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PLOS Genetics  2016 

Arabidopsis ERF1 Mediates Cross-Talk between Ethylene and Auxin Biosynthesis during Primary Root Elongation by Regulating ASA1 Expression

DOI: 10.1371/journal.pgen.1005760

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Abstract:

The gaseous phytohormone ethylene participates in the regulation of root growth and development in Arabidopsis. It is known that root growth inhibition by ethylene involves auxin, which is partially mediated by the action of the WEAK ETHYLENE INSENSITIVE2/ANTHRANILATE SYNTHASE α1 (WEI2/ASA1), encoding a rate-limiting enzyme in tryptophan (Trp) biosynthesis, from which auxin is derived. However, the molecular mechanism by which ethylene decreases root growth via ASA1 is not understood. Here we report that the ethylene-responsive AP2 transcription factor, ETHYLENE RESPONSE FACTOR1 (ERF1), plays an important role in primary root elongation of Arabidopsis. Using loss- and gain-of-function transgenic lines as well as biochemical analysis, we demonstrate that ERF1 can directly up-regulate ASA1 by binding to its promoter, leading to auxin accumulation and ethylene-induced inhibition of root growth. This discloses one mechanism linking ethylene signaling and auxin biosynthesis in Arabidopsis roots.

References

[1]  Gazzarrini S, McCourt P (2003) Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann Bot 91: 605–612. pmid:12714359 doi: 10.1093/aob/mcg064
[2]  Swarup R, Parry G, Graham N, Allen T, Bennett M (2002) Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol Biol 49: 411–426. pmid:12036264 doi: 10.1007/978-94-010-0377-3_12
[3]  Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, et al. (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19: 2186–2196. pmid:17630275 doi: 10.1105/tpc.107.052100
[4]  Le J, Vandenbussche F, Van Der Straeten D, Verbelen JP (2001) In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. Plant Physiol 125: 519–522. pmid:11161008 doi: 10.1104/pp.125.2.519
[5]  Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17: 181–195. doi: 10.1016/j.tplants.2012.02.001. pmid:22406007
[6]  Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, et al. (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19: 2197–2212. pmid:17630274 doi: 10.1105/tpc.107.052126
[7]  Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19: 2169–2185. pmid:17630276 doi: 10.1105/tpc.107.052068
[8]  Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17: 2230–2242. pmid:15980261 doi: 10.1105/tpc.105.033365
[9]  Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, et al. (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177–191. doi: 10.1016/j.cell.2008.01.047. pmid:18394997
[10]  Lei MG, Zhu CM, Liu YD, Karthikeyan AS, Bressan RA, et al. (2011) Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytologist 189: 1084–1095. doi: 10.1111/j.1469-8137.2010.03555.x. pmid:21118263
[11]  Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16: 1–18. pmid:11031228 doi: 10.1146/annurev.cellbio.16.1.1
[12]  Frankowski K, Kesy J, Kopcewicz J (2007) [Regulation of ethylene biosynthesis in plants]. Postepy Biochem 53: 66–73. pmid:17718390
[13]  Spanu P, Reinhardt D, Boller T (1991) Analysis and cloning of the ethylene-forming enzyme from tomato by functional expression of its mRNA in Xenopus laevis oocytes. EMBO J 10: 2007–2013. pmid:2065651
[14]  Hamilton AJ, Bouzayen M, Grierson D (1991) Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proc Natl Acad Sci U S A 88: 7434–7437. pmid:1714605 doi: 10.1073/pnas.88.16.7434
[15]  Abel S, Nguyen MD, Chow W, Theologis A (1995) ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin [corrected]. J Biol Chem 270: 19093–19099. pmid:7642574 doi: 10.1074/jbc.270.32.19093
[16]  Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136: 2982–3000. pmid:15466221 doi: 10.1104/pp.104.049999
[17]  Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14 Suppl: S131–151. pmid:12045274
[18]  Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95: 901–915. pmid:15753119 doi: 10.1093/aob/mci100
[19]  Benavente LM, Alonso JM (2006) Molecular mechanisms of ethylene signaling in Arabidopsis. Mol Biosyst 2: 165–173. pmid:16880934 doi: 10.1039/b513874d
[20]  Stepanova AN, Alonso JM (2009) Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol 12: 548–555. doi: 10.1016/j.pbi.2009.07.009. pmid:19709924
[21]  Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11: 479–485. doi: 10.1016/j.pbi.2008.06.011. pmid:18692429
[22]  Chang C, Stadler R (2001) Ethylene hormone receptor action in Arabidopsis. Bioessays 23: 619–627. pmid:11462215 doi: 10.1002/bies.1087
[23]  Chang C, Bleecker AB (2004) Ethylene biology. More than a gas. Plant Physiol 136: 2895–2899. pmid:15489282 doi: 10.1104/pp.104.900122
[24]  Bleecker AB (1999) Ethylene perception and signaling: an evolutionary perspective. Trends Plant Sci 4: 269–274. pmid:10407443 doi: 10.1016/s1360-1385(99)01427-2
[25]  Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72: 427–441. pmid:8431946 doi: 10.1016/0092-8674(93)90119-b
[26]  Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148–2152. pmid:10381874 doi: 10.1126/science.284.5423.2148
[27]  Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12: 3703–3714. pmid:9851977 doi: 10.1101/gad.12.23.3703
[28]  Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657. pmid:12893945 doi: 10.1126/science.1086391
[29]  Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140: 411–432. pmid:16407444 doi: 10.1104/pp.105.073783
[30]  Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29: 23–32. pmid:12060224 doi: 10.1046/j.1365-313x.2002.01191.x
[31]  Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, et al. (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42: 689–707. pmid:15918883 doi: 10.1111/j.1365-313x.2005.02405.x
[32]  Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, et al. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391–1406. pmid:9707537 doi: 10.2307/3870648
[33]  Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci U S A 94: 1035–1040. pmid:9023378 doi: 10.1073/pnas.94.3.1035
[34]  Maruyama Y, Yamoto N, Suzuki Y, Chiba Y, Yamazaki K, et al. (2013) The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi. Plant Sci 213: 79–87. doi: 10.1016/j.plantsci.2013.08.008. pmid:24157210
[35]  Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273: 26857–26861. pmid:9756931 doi: 10.1074/jbc.273.41.26857
[36]  Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165–178. pmid:12509529 doi: 10.1105/tpc.007468
[37]  Cao WH, Liu J, He XJ, Mu RL, Zhou HL, et al. (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143: 707–719. pmid:17189334 doi: 10.1104/pp.106.094292
[38]  Cao YR, Chen SY, Zhang JS (2008) Ethylene signaling regulates salt stress response: An overview. Plant Signal Behav 3: 761–763. pmid:19513226 doi: 10.4161/psb.3.10.5934
[39]  Cela J, Chang C, Munne-Bosch S (2011) Accumulation of gamma- rather than alpha-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52: 1389–1400. doi: 10.1093/pcp/pcr085. pmid:21719428
[40]  Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162: 1566–1582. doi: 10.1104/pp.113.221911. pmid:23719892
[41]  Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, et al. (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89: 1133–1144. pmid:9215635 doi: 10.1016/s0092-8674(00)80300-1
[42]  Cai XT, Xu P, Zhao PX, Liu R, Yu LH, et al. (2014) Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun 5: 5833. doi: 10.1038/ncomms6833. pmid:25524530
[43]  Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63: 563–590. doi: 10.1146/annurev-arplant-042811-105501. pmid:22404466
[44]  Fujita H, Syono K (1996) Genetic analysis of the effects of polar auxin transport inhibitors on root growth in Arabidopsis thaliana. Plant Cell Physiol 37: 1094–1101. pmid:9032965 doi: 10.1093/oxfordjournals.pcp.a029059
[45]  Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23: 267–278. pmid:10929120 doi: 10.1046/j.1365-313x.2000.00786.x
[46]  Zheng Z, Guo Y, Novak O, Dai X, Zhao Y, et al. (2013) Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol 9: 244–246. doi: 10.1038/nchembio.1178. pmid:23377040
[47]  Pickett FB, Wilson AK, Estelle M (1990) The aux1 Mutation of Arabidopsis Confers Both Auxin and Ethylene Resistance. Plant Physiol 94: 1462–1466. pmid:16667854 doi: 10.1104/pp.94.3.1462
[48]  Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139: 1393–1409. pmid:7768447
[49]  Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12: 2175–2187. pmid:9679062 doi: 10.1101/gad.12.14.2175
[50]  Rahman A, Amakawa T, Goto N, Tsurumi S (2001) Auxin is a positive regulator for ethylene-mediated response in the growth of Arabidopsis roots. Plant Cell Physiol 42: 301–307. pmid:11266581 doi: 10.1093/pcp/pce035
[51]  Pickett FB, Wilson AK, Estelle M (1990) The Aux1 Mutation Of Arabidopsis Confers Both Auxin And Ethylene Resistance. Plant Physiology 94: 1462–1466. pmid:16667854 doi: 10.1104/pp.94.3.1462
[52]  Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, et al. (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci U S A 100: 2992–2997. pmid:12606727 doi: 10.1073/pnas.0438070100
[53]  Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55: 335–347. doi: 10.1111/j.1365-313X.2008.03528.x. pmid:18435826
[54]  Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, et al. (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A 108: 18518–18523. doi: 10.1073/pnas.1108436108. pmid:22025721
[55]  Wang Y, Liu C, Li K, Sun F, Hu H, et al. (2007) Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. Plant Mol Biol 64: 633–644. pmid:17533512 doi: 10.1007/s11103-007-9182-7
[56]  Zhu Z, An F, Feng Y, Li P, Xue L, et al. (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci U S A 108: 12539–12544. doi: 10.1073/pnas.1103959108. pmid:21737749
[57]  Yu Y, Wang J, Zhang Z, Quan R, Zhang H, et al. (2013) Ethylene promotes hypocotyl growth and HY5 degradation by enhancing the movement of COP1 to the nucleus in the light. PLoS Genet 9: e1004025. doi: 10.1371/journal.pgen.1004025. pmid:24348273
[58]  An FY, Zhao QO, Ji YS, Li WY, Jiang ZQ, et al. (2010) Ethylene-Induced Stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 Is Mediated by Proteasomal Degradation of EIN3 Binding F-Box 1 and 2 That Requires EIN2 in Arabidopsis. Plant Cell 22: 2384–2401. doi: 10.1105/tpc.110.076588. pmid:20647342
[59]  Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, et al. (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17: 678–682. pmid:17363254 doi: 10.1016/j.cub.2007.02.047
[60]  Wang Z, Mao JL, Zhao YJ, Li CY, Xiang CB (2014) L-Cysteine inhibits root elongation through auxin/PLETHORA and SCR/SHR pathway in Arabidopsis thaliana. J Integr Plant Biol. doi: 10.1111/jipb.12213
[61]  De Cnodder T, Vissenberg K, Van Der Straeten D, Verbelen JP (2005) Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane- 1-carboxylic acid: a matter of apoplastic reactions. New Phytol 168: 541–550. pmid:16313637 doi: 10.1111/j.1469-8137.2005.01540.x
[62]  Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463–472. pmid:10589675 doi: 10.1016/s0092-8674(00)81535-4
[63]  Chang KN, Zhong S, Weirauch MT, Hon G, Pelizzola M, et al. (2013) Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. Elife 2: e00675. doi: 10.7554/eLife.00675. pmid:23795294
[64]  An F, Zhao Q, Ji Y, Li W, Jiang Z, et al. (2010) Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 22: 2384–2401. doi: 10.1105/tpc.110.076588. pmid:20647342
[65]  Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963–1971. pmid:9401121 doi: 10.2307/3870557
[66]  Lei ZY, Zhao P, Cao MJ, Cui R, Chen X, et al. (2007) High-throughput binary vectors for plant gene function analysis. Journal Of Integrative Plant Biology 49: 556–567. doi: 10.1111/j.1744-7909.2007.00442.x
[67]  Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34–41. pmid:17697981 doi: 10.1263/jbb.104.34
[68]  Zuo J, Niu QW, Chua NH (2000) Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24: 265–273. pmid:11069700 doi: 10.1046/j.1365-313x.2000.00868.x
[69]  Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. pmid:10069079 doi: 10.1046/j.1365-313x.1998.00343.x
[70]  Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907. pmid:3327686
[71]  Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127: 315–323. pmid:11553759 doi: 10.1104/pp.127.1.315
[72]  Wang HW, Zhang B, Hao YJ, Huang J, Tian AG, et al. (2007) The soybean Dof-type transcription factor genes, GmDof4 and GmDof11, enhance lipid content in the seeds of transgenic Arabidopsis plants. Plant J 52: 716–729. pmid:17877700 doi: 10.1111/j.1365-313x.2007.03268.x
[73]  Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2: 213–218. pmid:16163802 doi: 10.1038/nmeth0305-213
[74]  Mukhopadhyay A, Deplancke B, Walhout AJ, Tissenbaum HA (2008) Chromatin immunoprecipitation (ChIP) coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans. Nat Protoc 3: 698–709. doi: 10.1038/nprot.2008.38. pmid:18388953

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