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Analysis of the impact of indole-3-acetic acid (IAA) on gene expression during leaf senescence in Arabidopsis thaliana

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Abstract

Leaf senescence is an important developmental process for the plant life cycle. It is controlled by endogenous and environmental factors and can be positively or negatively affected by plant growth regulators. It is characterised by major and significant changes in the patterns of gene expression. Auxin, especially indole-3-acetic acid (IAA), is a plant growth hormone that affects plant growth and development. The effect of IAA on leaf senescence is still unclear. In this study, we performed microarray analysis to investigate the role of IAA on gene expression during senescence in Arabidopsis thaliana. We sprayed IAA on plants at 3 different time points (27, 31 or 35 days after sowing). Following spraying, PSII activity of the eighth leaf was evaluated daily by measurement of chlorophyll fluorescence parameters. Our results show that PSII activity decreased following IAA application and the IAA treatment triggered different gene expression responses in leaves of different ages.

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References

  • Allemeersch J, Durinck S, Vanderhaeghen R, Alard P, Maes R, Seeuws K et al (2005) Benchmarking the catma microarray: a novel tool for Arabidopsis transcriptome analysis. Plant Physiol 137:588–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  CAS  PubMed  Google Scholar 

  • Balazadeh S (2014) Stay-green not always stays green. Mol Plant 7:1264–1266

    Article  CAS  PubMed  Google Scholar 

  • Barbagallo RP, Oxborough K, Pallett KE, Baker NR (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol 132:485–493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bashri G, Prasad SM (2016) Exogenous IAA differentially affects growth, oxidative stress and antioxidants system in Cd stressed Trigonella foenum-graecum L. seedlings: toxicity alleviation by up-regulation of ascorbate-glutathione cycle. Ecotoxicol Environ Saf 132:329–338

    Article  CAS  PubMed  Google Scholar 

  • Breeze E, Harrison E, Page T, Warner N, Shen C, Zhang C, Buchanan-Wollaston V (2008) Transcriptional regulation of plant senescence: from functional genomics to systems biology. Plant Biol 10:99–109

    Article  CAS  PubMed  Google Scholar 

  • Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C et al (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnol J 1:3–22

    Article  CAS  PubMed  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. The Plant J 42:567–585

    Article  CAS  PubMed  Google Scholar 

  • Casazza AP, Rossini S, Rosso MG, Soave C (2005) Mutational and expression analysis of ELIP1 and ELIP2 in Arabidopsis thaliana. Plant Mol Biol 58:41–51

    Article  CAS  PubMed  Google Scholar 

  • Chamarro J, Östin A, Sandberg G (2001) Metabolism of indole-3-acetic acid by orange (Citrus sinensis) flavedo tissue during fruit development. Phytochemistry 57(179):187

    Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T et al (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative funcions in response to environmental stresses. Plant Cell 14:559–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M et al (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase D alpha retards abscisic acid-and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9:2183–2196

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farage-Barhom S, Burd S, Sonego L, Perl-Treves R, Lers A (2008) Expression analysis of the BFN1 nuclease gene promoter during senescence, abscission, and programmed cell death-related processes. J Exp Bot 59:3247–3258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer AM (2007) Nutrient remobilization during leaf senescence. In: Gan S (ed) Annual plant reviews volume 26: senescence processes in plants. https://doi.org/10.1002/9780470988855.ch5

  • Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC et al (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gören N, Çağ S (2007) The effect of Indole-3-acetic acid and benzyladenine on sequential leaf senescence on Helianthus annuus L. seedlings. Biotechnol Biotechnol Equip 21:322–327

    Article  Google Scholar 

  • Gregersen PL, Culetic A, Boschian L, Krupinska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622

    Article  CAS  PubMed  Google Scholar 

  • Haldimann P, Fracheboud Y, Stamp P (1996) Photosynthetic performance and resistance to photoinhibition of Zea mays L. leaves grown at sub-optimal temperature. Plant Cell Environ 19:85–92

    Article  CAS  Google Scholar 

  • He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hickman R, Hill C, Penfold CA, Breeze E, Bowden L, Moore JD et al (2013) A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves. The Plant J 75:26–39

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68:1361–1369

    Article  CAS  PubMed  Google Scholar 

  • Ji H, Wang S, Cheng C, Li R, Wang Z, Jenkins GI et al (2019) The RCC 1 family protein SAB 1 negatively regulates ABI 5 through multidimensional mechanisms during postgermination in Arabidopsis. New Phytol 222:907–922

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Liang G, Yang S, Yu D (2014) Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid-and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 26:230–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jibran R, Hunter DA, Dijkwel PP (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol 82:547–561

    Article  CAS  PubMed  Google Scholar 

  • Jones DC, Zheng W, Huang S, Du C, Zhao X, Yennamalli RM et al (2016) A clade-specific Arabidopsis gene connects primary metabolism and senescence. Front Plant Sci 7:983–987

    PubMed  PubMed Central  Google Scholar 

  • Ju L, Jing Y, Shi P, Liu J, Chen J, Yan J et al (2019) JAZ proteins modulate seed germination through interaction with ABI 5 in bread wheat and Arabidopsis. New Phytol 223:246–260

    Article  CAS  PubMed  Google Scholar 

  • Jung H, Lee DK, Do Choi Y, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller out growth. Plant Sci 236:304–312

    Article  CAS  PubMed  Google Scholar 

  • Jusoh M, Loh SH, Chuah TS, Aziz A, San Cha T (2015) Indole-3-acetic acid (IAA) induced changes in oil content, fatty acid profiles and expression of four fatty acid biosynthetic genes in Chlorella vulgaris at early stationary growth phase. Phytochemistry 111:65–71

    Article  CAS  PubMed  Google Scholar 

  • Karatas I, Ozturk L, Ersahin Y, Okatan Y (2010) Effects of auxin on photosynthetic pigments and some enzyme activities during dark-induced senescence of Tropaeolum leaves. Pak J Bot 42(3):1881–1888

    CAS  Google Scholar 

  • Katari MS, Nowicki SD, Aceituno FF, Nero D, Kelfer J, Thompson LP et al (2010) VirtualPlant: a software platform to support systems biology research. Plant Physiol 152:500–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Kim JH, Lyu J, Woo HR, Lim PO (2018) New insights into regulation of leaf senescence in Arabidopsis. J Exp Bot 69:787–799

    Article  CAS  PubMed  Google Scholar 

  • Li RH, Guo PG, Michael B, Stefania G, Salvatore C (2006) Evaluation of chlorophyll content and fluorescence parameters as indicators of drought tolerance in barley. Agr Sci China 5:751–757

    Article  CAS  Google Scholar 

  • Li W, Li X, Chao J, Zhang Z, Wang W, Guo Y (2018) NAC family transcription factors in tobacco and their potential role in regulating leaf senescence. Front Plant Sci 9:1900–1915

    Article  PubMed  PubMed Central  Google Scholar 

  • Lim PO, Nam HG (2007) Aging and senescence of the leaf organ. J Plant Biol 50:291–300

    Article  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17:410–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu C, Lu Q, Zhang J, Kuang T (2001) Characterization of photosynthetic pigment composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field. J Exp Bot 52:1805–1810

    Article  CAS  PubMed  Google Scholar 

  • Morris K, Mackerness SAH, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. The Plant J 23:677–685

    Article  CAS  PubMed  Google Scholar 

  • Mueller-Roeber B, Balazadeh S (2014) Auxin and its role in plant senescence. J Plant Growth Regul 33:21–33

    Article  CAS  Google Scholar 

  • Perea-Resa C, Rodríguez-Milla MA, Iniesto E, Rubio V, Salinas J (2017) Prefoldins negatively regulate cold acclimation in Arabidopsis thaliana by promoting nuclear proteasome-mediated HY5 degradation. Mol Plant 10:791–804

    Article  CAS  PubMed  Google Scholar 

  • Petti C, Nair M, DeBolt S (2014) The involvement of J-protein AtDjC17 in root development in Arabidopsis. Front Plant Sci 5:532–541

    Article  PubMed  PubMed Central  Google Scholar 

  • Rai MI, Wang X, Thibault DM, Kim HJ, Bombyk MM et al (2015) The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene. BMC Plant Biol 15:157. https://doi.org/10.1186/s12870-015-0554-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reeves WM, Lynch TJ, Mobin R, Finkelstein RR (2011) Direct targets of the transcription factors ABA-Insensitive (ABI) 4 and ABI5 reveal synergistic action by ABI4 and several bZIP ABA response factors. Plant Mol Biol 75:347–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Milla MA, Salinas J (2009) Prefoldins 3 and 5 play an essential role in Arabidopsis tolerance to salt stress. Mol Plant 2:526–534

    Article  CAS  PubMed  Google Scholar 

  • Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279:1371–1373

    Article  CAS  PubMed  Google Scholar 

  • Sağlam-Çağ S, Okatan Y (2014) The effects of zinc (Zn) and C14-indoleacetic acid (IAA) on leaf senescence ın Helianthus annuus L. Int J Plant Physiol Biochem 6:28–33

    Article  CAS  Google Scholar 

  • Sanjari S, Shirzadian-Khorramabad R, Shobbar Z-S, Shahbazi M (2019) Systematic analysis of NAC transcription factors’ gene family and identification of post-flowering drought stress responsive members in sorghum. Plant Cell Rep 38:361–376

    Article  CAS  PubMed  Google Scholar 

  • Sarwat M, Naqvi AR, Ahmad P, Ashraf M, Akram NA (2013) Phytohormones and microRNAs as sensors and regulators of leaf senescence: assigning macro roles to small molecules. Biotechnol Adv 31:1153–1171

    Article  CAS  PubMed  Google Scholar 

  • Sghaier N, Ayed RB, Gorai M, Rebai A (2018) Prediction of auxin response elements based on data fusion in Arabidopsis thaliana. Mol Biol Rep 45:763–772

    Article  CAS  PubMed  Google Scholar 

  • Sharabi-Schwager M, Samach A, Porat R (2010) Overexpression of the CBF2 transcriptional activator in Arabidopsis suppresses the responsiveness of leaf tissue to the stress hormone ethylene. Plant Biol 12:630–638

    CAS  PubMed  Google Scholar 

  • Shi H, Reiter RJ, Tan DX, Chan Z (2015) INDOLE- 3- ACETIC ACID INDUCIBLE 17 positively modulates natural leaf senescence through melatonin- mediated pathway in Arabidopsis. J Pineal Res 58:26–33

    Article  CAS  PubMed  Google Scholar 

  • Song C, Chung WS, Lim CO (2016) Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol Cells 39:477–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava LM (2002) Plant growth and development Hormones and Environment. Academic Press, California. ISBN 0-12-660570-X

    Google Scholar 

  • Thakur JK, Jain M, Tyagi AK, Khurana JP (2005) Exogenous auxin enhances the degradation of a light down-regulated and nuclear-localized OsiIAA1, an Aux/IAA protein from rice, via proteasome. Biochim Biophys Acta Gene Struct Expr 1730:196–205

    Article  CAS  Google Scholar 

  • Ueda H, Kusaba M (2015) Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 169:138–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Graaff E, Schwacke R, Schneider A, Desimone M, Flügge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson R, Kim H, Bakshi A, Binder B (2014) The ethylene receptors, ETHYLENE RESPSONE 1 and 2, have contrasting roles in seed germination of Arabidopsis thaliana during salt stress. Plant Physiol 165:1353–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu A, Allu AD, Garapati P, Siddiqui H et al (2012) JUGBURUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24:482–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • www.arabidopsis.org. Accessed 10 April 2019

  • Wyatt RE, Ainley WM, Nagao RT, Conner TW, Key JL (1993) Expression of the Arabidopsis AtAux2-11 auxin-responsive gene in transgenic plants. Plant Mol Biol 22:731–749

    Article  CAS  PubMed  Google Scholar 

  • Yamada Y, Umehara M (2015) Possible roles of strigolactones during leaf senescence. Plants 4:664–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:399–408

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, You J, Ou Y, Ma J, Wu X, Xu G (2015) Ultraviolet-B protection of ascorbate and tocopherol in plants related with their function on the stability on carotenoid and phenylpropanoid compounds. Plant Physiol Biochem 90:23–31

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Tian X, Li Y, Zhang L, Guan P, Kou X et al (2017) Molecular and functional characterization of wheat ARGOS genes influencing plant growth and stress tolerance. Front Plant Sci 8:170–177

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work is part of N.G-S’ PhD. thesis.

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Authors and Affiliations

  1. Division of Botany, Biology Department, Faculty of Science, Istanbul University, Istanbul, Turkey

    Nihal Gören-Sağlam & Gül Öz

  2. School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK

    Elizabeth Harrison, Emily Breeze & Vicky Buchanan-Wollaston

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  1. Nihal Gören-Sağlam
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  2. Elizabeth Harrison
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  4. Gül Öz
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N.G.-S., V.B.-W., E.H., E.B. and G.Ö designed the research; N.G.-S. did the experimental work, performed data analysis, wrote the paper, revised manuscript discussed with V.B.-W.

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Correspondence to Nihal Gören-Sağlam.

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Supplementary material 1 (XLS 1127 kb)

12298_2019_752_MOESM2_ESM.xlsx

Supplementary Table: Gene Ontology analysis of genes differentially expressed following IAA treatment. The previously reported relationship between the genes and senescence related expression was investigated using Mueller-Roeber and Balazadeh (2014) and column D and E indicate whether each gene was identified in this paper as being a senescence-associated gene (SAGs) or senescence downregulated gene (SDG), marked as (+) and (-), respectively. A: Genes within Ontology groups that were identified as being overrepresented amongst genes showing increased expression at following IAA treatment at 27, 31 and 35 DAS. B: Genes within Ontology groups that were identified as being overrepresented amongst genes showing decreased expression at following IAA treatment at 27, 31 and 35 DAS (XLSX 22 kb)

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Gören-Sağlam, N., Harrison, E., Breeze, E. et al. Analysis of the impact of indole-3-acetic acid (IAA) on gene expression during leaf senescence in Arabidopsis thaliana. Physiol Mol Biol Plants 26, 733–745 (2020). https://doi.org/10.1007/s12298-019-00752-7

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