Salt-Specific Gene Expression Reveals Elevated Auxin Levels in Arabidopsis thaliana Plants Grown Under Saline Conditions
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
35222469
PubMed Central
PMC8866861
DOI
10.3389/fpls.2022.804716
Knihovny.cz E-zdroje
- Klíčová slova
- IAA, auxin, growth, ionic, osmotic, plant, salinity, salt stress,
- Publikační typ
- časopisecké články MeSH
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 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
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Abogadallah G. M. (2010). Sensitivity of Trifolium alexandrinum L. to salt stress is related to the lack of long-term stress-induced gene expression. Plant Sci. 178 491–500. 10.1016/j.plantsci.2010.03.008 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 (Oryza sativa L.) genotypes. Plant Growth Regul. 53 53–63. 10.1007/s10725-007-9204-0 DOI
Alarcón M. V., Salguero J., Lloret P. G. (2019). Auxin modulated initiation of lateral roots is linked to pericycle cell length in Maize. Front. Plant Sci. 10:11. 10.3389/fpls.2019.00011 PubMed DOI PMC
Alexa A., Rahnenführer J., Lengauer T. (2006). Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22 1600–1607. 10.1093/bioinformatics/btl140 PubMed DOI
Arsuffi G., Braybrook S. A. (2018). Acid growth: an ongoing trip. J. Exp. Bot. 69 137–146. 10.1093/jxb/erx390 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. Front. Physiol. 8:509. 10.3389/fphys.2017.00509 PubMed DOI PMC
Bajguz A., Piotrowska A. (2009). Conjugates of auxin and cytokinin. Phytochemistry 70 957–969. 10.1016/j.phytochem.2009.05.006 PubMed DOI
Bartel B., Fink G. R. (1995). ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268 1745–1748. 10.1126/science.7792599 PubMed DOI
Bartling D., Seedorf M., Mithofer A., Weiler E. W. (1992). Cloning and expression of an Arabidopsis nitrilase which can convert indole-3-acetonitrile to the plant hormone, indole-3acetic acid. Eur. J. Biochem. 205 417–424. 10.1152/ajplung.1992.263.1.1-a PubMed DOI
Bassil E., Zhang S., Gong H., Tajima H., Blumwald E. (2019). Cation specificity of vacuolar NHX-type cation/H + Antiporters 1[OPEN]. Plant Physiol. 179 616–629. 10.1104/pp.18.01103 PubMed DOI PMC
Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate - A practical and powerful approach to multiple testing. J. R. Stat. Soc. 1 289–300. 10.2307/2346101 DOI
Berens M. L., Berry H. M., Mine A., Argueso C. T., Tsuda K. (2017). Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 55 401–425. 10.1146/annurev-phyto-080516-035544 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 Protective Chemical Agents in the Amelioration of Plant Abiotic Stress, eds Roychoudhury A., Tripathi D. K. (Hoboken, NJ: John Wiley & Sons Ltd; ). 10.1002/9781119552154.ch11 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 Chenopodium quinoa. Ann. Bot. 115 481–494. 10.1093/aob/mcu219 PubMed DOI PMC
Calderon-Villalobos L. I., Tan X., Zheng N., Estelle M. (2010). Auxin perception — structural insights. Cold Spring Harb. Perspect. Biol. 2:a005546. 10.1101/cshperspect.a005546 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. Int. J. Mol. Sci. 20:6343. 10.3390/ijms20246343 PubMed DOI PMC
Carillo P., Annunziata M. G., Pontecorvo G., Fuggi A., Woodrow P. (2011). “Salinity stress and salt tolerance,” in Abiotic Stress in Plants- Mechanisms and Adaptations, eds Shanker A., Venkateswaralu B. (Rijeka: In Tech; ).
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. Proc. Natl. Acad. Sci. U.S.A. 111 6497–6502. 10.1073/pnas.1319955111 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. BMC Plant Biol. 5:4. 10.1186/1471-2229-5-4 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 Sorghum bicolor. Plant Cell Physiol. 58 522–536. 10.1093/pcp/pcw231 PubMed DOI
Dixon D. P., Skipsey M., Grundy N. M., Edwards R. (2005). Stress-induced protein S-glutathionylation in arabidopsis. Plant Physiol. 138 2233–2244. 10.1104/pp.104.058917 PubMed DOI PMC
Donaldson L., Ludidi N., Knight M. R., Gehring C., Denby K. (2004). Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels. FEBS Lett. 569 317–320. 10.1016/j.febslet.2004.06.016 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. Plant Cell 25 324–341. 10.1105/tpc.112.107227 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. Mol. Plant 9 323–337. 10.1016/j.molp.2015.11.002 PubMed DOI
FAO, IFAD, UNICEF, WFP, and WHO (2018). The State of Food Security and Nutrition in the World 2018. Building Climate Resilience for Food Security and Nutrition. Rome: FAO.
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. Plant Cell 28 1769–1782. 10.1105/tpc.16.00182 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. Front. Plant Sci. 10:522. 10.3389/fpls.2019.00522 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. Curr. Biol. 23 2044–2050. 10.1016/j.cub.2013.08.042 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. Plant Physiol. 144 1763–1776. 10.1104/pp.107.103762 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 Triticum aestivum cv. Kharchia Local. Sci. Rep. 6:27752. 10.1038/srep27752 PubMed DOI PMC
Gray W. M. (2004). Hormonal regulation of plant growth and development. PLoS Biol. 2:e311. 10.1371/journal.pbio.0020311 PubMed DOI PMC
Grsic S., Sauerteig S., Neuhaus K., Albrecht M., Rossiter J., Ludwig-Muller J. (1998). Physiological analysis of transgenic Arabidopsis thaliana plants expressing one nitrilase isoform in sense or antisense direction. J. Plant Physiol. 153 446–456. 10.1016/S0176-1617(98)80173-9 DOI
Hagen G., Guilfoyle T. (2002). Auxin-responsive gene expression?: genes, promoters and regulatory factors. Plant Mol. Biol. 49 373–385. PubMed
Haugh G. W., Sommerville C. (1986). Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204 430–434.
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. Plant Cell Physiol. 51 1694–1706. 10.1093/pcp/pcq128 PubMed DOI
Howe E., Holton K., Nair S., Schlauch D., Sinha R., Quackenbush J. (2010). “MeV: multiexperiment viewer,” in Biomedical Informatics for Cancer Research, Vol. 15 eds Ochs M., Casagrande J., Davuluri R. (Boston, MA: Springer; ), 267–277. 10.1007/978-1-4419-5714-6 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. PLoS One 9:e107678. 10.1371/journal.pone.0107678 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. J. Integr. Plant Biol. 49 1003–1015. 10.1111/j.1672-9072.2007.00488.x DOI
Isayenkov S. V., Maathuis F. J. M. (2019). Plant salinity stress: many unanswered questions remain. Front. Plant Sci. 10:80. 10.3389/fpls.2019.00080 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 Arabidopsis thaliana. Plant J. 64 740–752. 10.1111/j.1365-313X.2010.04365.x PubMed DOI
Ivushkin K., Bartholomeus H., Bregt A. K., Pulatov A., Kempen B., de Sousa L. (2019). Global mapping of soil salinity change. Remote Sens. Environ. 231:111260. 10.1016/j.rse.2019.111260 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. J. Plant Physiol. 170 915–922. 10.1016/j.jplph.2013.02.002 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. Proc. Natl. Acad. Sci. U.S.A. 104 18848–18853. 10.1073/pnas.0709315104 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. Mol. Plant 6 275–286. 10.1093/mp/sst017 PubMed DOI
Jiang Y., Deyholos M. K. (2006). Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol. 6:25. 10.1186/1471-2229-6-25 PubMed DOI PMC
Julkowska M. M., Testerink C. (2015). Tuning plant signaling and growth to survive salt. Trends Plant Sci. 20 586–594. 10.1016/j.tplants.2015.06.008 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. Plant Physiol. 166 1387–1402. 10.1104/pp.114.248963 PubMed DOI PMC
Jung J.-H., Park C.-M. (2011). Auxin modulation of salt stress signaling in Arabidopsis seed germination. Plant Signal. Behav. 6 1198–1200. 10.4161/psb.6.8.15792 PubMed DOI PMC
Kasahara H. (2016). Current aspects of auxin biosynthesis in plants. Biosci. Biotechnol. Biochem. 80 34–42. 10.1080/09168451.2015.1086259 PubMed DOI
Klepek Y. S., Volke M., Konrad K. R., Wippel K., Hoth S., Hedrich R., et al. (2010). Arabidopsis thaliana POLYOL/MONOSACCHARIDE TRANSPORTERS 1 and 2: fructose and xylitol/H+ symporters in pollen and young xylem cells. J. Exp. Bot. 61 537–550. 10.1093/jxb/erp322 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. Front. Plant Sci. 7:1335. 10.3389/fpls.2016.01335 PubMed DOI PMC
Korver R. A., Koevoets I. T., Testerink C. (2018). Out of Shape during stress: a key role for auxin. Trends Plant Sci. 23 783–793. 10.1016/j.tplants.2018.05.011 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. Int. J. Mol. Sci. 19:3206. 10.3390/ijms19103206 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. Front. Plant Sci. 8:36. 10.3389/fpls.2017.00036 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 (Malus × domestica) subjected to drought, cold and high salinity. Sci. Rep. 9:9071. 10.1038/s41598-019-45266-0 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. Plant Physiol. 168 343–356. 10.1104/pp.15.00030 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 Arabidopsis thaliana. Int. J. Mol. Sci. 14 9979–9998. 10.3390/ijms14059979 PubMed DOI PMC
Ljung K. (2013). Auxin metabolism and homeostasis during plant development. Development 140 943–950. 10.1242/dev.086363 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. Ann. Math. Stat. 18 50–60. 10.1214/aoms/1177730491 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. Plant J. 97 148–163. 10.1111/tpj.14189 PubMed DOI PMC
Munns R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25 239–250. 10.1046/j.0016-8025.2001.00808.x PubMed DOI
Munns R., Tester M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59 651–681. 10.1146/annurev.arplant.59.032607.092911 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+ transporter gene. Nat. Biotechnol. 30 360–364. 10.1038/nbt.2120 PubMed DOI
Naser V., Shani E. (2016). Auxin response under osmotic stress. Plant Mol. Biol. 91 661–672. 10.1007/s11103-016-0476-5 PubMed DOI
Negrão S., Schmöckel S. M., Tester M. (2017). Evaluating physiological responses of plants to salinity stress. Ann. Bot. 119 1–11. 10.1093/aob/mcw191 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. Plant Cell 9 1781–1790. 10.1105/tpc.9.10.1781 PubMed DOI PMC
Novák O., Hényková E., Sairanen I., Kowalczyk M., Pospíšil T., Ljung K. (2012). Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 72 523–536. 10.1111/j.1365-313X.2012.05085.x PubMed DOI
Novak S. D., Luna L. J., Gamage R. N. (2014). Role of auxin in orchid development. Plant Signal. Behav. 9:e972277. 10.4161/psb.32169 PubMed DOI PMC
Overvoorde P., Fukaki H., Beeckman T. (2010). Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2:a001537. 10.1101/cshperspect.a001537 PubMed DOI PMC
Pavlović I., Pěnčík A., Novák O., Vujčić V., Radić Brkanac S., Lepeduš H., et al. (2018). Short-term salt stress in Brassica rapa seedlings causes alterations in auxin metabolism. Plant Physiol. Biochem. 125 74–84. 10.1016/j.plaphy.2018.01.026 PubMed DOI
Piotrowski M., Schönfelder S., Weiler E. W. (2001). The Arabidopsis thaliana Isogene NIT4 and Its orthologs in tobacco encode ??-Cyano-L-alanine Hydratase/Nitrilase. J. Biol. Chem. 276 2616–2621. 10.1074/jbc.M007890200 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 (Oryza sativa). Ann. Bot. 65 251–257.
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 Arabidopsis thaliana and salt-tolerant Thellungiella salsuginea. Plant Sci. 264 188–198. 10.1016/j.plantsci.2017.07.020 PubMed DOI
Ryu H., Cho Y.-G. (2015). Plant hormones in salt stress tolerance. J. Plant Biol. 58 147–155. 10.1007/s12374-015-0103-z DOI
Schmidt R. C., Müller A., Hain R., Bartling D., Weiler E. W. (1996). Transgenic tobacco plants expressing the Arabidopsis thaliana nitrilase II enzyme. Plant J. 9 683–691. 10.1046/j.1365-313X.1996.9050683.x PubMed DOI
Shabala S., Cuin T. (2007). Potassium transport and plant salt tolerance. Physiol. Plant. 133 651–669. 10.1111/j.1399-3054.2007.01008.x PubMed DOI
Shavrukov Y. (2013). Salt stress or salt shock: which genes are we studying? J. Exp. Bot. 64 119–127. 10.1093/jxb/ers316 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. Plant Cell 26 2129–2142. 10.1105/tpc.114.126037 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. Plant Physiol. 146 178–188. 10.1104/pp.107.109413 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 Jatropha curcas, enhances salt and freezing tolerance in transgenic Arabidopsis thaliana. Plant Sci. 181 623–631. 10.1016/j.plantsci.2011.06.014 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 Medicago sativa L., Medicago arborea L., and Their Hybrid (Alborea). Agronomy 8:231. 10.3390/agronomy8100231 DOI
Tilbrook J., Roy S. (2014). “Salinity tolerance,” in Plant Abiotic Stress, 2nd Edn, eds Jenks M. A., Hasegawa P. M. (New York, NY: Wiley-Blackwell; ), 134–178.
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. Development 143 3350–3362. 10.1242/dev.135111 PubMed DOI PMC
Van Zelm E., Zhang Y., Testerink C. (2020). Salt tolerance mechanisms of plants. Annu. Rev. Plant Biol. 71 403–433. 10.1146/annurev-arplant-050718-100005 PubMed DOI
Verma V., Ravindran P., Kumar P. P. (2016). Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 16:86. 10.1186/s12870-016-0771-y PubMed DOI PMC
Vorwerk S., Biernacki S., Hillebrand H., Janzik I., Müller A., Weiler E. W., et al. (2001). Enzymatic characterization of the recombinant Arabidopsis thaliana nitrilase subfamily encoded by the NIT2/NIT1/NIT3-gene cluster. Planta 212 508–516. 10.1007/s004250000420 PubMed DOI
Wang F., Chen Z.-H., Shabala S. (2017). Hypoxia sensing in plants: on a quest for ion channels as putative oxygen sensors. Plant Cell Physiol. 58 1126–1142. 10.1093/pcp/pcx079 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. Plant Physiol. Biochem. 71 37–48. 10.1016/j.plaphy.2013.06.020 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. Plant Cell 31 250–271. 10.1105/tpc.18.00528 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. J. Plant Physiol. 166 1637–1645. 10.1016/j.jplph.2009.04.009 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. Mol. Gen. Genet. 222 377–383. 10.1007/BF00633843 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. Commun. Biol. 1:186. 10.1038/s42003-018-0186-4 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. Front. Plant Sci. 10:1349. 10.3389/fpls.2019.01349 PubMed DOI PMC
Yang Y., Guo Y. (2018). Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol. 217 523–539. 10.1111/nph.14920 PubMed DOI
Zhao Y. (2018). Essential roles of local auxin biosynthesis in plant development and in adaptation to environmental changes. Annu. Rev. Plant Biol. 69 417–435. 10.1146/annurev-arplant-042817-040226 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. New Phytol. 189 1122–1134. 10.1111/j.1469-8137.2010.03545.x PubMed DOI
Zolla G., Heimer Y. M., Barak S. (2010). Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J. Exp. Bot. 61 211–224. 10.1093/jxb/erp290 PubMed DOI PMC
Zörb C., Geilfus C. M., Dietz K. J. (2019). Salinity and crop yield. Plant Biol. 21 31–38. 10.1111/plb.12884 PubMed DOI