The Triple Response Assay and Its Use to Characterize Ethylene Mutants in Arabidopsis

Part of the Methods in Molecular Biology book series (MIMB, volume 1573)


Exposure of plants to ethylene results in drastic morphological changes. Seedlings germinated in the dark in the presence of saturating concentrations of ethylene display a characteristic phenotype known as the triple response. This phenotype is robust and easy to score. In Arabidopsis the triple response is usually evaluated at 3 days post germination in seedlings grown in the dark in rich media supplemented with 10 μM of the ethylene precursor ACC in air or in unsupplemented media in the presence of 10 ppm ethylene. The triple response in Arabidopsis consists of shortening and thickening of hypocotyls and roots and exaggeration of the curvature of apical hooks. The search for Arabidopsis mutants that fail to show this phenotype in ethylene or, vice versa, display the triple response in the absence of exogenously supplied hormone has allowed the identification of the key components of the ethylene biosynthesis and signaling pathways. Herein, we describe a simple protocol for assaying the triple response in Arabidopsis. The method can also be employed in many other dicot species, with minor modifications to account for species-specific differences in germination. We also compiled a comprehensive table of ethylene-related mutants of Arabidopsis, including many lines with auxin-related defects, as wild-type levels of auxin biosynthesis, transport, signaling, and response are necessary for the normal response of plants to ethylene.

Key words

Phytohormone Ethylene ACC Triple response Arabidopsis Seedlings Germination Hypocotyl Root Apical hook Mutants 



We thank Jose Alonso, Begoña Orozco, and Delphine Pott for critical reading of the protocol and Anna Tsui for technical assistance. This work was supported by the National Science Foundation grant IOS 1444561 to A.N.S. and a Marie Curie COFUND U-Mobility postdoctoral fellowship to C.M. (cofunded by the University of Málaga and the EU 7FP GA NO. 246550).


  1. 1.
    Neljubow D (1901) Über die Horinzontale Nutation der Stengel von Pisum sativum und einiger anderer Pflanzen. Beih Bot Zentralb 10:128–139Google Scholar
  2. 2.
    Knight LI, Rose RC, Crocker W (1910) Effects of various gases and vapors upon etiolated seedlings of the sweet pea. Science 311(1):635–636Google Scholar
  3. 3.
    Ma B, He S-J, Duan K-X, Yin C-C, Chen H, Yang C et al (2013) Identification of rice ethylene-response mutants and characterization of MHZ7/OsEIN2 in distinct ethylene response and yield trait regulation. Mol Plant 6:1830–1848PubMedCrossRefGoogle Scholar
  4. 4.
    Yang C, Lu X, Ma B, Chen S-Y, Zhang J-S (2015) Ethylene signaling in rice and Arabidopsis: conserved and diverged aspects. Mol Plant 8:495–505PubMedCrossRefGoogle Scholar
  5. 5.
    Solano R, Ecker JR (1998) Ethylene gas: perception, signaling and response. Curr Opin Plant Biol 1:393–398PubMedCrossRefGoogle Scholar
  6. 6.
    Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086–1089PubMedCrossRefGoogle Scholar
  7. 7.
    Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G et al (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM 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 100:2992–2997PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    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 17:2230–2242PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Dolezal K et al (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191PubMedCrossRefGoogle Scholar
  12. 12.
    Hobbie LJ (1998) Auxin: molecular genetic approaches in Arabidopsis. Plant Physiol Biochem 36:91–102CrossRefGoogle Scholar
  13. 13.
    Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–562PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Chae HS, Faure F, Kieber JJ (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15:545–559PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Hansen M, Chae HS, Kieber JJ (2009) Regulation of ACS protein stability by cytokinin and brassinosteroids. Plant J 57:606–614PubMedCrossRefGoogle Scholar
  16. 16.
    Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo S-D et al (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23:3290–3302PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Su W, Howell SH (1992) A single genetic locus, ckr1, defines Arabidopsis mutants in which root growth is resistant to low concentrations of cytokinin. Plant Physiol 99:1569–1574PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Vogel JP, Woeste KE, Theologis A, Kieber JJ (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc Natl Acad Sci U S A 95:4766–4771PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Vogel JP, Schuerman P, Woeste K, Brandstatter I, Kieber JJ (1998) Isolation and characterization of Arabidopsis mutants defective in the induction of ethylene biosynthesis by cytokinin. Genetics 149:417–427PubMedPubMedCentralGoogle Scholar
  20. 20.
    Kushwah S, Jones AM, Laxmi A (2011) Cytokinin interplay with ethylene, auxin, and glucose signaling controls Arabidopsis seedling root directional growth. Plant Physiol 156:1851–1866PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Thole JM, Beisner ER, Liu J, Venkova SV, Strader LC (2014) Abscisic acid regulates root elongation through the activities of auxin and ethylene in Arabidopsis thaliana. G3 4:1259–1274PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Deslauriers SD, Larsen PB (2010) FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol Plant 3:626–640PubMedCrossRefGoogle Scholar
  25. 25.
    Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    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 139:1393–1409PubMedPubMedCentralGoogle Scholar
  27. 27.
    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 72:427–441PubMedCrossRefGoogle Scholar
  28. 28.
    Merchante C, Brumos J, Yun J, Hu Q, Spencer KR, Enríquez P et al (2015) Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2. Cell 163:684–697PubMedCrossRefGoogle Scholar
  29. 29.
    Larsen PB, Cancel JD (2003) Enhanced ethylene responsiveness in the Arabidopsis eer1 mutant results from a loss-of-function mutation in the protein phosphatase 2A A regulatory subunit, RCN1. Plant J 34:709–718PubMedCrossRefGoogle Scholar
  30. 30.
    Christians MJ, Robles LM, Zeller SM, Larsen PB (2008) The eer5 mutation, which affects a novel proteasome-related subunit, indicates a prominent role for the COP9 signalosome in resetting the ethylene-signaling pathway in Arabidopsis. Plant J 55:467–477PubMedCrossRefGoogle Scholar
  31. 31.
    De Paepe A, De Grauwe L, Bertrand S, Smalle J, Van Der Straeten D (2005) The Arabidopsis mutant eer2 has enhanced ethylene responses in the light. J Exp Bot 56:2409–2420PubMedCrossRefGoogle Scholar
  32. 32.
    Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C et al (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins. Cell 115:679–689PubMedCrossRefGoogle Scholar
  33. 33.
    Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657PubMedCrossRefGoogle Scholar
  34. 34.
    Zhao Y, Wei T, Yin KQ, Chen Z, Gu H, Qu LJ et al (2012) Arabidopsis RAP2.2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses. New Phytol 195:450–460PubMedCrossRefGoogle Scholar
  35. 35.
    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 12:3703–3714PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Rai MI, Wang X, Thibault DM, Kim HJ, Bombyk MM, Binder BM et al (2015) The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene. BMC Plant Biol 15:157PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Shi J, Habben JE, Archibald RL, Drummond BJ, Chamberlin MA, Williams RW et al (2015) Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and maize. Plant Physiol 169:266–282PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Wang Z, Cao H, Sun Y, Li X, Chen F, Carles A et al (2013) Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid-ethylene antagonism mediated by histone deacetylation. Plant Cell 25:149–166PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Li C, Xu J, Li J, Li Q, Yang H (2014) Involvement of Arabidopsis histone acetyltransferase HAC family genes in the ethylene signaling pathway. Plant Cell Physiol 55:426–435PubMedCrossRefGoogle Scholar
  40. 40.
    Liu Z, Wu Y, Yang F, Zhang Y, Chen S, Xie Q et al (2013) BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci U S A 110:6205–6210PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–522PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Kim BC, Soh MC, Kang BJ, Furuya M, Nam HG (1996) Two dominant photomorphogenic mutations of Arabidopsis thaliana identified as suppressor mutations of hy2. Plant J 9:441–456PubMedCrossRefGoogle Scholar
  43. 43.
    Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425PubMedCrossRefGoogle Scholar
  44. 44.
    Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168PubMedCrossRefGoogle Scholar
  45. 45.
    Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49:1025–1038PubMedCrossRefGoogle Scholar
  46. 46.
    Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM et al (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:379–393PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Li J, Dai X, Zhao Y (2006) A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol 140:899–908PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y 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 108:18518–18523PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Merchante C, Vallarino JG, Osorio S, Aragüez I, Villarreal N, Ariza MT et al (2013) Ethylene is involved in strawberry fruit ripening in an organ-specific manner. J Exp Bot 64:4421–4439PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X et al (2009) A combinatorial interplay among the 1-Aminocyclopropane-1-Carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183:979–1003PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 6:3386–3399CrossRefGoogle Scholar
  53. 53.
    Wang KL-C, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950PubMedCrossRefGoogle Scholar
  54. 54.
    Gingerich DJ, Gagne JM, Salter DW (2005) Cullin 3A and B assemble with members of the broad complex/tramtrack/bric-A-brac (BTB). J Biol Chem 280:18810–18821PubMedCrossRefGoogle Scholar
  55. 55.
    Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD (2009) The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J 57:332–345PubMedCrossRefGoogle Scholar
  56. 56.
    Tan S-T, Xue H-W (2014) Casein kinase 1 regulates ethylene synthesis by phosphorylating and promoting the turnover of ACS5. Cell Rep 9:1692–1702PubMedCrossRefGoogle Scholar
  57. 57.
    Yoo S-D, Cho Y-H, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–795PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    An F, Zhao Q, Ji Y, Li W, Jiang Z, Yu X 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 22:2384–2401PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H et al (2008) Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem 283:26996–27006PubMedCrossRefGoogle Scholar
  60. 60.
    Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Guan Y, Lu J, Xu J, McClure B, Zhang S (2014) Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis. Plant Physiol 165:528–533PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Han L, Li GJ, Yang KY, Mao G, Wang R, Liu Y et al (2010) Mitogen‐activated protein kinase 3 and 6 regulate Botrytis cinerea‐induced ethylene production in Arabidopsis. Plant J 64:114–127PubMedGoogle Scholar
  63. 63.
    Zheng Z, Guo Y, Novak O, Dai X, Zhao Y, Ljung K et al (2013) Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol 9:244–246PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Xu S-L, Rahman A, Baskin TI, Kieber JJ (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20:3065–3079PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Khanna R, Shen Y, Marion CM, Tsuchisaka A, Theologis A, Schäfer E et al (2007) The basic helix-loop-helix transcription factor PIF5 acts on ethylene biosynthesis and phytochrome signaling by distinct mechanisms. Plant Cell 19:3915–3929PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Dieterle M, Thomann A, Renou J-P, Parmentier Y, Cognat V, Lemonnier G et al (2005) Molecular and functional characterization of Arabidopsis cullin 3A. Plant J 41:386–399PubMedCrossRefGoogle Scholar
  67. 67.
    Thomann A, Brukhin V, Dieterle M, Gheyeselinck J, Vantard M, Grossniklaus U et al (2005) Arabidopsis CUL3A and CUL3B genes are essential for normal embryogenesis. Plant J 43:437–448PubMedCrossRefGoogle Scholar
  68. 68.
    Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J et al (2009) Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms. PLoS Genet 5:e1000328PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Woodward AW, Ratzel SE, Woodward EE, Shamoo Y, Bartel B (2007) Mutation of E1-CONJUGATING ENZYME-RELATED1 decreases RELATED TO UBIQUITIN conjugation and alters auxin response and development. Plant Physiol 144:976–987PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Bostick M, Lochhead SR, Honda A, Palmer S, Callis J (2004) Related to ubiquitin 1 and 2 are redundant and essential and regulate vegetative growth, auxin signaling, and ethylene production in Arabidopsis. Plant Cell 16:2418–2432PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Dharmasiri S, Dharmasiri N, Hellmann H, Estelle M (2003) The RUB/Nedd8 conjugation pathway is required for early development in Arabidopsis. EMBO J 22:1762–1770PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Larsen PB, Cancel JD (2004) A recessive mutation in the RUB1-conjugating enzyme, RCE1, reveals a requirement for RUB modification for control of ethylene biosynthesis and proper induction of basic chitinase and PDF1.2 in Arabidopsis. Plant J 38:626–638PubMedCrossRefGoogle Scholar
  73. 73.
    Zhong R, Ripperger A, Ye ZH (2000) Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiol 123:59–70PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Zhong R, Kays SJ, Schroeder BP, Ye Z-H (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14:165–179PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544PubMedCrossRefGoogle Scholar
  76. 76.
    Resnick JS, Wen C-K, Shockey JA, Chang C (2006) REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proc Natl Acad Sci U S A 103:7917–7922PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271PubMedCrossRefGoogle Scholar
  78. 78.
    Cancel JD, Larsen PB (2002) Loss-of-function mutations in the ethylene receptor ETR1 cause enhanced sensitivity and exaggerated response to ethylene in Arabidopsis. Plant Physiol 129:1557–1567PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Qu X, Hall BP, Gao Z, Schaller GE (2007) A strong constitutive ethylene-response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptors ETR1 and ERS1. BMC Plant Biol 7:3PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Sakai H, Hua J, Chen QG, Chang C, Bleecker AB (1998) ETR2 is an ETR1-like gene controlling ethylene signal transduction. Proc Natl Acad Sci U S A 95:5812–5817PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR et al (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10:1321–1332PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Hua J, Chang C, Sun Q, Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712–1714PubMedCrossRefGoogle Scholar
  83. 83.
    Zhao X-C, Qu X, Mathews DE, Schaller GE (2002) Effect of ethylene pathway mutations upon expression of the ethylene receptor ETR1 from Arabidopsis. Plant Physiol 130:1983–1991PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Liu Q, Xu C, Wen C-K (2010) Genetic and transformation studies reveal negative regulation of ERS1 ethylene receptor signaling in Arabidopsis. BMC Plant Biol 10:60PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Liu Q, Wen C-K (2012) Arabidopsis ETR1 and ERS1 differentially repress the ethylene response in combination with other ethylene receptor genes. Plant Physiol 158:1193–1207PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S et al (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease–related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393PubMedCrossRefGoogle Scholar
  87. 87.
    Woeste KE, Kieber JJ (2000) A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12:443–455PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Xu C, Zhou X, Wen C-K (2015) HYPER RECOMBINATION1 of the THO/TREX complex plays a role in controlling transcription of the REVERSION-TO-ETHYLENE SENSITIVITY1 gene in Arabidopsis. PLoS Genet 11:e1004956PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Tao S, Zhang Y, Wang X, Xu L, Fang X, Lu ZJ et al (2016) The THO/TREX complex active in miRNA biogenesis negatively regulates root-associated acid phosphatase activity induced by phosphate starvation. Plant Physiol 171:2841–2853PubMedPubMedCentralGoogle Scholar
  90. 90.
    Jauvion V, Elmayan T, Vaucheret H (2010) The conserved RNA trafficking proteins HPR1 and TEX1 are involved in the production of endogenous and exogenous small interfering RNA in Arabidopsis. Plant Cell 22:2697–2709PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Wang H, Sun Y, Chang J, Zheng F, Pei H, Yi Y et al (2016) Regulatory function of Arabidopsis lipid transfer protein 1 (LTP1) in ethylene response and signaling. Plant Mol Biol 91:471–484PubMedCrossRefGoogle Scholar
  92. 92.
    Chang J, Clay JM, Chang C (2014) Association of cytochrome b5 with ETR1 ethylene receptor signaling through RTE1 in Arabidopsis. Plant J 77:558–567PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Yu J, Wen C-K (2013) Arabidopsis aux1rcr1 mutation alters AUXIN RESISTANT1 targeting and prevents expression of the auxin reporter DR5:GUS in the root apex. J Exp Bot 64:371–933Google Scholar
  94. 94.
    Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152PubMedCrossRefGoogle Scholar
  95. 95.
    Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J et al (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci U S A 109:19486–19491PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144PubMedCrossRefGoogle Scholar
  97. 97.
    Binder BM, Walker JM, Gagne JM, Emborg TJ, Hemmann G, Bleecker AB et al (2007) The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19:509–523PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Olmedo G, Guo H, Gregory BD, Nourizadeh SD, Aguilar-Henonin L, Li H et al (2006) ETHYLENE-INSENSITIVE5 encodes a 5´–>3´ exoribonuclease required for regulation of the EIN3-targeting F-box proteins EBF1/2. Proc Natl Acad Sci U S A 103:13286–13293PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Potuschak T, Vansiri A, Binder BM, Lechner E, Vierstra RD, Genschik P (2006) The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell 18:3047–3057PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306:1046–1048PubMedCrossRefGoogle Scholar
  101. 101.
    Souret FF, Kastenmayer JP, Green PJ (2004) AtXRN4 Degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15:173–183PubMedCrossRefGoogle Scholar
  102. 102.
    Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677PubMedCrossRefGoogle Scholar
  103. 103.
    Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo S-D, Yanagisawa S et al (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc Natl Acad Sci U S A 101:6803–6808PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev 23:512–521PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Arciga Reyes L, Wootton L, Kieffer M, Davies B (2006) UPF1 is required for nonsense‐mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J 47:480–489PubMedCrossRefGoogle Scholar
  106. 106.
    Li W, Ma M, Feng Y, Li H, Wang Y, Ma Y et al (2015) EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell 163:670–683PubMedCrossRefGoogle Scholar
  107. 107.
    Hori K, Watanabe Y (2005) UPF3 suppresses aberrant spliced mRNA in Arabidopsis. Plant J 43:530–540PubMedCrossRefGoogle Scholar
  108. 108.
    Dufresne PJ, Ubalijoro E, Fortin MG, Laliberté J-F (2008) Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of turnip mosaic virus. J Gen Virol 89:2339–2348PubMedCrossRefGoogle Scholar
  109. 109.
    Larsen PB, Chang C (2001) The Arabidopsis eer1 mutant has enhanced ethylene responses in the hypocotyl and stem. Plant Physiol 125:1061–1073PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Garbers C, DeLong A, Deruére J, Bernasconi P, Söll D (1996) A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J 15:2115–2124PubMedPubMedCentralGoogle Scholar
  111. 111.
    Robles LM, Wampole JS, Christians MJ, Larsen PB (2007) Arabidopsis enhanced ethylene response 4 encodes an EIN3-interacting TFIID transcription factor required for proper ethylene response, including ERF1 induction. J Exp Bot 58:2627–2639PubMedCrossRefGoogle Scholar
  112. 112.
    Christians MJ, Larsen PB (2007) Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings. J Exp Bot 58:2237–2248PubMedCrossRefGoogle Scholar
  113. 113.
    Keith K, Kraml M, Dengler NG, McCourt P (1994) fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6:589–600PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Luerssen H, Kirik V, Herrmann P, Miséra S (1998) FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764PubMedCrossRefGoogle Scholar
  115. 115.
    Lumba S, Tsuchiya Y, Delmas F, Hezky J, Provart NJ, Shi Lu Q et al (2012) The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol 10:8PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Sun J, Ma Q, Mao T (2015) Ethylene regulates the Arabidopsis microtubule-associated protein WAVE-DAMPENED2-LIKE5 in etiolated hypocotyl elongation. Plant Physiol 169:325–337PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J et al (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257–273PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Laluk K, Luo H, Chai M, Dhawan R, Lai Z, Mengiste T (2011) Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 23:2831–2849PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194PubMedCrossRefGoogle Scholar
  120. 120.
    Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193–204PubMedCrossRefGoogle Scholar
  121. 121.
    Gy I, Gasciolli V, Lauressergues D, Morel J-B, Gombert J, Proux F et al (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–3461PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Chen H, Xiong L (2010) The bifunctional abiotic stress signalling regulator and endogenous RNA silencing suppressor FIERY1 is required for lateral root formation. Plant Cell Environ 33:2180–2190PubMedCrossRefGoogle Scholar
  123. 123.
    Adams E, Turner J (2010) COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J Exp Bot 61:4373–4386PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Chen G, Bi YR, Li N (2005) EGY1 encodes a membrane-associated and ATP-independent metalloprotease that is required for chloroplast development. Plant J 41:364–375PubMedCrossRefGoogle Scholar
  125. 125.
    Guo D, Gao X, Li H, Zhang T, Chen G, Huang P et al (2008) EGY1 plays a role in regulation of endodermal plastid size and number that are involved in ethylene-dependent gravitropism of light-grown Arabidopsis hypocotyls. Plant Mol Biol 66:345–360PubMedCrossRefGoogle Scholar
  126. 126.
    Ding L, Pandey S, Assmann SM (2008) Arabidopsis extra-large G proteins (XLGs) regulate root morphogenesis. Plant J 53:248–263PubMedCrossRefGoogle Scholar
  127. 127.
    Bueso E, Alejandro S, Carbonell P, Perez-Amador MA, Fayos J, Bellés JM et al (2007) The lithium tolerance of the Arabidopsis cat2 mutant reveals a cross-talk between oxidative stress and ethylene. Plant J 52:1052–1065PubMedCrossRefGoogle Scholar
  128. 128.
    Jing H-C, Sturre MJG, Hille J, Dijkwel PP (2002) Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J 32:51–63PubMedCrossRefGoogle Scholar
  129. 129.
    Jing H-C, Anderson L, Sturre MJG, Hille J, Dijkwel PP (2007) Arabidopsis CPR5 is a senescence-regulatory gene with pleiotropic functions as predicted by the evolutionary theory of senescence. J Exp Bot 58:3885–3894PubMedCrossRefGoogle Scholar
  130. 130.
    Boch J, Verbsky ML, Robertson TL, Larkin JC, Kunkel BN (2007) Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5. MPMI 11:1196–1206CrossRefGoogle Scholar
  131. 131.
    Bouquin T, Mattsson O, Naested H, Foster R, Mundy J (2003) The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J Cell Sci 116:791–801PubMedCrossRefGoogle Scholar
  132. 132.
    Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13:1025–1033PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey K (2002) The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14:1705–1721PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KL-C, Hussey PJ et al (2006) The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18:3058–3072PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585PubMedCrossRefGoogle Scholar
  137. 137.
    Poulios S, Vlachonasios KE (2016) Synergistic action of histone acetyltransferase GCN5 and receptor CLAVATA1 negatively affects ethylene responses in Arabidopsis thaliana. J Exp Bot 67:905–918PubMedCrossRefGoogle Scholar
  138. 138.
    Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914PubMedCrossRefGoogle Scholar
  139. 139.
    Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect arabidopsis growth, development, and gene expression. Plant Cell 15:626–638PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Li Z-G, Chen H-W, Li Q-T, Tao J-J, Bian X-H, Ma B et al (2015) Three SAUR proteins SAUR76, SAUR77 and SAUR78 promote plant growth in Arabidopsis. Sci Rep 5:12477PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Hayashi S, Hirayama T (2016) ahg12 is a dominant proteasome mutant that affects multiple regulatory systems for germination of Arabidopsis. Sci Rep 6:25351PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70PubMedGoogle Scholar
  143. 143.
    Aeschbacher RA, Hauser MT, Feldmann KA, Benfey PN (1995) The SABRE gene is required for normal cell expansion in Arabidopsis. Genes Dev 9:330–340PubMedCrossRefGoogle Scholar
  144. 144.
    Shin K, Lee S, Song W-Y, Lee R-A, Lee I, Ha K et al (2015) Genetic identification of ACC-RESISTANT2 reveals involvement of LYSINE HISTIDINE TRANSPORTER1 in the uptake of 1-aminocyclopropane-1-carboxylic acid in Arabidopsis thaliana. Plant Cell Physiol 56:572–582PubMedCrossRefGoogle Scholar
  145. 145.
    Svennerstam H, Ganeteg U, Bellini C, Näsholm T (2007) Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiol 143:1853–1860PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev 12:198–207PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721PubMedGoogle Scholar
  148. 148.
    Robles LM, Deslauriers SD, Alvarez AA, Larsen PB (2012) A loss-of-function mutation in the nucleoporin AtNUP160 indicates that normal auxin signalling is required for a proper ethylene response in Arabidopsis. J Exp Bot 63:2231–2241PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Kim T-H, Kim B-H, Yahalom A, Chamovitz DA, Arnim von AG (2004) Translational regulation via 5' mRNA leader sequences revealed by mutational analysis of the Arabidopsis translation initiation factor subunit eIF3h. Plant Cell 16:3341–3356PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Hobbie L, Estelle M (1994) Genetic approaches to auxin action. Plant Cell Environ 17:525–540PubMedCrossRefGoogle Scholar
  152. 152.
    Timpte C, Lincoln C, Pickett FB, Turner J, Estelle M (1995) The AXR1 and AUX1 genes of Arabidopsis function in separate auxin-response pathways. Plant J 8:561–589PubMedCrossRefGoogle Scholar
  153. 153.
    Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383PubMedCrossRefGoogle Scholar
  154. 154.
    Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M et al (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123:563–574PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Leyser HM, Pickett FB, Dharmasiri S, Estelle M (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10:403–413PubMedCrossRefGoogle Scholar
  156. 156.
    Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279:1371–1373PubMedCrossRefGoogle Scholar
  157. 157.
    Yang X, Lee S, So J-H, Dharmasiri S, Dharmasiri N, Ge L et al (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCF(TIR1). Plant J 40:772–782PubMedCrossRefGoogle Scholar
  158. 158.
    Hobbie L, McGovern M, Hurwitz LR, Pierro A, Liu NY, Bandyopadhyay A et al (2000) The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127:23–32PubMedGoogle Scholar
  159. 159.
    Hellmann H, Hobbie L, Chapman A, Dharmasiri S, Dharmasiri N, del Pozo C et al (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J 22:3314–3325PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Quint M, Ito H, Zhang W, Gray WM (2005) Characterization of a novel temperature-sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases. Plant J 43:371–383PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    Shen W-H, Parmentier Y, Hellmann H, Lechner E, Dong A, Masson J et al (2002) Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis. Mol Biol Cell 13:1916–1928PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Moon J, Zhao Y, Dai X, Zhang W, Gray WM, Huq E et al (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol 143:684–696PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15:2979–2991PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Strader LC, Monroe-Augustus M, Bartel B (2008) The IBR5 phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1-mediated repressor degradation. BMC Plant Biol 8:41PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Fortunati A, Piconese S, Tassone P, Ferrari S, Migliaccio F (2008) A new mutant of Arabidopsis disturbed in its roots, right-handed slanting, and gravitropism defines a gene that encodes a heat-shock factor. J Exp Bot 59:1363–1374PubMedCrossRefGoogle Scholar
  166. 166.
    LeClere S, Rampey RA, Bartel B (2004) IAR4, a gene required for auxin conjugate sensitivity in Arabidopsis, encodes a pyruvate dehydrogenase E1alpha homolog. Plant Physiol 135:989–999PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Pickett FB, Wilson AK, Estelle M (1990) The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol 94:1462–1466PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA et al (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950PubMedCrossRefGoogle Scholar
  169. 169.
    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 12:2175–2187PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, Kowalchyk M et al (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312:1218–1220PubMedCrossRefGoogle Scholar
  171. 171.
    Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J et al (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9:745–757PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J et al (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev 15:1985–1997PubMedPubMedCentralCrossRefGoogle Scholar
  173. 173.
    Kanyuka K, Praekelt U, Franklin KA, Billingham OE, Hooley R, Whitelam GC et al (2003) Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J 35:57–70PubMedCrossRefGoogle Scholar
  174. 174.
    Vandenbussche F, Smalle J, Le J, Saibo NJM, De Paepe A, Chaerle L et al (2003) The Arabidopsis mutant alh1 illustrates a cross talk between ethylene and auxin. Plant Physiol 131:1228–1238PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Shin K, Lee R-A, Lee I, Lee S, Park SK, Soh M-S (2013) Genetic identification of a second site modifier of ctr1-1 that controls ethylene-responsive and gravitropic root growth in Arabidopsis thaliana. Mol Cells 36:88–96PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Xu A, Zhang W, Wen C-K (2014) ENHANCING ctr1-10 ETHYLENE RESPONSE2 is a novel allele involved in CONSTITUTIVE TRIPLE-RESPONSE1-mediated ethylene receptor signaling in Arabidopsis. BMC Plant Biol 14:48PubMedPubMedCentralCrossRefGoogle Scholar
  177. 177.
    Cao XF, Linstead P, Berger F, Kieber J, Dolan L (1999) Differential ethylene sensitivity of epidermal cells is involved in the establishment of cell pattern in the Arabidopsis root. Physiol Plant 106:311–317PubMedCrossRefGoogle Scholar
  178. 178.
    Ferrari S, Piconese S, Tronelli G, Migliaccio F (2000) A new Arabidopsis thaliana root gravitropism and chirality mutant. Plant Sci 158:77–85PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2017

Authors and Affiliations

  1. 1.Departamento de Biología Molecular y Bioquímica, Instituto de Hortofruticultura Subtropical y Mediterranea (IHSM)-UMA-CSICUniversidad de MálagaMálagaSpain
  2. 2.Department of Plant and Microbial BiologyNorth Carolina State UniversityRaleighUSA
  3. 3.Genetics Graduate ProgramNorth Carolina State UniversityRaleighUSA

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