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Evidence of the functional role of the ethylene receptor genes SlETR4 and SlETR5 in ethylene signal transduction in tomato

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Abstract

Ethylene receptors are key factors for ethylene signal transduction. In tomato, six ethylene receptor genes (SlETR1SlETR6) have been identified. Mutations in different ethylene receptor genes result in different phenotypes that are useful for elucidating the roles of each gene. In this study, we screened mutants of two ethylene receptor genes, SLETR4 and SLETR5, from a Micro-Tom mutant library generated by TILLING. We identified two ethylene receptor mutants with altered phenotypes and named them Sletr4-1 and Sletr5-1. Sletr4-1 has a mutation between the transmembrane and GAF domains, while Sletr5-1 has a mutation within the GAF domain. Sletr4-1 showed increased hypocotyl and root lengths, compared to those of wild type plants, under ethylene exposure. Moreover, the fruit shelf life of this mutant was extended, titratable acidity was increased and total soluble solids were decreased, suggesting a reduced ethylene sensitivity. In contrast, in the absence of exogenous ethylene, the hypocotyl and root lengths of Sletr5-1 were shorter than those of the wild type, and the fruit shelf life was shorter, suggesting that these mutants have increased ethylene sensitivity. Gene expression analysis showed that SlNR was up-regulated in the Sletr5-1 mutant line, in contrast to the down-regulation observed in the Sletr4-1 mutant line, while the down-regulation of SlCTR1, SlEIN2, SlEIL1, SlEIL3, and SlERF.E4 was observed in Sletr4-1 mutant allele, suggesting that these two ethylene receptors have functional roles in ethylene signalling and demonstrating, for the first time, a function of the GAF domain of ethylene receptors. These results suggest that the Sletr4-1 and Sletr5-1 mutants are useful for elucidating the complex mechanisms of ethylene signalling through the analysis of ethylene receptors in tomato.

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References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in Plant Biology 2nd ed. Academic Press, Sandiego. ISBN:0-12-041451-1, pp 83–103

    Google Scholar 

  • Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055

    Article  CAS  PubMed  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  Google Scholar 

  • Aravind L, Ponting CP (1997) The GAF domain: An evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458–459

    Article  CAS  PubMed  Google Scholar 

  • Baldwin EA, Biggs RH (1988) Cell-wall lysing enzymes and products of cell-wall digestion elicit ethylene in citrus. Physiol Plant 73:58–64

    Article  CAS  Google Scholar 

  • Blecker AB, Patterson SE (1997) Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9:1169–1179

    Article  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340

    Article  CAS  PubMed  Google Scholar 

  • Cameron AC, Reid MS (2001) 1-MCP blocks ethylene induced petal abscission of Pelargonium peltatum but the effect is transients. Postharvest Biol Technol 22:169–177

    Article  CAS  Google Scholar 

  • Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57:1883–1897

    Article  CAS  PubMed  Google Scholar 

  • Choi SW, Hoshikawa K, Fujita S, Thi DP, Mizoguchi T, Ezura H, Ito E (2018) Evaluation of internal control genes for quantitative realtime PCR analyses for studying fruit development of dwarf tomato cultivar ‘Micro-Tom’. Plant Biotech. 18–0525

  • Ciardi J, Klee H (2001) Regulation of ethylene-mediated responses at the level of the receptor. Ann Bot 88:813–822

    Article  CAS  Google Scholar 

  • Crocker W, Knight LI, Rose RCA (1913) Delicate seedling test. Science 37:380–381

    Google Scholar 

  • Crouch I (2003) 1-Methylcyclopropene (Smartfreshtm) as an alternative to modified atmosphere and controlled atmosphere storage of apples and pears. Acta Horticlturae 600:433–436

    Article  CAS  Google Scholar 

  • Defilippi BG, Dandekar AM, Kader AA (2004) Impact of suppression of ethylene action and biosynthesis on flavor metabolites in apple (Malus domestica Borkh) fruits. J Agric Food Chem 52:5694–5701

    Article  CAS  PubMed  Google Scholar 

  • Evensen KB (1991) Ethylene responsiveness changes in Pelargonium X domesticum. Physiol. Plant 82:409–412

    CAS  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  Google Scholar 

  • Gao L, Zhao W, Qu H, Wang Q, Zhao L (2016) The yellow-fruited tomato 1 (yft1) mutant has altered fruit carotenoid accumulation and reduced ethylene production as a result of a genetic lesion in ETHYLENE INSENSITIVE2. Theor Appl Genets 129(4):717–728

    Article  CAS  Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell (Suppl) 16:S170–S180

    Article  CAS  Google Scholar 

  • Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–524

    Article  PubMed  PubMed Central  Google Scholar 

  • Hobson GE (1980) Effect of the introduction of non-ripening mutant genes on the composition and enzyme content of tomato fruit. J Sci Food Agric 31:578–584

    Article  CAS  Google Scholar 

  • Jones ML, Kim ES, Newman SE (2001) Role of ethylene and 1-MCP in flower development and petal abscission in zonal Pelargonium. Hort Sci 36:1305–1309

    Article  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Ann Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Kevany BM, Tieman DM, Taylor MG, Cin VD, Klee HJ (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–467

    Article  CAS  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 

  • Klay I, Gouia S, Liu M, Mila I, Khoudi H, Bernadec A, Bouzayen M, Pirello J (2018) Ethylene Response Factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Sci 274:137–145

    Article  CAS  PubMed  Google Scholar 

  • Klee H, Tieman D (2002) The tomato ethylene receptor gene family: form and function. Physiol Plant 115:336–341

    Article  CAS  PubMed  Google Scholar 

  • Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6:521–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lashbrook CC, Tieman DM, Klee HJ (1998) Differential regulation of the ETR gene family throughout plant development. Plant J 15:234–252

    Article  Google Scholar 

  • Leclercq J, Adams-Phillips LC, Zegzouti H, Jones B, Latché A, Giovannoni JJ, Pech JC, Bouzayen M (2002) LeCTR1, a tomato CTR1-like gene, demonstrates ethylene signaling ability in arabidopsis and novel expression patterns in tomato. Plant Physiol 130:1132–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mubarok S, Okabe Y, Fukuda N, Ariizumi T, Ezura H (2015) Potential use of a weak ethylene receptor mutant, Sletr1-2, as breeding material to extend fruit shelf life of tomato. J Agric Food Chem 63:7995–8007

    Article  CAS  PubMed  Google Scholar 

  • Mubarok S, Okabe Y, Fukuda N, Ariizumi T, Ezura H (2016) Favourable effect of a weak ethylene receptor mutation Sletr1-2 on postharvest fruit quality changes in tomatoes. Postharvest Biol Technol 120:1–9

    Article  CAS  Google Scholar 

  • Okabe Y, Asamizu E, Saito T, Matsukura C, Ariizumi T, Bres C, Rothan C, Mizaguchi T, Ezura H (2011) Tomato TILLING Technology: Development of a reverse genetic tool for the efficient isolation of mutants from micro-tom mutant libraries. Plant Cell Physiol 52:1994–2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Payton S, Fray RG, Brown S, Grierson D (1996) Ethylene receptor expression is regulated during fruit ripening, flower senescence and abscission. Plant Mol Biol 31:1227–1231

    Article  CAS  PubMed  Google Scholar 

  • Representative images showing the appearance (upper) and leaves (lower) of the two ethylene receptor mutants. The plant and leaves were taken at 60 days after sowing

  • Rick C, Butler L (1956) Cytogenetics of the Tomato. Adv. Genet 8:267–382

    Google Scholar 

  • Rodríguez GR, Pratta GR, Liberatti DR, Zorzoli R, Picardi LA (2010) Inheritance of shelf life and other quality traits of tomato fruit estimated from F1’s, F2’s and backcross generatios derived from standard cultivar, nor homozygote and wild cherry tomato. Euphytica 176:137–147

    Article  Google Scholar 

  • Saito T, Ariizumi T, Okabe Y, Asamizu E, Hiwasa-Tanase K, Fukuda N, Mizoguchi T, Yamazaki Y, Aoki K, Ezura H (2011) TOMATOMA: a novel tomato mutant database distributing Micro-Tom mutant collections. Plant Cell Physiol 52:283–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Shinozaki Y, Hao S, Kojima M, Sakakibara H, Ozeki-Iida Y, Zheng Y, Fei Z, Zhong S, Giovannoni JJ, Rose JKC, Okabe Y, Heta Y, Eura H, Ariizumi T (2015) Ethylene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism. Plant J 83:237–251

    Article  CAS  PubMed  Google Scholar 

  • Tieman DM, Klee HJ (1999) Differential expression of two novel members of the tomato ethylene-receptor family. Plant Physiol 120:165–172

    Article  CAS  PubMed  PubMed Central  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  CAS  Google Scholar 

  • Tieman DM, Ciardi JA, Taylor MG, Klee HJ (2001) Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J 26:47–58

    Article  CAS  Google Scholar 

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

  • Watanabe S, Mizoguchi T, Aoki K, Kubo Y, Mori H, Imanishi S, Yamazaki Y, Shibata D, Ezura H (2007) Ethylmethanesulfonate (EMS) mutagenesis of Solanum lycopersicum cv. Micro-Tom for large-scale mutant screens. Plant Biotechnol 24:33–38

    Article  CAS  Google Scholar 

  • Wilkinson J, Lanahan M, Yen H, Giovannoni J, Klee H (1995) An ethylene-inducible component of signal transduction encoded by Never-ripe. Science 270:1807–1809

    Article  CAS  PubMed  Google Scholar 

  • Winsor GW, Davies JN, Massey DM (1962) Composition of tomato fruit. IV. changes in some constituents of the fruit walls during ripening. J Sci Food Agricult 13(3):141–145

    Article  CAS  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosysnthesis and its regulation in higher plants. Ann Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Yang X, Song J, Campbell-Palmer L, Fillmore S, Zhang Z (2013) Effect of ethylene and 1-MCP on expression of genes involved in ethylene biosynthesis and perception during ripening of apple fruit. Postharvest BiolTechnol 78:55–66

    Article  CAS  Google Scholar 

  • Zhang ZG, Zhou HL, Chen T, Gong Y, Cao WH, Wang YJ, Zhang JS, Chen SY (2004) Evidence for serine/threonine and histidine kinase activity in the tobacco ethylene receptor protein NTHK2. Plant Physiol 136:2971–2981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou HL, Cao WH, Cao YR, Liu J, Hao YJ, Zhang JS, Chen SY (2006) Roles of ethylene receptor NTHK1 domains in plant growth, stress response and protein phosphorylation. FEBS Lett 580:1239–1250

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the National BioResearch Project (NBRP), MEXT, Japan for providing seeds from S. lycopersicum cv. Micro-Tom, Sletr4-1,and Sletr5-1. This study was supported by the JSPS KAKENHI [grant number25252008] to H.E. We also thank all members of our laboratory for their helpful discussions throughout the project.

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Correspondence to Hiroshi Ezura.

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Communicated by S. Hohmann.

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Mubarok, S., Hoshikawa, K., Okabe, Y. et al. Evidence of the functional role of the ethylene receptor genes SlETR4 and SlETR5 in ethylene signal transduction in tomato. Mol Genet Genomics 294, 301–313 (2019). https://doi.org/10.1007/s00438-018-1505-7

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