Decreased capacity for sodium export out of Arabidopsis chloroplasts impairs salt tolerance, photosynthesis and plant performance

Müller, Maria; Kunz, Hans‐Henning; Schroeder, Julian I.; Kemp, Grant; Young, Howard S.; Neuhaus, H. Ekkehard

doi:10.1111/tpj.12501

Cited by 64 publications

(57 citation statements)

References 65 publications

(100 reference statements)

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“…In this study, the authors also suggested that sodium influx could be balanced by the sodium: proton antiporter NHD1. This transporter, previously identified both in chloroplast and plasma membrane proteomes (15,101), was recently characterized as a sodium exporter of the chloroplast envelope (103). In the AT_CHLORO database, BASS2 was found associated with both envelope and thylakoid membranes, although NDH1 was not detected.…”

Section: Discussionmentioning

confidence: 99%

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Tomizioli

Lazar

Brugière

et al. 2014

Molecular & Cellular Proteomics

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Photosynthesis has shaped atmospheric and ocean chemistries and probably changed the climate as well, as oxygen is released from water as part of the photosynthetic process. In photosynthetic eukaryotes, this process occurs in the chloroplast, an organelle containing the most abundant biological membrane, the thylakoids. The thylakoids of plants and some green algae are structurally inhomogeneous, consisting of two main domains: the grana, which are piles of membranes gathered by stacking forces, and the stroma-lamellae, which are unstacked thylakoids connecting the grana. The major photosynthetic complexes are unevenly distributed within these compartments because of steric and electrostatic constraints. Although proteomic analysis of thylakoids has been instrumental to define its protein components, no extensive proteomic study of subthylakoid localization of proteins in the BBY (grana) and the stroma-lamellae fractions has been achieved so far. To fill this gap, we performed a complete survey of the protein composition of these thylakoid subcompartments using thylakoid membrane fractionations. We employed semiquantitative proteomics coupled with a data analysis pipeline and manual annotation to differentiate genuine BBY and stroma-lamellae proteins from possible contaminants. About 300 thylakoid (or potentially thylakoid) proteins were shown to be enriched in either the BBY or the stroma-lamellae fractions. Overall, present findings corroborate previous observations obtained for photosynthetic proteins that used nonproteomic approaches. The originality of the present proteomic relies in the identification of photosynthetic proteins whose differential distribution in the thylakoid subcompartments might explain already observed phenomenon such as LHCII docking. Besides, from the present localization results we can suggest new molecular actors for photosynthesis-linked activities. For instance, most PsbP-like subunits being differently localized in stroma-lamellae, these proteins could be linked to the PSI-NDH complex in the context of cyclic electron flow around PSI. In addition, we could identify about a hundred new likely minor thylakoid (or chloroplast) proteins, some of them being potential regulators of the chloroplast physiology. Molecular & Cellular Proteomics 13: 10.1074/mcp.M114.040923, 2147-2167, 2014.As primary producers, plants are at the basis of the food chain for most ecosystems and control the planet atmosphere via photosynthesis. In eukaryotes, this process, responsible for carbon fixation and for the release of gaseous oxygen into the atmosphere, takes place in a specialized compartment, the chloroplast. This semiautonomous organelle plays a number of essential functions, including photosynthesis, nitrogen assimilation, sulfur reduction and assimilation, synthesis of amino acids, fatty acids, and many secondary metabolites (1-6). The chloroplast is not the only type of plastids. Plastids are indeed found in every plant tissue (with a very few exceptions such as angiosperm pollen grains) and in...

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Section: Discussionmentioning

confidence: 99%

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Tomizioli

Lazar

Brugière

et al. 2014

Molecular & Cellular Proteomics

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“…In order to cope with salt stress, plants produce protective compounds, adjust their ion homeostasis, and remodel primary metabolism to serve the energy demand under stress (Deinlein et al, 2014;Müller et al, 2014). Focusing on Arabidopsis roots, which are the primary targets of salt stress, this study revealed a rapid and substantial reprogramming of the transcriptome leading to metabolic adaptation.…”

Section: Discussionmentioning

confidence: 99%

Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

et al. 2015

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ORCID IDs: 0000-0003-3058-7570 (A.F.); 0000-0002-7910-9118 (J.S.); 0000-0001-8122-5460 (M.J.M.); 0000-0002-6332-1712 (J.V.-C.); 0000-0002-5605-7984 (J.H.)Soil salinity increasingly causes crop losses worldwide. Although roots are the primary targets of salt stress, the signaling networks that facilitate metabolic reprogramming to induce stress tolerance are less understood than those in leaves. Here, a combination of transcriptomic and metabolic approaches was performed in salt-treated Arabidopsis thaliana roots, which revealed that the group S1 basic leucine zipper transcription factors bZIP1 and bZIP53 reprogram primary C-and N-metabolism. In particular, gluconeogenesis and amino acid catabolism are affected by these transcription factors. Importantly, bZIP1 expression reflects cellular stress and energy status in roots. In addition to the well-described abiotic stress response pathway initiated by the hormone abscisic acid (ABA) and executed by SnRK2 (Snf1-RELATED-PROTEIN-KINASE2) and AREB-like bZIP factors, we identify a structurally related ABA-independent signaling module consisting of SnRK1s and S1 bZIPs. Crosstalk between these signaling pathways recruits particular bZIP factor combinations to establish at least four distinct gene expression patterns. Understanding this signaling network provides a framework for securing future crop productivity.

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“…In C 3 plants where there is no such role for Na + , accumulation of Na + in the chloroplast may be deleterious. Indeed, using knockout lines of NHD1 in Arabidopsis, (Müller et al, 2014) showed that the inability to export Na + out of the chloroplast can impair the salt tolerance, photosynthesis and growth of the plants. It can be inferred from the NHD1 function in this study that proton pumps should also be crucial for Na + homeostasis in the chloroplast.…”

Section: Exclusion Of Na+ From Chloroplast Is Important For Salt Strementioning

confidence: 99%

The Role of Na+ and K+ Transporters in Salt Stress Adaptation in Glycophytes

et al. 2017

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Ionic stress is one of the most important components of salinity and is brought about by excess Na+ accumulation, especially in the aerial parts of plants. Since Na+ interferes with K+ homeostasis, and especially given its involvement in numerous metabolic processes, maintaining a balanced cytosolic Na+/K+ ratio has become a key salinity tolerance mechanism. Achieving this homeostatic balance requires the activity of Na+ and K+ transporters and/or channels. The mechanism of Na+ and K+ uptake and translocation in glycophytes and halophytes is essentially the same, but glycophytes are more susceptible to ionic stress than halophytes. The transport mechanisms involve Na+ and/or K+ transporters and channels as well as non-selective cation channels. Thus, the question arises of whether the difference in salt tolerance between glycophytes and halophytes could be the result of differences in the proteins or in the expression of genes coding the transporters. The aim of this review is to seek answers to this question by examining the role of major Na+ and K+ transporters and channels in Na+ and K+ uptake, translocation and intracellular homeostasis in glycophytes. It turns out that these transporters and channels are equally important for the adaptation of glycophytes as they are for halophytes, but differential gene expression, structural differences in the proteins (single nucleotide substitutions, impacting affinity) and post-translational modifications (phosphorylation) account for the differences in their activity and hence the differences in tolerance between the two groups. Furthermore, lack of the ability to maintain stable plasma membrane (PM) potentials following Na+-induced depolarization is also crucial for salt stress tolerance. This stable membrane potential is sustained by the activity of Na+/H+ antiporters such as SOS1 at the PM. Moreover, novel regulators of Na+ and K+ transport pathways including the Nax1 and Nax2 loci regulation of SOS1 expression and activity in the stele, and haem oxygenase involvement in stabilizing membrane potential by activating H+-ATPase activity, favorable for K+ uptake through HAK/AKT1, have been shown and are discussed.

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Decreased capacity for sodium export out of Arabidopsis chloroplasts impairs salt tolerance, photosynthesis and plant performance

Cited by 64 publications

References 65 publications

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

The Role of Na+ and K+ Transporters in Salt Stress Adaptation in Glycophytes

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