Abstract
Key message
The tomato mutant Never ripe ( Nr ), a loss-of-function for the ethylene receptor Sl ETR3, shows enhanced growth, associated with increased carbon assimilation and a rewiring of the central metabolism.
Abstract
Compelling evidence has demonstrated the importance of ethylene during tomato fruit development, yet its role on leaf central metabolism and plant growth remains elusive. Here, we performed a detailed characterization of Never ripe (Nr) tomato, a loss-of-function mutant for the ethylene receptor SlETR3, known for its fruits which never ripe. However, besides fruits, the Nr gene is also constitutively expressed in vegetative tissues. Nr mutant showed a growth enhancement during both the vegetative and reproductive stage, without an earlier onset of leaf senescence, with Nr plants exhibiting a higher number of leaves and an increased dry weight of leaves, stems, roots, and fruits. At metabolic level, Nr also plays a significant role with the mutant showing changes in carbon assimilation, carbohydrates turnover, and an exquisite reprogramming of a large number of metabolite levels. Notably, the expression of genes related to ethylene signaling and biosynthesis are not altered in Nr. We assess our results in the context of those previously published for tomato fruits and of current models of ethylene signal transduction, and conclude that ethylene insensitivity mediated by Nr impacts the whole central metabolism at vegetative stage, leading to increased growth rates.
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References
Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825. https://doi.org/10.1105/tpc.015685
Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489. https://doi.org/10.1073/pnas.0610717104
Aguiar T, Sant’anna-Santos B, Azevedo A, Ferreira R (2007) ANATI QUANTI: Quantitative analysis software for plant anatomy studies. Planta Daninha 25:649–659. https://doi.org/10.1590/S0100-83582007000400001
Araújo WL, Tohge T, Osorio S, Lohse M, Balbo I, Krahnert I, Sienkiewicz-Porzucek A, Usadel B, Nunes-Nesi A, Fernie AR (2012) Antisense inhibition of the 2-oxoglutarate dehydrogenase complex in tomato demonstrates its importance for plant respiration and during leaf senescence and fruit maturation. Plant Cell 24:2328–2351. https://doi.org/10.1105/tpc.112.099002
Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63. https://doi.org/10.3389/fpls.2013.00063
Arve LE, Torre S (2015) Ethylene is involved in high air humidity promoted stomatal opening of tomato (Lycopersicon esculentum) leaves. Funct Plant Biol 42:376. https://doi.org/10.1071/FP1424
Arvidsson S, Kwasniewski M, Riano-Pachon D, Mueller-Roeber B (2008) QuantPrime—a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinform 9:465. https://doi.org/10.1186/1471-2105-9-465
Azhar BJ, Zulfiqar A, Shakeel SN, Schaller GE (2019) Amplification and adaptation in the ethylene signaling pathway. Small Methods. https://doi.org/10.1002/smtd.201900452
Batista-Silva W, Medeiros DB, Rodrigues-Salvador A, Daloso DM, Omena-Garcia RP, Oliveira FS, Pino LE, Peres LEP, Nunes-Nesi A, Fernie AR, Zsögön A, Araújo WL (2018) Modulation of auxin signalling through DIAGETROPICA and ENTIRE differentially affects tomato plant growth via changes in photosynthetic and mitochondrial metabolism. Plant Cell Environ 42:448–465. https://doi.org/10.1111/pce.13413
Binder BM (2020) Ethylene signaling in plants. J Biol Chem 295:7710–7725. https://doi.org/10.1074/jbc.REV120.010854
Caldana C, Scheible W-R, Mueller-Roeber B, Ruzicic S (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3:7. https://doi.org/10.1186/1746-4811-3-7
Castagna A, Ederli L, Pasqualini S, Mensuali-Sodi A, Baldan B, Donnini S, Ranieri A (2007) The tomato ethylene receptor LE-ETR3 (NR) is not involved in mediating ozone sensitivity: causal relationships among ethylene emission, oxidative burst and tissue damage. New Phytol 174:342–356. https://doi.org/10.1111/j.1469-8137.2007.02010.x
Černý M, Kuklová A, Hoehenwarter W, Fragner L, Novák O, Rotková G, Jedelsky PL, Žáková K, Šmehilová M, Strnad M, Weckwerth W, Brzobohatý B (2013) Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation. J Exp Bot 64:4193–4206. https://doi.org/10.1093/jxb/ert227
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. https://doi.org/10.1126/science.8211181
Chen Y, Rofidal V, Hem S, Gil J, Nosarzewska J, Berger N, Demolombe V, Bouzayen M, Azhar BJ, Shakeel SN, Schaller GE, Binder BM, Santoni V, Chervin C (2019) Targeted proteomics allows quantification of ethylene receptors and reveals SlETR3 accumulation in Never-Ripe tomatoes. Front Plant Sci 10:1054. https://doi.org/10.3389/fpls.2019.01054
Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48. https://doi.org/10.1111/j.1365-313X.2005.02359.x
Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121:53–60. https://doi.org/10.1104/pp.121.1.53
Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–562. https://doi.org/10.1104/pp.124.2.553
Cross JM, von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, Palacios N, Stitt M (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol 142:1574–1588. https://doi.org/10.1104/pp.106.086629
Cuadros-Inostroza A, Caldana C, Redestig H, Kusano M, Lisec J, Peña-Cortés H, Willmitzer L, Hannah MA (2009) TargetSearch–a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinform 10:428. https://doi.org/10.1186/1471-2105-10-428
Daloso DM, Williams TCR, Antunes WC, Pinheiro DP, Müller C, Loureiro ME, Fernie AR (2016) Guard cell-specific upregulation of sucrose synthase 3 reveals that the role of sucrose in stomatal function is primarily energetic. New Phytol 209:1470–1483. https://doi.org/10.1111/nph.13704
De Pedro LF, Mignolli F, Scartazza A, Colavita JPM, Bouzo CA, Vidoz ML (2020) Maintenance of photosynthetic capacity in flooded tomato plants with reduced ethylene sensitivity. Physiol Plant. https://doi.org/10.1111/ppl.13141
Dubois M, Van den Broeck L, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23:311–323. https://doi.org/10.1016/j.tplants.2018.01.003
Dugardeyn J, Vandenbussche F, Van Der Straeten D (2008) To grow or not to grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis? J Exp Bot 59:1–16. https://doi.org/10.1093/jxb/erm349
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142. https://doi.org/10.1002/j.1537-2197.1968.tb06952.x
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9
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 12:1117–1126. https://doi.org/10.1105/tpc.12.7.1117
Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32:859–874. https://doi.org/10.1111/j.1365-3040.2009.01965.x
Gratão PL, Monteiro CC, Carvalho RF, Tezotto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissection of diageotropica and Never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96. https://doi.org/10.1016/j.plaphy.2012.04.009
Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602. https://doi.org/10.1046/j.1365-313X.1995.8040595.x
Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523. https://doi.org/10.1105/tpc.2.6.513
Hackett RM, Ho CW, Lin Z, Foote HC, Fray RG, Grierson D (2000) Antisense inhibition of the Nr gene restores normal ripening to the tomato Never-ripe mutant, consistent with the ethylene receptor-inhibition model. Plant Physiol 124:1079–1086. https://doi.org/10.1104/pp.124.3.1079
Harriman RW, Tieman DM, Handa AK (1991) Molecular cloning of tomato pectin methylesterase gene and its expression in rutgers, ripening inhibitor, nonripening, and never ripe tomato fruits. Plant Physiol 97:80–87. https://doi.org/10.1104/pp.97.1.80
Hobson GE (1967) The effects of alleles at the ‘Never ripe’ locus on the ripening of tomato fruit. Phytochemistry 6:1337–1341. https://doi.org/10.1016/S0031-9422(00)82875-7
Huang WN, Liu HK, Zhang HH, Chen Z, Guo YD, Kang YF (2013) Ethylene-induced changes in lignification and cell wall-degrading enzymes in the roots of mungbean (Vigna radiata) sprouts. Plant Physiol Biochem 73:412–419. https://doi.org/10.1016/j.plaphy.2013.10.020
Hunt R (1982) Plant growth analysis: second derivatives and compounded second derivatives of splined plant growth curves. Ann Bot 50:317–328. https://doi.org/10.1093/oxfordjournals.aob.a086371
Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard. J Exp Bot 62:4955–4963. https://doi.org/10.1093/jxb/err204
Kalve S, Fotschki J, Beeckman T, Vissenberg K, Beemster GTS (2014) Three-dimensional patterns of cell division and expansion throughout the development of Arabidopsis thaliana leaves. J Exp Bot 65:6385–6397. https://doi.org/10.1093/jxb/eru358
Khan NA (2004) Activity of 1-Aminocyclopropane carboxylic acid synthase in two mustard (Brassica juncea L.) cultivars differing in photosynthetic capacity. Photosynthetica 42:477–480. https://doi.org/10.1023/B:PHOT.0000046170.43688.8d
Kieber JJ, Schaller GE (2019) Behind the screen: how a simple seedling response helped unravel ethylene signaling in plants. Plant Cell 31:1402–1403. https://doi.org/10.1105/tpc.19.00342
Kim HJ, Lynch JP, Brown KM (2008) Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant Cell Environ 31:1744–1755. https://doi.org/10.1111/j.1365-3040.2008.01886.x
Klee HJ (2002) Control of ethylene-mediated processes in tomato at the level of receptors. J Exp Bot 53:2057–2063. https://doi.org/10.1093/jxb/erf062
Klee HJ, Tieman D (2002) The tomato ethylene receptor gene family: form and function. Physiol Plant 115:36–341. https://doi.org/10.1034/j.1399-3054.2002.1150302.x
Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6:521–530. https://doi.org/10.1105/tpc.6.4.521
Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: How ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270. https://doi.org/10.1007/s00299-011-1180-1
Linkies A, Müller K, Morris K, Turečková V, Wenk M, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, Leubner-Metzger G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822. https://doi.org/10.1105/tpc.109.070201
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–396. https://doi.org/10.1038/nprot.2006.59
Llop-Tous I, Barry CS, Grierson D (2000) Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiol 123:971–978. https://doi.org/10.1104/pp.123.3.971
Logan BA, Adams WW, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Funct Plant Biol 34:853–859. https://doi.org/10.1071/FP07113
Long SP, Bernacchi C (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401. https://doi.org/10.1093/jxb/erg262
Martins SCV, Galmés J, Molins A, DaMatta FM (2013) Improving the estimation of mesophyll conductance to CO2: on the role of electron transport rate correction and respiration. J Exp Bot 64:3285–3298. https://doi.org/10.1093/jxb/ert168
Martins SCV, Araújo WL, Tohge T, Fernie AR, DaMatta FM (2014) In high-light-acclimated coffee plants the metabolic machinery is adjusted to avoid oxidative stress rather than to benefit from extra light enhancement in photosynthetic yield. PLoS One 9:e94862. https://doi.org/10.1371/journal.pone.0094862
Martins AO, Omena-Garcia RP, Oliveira FS, Silva WA, Hajirezaei MR, Vallarino JG, Ribeiro DM, Fernie AR, Nunes-Nesi A, Araújo WL (2019) Differential root and shoot responses in the metabolism of tomato plants exhibiting reduced levels of gibberellin. Environ Exp Bot 157:331–343. https://doi.org/10.1016/j.envexpbot.2018.10.036
Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195. https://doi.org/10.1016/j.tplants.2012.02.001
Nazar R, Khan IR, Iqbal N, Masood A, Khan NA (2014) Involvement of ethylene in reversal of salt-inhibited photosynthesis by sulfur in mustard. Physiol Plant 152:331–344. https://doi.org/10.1111/ppl.12173
Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61:3–15. https://doi.org/10.1111/j.1365-313X.2009.04027.x
Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K (2012) Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J 72:523–536. https://doi.org/10.1111/j.1365-313X.2012.05085.x
Ogawara T, Higashi K, Kamada H, Ezura H (2003) Ethylene advances the transition from vegetative growth to flowering in Arabidopsis thaliana. J Plant Physiol 160:1335–1340. https://doi.org/10.1078/0176-1617-01129
Ögren E, Evans JR (1993) Photosynthetic light–response curves. Planta 189:182–190. https://doi.org/10.1007/BF00195075
Omena-Garcia RP, Martins AO, Medeiros DB, Vallarino JG, Ribeiro DM, Fernie AR, Araújo WL, Nunes-Nesi A (2019) Growth and metabolic adjustments in response to gibberellin deficiency in drought stressed tomato plants. Environ Exp Bot 159:95–107. https://doi.org/10.1016/j.envexpbot.2018.12.011
Osorio S, Alba R, Damasceno CMB, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JKC, Fei Z, Giovannoni JJ, Fernie AR (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157:405–425. https://doi.org/10.1104/pp.111.175463
Pantin F, Simonneau T, Rolland G, Dauzat M, Muller B (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiol 156:803–815. https://doi.org/10.1104/pp.111.176289
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. https://doi.org/10.1007/BF00040839
Pierik R, Cuppens MLC, Voesenek LACJ, Visser EJW (2004) Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in tobacco. Plant Physiol 136:2928–2936. https://doi.org/10.1104/pp.104.045120
Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183. https://doi.org/10.1016/j.tplants.2006.02.006
Pierik R, Djakovic-Petrovic T, Keuskamp DH, de Wit M, Voesenek LACJ (2009) Auxin and ethylene regulate elongation responses to neighbor proximity signals independent of gibberellin and DELLA proteins in Arabidopsis. Plant Physiol 149:1701–1712. https://doi.org/10.1104/pp.108.133496
Pilkington SM, Encke B, Krohn N, Höhne M, Stitt M, Pyl ET (2015) Relationship between starch degradation and carbon demand for maintenance and growth in Arabidopsis thaliana in different irradiance and temperature regimes. Plant Cell Environ 38:157–171. https://doi.org/10.1111/pce.12381
Poór P, Kovács J, Borbély P, Takács Z, Szepesi Á, Tari I (2015) Salt stress-induced production of reactive oxygen- and nitrogen species and cell death in the ethylene receptor mutant Never ripe and wild type tomato roots. Plant Physiol Biochem 97:313–322. https://doi.org/10.1016/j.plaphy.2015.10.021
Poorter H (2002) Plant growth and carbon economy. eLS. https://doi.org/10.1038/npg.els.0003200
Poorter H, Pothmann P (1992) Growth and carbon economy of a fast- growing and a slow-growing grass species as dependent on ontogeny. New Phytol 120:159–166. https://doi.org/10.1111/j.1469-8137.1992.tb01069.x
Poorter H, Van der Werf A (1998) Is inherent variation in RGR determined by LAR at low light and by NAR at high light? In: Lambers H, Poorter H, Van Vuuren MMI (eds). Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences. Backhuys Publishers. 309-336
Ribeiro DM, Araújo WL, Fernie AR, Schippers JHM, Mueller-Roeber B (2012) Translatome and metabolome effects triggered by gibberellins during rosette growth in Arabidopsis. J Exp Bot 63:2769–2786. https://doi.org/10.1093/jxb/err463
Rodeghiero M, Niinemets Ü, Cescatti A (2007) Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar, et al. model parameters? Plant Cell Environ 30:1006–1022. https://doi.org/10.1111/j.1365-3040.2007.001689.x
Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11–29. https://doi.org/10.1105/tpc.13.1.11
Rosado-Souza L, Scossa F, Chaves IS, Kleessen S, Salvador LFD, Milagre JC, Finger FL, Bhering LL, Sulpice R, Araújo WL, Nikoloski Z, Fernie AR, Nunes-Nesi A (2015) Exploring natural variation of photosynthetic, primary metabolism and growth parameters in a large panel of Capsicum chinense accessions. Planta 242:677–691. https://doi.org/10.1007/s00425-015-2332-2
Santelia D, Lawson T (2016) Rethinking guard cell metabolism. Plant Physiol 172:1371–1392. https://doi.org/10.1104/pp.16.00767
Schaller GE, Bleecker A (1995) Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270:1809–1811. https://doi.org/10.1126/science.270.5243.1809
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040. https://doi.org/10.1111/j.1365-3040.2007.01710.x
Shoji T, Yuan L (2020) ERF gene clusters: working together to regulate metabolism. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2020.07.015
Silva PO, Medina EF, Barros RS, Ribeiro DM (2014) Germination of salt-stressed seeds as related to the ethylene biosynthesis ability in three Stylosanthes species. J Plant Physiol 171:14–22. https://doi.org/10.1016/j.jplph.2013.09.004
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149. https://doi.org/10.1111/j.1365-3040.2007.01708.x
Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15:282–292. https://doi.org/10.1016/j.pbi.2012.03.016
Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7:137–155. https://doi.org/10.1093/mp/sst127
Tholen D, Voesenek LACJ, Poorter H (2004) Ethylene insensitivity does not increase leaf area or relative growth rate in Arabidopsis, Nicotiana tabacum, and Petunia x hybrida. Plant Physiol 134:1803–1812. https://doi.org/10.1104/pp.103.034389
Tholen D, Pons TL, Voesenek LACJ, Poorter H (2007) Ethylene insensitivity results in down-regulation of rubisco expression and photosynthetic capacity in tobacco. Plant Physiol 144:1305–1315. https://doi.org/10.1104/pp.107.099762
Tholen D, Pons TL, Voesenek LACJ, Poorter H (2008) The role of ethylene perception in the control of photosynthesis. Plant Signal Behav 3:108–109. https://doi.org/10.4161/psb.3.2.4968
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(10):5663–5668. https://doi.org/10.1073/pnas.090550597
Tucker GA, Grierson D (1982) Synthesis of polygalacturonase during tomato fruit ripening. Planta 155:64–67. https://doi.org/10.1007/BF00402933
Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562. https://doi.org/10.1111/j.1365-313X.2010.04262.x
Wang S, Liu J, Feng Y, Niu X, Giovannoni JJ, Liu Y (2008) Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J 55:89–103. https://doi.org/10.1111/j.1365-313X.2008.03489.x
Wang H, Liang X, Huang J, Zhang D, Lu H, Liu Z, Bi Y (2010) Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol 51:1754–1765. https://doi.org/10.1093/pcp/pcq134
Wilkinson JQ, Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by never-ripe. Science 270:1807–1809. https://doi.org/10.1126/science.270.5243.1807
Wilson RL, Kim H, Bakshi A, Binder BM (2014) The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol 165:1353–1366. https://doi.org/10.1104/pp.114.241695
Wuriyanghan H, Zhang B, Cao W-H, Ma B, Lei G, Liu Y-F, Wei W, Wu H-J, Chen L-J, Chen H-W, Cao Y-R, He S-J, Zhang W-K, Wang X-J, Chen S-Y, Zhang J-S (2009) The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell 21:1473–1494. https://doi.org/10.1105/tpc.108.065391
Yen HC, Lee S, Tanksley SD, Lanahan MB, Klee HJ, Giovannoni JJ (1995) The tomato Never-ripe locus regulates ethylene-inducible gene expression and is linked to a homolog of the Arabidopsis ETR1 gene. Plant Physiol 107:1343–1353. https://doi.org/10.1104/pp.107.4.1343
Yoong F, O’Brien LK, Truco MJ, Huo H, Sideman R, Hayes R, Michelmore RW, Bradford KJ (2016) Genetic variation for thermotolerance in lettuce seed germination is associated with temperature-sensitive regulation of ETHYLENE RESPONSE FACTOR1 (ERF1). Plant Physiol 170:472–488. https://doi.org/10.1104/pp.15.01251
Zhao XC, Schaller GE (2004) Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett 562:189–192. https://doi.org/10.1016/S0014-5793(04)00238-8
Zhu G, Ye N, Yang J, Peng X, Zhang J (2011) Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets. J Exp Bot 62:3907–3916. https://doi.org/10.1093/jxb/err088
Zsögön A, Peres LEP, Nguyen HT, Ball MC (2015) A mutation that eliminates bundle sheath extensions reduces leaf hydraulic conductance, stomatal conductance and assimilation rates in tomato (Solanum lycopersicum). New Phytol 205:618–626. https://doi.org/10.1111/nph.13084
Acknowledgements
The authors would like to acknowledge Dr. Jim Giovannoni (Boyce Thompson Institute for Plant Research, Ithaca, New York, USA) for sharing seeds used in this work. This work was supported by funding from the National Council for Scientific and Technological Development (CNPq-Brazil, Grant 402511/2016-6 to WLA) and the FAPEMIG (Foundation for Research Assistance of the Minas Gerais State, Brazil, Grant APQ-01171-17 and RED-00053-16). We also thank the scholarships granted by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES-Brazil—Finance Code 001) to VLN, AMP and LCC, and by the CNPq to CEAB. RS was supported by a Research Stimulus Grant (VICCI—Grant No: 14/S/819) funded by the Irish Department of Agriculture, Food and the Marine (DAFM). Research fellowships granted by CNPq-Brazil to DMR, ANN, AZ, and WLA are also gratefully acknowledged.
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Conception and design of the experiments: VLN and WLA. Performance of the experiments: VLN, AMP, ASP, VFS, LCC, and CEAB. Analysis of the data: VLN, RS, DMR, CC, AZ, ANN, and WLA. Contribution of reagents/materials/analysis tools: DMR, CC, AZ, ANN, and WLA. Writing of the manuscript: VLN, RS, DMR, AZ, ANN, and WLA.
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Communicated by Neal Stewart.
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Nascimento, V.L., Pereira, A.M., Pereira, A.S. et al. Physiological and metabolic bases of increased growth in the tomato ethylene-insensitive mutant Never ripe: extending ethylene signaling functions. Plant Cell Rep 40, 1377–1393 (2021). https://doi.org/10.1007/s00299-020-02623-y
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DOI: https://doi.org/10.1007/s00299-020-02623-y