The Pivotal Role of Ethylene in Plant Growth
2018; Elsevier BV; Volume: 23; Issue: 4 Linguagem: Inglês
10.1016/j.tplants.2018.01.003
ISSN1878-4372
AutoresMarieke Dubois, Lisa Van den Broeck, Dirk Inzé,
Tópico(s)Plant Stress Responses and Tolerance
ResumoAn increasing number of transcriptome studies in plants exposed to biotic or abiotic stress highlight a role for ethylene under a broad range of stresses. The role of ethylene under stress is dual: it regulates a defense response, mostly in full-grown leaves, and a growth response in young leaves. In young leaves, ethylene and the downstream ERFs emerge as central regulators of leaf growth inhibition, orchestrating both cell division and cell expansion. The knowledge of ethylene-mediated growth inhibition can be successfully implemented in crops to improve plant growth and stress tolerance. Being continuously exposed to variable environmental conditions, plants produce phytohormones to react quickly and specifically to these changes. The phytohormone ethylene is produced in response to multiple stresses. While the role of ethylene in defense responses to pathogens is widely recognized, recent studies in arabidopsis and crop species highlight an emerging key role for ethylene in the regulation of organ growth and yield under abiotic stress. Molecular connections between ethylene and growth-regulatory pathways have been uncovered, and altering the expression of ethylene response factors (ERFs) provides a new strategy for targeted ethylene-response engineering. Crops with optimized ethylene responses show improved growth in the field, opening new windows for future crop improvement. This review focuses on how ethylene regulates shoot growth, with an emphasis on leaves. Being continuously exposed to variable environmental conditions, plants produce phytohormones to react quickly and specifically to these changes. The phytohormone ethylene is produced in response to multiple stresses. While the role of ethylene in defense responses to pathogens is widely recognized, recent studies in arabidopsis and crop species highlight an emerging key role for ethylene in the regulation of organ growth and yield under abiotic stress. Molecular connections between ethylene and growth-regulatory pathways have been uncovered, and altering the expression of ethylene response factors (ERFs) provides a new strategy for targeted ethylene-response engineering. Crops with optimized ethylene responses show improved growth in the field, opening new windows for future crop improvement. This review focuses on how ethylene regulates shoot growth, with an emphasis on leaves. The sessility of plants is undoubtedly their most disadvantageous feature compared to other living organisms, and implies that their survival can be threatened by environmental perturbations. However, plants have developed fascinating mechanisms enabling rapid detection of changing conditions accompanied by highly complex molecular responses, resulting in remarkable phenotypic plasticity. During the vegetative growth stage, one tightly controlled process is plant growth. Under favorable conditions, root and shoot growth is crucial to enable continuous nutrient uptake and energy production through photosynthesis, respectively. Leaf growth, for example, is controlled by no less than six different cellular mechanisms, including precise orchestration of the switch between cell division, that drives the growth of very young leaf primordia, and cell expansion and differentiation (reviewed in [1Gonzalez N. et al.Leaf size control: complex coordination of cell division and expansion.Trends Plant Sci. 2012; 17: 332-340Abstract Full Text Full Text PDF PubMed Scopus (182) Google Scholar]). By contrast, sustaining growth under unfavorable conditions could be detrimental. For example, growth under drought stress would increase the evaporative surface of the plant, rendering the plant even more susceptible. Plants thus constantly evaluate whether the environmental signals are favorable for growth or not, and redirect their resources either for growth or for stress defense. At the physiological level, the integration of environmental signals into proper phenotypic responses is orchestrated by phytohormones. Ethylene, the smallest phytohormone with the simple C2H4 structure, is gaseous and therefore enables plant-to-plant communication. Since its discovery around one century ago, the multiple facets of this hormone as a signaling molecule have fascinated scientists, and this led to the unraveling of its biosynthesis and signaling (Box 1 and Figure 1), and the identification of its various functions: regulation of leaf development, senescence, fruit ripening, stimulation of germination, etc. Importantly, ethylene is produced in response to multiple environmental stresses (Figure 1), both abiotic and biotic, suggesting that it acts as a bridge between a changing environment and developmental adaptation. The abiotic stress conditions that trigger ethylene synthesis include submergence, heat, shade, exposure to heavy metals and high salt, low nutrient availability, and water deficiency [2Skirycz A. et al.Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest.Plant Cell. 2011; 23: 1876-1888Crossref PubMed Scopus (0) Google Scholar, 3Thao N.P. et al.Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress.Plant Physiol. 2015; 169: 73-84Crossref PubMed Scopus (23) Google Scholar, 4Zhang M. et al.The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses.Plant Mol. Biol. 2016; 91: 651-659Crossref PubMed Scopus (11) Google Scholar, 5Dubois M. et al.Time of day determines Arabidopsis transcriptome and growth dynamics under mild drought.Plant Cell Environ. 2017; 40: 180-189Crossref PubMed Scopus (3) Google Scholar, 6Savada R.P. et al.Heat stress differentially modifies ethylene biosynthesis and signaling in pea floral and fruit tissues.Plant Mol. Biol. 2017; 95: 313-331Crossref PubMed Scopus (0) Google Scholar].Box 1Recent Advances in Ethylene Biosynthesis and SignalingThe ethylene biosynthesis pathway consists of a simple, three-step process: methionine is converted into S-adenosyl methionine (SAM; see Glossary), which is further converted by ACC-synthases (ACS) to ACC, the direct precursor of ethylene (Figure 1). Recycling of methylthioadenosine enables rapid ethylene biosynthesis when necessary [85Sauter M. et al.Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis.Biochem. J. 2013; 451: 145-154Crossref PubMed Scopus (90) Google Scholar]. Because the conversion from ACC to ethylene is an exothermic reaction that only requires oxygen, ethylene biosynthesis is regulated at the level of ACS enzymes, which are also under post-translational control: they can be phosphorylated before ubiquitin-mediated protein degradation by, for instance, ETO1 and CUL3 [86Thomann A. et al.Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms.PLoS Genet. 2009; 5e1000328Crossref PubMed Scopus (0) Google Scholar, 87Yoon G.M. New insights into the protein turnover regulation in ethylene biosynthesis.Mol. Cells. 2015; 38: 597-603Crossref PubMed Google Scholar]. ACS induction and activation are responsive to environmental factors that trigger ethylene accumulation. As such, ACS genes are transcriptionally induced by drought [5Dubois M. et al.Time of day determines Arabidopsis transcriptome and growth dynamics under mild drought.Plant Cell Environ. 2017; 40: 180-189Crossref PubMed Scopus (3) Google Scholar] and by shade, under the control of PIF4 [58Nomoto Y. et al.Circadian clock- and PIF4-controlled plant growth: a coincidence mechanism directly integrates a hormone signaling network into the photoperiodic control of plant architectures in Arabidopsis thaliana.Plant Cell Physiol. 2012; 53: 1950-1964Crossref PubMed Scopus (52) Google Scholar]. ACS2 and ACS6 are post-translationally activated through phosphorylation by a MAPK-phosphorylation cascade involving MKK9 and MPK3/6 [88Xu J. Zhang S. Regulation of ethylene biosynthesis and signaling by protein kinases and phosphatases.Mol. Plant. 2014; 7: 939-942Abstract Full Text Full Text PDF Scopus (0) Google Scholar]. ACC levels are also regulated by conjugation and release from conjugates such as malonyl- or jasmonyl-ACC [89Van de Poel B. Van Der Straeten D. 1-Aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene!.Front. Plant Sci. 2014; 5: 640Crossref PubMed Scopus (35) Google Scholar]. The soluble ethylene precursor ACC can be taken up by the amino acid transporter LHT1 and further transported through the plant via the xylem (Figure 1) [90Shin K. et al.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. 2015; 56: 572-582Crossref PubMed Scopus (15) Google Scholar].In the destination organ, ethylene triggers a signaling cascade initiated by ethylene receptors in the ER and Golgi membrane: ERS1 (ETHYLENE RESPONSE SENSOR 1), ERS2, ETR1 (ETHYLENE RESISTANCE 1), ETR2 and EIN4 (ETHYLENE INSENSITIVE 4). These receptors are active in the absence of ethylene, and their activity can be controlled by complex formation with RTE1 (REVERSION TO ETHYLENE SENSITIVITY) and ARGOS proteins: these are positive regulators of the ethylene receptors, and thus are negative regulators of ethylene sensitivity [11Rai M.I. et al.The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene.BMC Plant Biol. 2015; 15: 157Crossref PubMed Scopus (12) Google Scholar, 91Resnick J.S. et al.REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis.Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 7917-7922Crossref PubMed Scopus (114) Google Scholar, 92Shi J. et al.Maize and Arabidopsis ARGOS proteins interact with ethylene receptor signaling complex, supporting a regulatory role for ARGOS in ethylene signal transduction.Plant Physiol. 2016; 171: 2783-2797Crossref PubMed Scopus (14) Google Scholar]. In the absence of ethylene, active receptors subsequently bind to and thereby activate the CTR1 protein [93Lacey R.F. Binder B.M. How plants sense ethylene gas – the ethylene receptors.J. Inorg. Biochem. 2014; 133: 58-62Crossref PubMed Scopus (12) Google Scholar]. The levels of the receptors are regulated by ethylene and CTR1: slightly increasing ethylene levels stimulate the transcription of the receptors and stabilization of CTR1, whereas higher ethylene levels push the receptor/CTR1 towards proteasome-mediated degradation [94Shakeel S.N. et al.Ethylene regulates levels of ethylene receptor/CTR1 signaling complexes in Arabidopsis thaliana.J. Biol. Chem. 2015; 290: 12415-12424Crossref PubMed Scopus (15) Google Scholar]. CTR1 is a kinase that represses EIN2, an ER-located membrane protein. When this repression is released in the presence of ethylene, EIN2 is dephosphorylated and cleaved, releasing a C-terminal fragment that either moves to P-bodies or to the nucleus [95Li W. et al.EIN2-directed translational regulation of ethylene signaling in Arabidopsis.Cell. 2015; 163: 670-683Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar, 96Merchante C. et al.Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2.Cell. 2015; 163: 684-697Abstract Full Text Full Text PDF PubMed Scopus (67) Google Scholar]. The downstream mode of action of the EIN2 fragment has long been a mystery, but recent studies have shown that it is involved in gene-specific regulation of translation [95Li W. et al.EIN2-directed translational regulation of ethylene signaling in Arabidopsis.Cell. 2015; 163: 670-683Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar, 96Merchante C. et al.Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2.Cell. 2015; 163: 684-697Abstract Full Text Full Text PDF PubMed Scopus (67) Google Scholar]. The EIN2 fragment binds to the 3'-untranslated regions (3'-UTRs) of EBF1 and EBF2 transcripts, thereby repressing their translation. EBF1 and EBF2 are two central F-box proteins that target the primary ethylene-responsive TFs EIN3 and EIN3-LIKE 1 (EIL1) for protein degradation in the absence of ethylene [97Guo H. Ecker J.R. Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor.Cell. 2003; 115: 667-677Abstract Full Text Full Text PDF PubMed Scopus (495) Google Scholar, 98Potuschak T. et al.EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2.Cell. 2003; 115: 679-689Abstract Full Text Full Text PDF PubMed Scopus (420) Google Scholar]. In the presence of ethylene, EIN3 and EIL1 induce the expression of numerous secondary transcription factors (TFs), the ERFs [99Nakano T. et al.Identification of genes of the plant-specific transcription-factor families cooperatively regulated by ethylene and jasmonate in Arabidopsis thaliana.J. Plant Res. 2006; 119: 407-413Crossref PubMed Scopus (0) Google Scholar]. The activity of some ERFs has been reported to be increased by phosphorylation through the MPK3/6-cascade that also regulates ethylene biosynthesis, providing dual-level regulation of the ERF-mediated response [24Meng X. et al.Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance.Plant Cell. 2013; 25: 1126-1142Crossref PubMed Scopus (143) Google Scholar, 100Yoo S.-D. Sheen J. MAPK signaling in plant hormone ethylene signal transduction.Plant Signal. Behav. 2008; 3: 848-849Crossref PubMed Google Scholar]. The ethylene biosynthesis pathway consists of a simple, three-step process: methionine is converted into S-adenosyl methionine (SAM; see Glossary), which is further converted by ACC-synthases (ACS) to ACC, the direct precursor of ethylene (Figure 1). Recycling of methylthioadenosine enables rapid ethylene biosynthesis when necessary [85Sauter M. et al.Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis.Biochem. J. 2013; 451: 145-154Crossref PubMed Scopus (90) Google Scholar]. Because the conversion from ACC to ethylene is an exothermic reaction that only requires oxygen, ethylene biosynthesis is regulated at the level of ACS enzymes, which are also under post-translational control: they can be phosphorylated before ubiquitin-mediated protein degradation by, for instance, ETO1 and CUL3 [86Thomann A. et al.Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms.PLoS Genet. 2009; 5e1000328Crossref PubMed Scopus (0) Google Scholar, 87Yoon G.M. New insights into the protein turnover regulation in ethylene biosynthesis.Mol. Cells. 2015; 38: 597-603Crossref PubMed Google Scholar]. ACS induction and activation are responsive to environmental factors that trigger ethylene accumulation. As such, ACS genes are transcriptionally induced by drought [5Dubois M. et al.Time of day determines Arabidopsis transcriptome and growth dynamics under mild drought.Plant Cell Environ. 2017; 40: 180-189Crossref PubMed Scopus (3) Google Scholar] and by shade, under the control of PIF4 [58Nomoto Y. et al.Circadian clock- and PIF4-controlled plant growth: a coincidence mechanism directly integrates a hormone signaling network into the photoperiodic control of plant architectures in Arabidopsis thaliana.Plant Cell Physiol. 2012; 53: 1950-1964Crossref PubMed Scopus (52) Google Scholar]. ACS2 and ACS6 are post-translationally activated through phosphorylation by a MAPK-phosphorylation cascade involving MKK9 and MPK3/6 [88Xu J. Zhang S. Regulation of ethylene biosynthesis and signaling by protein kinases and phosphatases.Mol. Plant. 2014; 7: 939-942Abstract Full Text Full Text PDF Scopus (0) Google Scholar]. ACC levels are also regulated by conjugation and release from conjugates such as malonyl- or jasmonyl-ACC [89Van de Poel B. Van Der Straeten D. 1-Aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene!.Front. Plant Sci. 2014; 5: 640Crossref PubMed Scopus (35) Google Scholar]. The soluble ethylene precursor ACC can be taken up by the amino acid transporter LHT1 and further transported through the plant via the xylem (Figure 1) [90Shin K. et al.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. 2015; 56: 572-582Crossref PubMed Scopus (15) Google Scholar]. In the destination organ, ethylene triggers a signaling cascade initiated by ethylene receptors in the ER and Golgi membrane: ERS1 (ETHYLENE RESPONSE SENSOR 1), ERS2, ETR1 (ETHYLENE RESISTANCE 1), ETR2 and EIN4 (ETHYLENE INSENSITIVE 4). These receptors are active in the absence of ethylene, and their activity can be controlled by complex formation with RTE1 (REVERSION TO ETHYLENE SENSITIVITY) and ARGOS proteins: these are positive regulators of the ethylene receptors, and thus are negative regulators of ethylene sensitivity [11Rai M.I. et al.The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene.BMC Plant Biol. 2015; 15: 157Crossref PubMed Scopus (12) Google Scholar, 91Resnick J.S. et al.REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis.Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 7917-7922Crossref PubMed Scopus (114) Google Scholar, 92Shi J. et al.Maize and Arabidopsis ARGOS proteins interact with ethylene receptor signaling complex, supporting a regulatory role for ARGOS in ethylene signal transduction.Plant Physiol. 2016; 171: 2783-2797Crossref PubMed Scopus (14) Google Scholar]. In the absence of ethylene, active receptors subsequently bind to and thereby activate the CTR1 protein [93Lacey R.F. Binder B.M. How plants sense ethylene gas – the ethylene receptors.J. Inorg. Biochem. 2014; 133: 58-62Crossref PubMed Scopus (12) Google Scholar]. The levels of the receptors are regulated by ethylene and CTR1: slightly increasing ethylene levels stimulate the transcription of the receptors and stabilization of CTR1, whereas higher ethylene levels push the receptor/CTR1 towards proteasome-mediated degradation [94Shakeel S.N. et al.Ethylene regulates levels of ethylene receptor/CTR1 signaling complexes in Arabidopsis thaliana.J. Biol. Chem. 2015; 290: 12415-12424Crossref PubMed Scopus (15) Google Scholar]. CTR1 is a kinase that represses EIN2, an ER-located membrane protein. When this repression is released in the presence of ethylene, EIN2 is dephosphorylated and cleaved, releasing a C-terminal fragment that either moves to P-bodies or to the nucleus [95Li W. et al.EIN2-directed translational regulation of ethylene signaling in Arabidopsis.Cell. 2015; 163: 670-683Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar, 96Merchante C. et al.Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2.Cell. 2015; 163: 684-697Abstract Full Text Full Text PDF PubMed Scopus (67) Google Scholar]. The downstream mode of action of the EIN2 fragment has long been a mystery, but recent studies have shown that it is involved in gene-specific regulation of translation [95Li W. et al.EIN2-directed translational regulation of ethylene signaling in Arabidopsis.Cell. 2015; 163: 670-683Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar, 96Merchante C. et al.Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2.Cell. 2015; 163: 684-697Abstract Full Text Full Text PDF PubMed Scopus (67) Google Scholar]. The EIN2 fragment binds to the 3'-untranslated regions (3'-UTRs) of EBF1 and EBF2 transcripts, thereby repressing their translation. EBF1 and EBF2 are two central F-box proteins that target the primary ethylene-responsive TFs EIN3 and EIN3-LIKE 1 (EIL1) for protein degradation in the absence of ethylene [97Guo H. Ecker J.R. Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor.Cell. 2003; 115: 667-677Abstract Full Text Full Text PDF PubMed Scopus (495) Google Scholar, 98Potuschak T. et al.EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2.Cell. 2003; 115: 679-689Abstract Full Text Full Text PDF PubMed Scopus (420) Google Scholar]. In the presence of ethylene, EIN3 and EIL1 induce the expression of numerous secondary transcription factors (TFs), the ERFs [99Nakano T. et al.Identification of genes of the plant-specific transcription-factor families cooperatively regulated by ethylene and jasmonate in Arabidopsis thaliana.J. Plant Res. 2006; 119: 407-413Crossref PubMed Scopus (0) Google Scholar]. The activity of some ERFs has been reported to be increased by phosphorylation through the MPK3/6-cascade that also regulates ethylene biosynthesis, providing dual-level regulation of the ERF-mediated response [24Meng X. et al.Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance.Plant Cell. 2013; 25: 1126-1142Crossref PubMed Scopus (143) Google Scholar, 100Yoo S.-D. Sheen J. MAPK signaling in plant hormone ethylene signal transduction.Plant Signal. Behav. 2008; 3: 848-849Crossref PubMed Google Scholar]. Arabidopsis (Arabidopsis thaliana) plants overproducing ethylene are generally dwarfed, and plant growth is reduced by exposure to ethylene [7Burg S.P. Burg E.A. Ethylene formation in pea seedlings; its relation to the inhibition of bud growth caused by indole-3-acetic acid.Plant Physiol. 1968; 43: 1069-1074Crossref PubMed Google Scholar, 8Vogel J.P. et al.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. 1998; 95: 4766-4771Crossref PubMed Scopus (0) Google Scholar, 9Qu X. et al.A strong constitutive ethylene-response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptors ETR1 and ERS1.BMC Plant Biol. 2007; 7: 3Crossref PubMed Scopus (0) Google Scholar]. Consequently, when the positive regulators of the ethylene signaling pathway (Box 1 and Figure 1) are mutated, plants are generally found to have larger rosettes with larger leaves in comparison to control plants. Increased growth has, for example, been observed upon mutation the endoplasmic reticulum (ER)- anchored protein EIN2 [10Feng G. et al.The Arabidopsis EIN2 restricts organ growth by retarding cell expansion.Plant Signal. Behav. 2015; 10e1017169Crossref PubMed Scopus (2) Google Scholar]. Conversely, mutants of negative regulators of ethylene signaling, such as the receptors ETR1 and ERS1 (Box 1), show a growth decrease [9Qu X. et al.A strong constitutive ethylene-response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptors ETR1 and ERS1.BMC Plant Biol. 2007; 7: 3Crossref PubMed Scopus (0) Google Scholar]. Accordingly, overexpression of the negative regulators ARGOS or ARGOS-LIKE (ARL) stimulates leaf growth in arabidopsis [11Rai M.I. et al.The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene.BMC Plant Biol. 2015; 15: 157Crossref PubMed Scopus (12) Google Scholar, 12Shi J. et al.Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and maize.Plant Physiol. 2015; 169: 266-282Crossref PubMed Scopus (43) Google Scholar]. Moreover, plant lines in which the ethylene sensitivity is reduced, or treatments reducing sensitivity to ethylene, cause larger leaves. For instance, plants overexpressing NEIP2 or TCTP, genes encoding proteins interacting with the Nicotiana tabacum ethylene receptor, show decreased ethylene sensitivity but improved growth [13Cao Y.-R. et al.Tobacco ankyrin protein NEIP2 interacts with ethylene receptor NTHK1 and regulates plant growth and stress responses.Plant Cell Physiol. 2015; 56: 803-818Crossref PubMed Scopus (8) Google Scholar, 14Tao J.-J. et al.Tobacco translationally controlled tumor protein interacts with ethylene receptor tobacco histidine kinase1 and enhances plant growth through promotion of cell proliferation.Plant Physiol. 2015; 169: 96-114Crossref PubMed Scopus (18) Google Scholar]. Similarly, Pseudomonas frederiksbergensis, a soil bacterium that reduces plant sensitivity to ethylene, promotes the growth of red pepper plants [15Chatterjee P. et al.Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth.Front. Plant Sci. 2017; 8: 705Crossref PubMed Scopus (0) Google Scholar]. Finally, some rhizosphere bacteria that promote plant growth do so by expressing ACC-DEAMINASE, decreasing the levels of 1-aminocyclopropane-1-carboxylic acid (ACC) in plants exposed to stress, and this has a positive effect on growth [16Chen L. et al.The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway.J. Exp. Bot. 2013; 64: 1565-1573Crossref PubMed Scopus (30) Google Scholar]. Exceptionally, ethylene has been reported to stimulate leaf growth. In the presence of very low ethylene concentrations, Poa alpina and Poa compressa show increased leaf elongation rates [17Fiorani F. et al.Ethylene emission and responsiveness to applied ethylene vary among Poa species that inherently differ in leaf elongation rates.Plant Physiol. 2002; 129: 1382-1390Crossref PubMed Scopus (0) Google Scholar], and also the primary leaves of sunflower (Helianthus annuus) are enlarged [18Lee S.H. Reid D.M. The role of endogenous ethylene in the expansion of Helianthus annuus leaves.Can. J. Bot. 1997; 75: 501-508Crossref PubMed Google Scholar]. However, the opposite effect was observed as soon as ethylene levels are increased to concentrations higher than this low growth-promoting optimum. This general negative correlation between ethylene sensitivity and leaf growth has led to the classification of ethylene as a growth-repressing hormone. In plants, where growth mainly occurs post-embryonically through well-orchestrated cell divisions, the progression through the cell cycle is tightly governed by more than 70 core cell-cycle proteins (reviewed in [19Polyn S. et al.Cell cycle entry, maintenance, and exit during plant development.Curr. Opin. Plant Biol. 2015; 23: 1-7Crossref PubMed Scopus (46) Google Scholar]). Controlled by endogenous cues and environmental signals, cell-cycle progression and regulation vary depending on the plant organ, and the effect of ethylene is similarly organ-dependent. For instance, during the early development of the apical hook, ethylene participates in stimulating cell divisions, although its contribution is not crucial for curving of the apical hook [20Raz V. Koornneef M. Cell division activity during apical hook development.Plant Physiol. 2001; 125: 219-226Crossref PubMed Scopus (0) Google Scholar]. Moreover, ethylene and the downstream transcription factors (TFs) ERF018 and ERF109 promote cell division during vasculature development in arabidopsis stems [21Etchells J.P. et al.Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling.PLoS Genet. 2012; 8e1002997Crossref PubMed Scopus (0) Google Scholar]. Thus, in these specific developmental contexts, ethylene can have a positive effect on cell division. In leaves of plants exposed to environmental stress, ethylene appears to have a negative effect on the cell cycle. When plants are exposed to less than 10 h of osmotic stress, ethylene mediates a temporary and reversible stop of the cell cycle. This is likely to occur through the inactivation of the CDKA by phosphorylation, possibly through the MPK3/6 pathway but independently from EIN3/EIL1 (Figure2) [2Skirycz A. et al.Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest.Plant Cell. 2011; 23: 1876-1888Crossref PubMed Scopus (0) Google Scholar]. Moreover, at least four mechanisms in leaves link ethylene to the exit of cell division and a shift to endoreduplication and differentiation. First, accumulation of ethylene and induction of the BOLITA TF (an ERF, Table 1) triggers the activation of type II TEOSINTE BRANCHED 1/CYCLOIDEA/PCF (TCP) genes (Figure 2) [22Marsch-Martinez N. et al.BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways.Plant Mol. Biol. 2006; 62: 825-843Crossref PubMed Scopus (48) Google Scholar]. These TCP proteins bind to the promoter of RETINOBLASTOMA RELATED 1 (RBR1), and the encoded protein phosphorylates E2Fa and thus represses the transcription of the E2F target genes, thereby inhibiting progression into the S-phase and cell division. Second, ethylene induces the expression of ERF5 and ERF6, two closely related TFs, in actively growing leaves of plants exposed to stress [2Skirycz A. et al.Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest.Plant Cell. 2011; 23: 1876-1888Crossref PubMed Scopus (0) Google Scholar, 23Dubois M. et al.ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis.Plant Physiol. 2013; 162: 319-332Crossref PubMed Scopus (97) Google Scholar, 24Meng X. et al.Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates pl
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