Updated Mechanisms of GCN5—The Monkey King of the Plant Kingdom in Plant Development and Resistance to Abiotic Stresses
<p>The roles and mechanisms of GCN5 in plant growth and development. In <span class="html-italic">Arabidopsis</span>, GCN5 plays different roles in the whole life cycle through different pathways. First, GCN5 interacts with ADA2b as a complex to regulate <span class="html-italic">SPL3/SPL9</span> directly through histone acetylation to involve the juvenile-to-adult vegetative phase, which is independent of the pathway of <span class="html-italic">miRNA156</span>-<span class="html-italic">SPLs</span> action. Interestingly, GCN5 also regulates <span class="html-italic">pri-miR156a</span> expression positively. Then, a module made of GCN5, TAF1, and HD1 contributes to the photomorphogenesis and vegetative development of plants through delicate histone acetylation regulation, in which GCN5 and TAF1 function synergistically, and HD1 functions oppositely with them. HY5, the key photomorphogenesis factor is responsible for the recruitment of GCN5 and TAF1 in different ways. GCN5 interacts with HY5 genetically and functions in the same way in morphogenesis regulation. While TAF1 functions synergistically with HY5. <span class="html-italic">RBCS-1A</span>, <span class="html-italic">CAB2</span>, and <span class="html-italic">IAA3</span> play different roles as target genes of histone acetyltransferase and histone deacetylase in this pathway. For root meristem development, GCN5, together with ADA2b, can increase transcripts of <span class="html-italic">PLT1</span> and <span class="html-italic">PLT2</span> by histone acetylation regulation to adjust the stem cells meristem, furthermore, ADA2b also functions independently of GCN5 to affect the stem cell niche maintenance. In rice, WOX11 can interact with ADA2b to recruit the GCN5 associated histone acetyltransferase complex and together regulate downstream <span class="html-italic">PIN9</span>, <span class="html-italic">CSLF6</span>, and other genes to facilitate the crown root meristem development. In trichome development, the GCN5-ADA2b complex regulates core genes <span class="html-italic">GL1</span>, <span class="html-italic">GL2,</span> and <span class="html-italic">GL3</span> through histone acetylation modifications to mediate trichome initiation and branching. In the stem cuticular wax formation, GCN5 regulates the <span class="html-italic">ECERIFERUM3</span> transcription by histone acetylation to influence cuticle membrane and wax biosynthesis. Considering the flowering, GCN5 and CLAVATA 1 regulate AG-WUS through direct histone acetylation modification to involve several floral organ developments synergistically, but the relationship between GCN5 and CLAVATA 1 is still unclear. However, it is unknown whether GCN5 affects seed development or germination associated traits. The images on the circle represent the different organs and developmental stages of <span class="html-italic">Arabidopsis thaliana</span>. GCN5 is indicated in the pink oval. The black arrows indicate active regulation, and the red bars indicate inhibition. The straight line represents the direct interaction, and the dashed line represents the indirect action. The histone acetylation modifications are represented with a graphic histone binding with the acetyl group (a red circle).</p> "> Figure 2
<p>The mechanisms of GCN5 in plant hormone biosynthesis and secondary metabolic pathways. (<b>A</b>) When ethylene is absent, GCN5 and CLV1 are involved in ethylene signaling through regulating some key genes transcription (e.g., <span class="html-italic">ERS1</span>, <span class="html-italic">ERF1</span>, <span class="html-italic">EBF2</span>, <span class="html-italic">CTR1</span>) by histone acetylation, which is dependent on the EIN3 factor; meanwhile, GCN5 and CLV1 also mediate <span class="html-italic">IAA3</span> and auxin signaling synergistically, proposing the crosslink between ethylene and auxin. But GCN5 and CLV1 show antagonistic actions on the histone acetylation of H3K9/14, which results in the up-regulation of <span class="html-italic">ERS1</span>, <span class="html-italic">ERF1</span>, <span class="html-italic">EBF2</span>, <span class="html-italic">CTR1</span> in the <span class="html-italic">clv1-1 gcn5-1</span> double mutant. Moreover, EIN3 can directly bind the promoters of <span class="html-italic">ERF1</span> and <span class="html-italic">EBF2</span> to control their transcription too (black curved arrow). (<b>B</b>) GCN5 regulates downstream targets <span class="html-italic">MYC2</span>, <span class="html-italic">DND2</span>, and <span class="html-italic">WRKY33</span> expression through histone acetylation, which inhibits the SA synthesis and accumulation; on the other hand, GCN5 mediates SA synthesis through an unidentified pathway independent of NahG and ICS1 to participate in SA-mediated plant immunity. (<b>C</b>) GCN5 can mediate the histone acetylation level of <span class="html-italic">GTL1</span> to affect its transcription and the associated cellulose synthesis. (<b>D</b>) In fatty acid synthesis, GCN5 can directly regulate histone acetylation of <span class="html-italic">FAD3</span> and others (e.g., <span class="html-italic">LACS2</span>, <span class="html-italic">LPP3</span>) to mediate their transcription expression, and involve the different steps of fatty acid synthesis and accumulation. DAG, diacyl glycerol; TAG, triglyceride. GCN5 is indicated in the pink oval. The black arrows indicate active regulation, and the red bars indicate inhibition. The straight line represents the direct action, and the dashed line represents the indirect action. The histone acetylation modifications are represented with a graphic histone binding with the acetyl group (a red circle).</p> "> Figure 3
<p>Underlying mechanisms of GCN5 in response to abiotic stresses and miRNA generation. (<b>A</b>) In response to heat stress, GCN5 directly functions on two key transcriptional factors HSFA3 and UVH6 encoding genes by histone acetylation modifications to activate their transcription, in turn, activating some heat shock protein functions and mediating plant heat resistance. (<b>B</b>) Encountering cold stress, CBFs recruit GCN5 and ADA2b through the DNA binding domain to activate its expression, then bind the <span class="html-italic">CRT</span> elements in the key genes <span class="html-italic">COR</span> promoter and promote transcription and increase the plant resistance to low-temperature stresses. However, the detailed mechanisms of interaction among GCN5, ADA2b, and CBFs are unclear. (<b>C</b>) In response to salt stress, GCN5 is up-regulated to promote the expression of downstream genes of <span class="html-italic">PGX3</span>, <span class="html-italic">CTL1</span>, <span class="html-italic">MYB54</span> through histone acetylation, in turn, to increase salt stress tolerance. (<b>D</b>) In iron deficiency, GCN5 regulates directly the histone acetylation of <span class="html-italic">FRD3</span>, <span class="html-italic">EXO70H2</span>, and <span class="html-italic">BOR1</span> to promote their expression, which in turn facilitates synthesis, transport, and homeostasis maintenance of iron in the cell. (<b>E</b>) In response to phosphate starvation, a long non-coding RNA (lncRNA) <span class="html-italic">AT4</span> is up-regulated and identified as a target of GCN5 through histone H3 acetylation modifications, then downstream <span class="html-italic">miR399</span> and its target <span class="html-italic">PHOSPHATE2</span> is repressed and promoted respectively to mediate phosphate proper distribution. (<b>F</b>) GCN5 is involved in the miRNA production by regulating the miRNA machinery <span class="html-italic">AGO1</span> and <span class="html-italic">DCL1</span> indirectly. Further, it can also regulate some miRNA genes directly by histone acetylation modifications. GCN5 is indicated in the pink oval. The black arrows indicate active regulation, and the red bars indicate inhibition. The straight line represents the direct action, and the dashed line represents the indirect action. The histone acetylation modifications are represented with a graphic histone binding with the acetyl group (a red circle).</p> "> Figure 4
<p>The molecular mechanisms of GCN5 involved in abiotic and biotic stresses on the genomic level. On the genomic level, the SAGA complex associated with GCN5 exerts dual and opposite effects on H3K14Ac level at the 5′ and 3′ ends of target genes as well as a positive role on H3K9Ac. Generally, the positive (e.g., <span class="html-italic">COR</span>) and negative (e.g., <span class="html-italic">CNGC12</span>, <span class="html-italic">AtHIR1</span>, and <span class="html-italic">WRKY57</span>) regulated genes are correlated with abiotic and biotic stress responses, respectively.</p> ">
Abstract
:1. Introduction
2. Roles and Mechanisms of GCN5 in Plant Growth and Development
2.1. Molecular Mechanisms of GCN5 Involved in Plant Vegetative Growth
2.2. Underlying Mechanisms of GCN5 Regulating Root Meristem
2.3. Underlying Mechanisms of GCN5 Regulating Shoot Meristems in Reproductive Growth
2.4. Mechanisms of GCN5 Mediating Trichome Development
2.5. Mechanisms of GCN5 Contributing to Stem Cuticular Wax Formation
3. The Mechanisms of GCN5 in Plant Hormonal and Secondary Metabolic Pathways
3.1. The Mechanisms of GCN5 Involved in Crosstalk of Ethylene and Auxin Pathways
3.2. Mechanisms of GCN5 Involved in the Regulation of Salicylic Acid
3.3. Mechanisms of GCN5 Involved in Cellulose Synthesis
3.4. Mechanisms of GCN5 in Fatty Acid Synthesis
4. Mechanisms of GCN5 Involved in Resistance to Abiotic Stresses
4.1. Mechanisms of GCN5 on Heat and Drought Stress Resistance
4.2. Effect and Mechanism of GCN5 on Cold Stress Tolerance
4.3. Mechanisms of GCN5 in Salt Stress Tolerance Reactions of Plants
4.4. Role and Mechanism of GCN5 in Mediating Iron Homeostasis in Plant
4.5. Mechanism of GCN5 Involved in Phosphate Starvation Response
5. Mechanism of GCN5 Involved in MiRNA Generation
6. Global Analysis of Binding Sites and Gene Expression Associated with GCN5 by Genome-Wide Approaches
7. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Name | Relationship to GCN5 | Gene Locus | Annotation | References | Developmental Events or Pathways |
---|---|---|---|---|---|
ADA2b | Synergy and PPI | AT4G16420 | HOMOLOG OF YEAST ADA2 2B | [8] | Constitutive and structural |
TAF1 | Indirect interaction | AT3G19040 | TBP-ASSOCIATED FACTOR 1 with histone acetyltransferase activity | [3] | Photomorphogenesis |
HD1 | Indirect interaction | AT4G38130 | Histone deacetylase 1, | [22] | |
HY5 | Indirect interaction | AT5G11260 | transcriptional activator of light signaling transcriptional activator of light signaling transcriptional activator of light signaling transcriptional activator of light signaling ELONGATED HYPOCOTYL 5, | [14] | |
CLV1 | Synergy/ Indirect interaction | AT1G75820 | CLAVATA1, transmembrane receptor kinase with an extracellular leucine-rich domain. | [33,47] | Shoot and root meristem |
WOX11 | Indirect interaction | Os07g48560 | WUSCHEL-related homeobox gene family | [30] | |
CBF1 | Synergy and PPI | AT4G25490 | C-REPEAT/DRE BINDING FACTOR 1, cold-induced transcription factor | [10] | Abiotic stress response |
AREB1 | PPI | Potri.002G125400 | ABA-Responsive Element Binding | [70] |
Gene Name | Relationship to GCN5 | Gene Locus | Annotation | References | Developmental Events or Pathways |
---|---|---|---|---|---|
mir156 | – | AT2G25095/ AT5G11977 | Micro RNA156 | [16,19] | Vegetative development and Photomorphogenesis |
SPL3 | Direct downstream target | AT2G33810 | SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 3 | [16] | |
SPL8 | Direct downstream target | AT1G02065 | SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 8 | [16] | |
SPL9 | Direct downstream target | AT2G42200 | SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 | [16] | |
IAA3 | Direct downstream target | AT1G04240 | INDOLE-3-ACETIC ACID INDUCIBLE 33 | [22] | |
RBCS-1A | Direct downstream target | AT1G67090 | RIBULOSE BISPHOSPHATE CARBOXYLASE SMALL CHAIN 1A | [22] | |
AG | Direct downstream target | AT4G18960 | AGAMOUS | [32,33] | Shoot and root meristem development |
WUS | Direct downstream target | AT2G17950 | WUSCHEL | [32,33] | |
PLT2 | Direct downstream target | AT1G51190 | PLETHORA2, key stem cell transcription factors | [29] | |
OsPIN9 | Direct downstream target | LOC_Os01g58860 | PIN-FORMED9, encodes an auxin efflux carrier | [30] | |
OsCSLF6 | Direct downstream target | LOC_Os08g06380 | CELLULOSE SYNTHASE-LIKE F6 | [30] | |
Os1BGLU5 | Direct downstream target | LOC_Os01g70520 | Beta-glucosidase homologue | [30] | |
GL1 | Direct downstream target | AT3G27920 | GLABRA1, core trichome initiation regulator genes | [37] | Trichome development |
GL2 | Direct downstream target | AT1G79840 | GLABRA2, core trichome initiation regulator genes | [37] | |
GL3 | Direct downstream target | AT5G41315 | GLABRA3, core trichome initiation regulator genes | [37] | |
DCL1 | Direct downstream target | AT1G01040 | DICER-LIKE 1, miRNA maturation | [20,84] | MiRNA generation and regulation |
SE | Direct downstream target | AT1G27100 | Zinc-finger domain protein SERRATE | [20,85] | |
HYL1 | Direct downstream target | AT1G09700 | HYPONASTIC LEAVES 1 | [20,88] | |
AGO1 | Direct downstream target | AT1G48410 | ARGONAUTE 1, an RNA Slicer that selectively recruits microRNAs and siRNA | [20,86] | |
CTL1 | Direct downstream target | AT1G05850 | CHITINASE-LIKE 1 gene, | [56] | Lipid metabolism, cell wall and oil composition |
FAD3 | Direct downstream target | AT2G29980 | FATTY ACID DESATURASE 3 | [62] | |
CER3 | Direct downstream target | AT5G57800 | ECERIFERUM3 | [41] | |
LACS2 | Direct downstream target | AT1G49430 | LONG-CHAIN ACYL-COA SYNTHETASE 2 | [62] | |
LPP3 | Direct downstream target | AT3G02600 | LIPID PHOSPHATE PHOSPHATASE 3 | [62] | |
PLAIIIb | Direct downstream target | AT3G54950 | PATATIN-RELATED PHOSPHOLIPASE IIIBETA | [62] | |
EIN3 | Direct downstream target | AT3G20770 | ETHYLENE INSENSITIVE 3 | [47] | Phytohormone and abiotic stresses response |
miR399 | Indirect | AT2G34202 | Stress response | [12] | |
HSFA3 | Direct downstream target | AT5G03720 | Heat Stress Transcription Factor3 | [9] | |
UVH6 | Direct downstream target | AT1G03190 | ULTRAVIOLET HYPERSENSITIVE 6 | [9] | |
MYB54 | Direct downstream target | AT1G73410 | MYB DOMAIN PROTEIN 54 | [57] | |
PGX3 | Direct downstream target | AT1G48100 | POLYGALACTURONASE INVOLVED IN EXPANSION3 | [57] | |
AT4 | Direct downstream target | AT5G03545 | Long non-coding RNA, response to phosphate starvation | [12,91] | |
FRD3 | Direct downstream target | AT3G08040 | FERRIC REDUCTASE DEFECTIVE3 | [62] | |
PtrNAC006 | Direct downstream target | Potri.002G081000 | NAC (NAM, no apical meristem) DOMAIN CONTAINING PROTEIN 006 | [70] | |
PtrNAC007 | Direct downstream target | Potri.007G099400 | NAC DOMAIN CONTAINING PROTEIN 007 | [70] | |
PtrNAC120 | Direct downstream target | Potri.001G404100 | NAC DOMAIN CONTAINING PROTEIN 120 | [70] |
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Gan, L.; Wei, Z.; Yang, Z.; Li, F.; Wang, Z. Updated Mechanisms of GCN5—The Monkey King of the Plant Kingdom in Plant Development and Resistance to Abiotic Stresses. Cells 2021, 10, 979. https://doi.org/10.3390/cells10050979
Gan L, Wei Z, Yang Z, Li F, Wang Z. Updated Mechanisms of GCN5—The Monkey King of the Plant Kingdom in Plant Development and Resistance to Abiotic Stresses. Cells. 2021; 10(5):979. https://doi.org/10.3390/cells10050979
Chicago/Turabian StyleGan, Lei, Zhenzhen Wei, Zuoren Yang, Fuguang Li, and Zhi Wang. 2021. "Updated Mechanisms of GCN5—The Monkey King of the Plant Kingdom in Plant Development and Resistance to Abiotic Stresses" Cells 10, no. 5: 979. https://doi.org/10.3390/cells10050979