Os05g0420300
SALT-RESPONSIVE ERF1 (SERF1) is a rice (Oryza sativa) transcription factor (TF) gene[1].
Contents
Annotated Information
Function
- Loss of SERF1 impairs the salt-inducible expression of genes encoding members of a mitogen-activated protein kinase(MAPK) cascade and salt tolerance–mediating TFs. SERF1-dependent genes are H2O2 responsive and demonstrate that SERF1 binds to the promoters of MAPK KINASE KINASE6 (MAP3K6), MAPK5, DEHYDRATION-RESPONSIVE ELEMENT BINDING2A (DREB2A), and ZINC FINGER PROTEIN179 (ZFP179) in vitro and in vivo(Figure 2)[1].
- SERF1 also directly induces its own gene expression. In addition, SERF1 is a phosphorylation target of MAPK5, resulting in enhanced transcriptional activity of SERF1 toward its direct target genes. In agreement, plants deficient for SERF1 are more sensitive to salt stress compared with the wild type, while constitutive overexpression of SERF1 improves salinity tolerance. SERF1 amplifies the reactive oxygen species–activated MAPK cascade signal during the initial phase of salt stress and translates the salt-induced signal into an appropriate expressional response resulting in salt tolerance[1].
- SERF1 is a positive regulator of short-Term and long-term salt stress tolerance[1][2]. Overexpression of SERF1 increases oxidative stress tolerance. Phosphorylation of SERF1 increases its ability to activate transcription of target genes. SERF1 is a phosphorylation target of MAPK5[1].
- Metabolic profiling and expression analysis show that the action of SERF1 in signal communication to the shoot is independent from ABA, but does affect the accumulation of ROS-related metabolites and transcripts under short-term salt stress[2].
- SERF1 suppresses grain filling and germination by repressing the expression of the RICE PROLAMN BOX-BINDING FACTOR(RPBF) gene and modulating starch metabolism.[3].
- SERF1 directly regulates RICE PROLAMIN-BOX BINDING FACTOR (RPBF), a TF that functions as a positive regulator of grain filling. Loss of SERF1 enhances RPBF expression resulting in larger grains with increased starch content, while SERF1 overexpression represses RPBF resulting in smaller grains.[3].
- Consistently, during 10 grain filling, starch biosynthesis genes such as GRANULE-BOUND STARCH 11 SYNTHASEI (GBSSI), STARCH SYNTHASEI (SSI), SSIIIa and ADP-GLUCOSE 12 PYROPHOSPHORYLASE LARGE SUBUNIT2 (AGPL2) are upregulated in SERF1 knock-out grains. Moreover, SERF1 is a direct upstream regulator of GBSSI. In addition, SERF1 negatively regulates germination by controlling RPBF expression, which mediates the gibberellic acid (GA)-induced expression of RICE AMYLASE1A (RAmy1A). Loss of SERF1 results in more rapid seedling establishment, while SERF1 overexpression has the opposite effect. Our study reveals that SERF1 18 represents a negative regulator of grain filling and seedling establishment by timing the expression of RPBF[3].
GO assignment(s): GO:0006814, GO:0006885, GO:0015299, GO:0015385, GO:0016021
Mutation
- A homozygous T-DNA knockout line[1]:
- serf1
- The absence of full-length SERF1 transcript in homozygous serf1 plants was confirmed by quantitative RT-PCR (qRT-PCR).
- Three independent transgenic lines[1]:
- KD 3-1
- KD 4-1
- KD 5-1
- After application of salt (200 mM NaCl), the leaf temperature increased in all lines. However, from 15 min onwards, serf1 and the SERF1 knockdown lines KD 4-1 and KD 5-1 exhibited higher leaf temperature compared with control lines, which suggesting that loss or knockdown of SERF1 decreases the tolerance to osmotic stress induced by salt treatment.
- By contrast, SERF1 overexpression lines showed lower leaf temperatures after 25 min of salt stress compared with the empty vector (EV) line.
- Leaf temperature of mock-treated serf1 plants did not differ from the wild type; likewise, SERF1 knockdown and overexpression plants and their respective controls showed similar leaf temperatures under control conditions.
- The rapid decline in sugars might be symptomatic to the salt sensitivity of serf1, as sugars not only act in energy metabolism but also function as osmoprotectants[2].
Expression
- SERF1 expression is induced within 10 min of salt stress and reaches maximal expression after 60 min of treatment.
- Schmidt et al. tested the expressional response of SERF1 in wild-type roots and leaves upon H2O2, ABA, or mannitol application (Figure 1A). Application of of ABA or mannitol did not affect the expression of SERF1.
By contrast, as observed for salt stress, H2O2 treatment caused an upregulation of SERF1 within 30 min exclusively in roots, albeit an induction was also observed after 3 h of treatment. Rice plants expressing a b-glucuronidase (GUS) reporter gene fused to a 1-kb promoter of SERF1 exhibited GUS activity in the vascular cylinder of the root and the main and commissural veins of leaves(Figure 1B).
- Also, decreased expression of SERF1 in knockdown lines resulted in a stronger reduction of chlorophyll after MV and H2O2 treatment compared with the EV line. By contrast, leaves of plants overexpressing SERF1 showed higher levels of chlorophyll after either MV or H2O2 treatment compared with EV leaves. Thus, SERF1 is a positive regulator of oxidative stress tolerance. SERF1 overexpression lines showed enhanced expression of DREB2A, AP37, ZFP179, ZFP182, ZFP252, SNAC1, SNAC2, and NAC5 under control conditions[1].
Localization
Although SERF1 does not contain a known nuclear localization signal, stable transformation of rice plants with a construct encoding a CFP-tagged version of SERF1 revealed nuclear localization of SERF1 in leaf epidermal cells (Figure 1C)[1].
Evolution
- The rice genome encodes 15 group II ERF genes of the DREB subfamily, which can be subdivided into three classes. SERF1 belongs to group IIc ERFs, which lack both the EAR motif and CMII-3 motif found in members of the groups IIa and IIb (Nakano et al., 2006)[4].
- The corresponding proteins share a highly conserved AP2 DNA binding domain, the C terminus of SERF1 bears two conserved predicted helical structures(H1 and H2), of which the latter is only found in monocots. One of the two SERF1 homologs in Arabidopsis is a potential MAPK phosphorylation target[5], suggesting that SERF1 might represent a target of a rice MAPK cascade.[1].
Knowledge Extension
- In summary, Schmidt et al. discovered an H2O2-mediated molecular signaling cascade important for the initial response to salinity in rice (Figure 2). SERF1 is a phosphorylation target of a salt-responsive MAPK, thereby promoting the expression of MAPK cascade genes (MAPK5 and MAP3K6), salt tolerance–mediating TF genes (ZFP179 and DREB2A), and itself through direct interaction with the corresponding promoters in planta.
- In essence, salt stress results in a wave of H2O2 production[6] that activates SERF1 through the MAPK pathway. Posttranslational regulation of H2O2-dependent SERF1 expression is consistent with the observation that ROS signals occur rapidly during environmental changes[6][7].
- This first ROS wave is propagated at the transcriptional level through SERF1. However, as the transcriptional activity of SERF1 is modulated by phosphorylation, only a persistent salt stress signal will further boost the expression of target genes. In such a scenario, a transient stress can be sensed rapidly, and activation of stress genes is stopped before full activation of the acclimation program. Among the plant transcription factors, ethylene response factor (ERF) is one of the largest subfamilies of Apetala2 (AP2)/ERF transcription factor family and is characterized with single AP2 domain. ERFs are a double-edged sword; though most of the ERFs are activators of stress-responsive genes, certain ERF could act as repressor[1][8].
The expression of ERFs may be ethylene dependent or independent and is regulated by feedback mechanism. Apart from above regulation mechanism, expressions of ERFs are post-transcriptionally regulated by microRNAs (miRNAs), and miRNA expressions are in turn regulated by ERFs[8].
Labs working on this gene
- Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany
- Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany
- Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche, Genetic Improvement and Adaptation of Mediterranean and Tropical Plants, 34398 Montpellier, cedex 5, France
- Department of Molecular Genetics, Centre for Research in Agricultural Genomics, Consejo Superior de Investigaciones Científicos, Institute of Agro-food Research and Technology, Autonomus University of Barcelona, University of Barcelona, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
References
- ↑ 1.00 1.01 1.02 1.03 1.04 1.05 1.06 1.07 1.08 1.09 1.10 1.11 1.12 Schmidt R, Mieulet D, Hubberten H M, et al. SALT-RESPONSIVE ERF1 regulates reactive oxygen species–dependent signaling during the initial response to salt stress in rice[J]. The Plant Cell Online, 2013, 25(6): 2115-2131.
- ↑ 2.0 2.1 2.2 Schmidt R, Caldana C, Mueller-Roeber B, et al. The contribution of SERF1 to root-to-shoot signaling during salinity stress in rice[J]. Plant signaling & behavior, 2014, 9(1): e27540.
- ↑ 3.0 3.1 3.2 Schmidt R, Schippers J H M, Mieulet D, et al. SALT-RESPONSIVE ERF1 is a negative regulator of grain filling and gibberellin-mediated seedling establishment in rice[J]. Molecular plant, 2013: sst131.
- ↑ Nakano T, Suzuki K, Fujimura T, et al. Genome-wide analysis of the ERF gene family in Arabidopsis and rice[J]. Plant physiology, 2006, 140(2): 411-432.
- ↑ Popescu S C, Popescu G V, Bachan S, et al. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays[J]. Genes & development, 2009, 23(1): 80-92.
- ↑ 6.0 6.1 Mittler R, Vanderauwera S, Suzuki N, et al. ROS signaling: the new wave?[J]. Trends in plant science, 2011, 16(6): 300-309.
- ↑ Hong C Y, Chao Y Y, Yang M Y, et al. NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid[J]. Plant and soil, 2009, 320(1-2): 103-115.
- ↑ 8.0 8.1 Thirugnanasambantham K, Durairaj S, Saravanan S, et al. Role of Ethylene Response Transcription Factor (ERF) and Its Regulation in Response to Stress Encountered by Plants[J]. Plant Molecular Biology Reporter, 2014: 1-11.