Overexpression of GSK3-like Kinase 5 (OsGSK5) in rice (Oryza sativa) enhances salinity tolerance in part via preferential carbon allocation to root starch
Maysaya Thitisaksakul A C , Maria C. Arias B , Shaoyun Dong A and Diane M. Beckles A DA Department of Plant Sciences, University of California, One Shields Avenue, Davis, CA 95616, USA.
B Unité de Glycobiologie Structurale et Fonctionnelle, Université des Sciences et Technologies de Lille, Unité Mixte de Recherche du Centre National de la Recherche Scientifique no. 8576, 59655 Villeneuve D’Ascq cedex, France.
C Present address: Department of Biochemistry, Faculty of Science, Khon Kaen University, Khon Kaen 40002, Thailand.
D Corresponding author. Email: dmbeckles@ucdavis.edu
Functional Plant Biology 44(7) 705-719 https://doi.org/10.1071/FP16424
Submitted: 4 December 2016 Accepted: 1 April 2017 Published: 8 May 2017
Abstract
Rice (Oryza sativa L.) is very sensitive to soil salinity. To identify endogenous mechanisms that may help rice to better survive salt stress, we studied a rice GSK3-like isoform (OsGSK5), an orthologue of a Medicago GSK3 previously shown to enhance salinity tolerance in Arabidopsis by altering carbohydrate metabolism. We wanted to determine whether OsGSK5 functions similarly in rice. OsGSK5 was cloned and sequence, expression, evolutionary and functional analyses were conducted. OsGSK5 was expressed highest in rice seedling roots and was both salt and sugar starvation inducible in this tissue. A short-term salt-shock (150 mM) activated OsGSK5, whereas moderate (50 mM) salinity over the same period repressed the transcript. OsGSK5 response to salinity was due to an ionic effect since it was unaffected by polyethylene glycol. We engineered a rice line with 3.5-fold higher OsGSK5 transcript, which better tolerated cultivation on saline soils (EC = 8 and 10 dS m–2). This line produced more panicles and leaves, and a higher shoot biomass under high salt stress than the control genotypes. Whole-plant 14C-tracing and correlative analysis of OsGSK5 transcript with eco-physiological assessments pointed to the accelerated allocation of carbon to the root and its deposition as starch, as part of the tolerance mechanism.
Additional keywords: carbohydrate, carbon allocation, carbon partitioning, salinity, salt stress, starch metabolism.
References
Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology 155, 64–69.| Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagsLo%3D&md5=207cd9dd3ec358fe85a2cc1cbf88104aCAS |
Amirjani MR (2011) Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice. International Journal of Botany 7, 73–81.
| Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12jurbJ&md5=f8fd5ecb4f100b4275a36c7354d720beCAS |
Balibrea ME, Santa Cruz AM, Bolarín MC, Pérez-Alfocea F (1996) Sucrolytic activities in relation to sink strength and carbohydrate composition in tomato fruit growing under salinity. Plant Science 118, 47–55.
| Sucrolytic activities in relation to sink strength and carbohydrate composition in tomato fruit growing under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjsFOlsbY%3D&md5=c869d77b2b75af43cf4b0a7ca9ae6410CAS |
Balibrea ME, Dell’Amico J, Bolarin MC, Perez-Alfocea F (2000) Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiologia Plantarum 110, 503–511.
| Carbon partitioning and sucrose metabolism in tomato plants growing under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpsFek&md5=d594744cbe833289b91a7c94c96a404fCAS |
Castillo E, Tuong TP, Ismail A, Inubushi K (2007) Response to salinity in rice: comparative effects of osmotic and ionic stresses. Plant Production Science 10, 159–170.
| Response to salinity in rice: comparative effects of osmotic and ionic stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1GhsLc%3D&md5=9d11e40b5b06cc9aa5a40a67129a0255CAS |
Centeno DC, Osorio S, Nunes-Nesi A, Bertolo ALF, Carneiro RT, Araújo WL, Steinhauser M-C, Michalska J, Rohrmann J, Geigenberger P, Oliver SN, Stitt M, Carrari F, Rose JKC, Fernie AR (2011) Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. The Plant Cell 23, 162–184.
| Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFalsLg%3D&md5=1d37e3944d6f85713ff47b6e1c84cb5eCAS |
Cha-um S, Trakulyingcharoen T, Smitamana P, Kirdmanee C (2009) Salt tolerance in two rice cultivars differing salt tolerant abilities in responses to iso-osmotic stress. Australian Journal of Crop Science 3, 221–230.
Chen HJ, Chen JY, Wang SJ (2008) Molecular regulation of starch accumulation in rice seedling leaves in response to salt stress. Acta Physiologiae Plantarum 30, 135–142.
| Molecular regulation of starch accumulation in rice seedling leaves in response to salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVWms74%3D&md5=f69650267e23835499704208b1ee9424CAS |
Cohen P, Frame S (2001) The renaissance of GSK3. Nature Reviews. Molecular Cell Biology 2, 769–776.
| The renaissance of GSK3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVajsLc%3D&md5=f1f6c33ccc4b49bd9bf3eade72484ee7CAS |
Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective, and adaptive system for expressing rice development. Crop Science 40, 436–443.
| A uniform, objective, and adaptive system for expressing rice development.Crossref | GoogleScholarGoogle Scholar |
Dal Santo S, Stampfl H, Krasensky J, Kempa S, Gibon Y, Petutschnig E, Rozhon W, Heuck A, Clausen T, Jonak C (2012) Stress-induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis. The Plant Cell 24, 3380–3392.
| Stress-induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFeku7jN&md5=142882c5da88824957d5079165e7d73bCAS |
Danchin EGJ, Rosso M-N, Vieira P, de Almeida-Engler J, Coutinho PM, Henrissat B, Abad P (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proceedings of the National Academy of Sciences of the United States of America 107, 17651–17656.
| Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlamtLbN&md5=58cb64543a519f596d292f5b09a369a2CAS |
Dardick C, Chen J, Richter T, Ouyang S, Ronald P (2007) The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiology 143, 579–586.
| The rice kinase database. A phylogenomic database for the rice kinome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWnsL8%3D&md5=46fc6bddf97a8c0b731edc43bf7b4c0bCAS |
Dubey RS, Singh AK (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biologia Plantarum 42, 233–239.
| Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVCksLc%3D&md5=c4ad7c5b4df2c7960fc94705c3c00192CAS |
Gao Z, Sagi M, Lips SH (1998) Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity. Plant Science 135, 149–159.
| Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFOkur0%3D&md5=25e282ad710815a08da1a11ed2d6f7f0CAS |
Geiger DR, Servaites JC, Fuchs MA (2000) Role of starch in carbon translocation and partitioning at the plant level. Functional Plant Biology 27, 571–582.
| Role of starch in carbon translocation and partitioning at the plant level.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslars74%3D&md5=3cd4c3bd62fc3e991e2d8e344605c453CAS |
He J-X, Gendron JM, Yang Y, Li J, Wang Z-Y (2002) The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 99, 10185–10190.
| The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslKgur4%3D&md5=506ad4574cee037545b432b6775be1cbCAS |
Henry C, Bledsoe SW, Griffiths CA, Kollman A, Paul MJ, Sakr S, Lagrimini LM (2015) Differential role for trehalose metabolism in salt-stressed maize. Plant Physiology 169, 1072–1089.
| Differential role for trehalose metabolism in salt-stressed maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVWjt74%3D&md5=283bba1ef15580caa1b7dad7ac7e8b9aCAS |
Jonak C, Hirt H (2002) Glycogen synthase kinase 3/SHAGGY-like kinases in plants: an emerging family with novel functions. Trends in Plant Science 7, 457–461.
| Glycogen synthase kinase 3/SHAGGY-like kinases in plants: an emerging family with novel functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVWgsLc%3D&md5=064a396cfa0b0fb08209381fe951f2beCAS |
Kempa S, Rozhon W, Samaj J, Erban A, Baluska F, Becker T, Haselmayer J, Schleiff E, Kopka J, Hirt H, Jonak C (2007) A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism. The Plant Journal 49, 1076–1090.
| A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFGitbo%3D&md5=569034024f44c5877709e49089cd7ab2CAS |
Kempa S, Krasensky J, Dal Santo S, Kopka J, Jonak C (2008) A central role of abscisic acid in stress-regulated carbohydrate metabolism. PLoS One 3, e3935
| A central role of abscisic acid in stress-regulated carbohydrate metabolism.Crossref | GoogleScholarGoogle Scholar |
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Science 40, 482–487.
| Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsF2mt7o%3D&md5=9425ca75eedcaa710a5f1c1ddacf3812CAS |
Khelil A, Menu T, Ricard B (2007) Adaptive response to salt involving carbohydrate metabolism in leaves of a salt-sensitive tomato cultivar. Plant Physiology and Biochemistry 45, 551–559.
| Adaptive response to salt involving carbohydrate metabolism in leaves of a salt-sensitive tomato cultivar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot12qs7c%3D&md5=1ba1da33b8d62e8df40f4d8bbde32d39CAS |
Koh S, Lee SC, Kim MK, Koh JH, Lee S, An G, Choe S, Kim SR (2007) T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Molecular Biology 65, 453–466.
| T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2itbfK&md5=29c3e4586fe2bf0a7f9852f144add0a8CAS |
Kölling K, Müller A, Flütsch P, Zeeman SC (2013) A device for single leaf labelling with CO2 isotopes to study carbon allocation and partitioning in Arabidopsis thaliana. Plant Methods 9, 45
| A device for single leaf labelling with CO2 isotopes to study carbon allocation and partitioning in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Lecourieux F, Lecourieux D, Vignault C, Delrot S (2010) A sugar-inducible protein kinase, VvSK1, regulates hexose transport and sugar accumulation in grapevine cells. Plant Physiology 152, 1096–1106.
| A sugar-inducible protein kinase, VvSK1, regulates hexose transport and sugar accumulation in grapevine cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsFegurw%3D&md5=5fead7f432e39caf566990097d84460fCAS |
Lefèvre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Science 161, 943–952.
| Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |
Leitz G, Kang B-H, Schoenwaelder MEA, Staehelin LA (2009) Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. The Plant Cell 21, 843–860.
| Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFylur8%3D&md5=7e26561b0ff57d69bec7ecdd39c5fdacCAS |
Lemoine R, La Camera S, Atanassova R, Deedaldeechamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Theevenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in Plant Science 4, 272
| Source-to-sink transport of sugar and regulation by environmental factors.Crossref | GoogleScholarGoogle Scholar |
Lu C-A, Ho T-hD, Ho S-L, Yu S-M (2002) Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of α-amylase gene expression. The Plant Cell 14, 1963–1980.
| Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of α-amylase gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslCgsrg%3D&md5=51eafb5784b422e9a527e7eec99f1e4cCAS |
Luengwilai K, Beckles MD (2010) Climacteric ethylene is not essential for initiating chilling injury in tomato (Solanum lycopersicum) cv. Ailsa Craig. Journal of Stored Products and Postharvest Research 1, 1–8.
Luengwilai K, Fiehn OE, Beckles DM (2010) Comparison of leaf and fruit metabolism in two tomato (Solanum lycopersicum L.) genotypes varying in total soluble solids. Journal of Agricultural and Food Chemistry 58, 11790–11800.
| Comparison of leaf and fruit metabolism in two tomato (Solanum lycopersicum L.) genotypes varying in total soluble solids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGkt7vN&md5=450919abe4dda1d1a93a49cfb02969e8CAS |
Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annual Review of Plant Biology 61, 443–462.
| Genetic engineering for modern agriculture: challenges and perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslSjsLc%3D&md5=a81cf185aa622ac0bd0cafa5547515dbCAS |
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=2f4c6c7e2f9463e9f6a3ba186035af1dCAS |
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=b30f07d810b3303a6dcacfac2b459d6cCAS |
Nobuta K, Venu RC, Lu C, Belo A, Vemaraju K, Kulkarni K, Wang WZ, Pillay M, Green PJ, Wang GL, Meyers BC (2007) An expression atlas of rice mRNAs and small RNAs. Nature Biotechnology 25, 473–477.
| An expression atlas of rice mRNAs and small RNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVeksLY%3D&md5=7496441103e2b0b67000f4b7da330e05CAS |
Okawa S, Makino A, Mae T (2002) Shift of the major sink from the culm to the panicle at the early stage of grain filling in rice (Oryza sativa L. cv. Sasanishiki). Soil Science and Plant Nutrition 48, 237–242.
| Shift of the major sink from the culm to the panicle at the early stage of grain filling in rice (Oryza sativa L. cv. Sasanishiki).Crossref | GoogleScholarGoogle Scholar |
Osorio S, Ruan YL, Fernie AR (2014) An update on source-to-sink carbon partitioning in tomato. Frontiers in Plant Science 5, 516
| An update on source-to-sink carbon partitioning in tomato.Crossref | GoogleScholarGoogle Scholar |
Papademetriou MK (2000) Rice production in the Asia-Pacific region: issues and perspectives. In ‘Bridging the rice yield gap in the Asia-Pacific region’. (Eds MK Papademetriou, FJ Dent, EM Herath) pp. 4–25. (FAO: Bangkok)
Park C-J, Bart R, Chern M, Canlas PE, Bai W, Ronald PC (2010) Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One 5, e9262
| Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice.Crossref | GoogleScholarGoogle Scholar |
Pattanagul W, Thitisaksakul M (2008) Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian Journal of Experimental Biology 46, 736–742.
Pérez-Alfocea F, Balibrea ME, Cruz AS, Estañ MT (1996) Agronomical and physiological characterization of salinity tolerance in a commercial tomato hybrid. Plant and Soil 180, 251–257.
| Agronomical and physiological characterization of salinity tolerance in a commercial tomato hybrid.Crossref | GoogleScholarGoogle Scholar |
Qi X, Chanderbali AS, Wong GK-S, Soltis DE, Soltis PS (2013) Phylogeny and evolutionary history of glycogen synthase kinase 3/SHAGGY-like kinase genes in land plants. BMC Evolutionary Biology 13, 143
| Phylogeny and evolutionary history of glycogen synthase kinase 3/SHAGGY-like kinase genes in land plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Wmtb3I&md5=5c4aab74540900da61cb42d725b88983CAS |
Rambaldi D, Ciccarelli FD (2009) FancyGene: dynamic visualization of gene structures and protein domain architectures on genomic loci. Bioinformatics 25, 2281–2282.
| FancyGene: dynamic visualization of gene structures and protein domain architectures on genomic loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVelu7bF&md5=84ccc6bbe20f39a2ac597bc849596674CAS |
Rosa M, Hilal M, Gonzalez JA, Prado FE (2009) Low-temperature effect on enzyme activities involved in sucrose-starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings. Plant Physiology and Biochemistry 47, 300–307.
| Low-temperature effect on enzyme activities involved in sucrose-starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVGrtLk%3D&md5=03aa439f9a2e273a74ac473e84a30cd7CAS |
Saidi Y, Hearn TJ, Coates JC (2012) Function and evolution of ‘green’ GSK3/Shaggy-like kinases. Trends in Plant Science 17, 39–46.
| Function and evolution of ‘green’ GSK3/Shaggy-like kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVSnsw%3D%3D&md5=a2d0fd5a8fb7eb995bb9e3407b1ba6a5CAS |
Sato-Nara K, Nagasaka A, Yamashita H, Ishida J, Enju A, Seki M, Shinozaki K, Suzuki H (2004) Identification of genes regulated by dark adaptation and far-red light illumination in roots of Arabidopsis thaliana. Plant, Cell & Environment 27, 1387–1394.
| Identification of genes regulated by dark adaptation and far-red light illumination in roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Oqtw%3D%3D&md5=12f6fc4ba3bdfe756baf7d3931ab72dcCAS |
Scofield GN, Hirose T, Aoki N, Furbank RT (2007) Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. Journal of Experimental Botany 58, 3155–3169.
| Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Kmt7%2FK&md5=d248e39c39d640f4d03e3000c0866b2dCAS |
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498–2504.
| Cytoscape: a software environment for integrated models of biomolecular interaction networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFWrtr4%3D&md5=f1576cd411499a27bf31104615a7331aCAS |
Shavrukov Y (2013) Salt stress or salt shock: which genes are we studying? Journal of Experimental Botany 64, 119–127.
| Salt stress or salt shock: which genes are we studying?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2gsbnN&md5=c2dec0df33385a1697851390c1a8a8feCAS |
Smith AM, Coupland G, Dolan L, Harberd N, Jones J, Martin C, Sablowki RAA (2009) ‘Environmental stress.’ (Garland Press: New York)
Sonnewald U, Willmitzer L (1992) Molecular approaches to sink–source interactions. Plant Physiology 99, 1267–1270.
| Molecular approaches to sink–source interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtVyrt74%3D&md5=c6d70bc334cfc6d3c5c32af64ce74aa8CAS |
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=e98e9bef793e8611cae6caa1ca5b7bf3CAS |
Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15, 282–292.
| Starch turnover: pathways, regulation and role in growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFGgtLs%3D&md5=a3c58ec80e7689dfa4e300fe88588113CAS |
Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake. The Plant Journal 61, 1067–1091.
| Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFKntLw%3D&md5=0e367cdee27333ac99fc58d769e72eefCAS |
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=0304eb60d01d281ee6e41bc3d051047bCAS |
Theerawitaya C, Boriboonkaset T, Cha-um S, Supaibulwatana K, Kirdmanee C (2012) Transcriptional regulations of the genes of starch metabolism and physiological changes in response to salt stress rice (Oryza sativa L.) seedlings. Physiology and Molecular Biology of Plants 18, 197–208.
| Transcriptional regulations of the genes of starch metabolism and physiological changes in response to salt stress rice (Oryza sativa L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFCjt7Y%3D&md5=2e70207d302573a75e48d667f1e004f0CAS |
Thitisaksakul M, Jiménez RC, Arias MC, Beckles DM (2012) Effects of environmental factors on cereal starch biosynthesis and composition. Journal of Cereal Science 56, 67–80.
| Effects of environmental factors on cereal starch biosynthesis and composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVSqu7g%3D&md5=a35aa48533918eaf471c5719aa191d4fCAS |
Thitisaksakul M, Tananuwong K, Shoemaker CF, Chun A, Tanadul OU, Labavitch JM, Beckles DM (2015) Effects of timing and severity of salinity stress on rice (Oryza sativa L.) yield, grain composition, and starch functionality. Journal of Agricultural and Food Chemistry 63, 2296–2304.
| Effects of timing and severity of salinity stress on rice (Oryza sativa L.) yield, grain composition, and starch functionality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtl2js7g%3D&md5=e8263e0ea45f5d2017168df6a5b72ce7CAS |
Verslues PE, Zhu JK (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochemical Society Transactions 33, 375–379.
| Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFWjsbo%3D&md5=1c51d6fcff364305da5f54506fdac9dbCAS |
Wanichthanarak K, Fan S, Grapov D, Barupal DK, Fiehn O (2017) Metabox: A toolbox for metabolomic data analysis, interpretation and integrative exploration. PLoS One 12, e0171046
| Metabox: A toolbox for metabolomic data analysis, interpretation and integrative exploration.Crossref | GoogleScholarGoogle Scholar |
Wong ML, Medrano JF (2005) Real-time PCR for mRNA quantitation. BioTechniques 39, 75–85.
| Real-time PCR for mRNA quantitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlCnur4%3D&md5=19d57ca8350932add975ba2ce1240fdfCAS |
Yaling S, Lizhong X (2012) Systematic analysis of glycogen synthase kinase 3 genes in rice reveals their differential responses to phytohormones and abiotic stresses. Journal of Huazhong Agricultural University 31, 1–9.
Yeo A (1999) Predicting the interaction between the effects of salinity and climate change on crop plants. Scientia Horticulturae 78, 159–174.
| Predicting the interaction between the effects of salinity and climate change on crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFaisb8%3D&md5=7a8cd54cf16690a8bff0287cf56734e2CAS |
Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C (2010) Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. ‘Micro-Tom’) fruits in an ABA- and osmotic stress-independent manner. Journal of Experimental Botany 61, 563–574.
| Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. ‘Micro-Tom’) fruits in an ABA- and osmotic stress-independent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlGrsA%3D%3D&md5=21ece0c66195c6d7072cf324116029f5CAS |
Yoo MJ, Albert VA, Soltis PS, Soltis DE (2006) Phylogenetic diversification of glycogen synthase kinase 3/SHAGGY-like kinase genes in plants. BMC Plant Biology 6, 3
| Phylogenetic diversification of glycogen synthase kinase 3/SHAGGY-like kinase genes in plants.Crossref | GoogleScholarGoogle Scholar |
Youn J-H, Kim T-W (2015) Functional insights of plant GSK3-like kinases: multi-taskers in diverse cellular signal transduction pathways. Molecular Plant 8, 552–565.
| Functional insights of plant GSK3-like kinases: multi-taskers in diverse cellular signal transduction pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpsFeksL0%3D&md5=d7af9e6de7b36c24a459670a83009607CAS |