Although multigene families are often believed to indicate functional redundancy, fully redundant biological roles are unlikely to remain conserved over evolutionary timescales. Instead, sub-functionalization of duplicated genes often occurs, allowing the fine-tuning of physiological processes and enhancing the ability of an organism to survive in a non-stable environment. In the case of OsHKT2;1, the authors realized that OsHKT2;1 is expressed in roots, its expression is upregulated under conditions of K+ starvation and that OsHKT2;1 transports Na+. This combined knowledge allowed them to set up experimental conditions provoking a phenotype that clearly shows a role of OsHKT2;1 in plant biology. The results from Horie and co-workers underline that the transport of K+ and Na+ are tightly connected processes that are dependent on the nutritional status of the plant. This is also evident in another paper published recently in The EMBO Journal. Santiago Alejandro and co-workers from laboratories in Valencia and Málaga (Spain) discovered another new and unexpected component in plant ion homeostasis (Alejandro et al, 2007). Through screening of an Arabidopsis ‘activation tagging’ lines library, these authors identified a gene, called QSO2, which, on overexpression, confers superior tolerance to toxic concentrations of the cation nonspermidine, a non-metabolizable polyamine. By contrast, tolerance to this chemical was lowered when QSO2 was disrupted through integration of foreign DNA—in so-called T-DNA insertion lines. A high level of expression of QSO2 also led to tolerance against Na+, and Li+, and decreased accumulation of these toxic ions, whereas the accumulation of non-toxic K+ was increased (Fig 1B; the opposite was observed in the qso2 mutant lines). The interesting thing about QSO2 is that it encodes an ‘uncommon’ enzyme—the flavoprotein quiescin sulphydryl oxidase (QSO). It has been proposed that QSOs participate in oxidative folding of disulphide-containing secreted proteins in plants and animals (Coppock & Thorpe, 2006). These proteins enter the secretory pathway and are located in the endoplasmic reticulum, the Golgi apparatus or outside the cell. The domain structure of QSOs was originally identified in human fibroplasts, but their physiological functions remain only poorly defined. Although the precise mode of action of the plant enzyme is not yet known, the recent report by Alejandro et al (2007) indicates an important role in adjusting ion homeostasis. Experimental evidence suggests that QSO2 regulates ion transport at the root symplast–xylem loading interface; however, the well-known xylem parenchyma-expressed outward-rectifying K+ channel SKOR (Gaymard et al, 1998) is not required for this mechanism. Future experiments will therefore have to clarify with which other proteins QSO2 interacts to fully exploit its control function. Another environmental stress that strongly affects plant growth is water scarcity. When exposed to drought, plants accumulate the hormone abscisic acid (ABA), which triggers the closure of stomata—the pores in the leaf epidermis that allow gas exchange for photosynthesis (CO2 uptake) and transpiration (water vapour release). During stomatal opening under favourable conditions, activation of a plasma-membrane-localized proton pump—H+-ATPase—establishes a negative membrane voltage that drives the uptake of K+ (Fig 1C). For stomatal closure, anion channels that depolarize the membrane are activated, setting conditions for long-term K+/anion efflux. The question of whether deactivation of the proton pump is needed for stomatal closure, or whether the activation of anion channels is sufficient to sustain the membrane depolarization necessary to drive K+ efflux, has remained unsolved. This question is difficult to address as several different H+-ATPases with a broad functional overlap are assumed to be expressed in guard cells. However, researchers from Gif-sur-Yvette and Cadarache in France have now found the answer, which they have published in The EMBO Journal. In a physiological screen, Sylvain Merlot and co-workers had previously identified Arabidopsis mutants called OPEN STOMATA 1 (OST1) and OST2. Both mutants show impaired guard-cell movements: stomata do not close properly (Merlot et al, 2002). Positional cloning of the OST2 locus revealed its identity with the known AHA1 gene that codes for a plasma-membrane H+-ATPase that is expressed in the guard cells. Two dominant change-of-function alleles of OST2 were identified as coding for AHA1-P68S and AHA1-L169F-G867S pump variants, respectively. Both mutations disrupt the auto-inhibitory regulation of the AHA1 pump and cause its constitutive activity. Interestingly, this pump deregulation selectively abolishes the stomatal response to ABA, but to a much lesser extent the response to CO2 or darkness (Merlot et al, 2007). Time-delayed downregulation of guard-cell H+-ATPase activity is therefore an essential component of ABA-induced stomatal closure. These studies highlight that transport processes in plants are tightly regulated. We are just starting to understand the mechanisms that fine-tune membrane transporter proteins and therefore the basis of ion homeostasis in plants. Further insights are eagerly awaited in the near future. Biography Bernd Mueller-Roeber & Ingo Dreyer are at the Universität Potsdam, Institut für Biochemie und Biologie, Molekularbiologie, Karl-Liebknecht-Strasse 24-25, Haus 20, D-14476 Potsdam/Golm, Germany References Alejandro S, Rodríguez PL, Bellés JM, Yenush L, García-Sanchez ML, Fernández JA, Serrano R (2007) An Arabidopsis quiescin-sulphydryl oxidase regulates cation homeostasis at the root symplast–xylem interface. EMBO J [doi: accession:10.1038/sj.emboj.7601757 ]Wiley Online LibraryWeb of Science®Google Scholar Coppock DL, Thorpe C (2006) Multidomain flavin-dependent sulfhydryl oxidases. Antioxid Redox Signal 8: 300–311CrossrefCASPubMedWeb of Science®Google Scholar Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34: 788–801Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrire N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94: 647–655Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26: 3003–3014Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Merlot S, Mustilli AC, Genty B, North H, Lefebvre V, Sotta B, Vavasseur A, Giraudat J (2002) Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. Plant J 30: 601–609Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Merlot S et al (2007) Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J [doi: accession:10.1038/sj.emboj.7601750 ]Wiley Online LibraryWeb of Science®Google Scholar Platten JD et al (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci 11: 372–374CrossrefCASPubMedWeb of Science®Google Scholar Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10: 615–620CrossrefCASPubMedWeb of Science®Google Scholar Previous ArticleNext Article Volume 8Issue 81 August 2007In this issue FiguresReferencesRelatedDetailsLoading ...