Soil salinization is increasing globally, driving a reduction in crop yields that threatens food security. Salinity stress reduces plant growth by exerting two stresses on plants: rapid shoot ion-independent effects which are largely osmotic and delayed ionic effects that are specific to salinity stress. In this study we set out to delineate the osmotic from the ionic effects of salinity stress. Arabidopsis thaliana plants were germinated and grown for two weeks in media supplemented with 50, 75, 100, or 125 mM NaCl (that imposes both an ionic and osmotic stress) or iso-osmolar concentrations (100, 150, 200, or 250 mM) of sorbitol, that imposes only an osmotic stress. A subsequent transcriptional analysis was performed to identify sets of genes that are differentially expressed in plants grown in (1) NaCl or (2) sorbitol compared to controls. A comparison of the gene sets identified genes that are differentially expressed under both challenge conditions (osmotic genes) and genes that are only differentially expressed in plants grown on NaCl (ionic genes, hereafter referred to as salt-specific genes). A pathway analysis of the osmotic and salt-specific gene lists revealed that distinct biological processes are modulated during growth under the two conditions. The list of salt-specific genes was enriched in the gene ontology (GO) term "response to auxin." Quantification of the predominant auxin, indole-3-acetic acid (IAA) and IAA biosynthetic intermediates revealed that IAA levels are elevated in a salt-specific manner through increased IAA biosynthesis. Furthermore, the expression of NITRILASE 2 (NIT2), which hydrolyses indole-3-acetonitile (IAN) into IAA, increased in a salt-specific manner. Overexpression of NIT2 resulted in increased IAA levels, improved Na:K ratios and enhanced survival and growth of Arabidopsis under saline conditions. Overall, our data suggest that auxin is involved in maintaining growth during the ionic stress imposed by saline conditions.

Center for Complex Network Intelligence Tsinghua Laboratory of Brain and Intelligence Department of Biomedical Engineering Tsinghua University Beijing China

Center for Complex Network Intelligence Tsinghua Laboratory of Brain and Intelligence Department of Computer Science Tsinghua University Beijing China

Center for Systems Biology Dresden Dresden Germany

Department of Chemistry Biology and Biotechnology University of Perugia Perugia Italy

Department of Molecular and Cell Biology University of Cape Town Rondebosch South Africa

Department of Plant Sciences University of Cambridge Cambridge United Kingdom

International Centre for Genetic Engineering and Biotechnology Cape Town South Africa

Laboratory of Growth Regulators Institute of Experimental Botany of the Czech Academy of Sciences and Faculty of Science of Palacký University Olomouc Czechia

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Abogadallah G. M. (2010). Sensitivity of DOI

Ahmad M. S. A., Javed F., Ashraf M. (2007). Iso-osmotic effect of NaCl and PEG on growth, cations and free proline accumulation in callus tissue of two indica rice ( DOI

Alarcón M. V., Salguero J., Lloret P. G. (2019). Auxin modulated initiation of lateral roots is linked to pericycle cell length in Maize. PubMed DOI PMC

Alexa A., Rahnenführer J., Lengauer T. (2006). Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. PubMed DOI

Arsuffi G., Braybrook S. A. (2018). Acid growth: an ongoing trip. PubMed DOI

Assaha D. V. M., Ueda A., Saneoka H., Al-Yahyai R., Yaish M. W. (2017). The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. PubMed DOI PMC

Bajguz A., Piotrowska A. (2009). Conjugates of auxin and cytokinin. PubMed DOI

Bartel B., Fink G. R. (1995). ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. PubMed DOI

Bartling D., Seedorf M., Mithofer A., Weiler E. W. (1992). Cloning and expression of an PubMed DOI

Bassil E., Zhang S., Gong H., Tajima H., Blumwald E. (2019). Cation specificity of vacuolar NHX-type cation/H + Antiporters 1[OPEN]. PubMed DOI PMC

Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate - A practical and powerful approach to multiple testing. DOI

Berens M. L., Berry H. M., Mine A., Argueso C. T., Tsuda K. (2017). Evolution of hormone signaling networks in plant defense. PubMed DOI

Bhatt D., Nath M., Sharma M., Bhatt M. D., Bisht D. S., Butani N. V. (2020). “Role of growth regulators and phytohormones in overcoming environmental stress,” in DOI

Bose J., Rodrigo-Moreno A., Lai D., Xie Y., Shen W., Shabala S. (2015). Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and PubMed DOI PMC

Calderon-Villalobos L. I., Tan X., Zheng N., Estelle M. (2010). Auxin perception — structural insights. PubMed DOI PMC

Cao X., Yang H., Shang C., Ma S., Liu L., Cheng J. (2019). The roles of auxin biosynthesis YUCCA gene family in plants. PubMed DOI PMC

Carillo P., Annunziata M. G., Pontecorvo G., Fuggi A., Woodrow P. (2011). “Salinity stress and salt tolerance,” in

Choi W. G., Toyota M., Kim S. H., Hilleary R., Gilroy S. (2014). Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. PubMed DOI PMC

Cutler S. R., Somerville C. R. (2005). Imaging plant cell death: GFP-Nit1 aggregation marks an early step of wound and herbicide induced cell death. PubMed DOI PMC

de Souza Miranda R., Mesquita R. O., Costa J. H., Alvarez-Pizarro J. C., Prisco J. T., Gomes-Filho E. (2017). Integrative control between proton pumps and SOS1 antiporters in roots is crucial for maintaining low Na+ accumulation and salt tolerance in ammonium-supplied PubMed DOI

Dixon D. P., Skipsey M., Grundy N. M., Edwards R. (2005). Stress-induced protein S-glutathionylation in arabidopsis. PubMed DOI PMC

Donaldson L., Ludidi N., Knight M. R., Gehring C., Denby K. (2004). Salt and osmotic stress cause rapid increases in PubMed DOI

Duan L., Dietrich D., Ng H., Yeen M., Bhalerao R., Bennett M. J., et al. (2013). Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. PubMed DOI PMC

Falhof J., Pedersen J. T., Fuglsang A. T., Palmgren M. (2016). Plasma Membrane H + -ATPase regulation in the center of plant physiology. PubMed DOI

FAO, IFAD, UNICEF, WFP, and WHO (2018).

Feng W., Lindner H., Robbins N. E., Dinneny J. R. (2016). Growing out of stress: the role of cell- and organ-scale growth control in plant water-stress responses. PubMed DOI PMC

Fu Y., Yang Y., Chen S., Ning N., Hu H. (2019). Arabidopsis IAR4 modulates primary root growth under salt stress through ROS-mediated modulation of auxin distribution. PubMed DOI PMC

Galvan-Ampudia C. S., Julkowska M. M., Darwish E., Gandullo J., Korver R. A., Brunoud G., et al. (2013). Halotropism is a response of plant roots to avoid a saline environment. PubMed DOI

Gévaudant F., Duby G., Von Stedingk E., Zhao R., Morsomme P., Boutry M. (2007). Expression of a constitutively activated plasma membrane H +-ATPase alters plant development and increases salt tolerance. PubMed DOI PMC

Goyal E., Amit S. K., Singh R. S., Mahato A. K., Chand S., Kanika K. (2016). Transcriptome profiling of the salt-stress response in PubMed DOI PMC

Gray W. M. (2004). Hormonal regulation of plant growth and development. PubMed DOI PMC

Grsic S., Sauerteig S., Neuhaus K., Albrecht M., Rossiter J., Ludwig-Muller J. (1998). Physiological analysis of transgenic DOI

Hagen G., Guilfoyle T. (2002). Auxin-responsive gene expression?: genes, promoters and regulatory factors. PubMed

Haugh G. W., Sommerville C. (1986). Sulfonylurea-resistant mutants of

Hong S. M., Bahn S. C., Lyu A., Jung H. S., Ahn J. H. (2010). Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. PubMed DOI

Howe E., Holton K., Nair S., Schlauch D., Sinha R., Quackenbush J. (2010). “MeV: multiexperiment viewer,” in DOI

Iglesias M. J., Terrile M. C., Windels D., Lombardo M. C., Bartoli C. G., Vazquez F., et al. (2014). MiR393 regulation of auxin signaling and redox-related components during acclimation to salinity in Arabidopsis. PubMed DOI PMC

Iqbal M., Ashraf M. (2007). Seed treatment with auxins modulates growth and ion partitioning in salt - stressed wheat plants seed treatment with auxins modulates growth and ion partitioning in salt-stressed wheat plants. DOI

Isayenkov S. V., Maathuis F. J. M. (2019). Plant salinity stress: many unanswered questions remain. PubMed DOI PMC

Ivanchenko M. G., Napsucialy-Mendivil S., Dubrovsky J. G. (2010). Auxin-induced inhibition of lateral root initiation contributes to root system shaping in PubMed DOI

Ivushkin K., Bartholomeus H., Bregt A. K., Pulatov A., Kempen B., de Sousa L. (2019). Global mapping of soil salinity change. DOI

Janicka-Russak M., Kabała K., Wdowikowska A., Kłobus G. (2013). Modification of plasma membrane proton pumps in cucumber roots as an adaptation mechanism to salt stress. PubMed DOI

Jenrich R., Trompetter I., Bak S., Olsen C. E., Moller B. L., Piotrowski M. (2007). Evolution of heteromeric nitrilase complexes in Poaceae with new functions in nitrile metabolism. PubMed DOI PMC

Ji H., Pardo J. M., Batelli G., Van Oosten M. J., Bressan R. A., Li X. (2013). The salt overly sensitive (SOS) pathway: established and emerging roles. PubMed DOI

Jiang Y., Deyholos M. K. (2006). Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. PubMed DOI PMC

Julkowska M. M., Testerink C. (2015). Tuning plant signaling and growth to survive salt. PubMed DOI

Julkowska M. M., Hoefsloot H. C. J., Mol S., Feron R., de Boer G. J., Haring M. A., et al. (2014). Capturing Arabidopsis root architecture dynamics with ROOT - FIT reveals diversity in responses to salinity. PubMed DOI PMC

Jung J.-H., Park C.-M. (2011). Auxin modulation of salt stress signaling in Arabidopsis seed germination. PubMed DOI PMC

Kasahara H. (2016). Current aspects of auxin biosynthesis in plants. PubMed DOI

Klepek Y. S., Volke M., Konrad K. R., Wippel K., Hoth S., Hedrich R., et al. (2010). PubMed DOI PMC

Koevoets I. T., Venema J. H., Elzenga J. T. M., Testerink C. (2016). Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. PubMed DOI PMC

Korver R. A., Koevoets I. T., Testerink C. (2018). Out of Shape during stress: a key role for auxin. PubMed DOI PMC

Ku Y.-S., Sintaha M., Cheung M.-Y., Lam H.-M. (2018). Plant hormone signaling crosstalks between biotic and abiotic stress responses. PubMed DOI PMC

Lehmann T., Janowitz T., Sánchez-Parra B., Alonso M.-M. P., Trompetter I., Piotrowski M., et al. (2017). Arabidopsis NITRILASE 1 Contributes to the regulation of root growth and development through modulation of auxin biosynthesis in seedlings. PubMed DOI PMC

Li X., Li M., Zhou B., Yang Y., Wei Q., Zhang J. (2019). Transcriptome analysis provides insights into the stress response crosstalk in apple ( PubMed DOI PMC

Liu W., Li R.-J., Han T.-T., Cai W., Fu Z.-W., Lu Y.-T. (2015). Salt Stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. PubMed DOI PMC

Liu Y., Ji X., Zheng L., Nie X., Wang Y. (2013). Microarray analysis of transcriptional responses to abscisic acid and salt stress in PubMed DOI PMC

Ljung K. (2013). Auxin metabolism and homeostasis during plant development. PubMed DOI

Mann H. B., Whitney D. R. (1947). On a test of whether one of two random variables is stochastically larger than the other. DOI

Morton M. J. L., Awlia M., Al-Tamimi N., Saade S., Pailles Y., Negrão S., et al. (2019). Salt stress under the scalpel – dissecting the genetics of salt tolerance. PubMed DOI PMC

Munns R. (2002). Comparative physiology of salt and water stress. PubMed DOI

Munns R., Tester M. (2008). Mechanisms of salinity tolerance. PubMed DOI

Munns R., James R. A., Xu B., Athman A., Conn S. J., Jordans C., et al. (2012). Wheat grain yield on saline soils is improved by an ancestral Na PubMed DOI

Naser V., Shani E. (2016). Auxin response under osmotic stress. PubMed DOI

Negrão S., Schmöckel S. M., Tester M. (2017). Evaluating physiological responses of plants to salinity stress. PubMed DOI PMC

Normanly J., Grisafi P., Fink G. R., Barteld B. (1997). Arabidopsis mutants resistant to the auxin effects of indole-3-acetonitrile are defective in the nitrilase encoded by the NITI Gene Col-0. PubMed DOI PMC

Novák O., Hényková E., Sairanen I., Kowalczyk M., Pospíšil T., Ljung K. (2012). Tissue-specific profiling of the PubMed DOI

Novak S. D., Luna L. J., Gamage R. N. (2014). Role of auxin in orchid development. PubMed DOI PMC

Overvoorde P., Fukaki H., Beeckman T. (2010). Auxin control of root development. PubMed DOI PMC

Pavlović I., Pěnčík A., Novák O., Vujčić V., Radić Brkanac S., Lepeduš H., et al. (2018). Short-term salt stress in PubMed DOI

Piotrowski M., Schönfelder S., Weiler E. W. (2001). The PubMed DOI

Prakash L., Prathapasenan G. (1990). NaCl-and gibberellic acid-induced changes in the content of auxin and the activities of cellulase and pectin lyase during leaf growth in rice (

Prerostova S., Dobrev P. I., Gaudinova A., Hosek P., Soudek P., Knirsch V., et al. (2017). Hormonal dynamics during salt stress responses of salt-sensitive PubMed DOI

Ryu H., Cho Y.-G. (2015). Plant hormones in salt stress tolerance. DOI

Schmidt R. C., Müller A., Hain R., Bartling D., Weiler E. W. (1996). Transgenic tobacco plants expressing the PubMed DOI

Shabala S., Cuin T. (2007). Potassium transport and plant salt tolerance. PubMed DOI

Shavrukov Y. (2013). Salt stress or salt shock: which genes are we studying? PubMed DOI

Spartz A. K., Ren H., Park M. Y., Grandt K. N., Lee H., Murphy A. S., et al. (2014). SAUR inhibition of PP2C-D phosphatases activates plasma membrane H + -ATPases to promote cell expansion in Arabidopsis. PubMed DOI PMC

Sun F., Zhang W., Hu H., Li B., Wang Y., Zhao Y., et al. (2008). Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. PubMed DOI PMC

Tang M., Liu X., Deng H., Shen S. (2011). Over-expression of JcDREB, a putative AP2/EREBP domain-containing transcription factor gene in woody biodiesel plant PubMed DOI

Tani E., Sarri E., Goufa M., Asimakopoulou G., Psychogiou M., Bingham E., et al. (2018). Seedling growth and transcriptional responses to salt shock and stress in DOI

Tilbrook J., Roy S. (2014). “Salinity tolerance,” in

van den Berg T., Korver R. A., Testerink C., ten Tusscher K. H. W. J. (2016). Modeling halotropism: a key role for root tip architecture and reflux loop remodeling in redistributing auxin. PubMed DOI PMC

Van Zelm E., Zhang Y., Testerink C. (2020). Salt tolerance mechanisms of plants. PubMed DOI

Verma V., Ravindran P., Kumar P. P. (2016). Plant hormone-mediated regulation of stress responses. PubMed DOI PMC

Vorwerk S., Biernacki S., Hillebrand H., Janzik I., Müller A., Weiler E. W., et al. (2001). Enzymatic characterization of the recombinant PubMed DOI

Wang F., Chen Z.-H., Shabala S. (2017). Hypoxia sensing in plants: on a quest for ion channels as putative oxygen sensors. PubMed DOI

Wang M., Wang Y., Sun J., Ding M., Deng S., Hou P., et al. (2013). Overexpression of PeHA1 enhances hydrogen peroxide signaling in salt-stressed Arabidopsis. PubMed DOI

Wang P., Shen L., Guo J., Jing W., Qu Y., Li W., et al. (2019). Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED 2 auxin efflux transporter in response to salt stress. PubMed DOI PMC

Wang Y., Li K., Li X. (2009). Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. PubMed DOI

Wilson A. K., Pickett F. B., Turner J. C., Estelle M. (1990). A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. PubMed DOI

Woodward J. D., Trompetter I., Sewell B. T., Piotrowski M. (2018). Substrate specificity of plant nitrilase complexes is affected by their helical twist. PubMed DOI PMC

Yang J., Duan G., Li C., Liu L., Han G., Zhang Y., et al. (2019). The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. PubMed DOI PMC

Yang Y., Guo Y. (2018). Elucidating the molecular mechanisms mediating plant salt-stress responses. PubMed DOI

Zhao Y. (2018). Essential roles of local auxin biosynthesis in plant development and in adaptation to environmental changes. PubMed DOI

Zhao Y., Wang T., Zhang W., Li X. (2011). SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. PubMed DOI

Zolla G., Heimer Y. M., Barak S. (2010). Mild salinity stimulates a stress-induced morphogenic response in PubMed DOI PMC

Zörb C., Geilfus C. M., Dietz K. J. (2019). Salinity and crop yield. PubMed DOI