Abstract

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.

Highlights

  • More than one billion hectares of land worldwide are considered saline, and this number is growing annually due to an increased occurrence of drought, the use of brackish water for irrigation and poor farming practices (FAO, IFAD, UNICEF, WFP, and WHO, 20181; Ivushkin et al, 2019)

  • To investigate how plants cope with the delayed ionic effects of salinity stress, Arabidopsis Col-0 was germinated and grown for two weeks in Arabidopsis thaliana salt (ATS) media supplemented with varying concentrations of NaCl (50, 75, 100, and 125 mM) or iso-osmolar concentrations of sorbitol (100, 150, 200, and 250 mM) and microarray analysis was used to profile the transcriptome

  • This dose range was chosen based on an initial hydroponic experiment in which it was found that Arabidopsis Col-0 could survive when grown for more than two weeks in the presence of 50-125 mM NaCl and could reach maturity when grown in 50-100 mM NaCl

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Summary

Introduction

More than one billion hectares of land worldwide are considered saline, and this number is growing annually due to an increased occurrence of drought, the use of brackish water for irrigation and poor farming practices (FAO, IFAD, UNICEF, WFP, and WHO, 20181; Ivushkin et al, 2019). Following exposure to salt, the plant experiences rapid ion-independent, osmotic stress that dramatically reduces the shoot growth rate (Munns and Tester, 2008; Carillo et al, 2011) These effects are largely due to loss of turgor that prompts stomatal closure and, inhibits photosynthesis (Shabala and Cuin, 2007; Tilbrook and Roy, 2014; Julkowska and Testerink, 2015; Morton et al, 2019; Van Zelm et al, 2020). The osmotic and ionic stresses imposed by salinity are generally considered to be separated both spatially and temporally, it should be noted that more rapid salt-specific signal transduction and fast Na+-induced growth responses have been demonstrated in roots prior to Na+ having accumulated to toxic levels in the shoot (Choi et al, 2014; Van Zelm et al, 2020)

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