Altered Root Growth, Auxin Metabolism and Distribution in Arabidopsis thaliana Exposed to Salt and Osmotic Stress

. 2021 Jul 27 ; 22 (15) : . [epub] 20210727

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34360759

Salt and osmotic stress are the main abiotic stress factors affecting plant root growth and architecture. We investigated the effect of salt (100 mM NaCl) and osmotic (200 mM mannitol) stress on the auxin metabolome by UHPLC-MS/MS, auxin distribution by confocal microscopy, and transcript levels of selected genes by qRT-PCR in Arabidopsis thaliana ecotype Columbia-0 (Col-0) and DR5rev::GFP (DR5) line. During long-term stress (13 days), a stability of the auxin metabolome and a tendency to increase indole-3-acetic acid (IAA) were observed, especially during salt stress. Short-term stress (3 h) caused significant changes in the auxin metabolome, especially NaCl treatment resulted in a significant reduction of IAA. The data derived from auxin profiling were consistent with gene expressions showing the most striking changes in the transcripts of YUC, GH3, and UGT transcripts, suggesting disruption of auxin biosynthesis, but especially in the processes of amide and ester conjugation. These data were consistent with the auxin distribution observed in the DR5 line. Moreover, NaCl treatment caused a redistribution of auxin signals from the quiescent center and the inner layers of the root cap to the epidermal and cortical cells of the root elongation zone. The distribution of PIN proteins was also disrupted by salt stress; in particular, PIN2 was suppressed, even after 5 min of treatment. Based on our results, the DR5 line was more sensitive to the applied stresses than Col-0, although both lines showed similar trends in root morphology, as well as transcriptome and metabolome parameters under stress conditions.

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Daliakopoulos I.N., Panagea I.S., Tsanis I.K., Grillakis M.G., Koutroulis A.G., Hessel R., Mayor A.G., Ritsema C.J. Yield response of Mediterranean rangelands under a changing climate. Land Degrad. Dev. 2017;28:1962–1972. doi: 10.1002/ldr.2717. DOI

Petersson S.V., Johansson A.I., Kowalczyk M., Makoveychuk A., Wang J.Y., Moritz T., Grebe M., Benfey P.N., Sandberg G., Ljung K. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell. 2009;21:1659–1668. doi: 10.1105/tpc.109.066480. PubMed DOI PMC

Clark N.M., de Luis Balaguer M.A., Sozzani R. Experimental data and computational modeling link auxin gradient and development in the Arabidopsis root. Front. Plant Sci. 2014;5:328. doi: 10.3389/fpls.2014.00328. PubMed DOI PMC

Korver R.A., Koevoets I.T., Testerink C. Out of shape during stress: A key role for auxin. Trends Plant Sci. 2018;23:783–793. doi: 10.1016/j.tplants.2018.05.011. PubMed DOI PMC

Ljung K., Hull A.K., Celenza J., Yamada M., Estelle M., Normanly J., Sandberg G. Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell. 2005;17:1090–1104. doi: 10.1105/tpc.104.029272. PubMed DOI PMC

Du Y., Scheres B. Lateral root formation and the multiple roles of auxin. J. Exp. Bot. 2018;69:155–167. doi: 10.1093/jxb/erx223. PubMed DOI

Tivendale N.D., Ross J.J., Cohen J.D. The shifting paradigms of auxin biosynthesis. Trends Plant Sci. 2014;19:44–51. doi: 10.1016/j.tplants.2013.09.012. PubMed DOI

Di D.-W., Zhang C., Luo P., An C.-W., Guo G.-Q. The biosynthesis of auxin: How many paths truly lead to IAA? Plant Growth Regul. 2016;78:275–285. doi: 10.1007/s10725-015-0103-5. DOI

Olatunji D., Geelen D., Verstraeten I. Control of endogenous auxin levels in plant root development. Int. J. Mol. Sci. 2017;18:2587. doi: 10.3390/ijms18122587. PubMed DOI PMC

Zhang J., Peer W.A. Auxin homeostasis: The DAO of catabolism. J. Exp. Bot. 2017;68:3145–3154. doi: 10.1093/jxb/erx221. PubMed DOI

Smolko A., Ludwig-Müller J., Salopek-Sondi B. Auxin Amidohydrolases—From Structure to Function: Revisited. Croat. Chem. Acta. 2018;91:233–239. doi: 10.5562/cca3356. DOI

Casanova-Sáez R., Mateo-Bonmatí E., Ljung K. Auxin metabolism in plants. Cold Spring Harb. Perspect. Biol. 2021;13:a039867. doi: 10.1101/cshperspect.a039867. PubMed DOI PMC

Kanehisa M. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000;28:27–30. doi: 10.1093/nar/28.1.27. PubMed DOI PMC

Normanly J., Slovin J.P., Cohen J.D. Auxin biosynthesis and metabolism. In: Davies P.J., editor. Plant Hormones. Springer; Dordrecht, The Netherlands: 2010. pp. 36–62.

Ludwig-Müller J. Auxin conjugates: Their role for plant development and in the evolution of land plants. J. Exp. Bot. 2011;62:1757–1773. doi: 10.1093/jxb/erq412. PubMed DOI

Bartel B., LeClere S., Magidin M., Zolman B.K. Inputs to the active indole-3-acetic acid pool: De novo synthesis, conjugate hydrolysis, and indole-3-butyric acid β-oxidation. J. Plant Growth Regul. 2001;20:198–216. doi: 10.1007/s003440010025. DOI

Sánchez-García A.B., Ibáñez S., Cano A., Acosta M., Pérez-Pérez J.M. A comprehensive phylogeny of auxin homeostasis genes involved in adventitious root formation in carnation stem cuttings. PLoS ONE. 2018;13:e0196663. doi: 10.1371/journal.pone.0196663. PubMed DOI PMC

Korasick D.A., Enders T.A., Strader L.C. Auxin biosynthesis and storage forms. J. Exp. Bot. 2013;64:2541–2555. doi: 10.1093/jxb/ert080. PubMed DOI PMC

Tanaka K., Hayashi K., Natsume M., Kamiya Y., Sakakibara H., Kawaide H., Kasahara H. UGT74D1 Catalyzes the Glucosylation of 2-Oxindole-3-Acetic Acid in the Auxin Metabolic Pathway in Arabidopsis. Plant Cell Physiol. 2014;55:218–228. doi: 10.1093/pcp/pct173. PubMed DOI PMC

Sugawara S., Hishiyama S., Jikumaru Y., Hanada A., Nishimura T., Koshiba T., Zhao Y., Kamiya Y., Kasahara H. Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2009;106:5430–5435. doi: 10.1073/pnas.0811226106. PubMed DOI PMC

Tzin V., Galili G. The Biosynthetic Pathways for Shikimate and Aromatic Amino Acids in Arabidopsis thaliana. Arabidopsis Book. 2010;8:e0132. doi: 10.1199/tab.0132. PubMed DOI PMC

Abualia R., Benkova E., Lacombe B. Transporters and Mechanisms of Hormone Transport in Arabidopsis. In: Maurel C.B., editor. Membrane Transport in Plants. Volume 87. Academic Press; Cambridge, MA, USA: 2018. pp. 115–138. DOI

Mohanta T.K., Bashir T., Hashem A., Abd_Allah E.F., Khan A.L., Al-Harrasi A.S. Molecular players of auxin transport systems: Advances in genomic and molecular events. J. Plant Interact. 2018;13:483–495. doi: 10.1080/17429145.2018.1523476. DOI

Koevoets I.T., Venema J.H., Elzenga J.T.M., Testerink C. Roots Withstanding their Environment: Exploiting Root System Architecture Responses to Abiotic Stress to Improve Crop Tolerance. Front. Plant Sci. 2016;7:1335. doi: 10.3389/fpls.2016.01335. PubMed DOI PMC

Mroue S., Simeunovic A., Robert H.S. Auxin production as an integrator of environmental cues for developmental growth regulation. J. Exp. Bot. 2018;69:201–212. doi: 10.1093/jxb/erx259. PubMed DOI

Liang W., Ma X., Wan P., Liu L. Plant salt-tolerance mechanism: A review. Biochem. Biophys. Res. Commun. 2018;495:286–291. doi: 10.1016/j.bbrc.2017.11.043. PubMed DOI

Salopek-Sondi B., Pavlović I., Smolko A., Šamec D. Auxin as a Mediator of Abiotic Stress Responses. In: Pandey G., editor. Mechanism of Plant Hormone Signaling under Stress. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2017. pp. 1–36.

Wang Y., Li K., Li X. Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J. Plant Physiol. 2009;166:1637–1645. doi: 10.1016/j.jplph.2009.04.009. PubMed DOI

Julkowska M.M., Hoefsloot H.C.J., Mol S., Feron R., de Boer G.-J., Haring M.A., Testerink C. Capturing Arabidopsis Root Architecture Dynamics with ROOT-FIT Reveals Diversity in Responses to Salinity. Plant Physiol. 2014;166:1387–1402. doi: 10.1104/pp.114.248963. PubMed DOI PMC

Ryu H., Cho Y.-G. Plant hormones in salt stress tolerance. J. Plant Biol. 2015;58:147–155. doi: 10.1007/s12374-015-0103-z. DOI

Pavlović I., Pěnčík A., Novák O., Vujčić V., Radić Brkanac S., Lepeduš H., Strnad M., Salopek-Sondi B. Short-term salt stress in Brassica rapa seedlings causes alterations in auxin metabolism. Plant Physiol. Biochem. 2018;125:74–84. doi: 10.1016/j.plaphy.2018.01.026. PubMed DOI

Julkowska M.M., Koevoets I.T., Mol S., Hoefsloot H., Feron R., Tester M.A., Keurentjes J.J.B., Korte A., Haring M.A., de Boer G.-J., et al. Genetic Components of Root Architecture Remodeling in Response to Salt Stress. Plant Cell. 2017;29:3198–3213. doi: 10.1105/tpc.16.00680. PubMed DOI PMC

Galvan-Ampudia C.S., Testerink C. Salt stress signals shape the plant root. Curr. Opin. Plant Biol. 2011;14:296–302. doi: 10.1016/j.pbi.2011.03.019. PubMed DOI

Liu W., Li R.-J., Han T.-T., Cai W., Fu Z.-W., Lu Y.-T. Salt Stress Reduces Root Meristem Size by Nitric Oxide-Mediated Modulation of Auxin Accumulation and Signaling in Arabidopsis. Plant Physiol. 2015;168:343–356. doi: 10.1104/pp.15.00030. PubMed DOI PMC

Zhang J., Lin J.E., Harris C., Campos Mastrotti Pereira F., Wu F., Blakeslee J.J., Peer W.A. DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2016;113:11010–11015. doi: 10.1073/pnas.1604769113. PubMed DOI PMC

Liu L., Guo G., Wang Z., Ji H., Mu F., Li X. Auxin in Plant Growth and Stress Responses. In: Phan Tran L.-S., Pal S., editors. Phytohormones: A Window to Metabolism, Signaling and Biotechnological Applications. Springer; New York, NY, USA: 2014. pp. 1–35.

Šimura J., Antoniadi I., Široká J., Tarkowská D., Strnad M., Ljung K., Novák O. Plant hormonomics: Multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 2018;177:476–489. doi: 10.1104/pp.18.00293. PubMed DOI PMC

Křeček P., Skůpa P., Libus J., Naramoto S., Tejos R., Friml J., Zažímalová E. The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 2009;10:249. doi: 10.1186/gb-2009-10-12-249. PubMed DOI PMC

Jiang K., Moe-Lange J., Hennet L., Feldman L.J. Salt Stress Affects the Redox Status of Arabidopsis Root Meristems. Front. Plant Sci. 2016;7:81. doi: 10.3389/fpls.2016.00081. PubMed DOI PMC

Feraru E., Friml J. PIN Polar Targeting. Plant Physiol. 2008;147:1553–1559. doi: 10.1104/pp.108.121756. PubMed DOI PMC

Fu Y., Yang Y., Chen S., Ning N., Hu H. Arabidopsis IAR4 Modulates Primary Root Growth Under Salt Stress Through ROS-Mediated Modulation of Auxin Distribution. Front. Plant Sci. 2019;10:522. doi: 10.3389/fpls.2019.00522. PubMed DOI PMC

Kilian J., Whitehead D., Horak J., Wanke D., Weinl S., Batistic O., D’Angelo C., Bornberg-Bauer E., Kudla J., Harter K. The AtGenExpress global stress expression data set: Protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 2007;50:347–363. doi: 10.1111/j.1365-313X.2007.03052.x. PubMed DOI

Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V., Provart N.J. An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets. PLoS ONE. 2007;2:e718. doi: 10.1371/journal.pone.0000718. PubMed DOI PMC

Boyes D.C., Zayed A.M., Ascenzi R., McCaskill A.J., Hoffman N.E., Davis K.R., Görlach J. Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell. 2001;13:1499–1510. doi: 10.1105/TPC.010011. PubMed DOI PMC

Livak K.J., Schmittgen T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Yan S., Che G., Ding L., Chen Z., Liu X., Wang H., Zhao W., Ning K., Zhao J., Tesfamichael K., et al. Different cucumber CsYUC genes regulate response to abiotic stresses and flower development. Sci. Rep. 2016;6:20760. doi: 10.1038/srep20760. PubMed DOI PMC

Shi H., Chen L., Ye T., Liu X., Ding K., Chan Z. Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol. Biochem. 2014;82:209–217. doi: 10.1016/j.plaphy.2014.06.008. PubMed DOI

Kim J.I., Baek D., Park H.C., Chun H.J., Oh D.-H., Lee M.K., Cha J.-Y., Kim W.-Y., Kim M.C., Chung W.S., et al. Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol. Plant. 2013;6:337–349. doi: 10.1093/mp/sss100. PubMed DOI

Ke Q., Wang Z., Ji C.Y., Jeong J.C., Lee H.-S., Li H., Xu B., Deng X., Kwak S.-S. Transgenic poplar expressing Arabidopsis YUCCA6 exhibits auxin-overproduction phenotypes and increased tolerance to abiotic stress. Plant Physiol. Biochem. 2015;94:19–27. doi: 10.1016/j.plaphy.2015.05.003. PubMed DOI

Park J.-E., Park J.-Y., Kim Y.-S., Staswick P.E., Jeon J., Yun J., Kim S.-Y., Kim J., Lee Y.-H., Park C.-M. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 2007;282:10036–10046. doi: 10.1074/jbc.M610524200. PubMed DOI

Kirungu J.N., Magwanga R.O., Lu P., Cai X., Zhou Z., Wang X., Peng R., Wang K., Liu F. Functional characterization of Gh_A08G1120 (GH3.5) gene reveal their significant role in enhancing drought and salt stress tolerance in cotton. BMC Genet. 2019;20:62. doi: 10.1186/s12863-019-0756-6. PubMed DOI PMC

Kong W., Zhong H., Deng X., Gautam M., Gong Z., Zhang Y., Zhao G., Liu C., Li Y. Evolutionary analysis of GH3 genes in six Oryza species/subspecies and their expression under salinity stress in Oryza sativa ssp. japonica. Plants. 2019;8:30. doi: 10.3390/plants8020030. PubMed DOI PMC

Kong W., Zhang Y., Deng X., Li S., Zhang C., Li Y. Comparative genomic and transcriptomic analysis suggests the evolutionary dynamic of GH3 genes in Gramineae crops. Front. Plant Sci. 2019;10:1297. doi: 10.3389/fpls.2019.01297. PubMed DOI PMC

Kinoshita N., Wang H., Kasahara H., Liu J., MacPherson C., Machida Y., Kamiya Y., Hannah M.A., Chua N.-H. IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell. 2012;24:3590–3602. doi: 10.1105/tpc.112.097006. PubMed DOI PMC

Rehman H.M., Nawaz M.A., Shah Z.H., Ludwig-Müller J., Chung G., Ahmad M.Q., Yang S.H., Lee S.I. Comparative genomic and transcriptomic analyses of Family-1 UDP glycosyltransferase in three Brassica species and Arabidopsis indicates stress-responsive regulation. Sci. Rep. 2018;8:1875. doi: 10.1038/s41598-018-19535-3. PubMed DOI PMC

Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602. doi: 10.1016/S0092-8674(03)00924-3. PubMed DOI

Friml J., Vieten A., Sauer M., Weijers D., Schwarz H., Hamann T., Offringa R., Jürgens G. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature. 2003;426:147–153. doi: 10.1038/nature02085. PubMed DOI

Scholl R.L., May S.T., Ware D.H. Seed and Molecular Resources for Arabidopsis. Plant Physiol. 2000;124:1477–1480. doi: 10.1104/pp.124.4.1477. PubMed DOI PMC

Abas L., Benjamins R., Malenica N., Paciorek T., Wišniewska J., Moulinier–Anzola J.C., Sieberer T., Friml J., Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 2006;8:249–256. doi: 10.1038/ncb1369. PubMed DOI

Vieten A., Vanneste S., Wisniewska J., Benkova E., Benjamins R., Beeckman T., Luschnig C., Friml J. Functional redundancy of PIN proteins is accompanied by auxin-dependentcross-regulation of PIN expression. Development. 2005;132:4521–4531. doi: 10.1242/dev.02027. PubMed DOI

Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., Scheres B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005;433:39–44. doi: 10.1038/nature03184. PubMed DOI

Shahzad Z., Kellermeier F., Armstrong E.M., Rogers S., Lobet G., Amtmann A., Hills A. EZ-Root-VIS: A software pipeline for the rapid analysis and visual reconstruction of root system architecture. Plant Physiol. 2018;177:1368–1381. doi: 10.1104/pp.18.00217. PubMed DOI PMC

Gu X., Xu T., He Y. A Histone H3 Lysine-27 Methyltransferase complex represses lateral root formation in Arabidopsis thaliana. Mol. Plant. 2014;7:977–988. doi: 10.1093/mp/ssu035. PubMed DOI

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC

Pěnčík A., Casanova-Sáez R., Pilařová V., Žukauskaitė A., Pinto R., Micol J.L., Ljung K., Novák O. Ultra-rapid auxin metabolite profiling for high-throughput mutant screening in Arabidopsis. J. Exp. Bot. 2018;69:2569–2579. doi: 10.1093/jxb/ery084. PubMed DOI PMC

Arvidsson S., Kwasniewski M., Riano-Pachon D.M., Mueller-Roeber B. QuantPrime—A flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinform. 2008;9:465. doi: 10.1186/1471-2105-9-465. PubMed DOI PMC

Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T.L. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012;13:134. doi: 10.1186/1471-2105-13-134. PubMed DOI PMC

Czechowski T., Stitt M., Altmann T., Udvardi M.K., Scheible W.-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139:5–17. doi: 10.1104/pp.105.063743. PubMed DOI PMC

Ruijter J.M., Ramakers C., Hoogaars W.M.H., Karlen Y., Bakker O., van den Hoff M.J.B., Moorman A.F.M. Amplification efficiency: Linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 2009;37:e45. doi: 10.1093/nar/gkp045. PubMed DOI PMC

Waese J., Fan J., Pasha A., Yu H., Fucile G., Shi R., Cumming M., Kelley L.A., Sternberg M.J., Krishnakumar V., et al. ePlant: Visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell. 2017;29:1806–1821. doi: 10.1105/tpc.17.00073. PubMed DOI PMC

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