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Appearance and elaboration of the ethylene receptor family during land plant evolution

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Abstract

Ethylene is perceived following binding to endoplasmic reticulum-localized receptors, which in Arabidopsis thaliana, include ETR1, ERS1, EIN4, ETR2, and ERS2. These receptors fall into two subfamilies based on conservation of features within their histidine kinase domain. Subfamily 1 contains ETR1 and ERS1 whereas subfamily 2 contains EIN4, ETR2, and ERS2. Because ethylene receptors are found only in plants, this raises questions of when each receptor evolved. Here it is shown that subfamily 1 receptors encoded by a multigene family are present in all charophytes examined, these being most homologous to ETR1 based on their evolutionary relationship as well as containing histidine kinase and receiver domains. In charophytes and Physcomitrella patens, one or more gene family members contain the intron characteristic of subfamily 2 genes, indicating the first step in subfamily 2 receptor evolution. ERS1 homologs appear in basal angiosperm species after Amborella trichopoda and, in some early and basal angiosperm species and monocots in general, it is the only subfamily 1 receptor present. Distinct EIN4 and ETR2 homologs appear only in core eudicots and ERS2 homologs appear only in the Brassicaceae, suggesting it is the most recent receptor to evolve. These findings show that a subfamily 1 receptor had evolved and a subfamily 2 receptor had begun to evolve in plants prior to the colonization of land and only these two existed up to the appearance of the first basal angiosperm. The appearance of ERS2 in the Brassicaceae suggests ongoing evolution of the ethylene receptor family.

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Abbreviations

ACO:

ACC oxidase

ACS:

ACC synthase

CC:

Coiled coil

CTR1:

Constitutive triple response1

Cys:

Cysteine

EST:

Expressed sequence tag

GAF:

cGMP-specific phosphodiesterases, adenylyl cyclases and FhlA

Tyr:

Tyrosine

References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic Press Inc, San Diego

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Amborella Genome Project (2013) The Amborella genome and the evolution of flowering plants. Science 342:1241089

    Article  Google Scholar 

  • Binder BM, Chang C, Schaller GE (2012) Perception of ethylene by plants-ethylene receptors. Annual plant reviews, the plant hormone ethylene 44. Wiley, Hoboken, pp 117–145

    Chapter  Google Scholar 

  • Bleecker AB (1999) Ethylene signaling: an evolutionary perspective. Trends Plant Sci 4:269–274

    Article  PubMed  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Ann Rev Cell Dev Biol 16:1–18

    Article  CAS  Google Scholar 

  • Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086–1089

    Article  CAS  PubMed  Google Scholar 

  • Bleecker AB, Esch JJ, Hall AE, Rodríguez FI, Binder BM (1998) The ethylene-receptor family from Arabidopsis: structure and function. Philos Trans R Soc Lond B Biol Sci 353:1405–1412

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chang C, Shockey JA (1999) The ethylene-response pathway: signal perception to gene regulation. Curr Opin Plant Biol 2:352–358

    Article  CAS  PubMed  Google Scholar 

  • Chang C, Stadler R (2001) Ethylene hormone receptor action in Arabidopsis. Bioessays 23:619–627

    Article  CAS  PubMed  Google Scholar 

  • Chang C, Stewart RC (1998) The two-component system. Regulation of diverse signaling pathways in prokaryotes and eukaryotes. Plant Physiol 117:723–731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544

    Article  CAS  PubMed  Google Scholar 

  • 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 89:1133–1144

    Article  CAS  PubMed  Google Scholar 

  • Chen QG, Bleecker AB (1995) Analysis of ethylene signal-transduction kinetics associated with seedling-growth response and chitinase induction in wild-type and mutant Arabidopsis. Plant Physiol 108:597–607

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen JF, Gallie DR (2010) Analysis of the functional conservation of ethylene receptors between maize and Arabidopsis. Plant Mol Biol 74:405–421

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem 277:19861–19866

    Article  CAS  PubMed  Google Scholar 

  • Clark KL, Larsen PB, Wang X, Chang C (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci USA 95:5401–5406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Mol Biol 48:223–250

    Article  CAS  Google Scholar 

  • Drew MC, Jackson MB, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L. Planta 147:83–88

    Article  CAS  PubMed  Google Scholar 

  • Drew MC, He C-J, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127

    Article  CAS  PubMed  Google Scholar 

  • Gallie DR, Young TE (2004) The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize. Mol Gen Genomics 271:267–281

    Article  CAS  Google Scholar 

  • Gallie DR, Geisler-Lee J, Chen J, Jolley B (2009) Tissue-specific expression of the ethylene biosynthetic machinery regulates root growth in maize. Plant Mol Biol 69:195–211

    Article  CAS  PubMed  Google Scholar 

  • Gamble RL, Coonfield ML, Schaller GE (1998) Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci USA 95:7825–7829

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gao Z, Wen CK, Binder BM, Chen YF, Chang J, Chiang YH, Kerris RJ 3rd, Chang C, Schaller GE (2008) Heteromeric interactions among ethylene receptors mediate signaling in Arabidopsis. J Biol Chem 283:23801–23810

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nuclic Acid Res 31:3784–3788

    Article  CAS  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nuclic Acid Res 40:D1178–D1186

    Article  CAS  Google Scholar 

  • Grefen C, Städele K, Růzicka K, Obrdlik P, Harter K, Horák J (2008) Subcellular localization and in vivo interaction of the Arabidopsis thaliana ethylene receptor family members. Mol Plant 1:308–320

    Article  CAS  PubMed  Google Scholar 

  • Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hall AE, Bleecker AB (2003) Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell 15:2032–2041

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N, Moriyama T, Ikeuchi M, Watanabe M, Wada H, Kobayashi K, Saito M, Masuda T, Sasaki-Sekimoto Y, Mashiguchi K, Awai K, Shimojima M, Masuda S, Iwai M, Nobusawa T, Narise T, Kondo S, Saito H, Sato R, Murakawa M, Ihara Y, Oshima-Yamada Y, Ohtaka K, Satoh M, Sonobe K, Ishii M, Ohtani R, Kanamori-Sato M, Honoki R, Miyazaki D, Mochizuki H, Umetsu J, Higashi K, Shibata D, Kamiya Y, Sato N, Nakamura Y, Tabata S, Ida S, Kurokawa K, Ohta H (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Chang C, Sun Q, Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712–1714

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10:1321–1332

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C (2015) Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat Plants 1:14004

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Le SQ, Gascuel O (2008) LG: an improved, general amino-acid replacement matrix. Mol Biol Evol 25:1307–1320

    Article  CAS  PubMed  Google Scholar 

  • Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336

    Article  CAS  PubMed  Google Scholar 

  • Lohrmann J, Harter K (2002) Plant two-component signaling systems and the role of response regulators. Plant Physiol 128:363–369

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mattoo AK, Suttle JC (1991) The Plant Hormone Ethylene. FL CRC Press, Boca Raton

    Google Scholar 

  • Mount SM, Chang C (2002) Evidence for a plastid origin of plant ethylene receptor genes. Plant Physiol 130:10–14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moussatche P, Klee HJ (2004) Autophosphorylation activity of the Arabidopsis ethylene receptor multigene family. J Biol Chem 279:48734–48741

    Article  CAS  PubMed  Google Scholar 

  • Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R, Sahlin K, Sherwood E, Elfstrand M, Gramzow L, Holmberg K, Hällman J, Keech O, Klasson L, Koriabine M, Kucukoglu M, Käller M, Luthman J, Lysholm F, Niittylä T, Olson A, Rilakovic N, Ritland C, Rosselló JA, Sena J, Svensson T, Talavera-López C, Theißen G, Tuominen H, Vanneste K, Wu ZQ, Zhang B, Zerbe P, Arvestad L, Bhalerao R, Bohlmann J, Bousquet J, Garcia Gil R, Hvidsten TR, de Jong P, MacKay J, Morgante M, Ritland K, Sundberg B, Thompson SL, Van de Peer Y, Andersson B, Nilsson O, Ingvarsson PK, Lundeberg J, Jansson S (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584

    Article  CAS  PubMed  Google Scholar 

  • O’Malley RC, Rodriguez FI, Esch JJ, Binder BM, O’Donnell P, Klee HJ, Bleecker AB (2005) Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. Plant J 41:651–659

    Article  PubMed  Google Scholar 

  • Qu X, Hall B, 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 7:3

    Article  PubMed Central  PubMed  Google Scholar 

  • Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999) A copper co-factor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998

    Article  CAS  PubMed  Google Scholar 

  • Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM (1998) ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci USA 95:5812–5817

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schaller GE (1997) Ethylene and cytokinin signalling in plants: the role of two-component systems. Essays Biochem 32:101–111

    CAS  PubMed  Google Scholar 

  • Schaller GE (2012) Ethylene and the regulation of plant development. BMC Biol 10:9. doi:10.1186/1741-7007-10-9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schaller GE, Ladd AN, Lanahan MB, Spanbauer JM, Bleecker AB (1995) The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer. J Biol Chem 270:12526–12530

    Article  CAS  PubMed  Google Scholar 

  • Shakeel SN, Wang X, Binder BM, Schaller GE (2013) Mechanisms of signal transduction by ethylene: overlapping and non-overlapping signalling roles in a receptor family. AoB Plants 5:plt010

    Article  PubMed Central  PubMed  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Genes Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Development 12:3703–3714

    CAS  Google Scholar 

  • Stepanova AN, Alonso JM (2005) Arabidopsis ethylene signaling pathway. Sci STKE 276:cm4

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tieman DM, Taylor MG, Ciardi JA, Klee HJ (2000) The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc Natl Acad Sci USA 97:5663–5668

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Timme RE, Delwiche CF (2010) Uncovering the evolutionary origin of plant molecular processes: comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biol 10:96

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang W, Hall AE, O’Malley R, Bleecker AB (2003) Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc Natl Acad Sci USA 100:352–357

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang W, Esch JJ, Shiu SH, Agula H, Binder BM, Chang C, Patterson SE, Bleecker AB (2006) Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell 18:3429–3442

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whalen MC, Feldman LJ (1988) The effect of ethylene on root growth of Zea mays seedlings. Can J Bot 66:719–723

    Article  CAS  PubMed  Google Scholar 

  • Xie F, Liu Q, Wen C-K (2006) Receptor signal output mediated by the ETR1 N-terminus is primarily subfamily I receptor dependent. Plant Physiol 142:492–508

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yau CP, Wang L, Yu M, Zee SY, Yip WK (2004) Differential expression of three genes encoding an ethylene receptor in rice during development, and in response to indole-3-acetic acid and silver ions. J Exp Bot 55:547–556

    Article  CAS  PubMed  Google Scholar 

  • Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751

    PubMed Central  CAS  PubMed  Google Scholar 

  • Young TE, Meeley RB, Gallie DR (2004) ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J 40:813–825

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the University of California Agricultural Experiment Station.

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Gallie, D.R. Appearance and elaboration of the ethylene receptor family during land plant evolution. Plant Mol Biol 87, 521–539 (2015). https://doi.org/10.1007/s11103-015-0296-z

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