Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Salinity effects on chloroplast PSII performance in glycophytes and halophytes1

William J. Percey A , Andrew McMinn B , Jayakumar Bose A C , Michael C. Breadmore D , Rosanne M. Guijt E and Sergey Shabala A F
+ Author Affiliations
- Author Affiliations

A School of Land and Food, University of Tasmania, Private Bag 54, Hobart 7001, Australia.

B Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart 7001, Australia.

C ARC Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, University of Adelaide, PMB 1, Glen Osmond, SA 5064, Australia.

D Australian Centre for Research on Separation Science (ACROSS) and School of Chemistry, University of Tasmania, Private Bag 75, Hobart 7001, Australia.

E School of Medicine and Australian Centre for Research on Separation Science, University of Tasmania, Private Bag 34, Hobart 7001, Australia.

F Corresponding author. Email: sergey.shabala@utas.edu.au

Functional Plant Biology 43(11) 1003-1015 https://doi.org/10.1071/FP16135
Submitted: 8 April 2016  Accepted: 12 June 2016   Published: 8 August 2016

Abstract

The effects of NaCl stress and K+ nutrition on photosynthetic parameters of isolated chloroplasts were investigated using PAM fluorescence. Intact mesophyll cells were able to maintain optimal photosynthetic performance when exposed to salinity for more than 24 h whereas isolated chloroplasts showed declines in both the relative electron transport rate (rETR) and the maximal photochemical efficiency of PSII (Fv/Fm) within the first hour of treatment. The rETR was much more sensitive to salt stress compared with Fv/Fm, with 40% inhibition of rETR observed at apoplastic NaCl concentration as low as 20 mM. In isolated chloroplasts, absolute K+ concentrations were more essential for the maintenance of the optimal photochemical performance (Fv/Fm values) rather than sodium concentrations per se. Chloroplasts from halophyte species of quinoa (Chenopodium quinoa Willd.) and pigface (Carpobrotus rosii (Haw.) Schwantes) showed less than 18% decline in Fv/Fm under salinity, whereas the Fv/Fm decline in chloroplasts from glycophyte pea (Pisum sativum L.) and bean (Vicia faba L.) species was much stronger (31 and 47% respectively). Vanadate (a P-type ATPase inhibitor) significantly reduced Fv/Fm in both control and salinity treated chloroplasts (by 7 and 25% respectively), whereas no significant effects of gadolinium (blocker of non-selective cation channels) were observed in salt-treated chloroplasts. Tetraethyl ammonium (TEA) (K+ channel inhibitor) and amiloride (inhibitor of the Na+/H+ antiporter) increased the Fv/Fm of salinity treated chloroplasts by 16 and 17% respectively. These results suggest that chloroplasts’ ability to regulate ion transport across the envelope and thylakoid membranes play a critical role in leaf photosynthetic performance under salinity.

Additional keywords: membrane transport, non-stomatal limitation, photosynthesis, potassium, ROS, sodium.


References

Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. Journal of Plant Physiology 171, 670–687.
Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment.Crossref | GoogleScholarGoogle Scholar | 24635902PubMed |

Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.
Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Sju7s%3D&md5=6688aabcf679abfc54fb1be83a974cadCAS | 10455050PubMed |

Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391–396.
Production and scavenging of reactive oxygen species in chloroplasts and their functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksbY%3D&md5=02aa399fad32027ca0622e210b7c849bCAS | 16760493PubMed |

Belkhodja R, Morales F, Abadia A, Medrano H, Abadia J (1999) Effects of salinity on chlorophyll fluorescence and photosynthesis of barley (Hordeum vulgare L.) grown under a triple-line-source sprinkler system in the field. Photosynthetica 36, 375–387.
Effects of salinity on chlorophyll fluorescence and photosynthesis of barley (Hordeum vulgare L.) grown under a triple-line-source sprinkler system in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFOktbY%3D&md5=4fd0abad66b4415bb9ae37fe7b73d570CAS |

Benzarti M, Ben Rejeb K, Debez A, Messedi D, Abdelly C (2012) Photosynthetic activity and leaf antioxidative responses of Atriplex portulacoides subjected to extreme salinity. Acta Physiologiae Plantarum 34, 1679–1688.
Photosynthetic activity and leaf antioxidative responses of Atriplex portulacoides subjected to extreme salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFeqs7s%3D&md5=3a83179bcfb7546f1f914c96956cee90CAS |

Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiology 78, 163–167.
Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktVags74%3D&md5=549b3d5248866d04f04553c6dcd8c0efCAS | 16664191PubMed |

Bonales-Alatorre E, Pottosin I, Shabala L, Chen ZH, Zeng F, Jacobsen SE, Shabala S (2013a) Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa. International Journal of Molecular Sciences 14, 9267–9285.
Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa.Crossref | GoogleScholarGoogle Scholar | 23629664PubMed |

Bonales-Alatorre E, Shabala S, Chen ZH, Pottosin I (2013b) Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, quinoa. Plant Physiology 162, 940–952.
Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, quinoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Oqs7g%3D&md5=0b5144f02b96923d169e3d3c9d1a6647CAS | 23624857PubMed |

Bose J, Pottosin II, Shabala SS, Palmgren MG, Shabala S (2011) Calcium efflux systems in stress signaling and adaptation in plants. Frontiers in Plant Science 2, 1–17.
Calcium efflux systems in stress signaling and adaptation in plants.Crossref | GoogleScholarGoogle Scholar |

Bose J, Rodrigo-Moreno A, Shabala S (2014a) ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany 65, 1241–1257.
ROS homeostasis in halophytes in the context of salinity stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htbY%3D&md5=75f259e49c111146271aa61a36df1a47CAS | 24368505PubMed |

Bose J, Shabala L, Pottosin I, Zeng F, Velarde-Buendia AM, Massart A, Poschenrieder C, Hariadi Y, Shabala S (2014b) Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley. Plant, Cell & Environment 37, 589–600.
Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaksL4%3D&md5=f2dfac704903f1d874dd58e2b44f127fCAS |

Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiologia Plantarum 133, 637–650.
Cellular mechanisms of potassium transport in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit7w%3D&md5=959dddc032af2ef77ed2235bb026266eCAS | 18312500PubMed |

Brugnoli E, Björkman O (1992) Growth of cotton under continuous salinity stress: influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy. Planta 187, 335–347.
Growth of cotton under continuous salinity stress: influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1ygtLo%3D&md5=72d5ec426d1f913b7ad1e1099bcf93c5CAS | 24178074PubMed |

Bulychev AA, Vredenberg WJ (1976) The effect of cations and membrane permeability modifying agents on the dark kinetics of the photoelectric response in isolated chloroplasts. Biochimica et Biophysica Acta – Bioenergetics 423, 548–556.
The effect of cations and membrane permeability modifying agents on the dark kinetics of the photoelectric response in isolated chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XhtFymuro%3D&md5=0795ace304e68ebcc9477e7c1a84d6fbCAS |

Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. Journal of Plant Nutrition and Soil Science 168, 521–530.
The role of potassium in alleviating detrimental effects of abiotic stresses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFCntL8%3D&md5=5c048e996446f5be000680cfb41efc87CAS |

Cakmak I, Hengeler C, Marschner H (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. Journal of Experimental Botany 45, 1251–1257.
Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsl2ktr4%3D&md5=8fab6873c4c6bd8d01f655fdded15fdbCAS |

Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiology 131, 676–683.
Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjs70%3D&md5=0a69784c5b825d8593f0bbc4185a649bCAS | 12586891PubMed |

Carmeli C, Tadmor O, Lifshitz Y, Ophir R, Carmeli S (1992) Inhibition of chloroplast CF1-ATPase by vanadate. FEBS Letters 299, 227–230.
Inhibition of chloroplast CF1-ATPase by vanadate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xkt1agsr0%3D&md5=6fa5af9a43cadaccf19c7ca05fbec782CAS | 1531965PubMed |

Carraretto L, Formentin E, Teardo E, Checchetto V, Tomizioli M, Morosinotto T, Giacometti GM, Finazzi G, Szabo I (2013) A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants. Science 342, 114–118.
A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFelsb7E&md5=0a029cd7cc983df1cdf51c0e795c0b7fCAS | 24009357PubMed |

Checchetto V, Teardo E, Carraretto L, Formentin E, Bergantino E, Giacometti GM, Szabo I (2013) Regulation of photosynthesis by ion channels in cyanobacteria and higher plants. Biophysical Chemistry
Regulation of photosynthesis by ion channels in cyanobacteria and higher plants.Crossref | GoogleScholarGoogle Scholar | 23891570PubMed |

Cheeseman JM (2013) The integration of activity in saline environments: problems and perspectives. Functional Plant Biology 40, 759–774.

Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. Journal of Experimental Botany 54, 657–661.
Potassium activities in cell compartments of salt-grown barley leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1arurw%3D&md5=ae6201f14483561065098148737f8394CAS | 12554708PubMed |

Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant, Cell & Environment 34, 947–961.
Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1Sgtbw%3D&md5=c69c8e11d1e12ebde25d65c05697bef1CAS |

de Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environmental and Experimental Botany 56, 87–94.
Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes.Crossref | GoogleScholarGoogle Scholar |

Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus – the protective role of polyamines. Biochimica et Biophysica Acta – Bioenergetics 1767, 272–280.
Salt stress impact on the molecular structure and function of the photosynthetic apparatus – the protective role of polyamines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1aqurc%3D&md5=807e74244d296537669507b03d6d1bdeCAS |

Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123, 1468–1479.
Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1KmtL0%3D&md5=7b1ad2f920309e6e0948c07f83dc596cCAS | 20375061PubMed |

Demmig B, Gimmler H (1983) Properties of the isolated intact chloroplast at cytoplasmic K+ concentrations: I. Light-induced cation uptake into intact chloroplasts is driven by an electrical potential difference. Plant Physiology 73, 169–174.
Properties of the isolated intact chloroplast at cytoplasmic K+ concentrations: I. Light-induced cation uptake into intact chloroplasts is driven by an electrical potential difference.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvFWqsrk%3D&md5=a46f25d5ffae91c336a1418c21f8cbe6CAS | 16663169PubMed |

Demmig B, Winter K (1986) Sodium, potassium, chloride and proline concentrations of chloroplasts isolated from a halophyte, Mesembryanthemum crystallinum L. Planta 168, 421–426.
Sodium, potassium, chloride and proline concentrations of chloroplasts isolated from a halophyte, Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltFahtLw%3D&md5=28da312165afd90a4fd0655c8d513511CAS | 24232155PubMed |

Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiology 119, 1379–1386.
Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFyls78%3D&md5=9209faf0078e6db61bd2309909543dd2CAS | 10198097PubMed |

Evans AR, Hall D, Pritchard J, Newbury HJ (2012) The roles of the cation transporters CHX21 and CHX23 in the development of Arabidopsis thaliana. Journal of Experimental Botany 63, 59–67.
The roles of the cation transporters CHX21 and CHX23 in the development of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yms7vM&md5=ec1f5878c76cd5bc68be6fe93bf8566fCAS | 21976771PubMed |

Fang Z, Mi F, Berkowitz GA (1995) Molecular and physiological analysis of a thylakoid K+ channel protein. Plant Physiology 108, 1725–1734.

Flowers TJ (1974) Salt tolerance in Suaeda maritima (L) Dum. Journal of Experimental Botany 25, 101–110.
Salt tolerance in Suaeda maritima (L) Dum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXltFKjt7g%3D&md5=6649faf737c3ad15cffdd1d7fc25f6a7CAS |

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=ead9e0f52d5a777986f79fa03e42e1abCAS | 18565144PubMed |

Flowers TJ, Hajibagheri MA (2001) Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant and Soil 231, 1–9.
Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVSjt7c%3D&md5=8fe546ef544788ef21c5535dea6a0735CAS |

Flügge UI (2000) Transport in and out of plastids: does the outer envelope membrane control the flow? Trends in Plant Science 5, 135–137.
Transport in and out of plastids: does the outer envelope membrane control the flow?Crossref | GoogleScholarGoogle Scholar | 10740292PubMed |

Galamba N (2012) Mapping structural perturbations of water in ionic solutions. The Journal of Physical Chemistry B 116, 5242–5250.
Mapping structural perturbations of water in ionic solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVylsb0%3D&md5=5cb8bb101d2c6590cfe6cfc602ddac47CAS | 22480309PubMed |

Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Critical Reviews in Plant Sciences 18, 227–255.
Salt tolerance and crop potential of halophytes.Crossref | GoogleScholarGoogle Scholar |

Greenway H, Osmond C (1972) Salt responses of enzymes from species differing in salt tolerance. Plant Physiology 49, 256–259.
Salt responses of enzymes from species differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xps1amtg%3D%3D&md5=cef8be26b31d81dbfeff75bdc64bed68CAS | 16657936PubMed |

Gupta AS, Alscher RG, McCune D (1991) Response of photosynthesis and cellular antioxidants to ozone in Populus leaves. Plant Physiology 96, 650–655.
Response of photosynthesis and cellular antioxidants to ozone in Populus leaves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnitVertw%3D%3D&md5=da3b905e8e7b97c6d4397c8a8ba1d2dfCAS | 16668235PubMed |

Hall JL, Flowers TJ (1973) The effect of salt on protein synthesis in the halophyte Suaeda maritima. Planta 110, 361–368.
The effect of salt on protein synthesis in the halophyte Suaeda maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXhtlentrw%3D&md5=89d716f2eddcd58fae300e14b738867eCAS | 24474465PubMed |

Hernández J, Olmos E, Corpas F, Sevilla F, del Río LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Science 105, 151–167.
Salt-induced oxidative stress in chloroplasts of pea plants.Crossref | GoogleScholarGoogle Scholar |

Hochman Y, Carmeli S, Carmeli C (1993) Vanadate, a transition state inhibitor of chloroplast CF1-ATPase. Journal of Biological Chemistry 268, 12373–12379.

Holland D, Roberts S, Beardall J (2004) Assessment of the nutrient status of phytoplankton: a comparison between conventional bioassays and nutrient-induced fluorescence transients (NIFTs). Ecological Indicators 4, 149–159.
Assessment of the nutrient status of phytoplankton: a comparison between conventional bioassays and nutrient-induced fluorescence transients (NIFTs).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVeju7w%3D&md5=2558597a7f90c0da9843d0e53d6da783CAS |

Hughes FM, Bortner CD, Purdy GD, Cidlowski JA (1997) Intracellular K+ suppresses the activation of apoptosis in lymphocytes. The Journal of Biological Chemistry 272, 30567–30576.
Intracellular K+ suppresses the activation of apoptosis in lymphocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnslGgsLc%3D&md5=e4a43ec6be0c76997a30cd7fabcc25ccCAS | 9374553PubMed |

Jin SH, Huang JQ, Li XQ, Zheng BS, Wu JS, Wang ZJ, Liu GH, Chen M (2011) Effects of potassium supply on limitations of photosynthesis by mesophyll diffusion conductance in Carya cathayensis. Tree Physiology 31, 1142–1151.
Effects of potassium supply on limitations of photosynthesis by mesophyll diffusion conductance in Carya cathayensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFSqtb3E&md5=63cdc11a1700c160591c9ddf9e7f6c31CAS | 21990026PubMed |

Kleyman TR, Cragoe EJ (1988) Amiloride and its analogs as tools in the study of ion transport. Journal of Membrane Biology 105, 1–21.
Amiloride and its analogs as tools in the study of ion transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjvVKj&md5=76fe183ef44ff8536eb64bcbe901e44cCAS | 2852254PubMed |

Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytologist 189, 54–81.
Sodium transport in plants: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGhug%3D%3D&md5=a025ecb1a12065fcec42b5c5667cfc23CAS | 21118256PubMed |

Kronzucker HJ, Szczerba MW, Moazami-Goudarzi M, Britto DT (2006) The cytosolic Na+ : K+ ratio does not explain salinity-induced growth impairment in barley: a dual-tracer study using 42K+ and 24Na. Plant, Cell & Environment 29, 2228–2237.
The cytosolic Na+ : K+ ratio does not explain salinity-induced growth impairment in barley: a dual-tracer study using 42K+ and 24Na.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVahsg%3D%3D&md5=70b8f5870f979868c8469994fbecdbbdCAS |

Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant and Soil 369, 1–23.
Sodium as nutrient and toxicant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFCiurY%3D&md5=4636892438f752a472e0d4a7d5726bceCAS |

Leigh RA (2001) Potassium homeostasis and membrane transport. Journal of Plant Nutrition and Soil Science 164, 193–198.
Potassium homeostasis and membrane transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlOrtL0%3D&md5=9690bb7eae8a66278a1b530bd8641017CAS |

Mancinelli R, Botti A, Bruni F, Ricci MA, Soper AK (2007) Hydration of sodium, potassium, and chloride ions in solution and the concept of structure maker/breaker. The Journal of Physical Chemistry B 111, 13570–13577.
Hydration of sodium, potassium, and chloride ions in solution and the concept of structure maker/breaker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Ohsb3E&md5=d5c2ec5208ec8f82d2916efd7754c212CAS | 17988114PubMed |

Maury WJ, Huber SC, Moreland DE (1981) Effects of magnesium on intact chloroplasts: ii. cation specificity and involvement of the envelope ATPase in (sodium) potassium/proton exchange across the envelope. Plant Physiology 68, 1257–1263.
Effects of magnesium on intact chloroplasts: ii. cation specificity and involvement of the envelope ATPase in (sodium) potassium/proton exchange across the envelope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XkvFWruw%3D%3D&md5=62796a9c2220b99e498d0a39e2258921CAS | 16662089PubMed |

Meloni DA, Oliva MA, Ruiz HA, Martinez CA (2001) Contribution of proline and inorganic solutes to osmotic adjustment in cotton under salt stress. Journal of Plant Nutrition 24, 599–612.
Contribution of proline and inorganic solutes to osmotic adjustment in cotton under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlOlsb4%3D&md5=d1e95d8e36c67ad81bf9d9e823260ceaCAS |

Mi F, Peters JS, Berkowitz GA (1994) Characterization of a chloroplast inner envelope K+ channel. Plant Physiology 105, 955–964.
Characterization of a chloroplast inner envelope K+ channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFWlsrc%3D&md5=2942970612e8d12aa0ebddf06830fd6eCAS | 8058841PubMed |

Miller C (1993) Potassium selectivity in proteins: oxygen cage or pi in the face? Science 261, 1692–1693.
Potassium selectivity in proteins: oxygen cage or pi in the face?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivVGj&md5=3d5b1d68150b63a736b90daf4679db04CAS | 8397443PubMed |

Morant-Manceau A, Pradier E, Tremblin G (2004) Osmotic adjustment, gas exchanges and chlorophyll fluorescence of a hexaploid triticale and its parental species under salt stress. Journal of Plant Physiology 161, 25–33.
Osmotic adjustment, gas exchanges and chlorophyll fluorescence of a hexaploid triticale and its parental species under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1eiurs%3D&md5=587d87e580118872f0a690654b4488d7CAS | 15002661PubMed |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=ec575b5a94258a1c6a8d564f45b9464eCAS |

Munns R (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
Approaches to increasing the salt tolerance of wheat and other cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1GlsrY%3D&md5=1d6a1d640c63bd0d75ff2231876f67ddCAS | 16510517PubMed |

Munns R, Sharp RE (1993) Involvement of abscisic acid in controlling plant growth in soil of low water potential. Australian Journal of Plant Physiology 20, 425–437.
Involvement of abscisic acid in controlling plant growth in soil of low water potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFyktrg%3D&md5=353b478ee2b24ae08d40af1ce44deee5CAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=dd68a82a6d2c6414e1266213f98edac3CAS | 18444910PubMed |

Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annual Review of Plant Biology 57, 521–565.
Structure and function of photosystems I and II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKht7w%3D&md5=32749f59e0f1ecdb40e230f66004bb5bCAS | 16669773PubMed |

Nitsos RE, Evans HJ (1969) Effects of univalent cations on the activity of particulate starch synthetase. Plant Physiology 44, 1260–1266.
Effects of univalent cations on the activity of particulate starch synthetase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhvVOhtg%3D%3D&md5=fe027310c7724f22f848767c17833968CAS | 16657200PubMed |

Osmond CB, Greenway H (1972) Salt responses of carboxylation enzymes from species differing in salt tolerance. Plant Physiology 49, 260–263.
Salt responses of carboxylation enzymes from species differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xot1OntA%3D%3D&md5=6a8b625419b989aa4460c7841c257e1fCAS | 16657937PubMed |

Pang CH, Zhang SJ, Gong ZZ, Wang BS (2005) NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa. Physiologia Plantarum 125, 490–499.
NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWms7fM&md5=5d10d3ba5270166b87988fde0632715eCAS |

Pardo JM, Cubero B, Leidi EO (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. Journal of Experimental Botany 57, 1181–1199.
Alkali cation exchangers: roles in cellular homeostasis and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls78%3D&md5=f71d97ca61821db96ba58d433c185ec5CAS | 16513813PubMed |

Parida AK, Das AB, Mittra B (2003) Effects of NaCl stress on the structure, pigment complex composition, and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts. Photosynthetica 41, 191–200.
Effects of NaCl stress on the structure, pigment complex composition, and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSqtrbM&md5=54a9ad525e7b2973f99458e176397d1fCAS |

Percey WJ, Shabala L, Breadmore MC, Guijt RM, Bose J, Shabala S (2014) Ion transport in broad bean leaf mesophyll under saline conditions. Planta 240, 729–743.
Ion transport in broad bean leaf mesophyll under saline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtF2qu7fF&md5=51730826bdd2252496af285c11698f25CAS | 25048444PubMed |

Pérez-Alfocea F, Estan MT, Caro M, Guerrier G (1993) Osmotic adjustment in Lycopersicon esculentum and L. Pennellii under NaCl and polyethylene glycol 6000 iso-osmotic stresses. Physiologia Plantarum 87, 493–498.
Osmotic adjustment in Lycopersicon esculentum and L. Pennellii under NaCl and polyethylene glycol 6000 iso-osmotic stresses.Crossref | GoogleScholarGoogle Scholar |

Petrou K, Doblin MA, Smith RA, Ralph PJ, Shelly K, Beardall J (2008) State transitions and nonphotochemical quenching during a nutrient-induced fluorescence transient in phosphorus-starved Dunaliella tertiolicta. Journal of Phycology 44, 1204–1211.
State transitions and nonphotochemical quenching during a nutrient-induced fluorescence transient in phosphorus-starved Dunaliella tertiolicta.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC28fms1Ggsg%3D%3D&md5=222436c632d4192967f686eaf974d98cCAS | 27041717PubMed |

Pfeil BE, Schoefs B, Spetea C (2014) Function and evolution of channels and transporters in photosynthetic membranes. Cellular and Molecular Life Sciences 71, 979–998.
Function and evolution of channels and transporters in photosynthetic membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVOjtb%2FM&md5=e23086c40d9fd6660b4b9e78fe3648d1CAS | 23835835PubMed |

Pflüger R, Mengel K (1972) Die photochemische aktivität von chloroplasten aus unterschiedlich mit kalium ernährten pflanzen. Plant and Soil 36, 417–425.
Die photochemische aktivität von chloroplasten aus unterschiedlich mit kalium ernährten pflanzen.Crossref | GoogleScholarGoogle Scholar |

Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochimica et Biophysica Acta – Bioenergetics 1807, 989–998.
The biogenesis and physiological function of chloroplast superoxide dismutases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntVyltrY%3D&md5=c0dc8a97c2b7d7eae92bf9bc707024b3CAS |

Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta – Bioenergetics 1787, 1151–1160.
Production of reactive oxygen species by photosystem II.Crossref | GoogleScholarGoogle Scholar |

Pottosin II, Schönknecht G (1996) Ion channel permeable for divalent and monovalent cations in native spinach thylakoid membranes. Journal of Membrane Biology 152, 223–233.
Ion channel permeable for divalent and monovalent cations in native spinach thylakoid membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltVaktrc%3D&md5=d68486a71279f85516ca41634dad9fb4CAS | 8672080PubMed |

Pottosin II, Muñiz J, Shabala S (2005) Fast-activating channel controls cation fluxes across the native chloroplast envelope. Journal of Membrane Biology 204, 145–156.
Fast-activating channel controls cation fluxes across the native chloroplast envelope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFemurzJ&md5=bd8c52be176655555fe245080ae4f8d9CAS | 16245037PubMed |

Pottosin I, Shabala S (2016) Transport across chloroplast membranes: optimizing photosynthesis for adverse environmental conditions. Molecular Plant 9, 356–370.
Transport across chloroplast membranes: optimizing photosynthesis for adverse environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XjvVGqsrg%3D&md5=73cda242d5db854e8f9cb334750c9f1fCAS | 26597501PubMed |

Qiu-Fang Z, Yuan-Yuan L, Cai-Hong P, Cong-Ming L, Wang B-S (2005) NaCl enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L. Plant Science 168, 423–430.
NaCl enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L.Crossref | GoogleScholarGoogle Scholar |

Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant, Cell & Environment 32, 237–249.
Quantifying the three main components of salinity tolerance in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVKlsL4%3D&md5=bf1f1a37c3894cfc3b461d309c4b40d4CAS |

Rexroth S, Meyer ZU, Tittingdorf JMW, Schwaßmann HJ, Krause F, Seelert H, Dencher NA (2004) Dimeric H+-ATP synthase in the chloroplast of Chlamydomonas reinhardtii. Biochimica et Biophysica Acta – Bioenergetics 1658, 202–211.
Dimeric H+-ATP synthase in the chloroplast of Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvV2lurs%3D&md5=003a9b30b3bc29d26d41aea236381f78CAS |

Robinson SP, Downton W (1985) Potassium, sodium and chloride ion concentrations in leaves and isolated chloroplasts of the halophyte Suaeda australis R.Br. Australian Journal of Plant Physiology 12, 471–479.
Potassium, sodium and chloride ion concentrations in leaves and isolated chloroplasts of the halophyte Suaeda australis R.Br.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltVemsg%3D%3D&md5=28ada96cf244051fcf422d15b3af6ae3CAS |

Rott M, Martins NF, Thiele W, Lein W, Bock R, Kramer DM, Schottler MA (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. The Plant Cell 23, 304–321.
ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFCksbk%3D&md5=d64c633c06b79f941d7472dac0ad9adcCAS | 21278125PubMed |

Ryan KG, Ralph P, McMinn A (2004) Acclimation of Antarctic bottom-ice algal communities to lowered salinities during melting. Polar Biology 27, 679–686.
Acclimation of Antarctic bottom-ice algal communities to lowered salinities during melting.Crossref | GoogleScholarGoogle Scholar |

Schubert S, Lauchli A (1990) Sodium exclusion mechanisms at the root surface of two maize cultivars. Plant and Soil 123, 205–209.
Sodium exclusion mechanisms at the root surface of two maize cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXltFamurk%3D&md5=2a0bd786fd0b813447233b5f7c788426CAS |

Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164, 151–162.
Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktlGjs7o%3D&md5=4c98fcd9b6f7873e75fcde5629cb6da9CAS | 24249556PubMed |

Shabala S (2000) Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant, Cell & Environment 23, 825–837.
Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmt1CitLo%3D&md5=c168d7d90873dde668175e281145771eCAS |

Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiologia Plantarum 151, 257–279.
Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXps1OjtL0%3D&md5=a0acade96ec4a194c130a751673c8ed0CAS | 24506225PubMed |

Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhoud D, Shabala S (2012) Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiologia Plantarum 146, 26–38.
Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWltb3E&md5=2dd705a8942a4ce03628de4ad0f166c2CAS | 22324972PubMed |

Shabala S, Mackay A (2011) Ion transport in halophytes. Advances in Botanical Research 57, 151–199.
Ion transport in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1Sit74%3D&md5=0be98b691971716a3ef0e5235d525e71CAS |

Shabala S, Bose J, Hedrich R (2014) Salt bladders: do they matter? Trends in Plant Science 19, 687–691.
Salt bladders: do they matter?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVart73M&md5=d9ff5e40cfcebf189aa8e9abb0f282c1CAS | 25361704PubMed |

Shabala S, Bose J, Fuglsang AT, Pottosin I (2016) On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils. Journal of Experimental Botany 67, 1015–1031.
On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils.Crossref | GoogleScholarGoogle Scholar | 26507891PubMed |

Sirault XRR, James RA, Furbank RT (2009) A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Functional Plant Biology 36, 970–977.
A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOgs7rI&md5=e1ddc0bd079fca8d9a056b6b41c68b74CAS |

Song C-P, Guo Y, Qiu Q, Lambert G, Galbraith DW, Jagendorf A, Zhu JK (2004) A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 101, 10211–10216.
A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFOhsb0%3D&md5=d80b6167acfba95cab90042c57db6cc7CAS | 15220473PubMed |

Speer M, Kaiser WM (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiology 97, 990–997.
Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhvVGqtA%3D%3D&md5=a3aa5073ce9d96c0f59cb8ce435b538cCAS | 16668541PubMed |

Szczerba MW, Britto DT, Kronzucker HJ (2006) Rapid, futile K+ cycling and pool-size dynamics define low-affinity potassium transport in barley. Plant Physiology 141, 1494–1507.
Rapid, futile K+ cycling and pool-size dynamics define low-affinity potassium transport in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKitL8%3D&md5=2566acb073f86af564067397b262c38dCAS | 16815955PubMed |

Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9̊A. Nature 473, 55–60.
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9̊A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkslCmtLg%3D&md5=7fd25326e97d46737100f5c2019714a7CAS | 21499260PubMed |

Vander Meulen KA, Hobson A, Yocum CF (2002) Calcium depletion modifies the structure of the photosystem II O2-evolving complex. Biochemistry 41, 958–966.
Calcium depletion modifies the structure of the photosystem II O2-evolving complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptFyjsbw%3D&md5=4aaa5d0b801e443f0192beda8cd3622eCAS | 11790119PubMed |

Wakeel A, Farooq M, Qadir M, Schubert S (2011) Potassium substitution by sodium in plants. Critical Reviews in Plant Sciences 30, 401–413.
Potassium substitution by sodium in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFOrt7g%3D&md5=945b2e1f288dc3bb2be3b23a71c52a19CAS |

Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proceedings of the National Academy of Sciences of the United States of America 93, 10510–10514.
Potassium homeostasis in vacuolate plant cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrmtFKhug%3D%3D&md5=7949f94fdf534adeeb145709127a4e82CAS | 11607707PubMed |

Wang R, Chen S, Deng L, Fritz E, Hüttermann A, Polle A (2007) Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees 21, 581–591.
Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptVGks7w%3D&md5=c01576c10be14df32556b0395486cf08CAS |

Wignarajah K, Baker NR (1981) Salt induced responses of chloroplast activities in species of differing salt tolerance – photosynthetic electron-transport in Aster Tripolium and Pisum Sativum. Physiologia Plantarum 51, 387–393.
Salt induced responses of chloroplast activities in species of differing salt tolerance – photosynthetic electron-transport in Aster Tripolium and Pisum Sativum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXitVGlsbg%3D&md5=b9d4a6de9fb7e53640f2d7909533fc38CAS |

Wu H, Shabala L, Barry K, Zhou M, Shabala S (2013) Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley. Physiologia Plantarum 149, 515–527.
Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslyhtLnL&md5=1665f79029b20a93683151c26f65a4c2CAS |

Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology 19, 765–768.
Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslektLw%3D&md5=bc6a34679e89391b15b24f16c3e30e3aCAS | 11479571PubMed |