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Functional analyses of plant-specific histone deacetylases : Their role in root development, stress responses and symbiotic interactions

  • Li, Huchen
Publication Date
Jan 01, 2017
Wageningen University and Researchcenter Publications
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<p>Plants have a sessile lifestyle. To ensure survival, they develop a potential to respond to environmental cues to set up an adaptive growth and development. This adaptation involves transcriptional reprogramming of the genome through chromatin-based mechanisms relying on the dynamic interplay of transcription factors (TFs), post-translational modification of histones, the deposition of histone variants, DNA methylation, and nucleosome remodeling. This thesis is focused on a role of one group of histone post-translational modifiers, plant-specific histone deacetylases (HDTs), in plant development under control condition and variable stresses/symbiotic interactions.</p> <p>It is well known that HDTs are involved in plant responses to environmental stresses. However, whether they play a role in regulating plant growth and development is elusive. In this thesis it is shown that <em>Arabidopsis thaliana</em> AtHDT1/2 regulate the cell fate switch from division to expansion in the Arabidopsis root. Knock-down of <em>AtHDT1/2</em> (<em>hdt1,2i</em>) causes that this switch occurs earlier and results in less cells in the root meristem. This process slows down root growth. One target of AtHDT1/2, <em>AtGA2ox2,</em> is identified here. Its overexpression displays the same root phenotype as <em>hdt1/2i</em> , and its knock-out partially rescues <em>hdt1,2i</em> root meristem phenotype. AtGA2ox2 inactivates gibberellin (GA4) whose application increases root meristem cell number in WT, but not in <em>hdt1,2i</em>. Based on these data, we conclude that AtHDT1/2 repress the transcription of <em>AtGA2ox2</em>, and likely fine-tunes GA homeostasis to regulate the switch from cell division to expansion in root tips.</p> <p>HDTs respond to salt stress in Arabidopsis seedlings. Halotropism is a novel reported tropism allowing roots to avoid a saline environment. Whether the AtHDT1/2-<em>AtGA2ox2</em> module is operational in halotropism is studied here. We show that <em>hdt1,2i</em> mutants respond more severe in halotropism. AtHDT1/2, as well as <em>AtGA2ox2</em> display asymmetric localization patterns in halotropism with AtHDT1/2 reduced and <em>AtGA2ox2</em> induced at high salt side of root tips. Our data indicate that their asymmetric patterns likely results in less GA at high salt side of root tips and this is required for halotropism establishment. In line with this, both constitutive expression of <em>AtHDT2</em> and exogenous GA application reduce halotropic response. A reduction of GA in root tips causes an earlier switch from cell division to expansion. We discuss that this earlier switch enables roots rapidly to bend away from saline environment.</p> <p>It has been shown that HDTs play a role under biotic stress in rice and tobacco leaves. We demonstrate that they are also involved in response to biotic stress in Arabidopsis leaves. Arabidopsis <em>hdt2</em> mutants are more susceptible to virulent<em> Pseudomonas syringae</em> pv. tomato <em>PstDC3000</em>, whereas <em>AtHDT2</em> overexpression mutants are more resistant. In addition, we detected a translocation of AtHDT2 from nucleolus to nucleoplasm after the perception of flagellin22 in Arabidopsis leaf cells. This translocation is not observed under abiotic stress. A mechanism controlling this translocation is identified. AtMPK3 is activated under biotic stress, it interacts with and phosphorylates AtHDT2. This leads to the accumulation of AtHDT2 in nucleoplasm where it contributes to the repression of defense genes.</p> <p>During the interaction with symbiotic microorganisms, plants could develop a symbiotic organ/structure. For example, legumes of which <em>Medicago truncatula</em> is a model, can form root nodules or arbuscules by interacting with rhizobia or arbuscular mycorrhiza.</p> <p>We show that nodule-specific knock-down of <em>MtHDT1/2/3</em> (<em>MtHDTs RNAi</em>) blocks nodule primordia development and affects the function of nodule meristem. This is consistent with their roles in controlling cell division during root development and suggests that the function of nodule and root meristems is closely related. However, MtHDT2 gains a new sub-nuclear localization pattern in nodule meristem by using a not yet known mechanism, different from that in root meristem. This suggests that these two meristems have different transcriptional landscapes. In the nodule infection zone <em>MtHDTs </em>are also expressed and in <em>MtHDTs RNAi</em> the intracellular release of rhizobia is markedly reduced. Expression of <em>MtHMGR1</em> and its paralogs, encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductases are down-regulated in <em>MtHDTs RNAi</em>. It has been shown MtHMGR1 interacts with MtDMI2, a component of Nod factor signalling pathway, to control rhizobial infection. Knock-down of <em>MtHMGR1/MtDMI2</em>, as well as inhibiting MtHMGRs enzymatic activity blocks nodule primordia development and rhizobial infection in nodule primordia/mature nodules. This phenotype partially resembles <em>MtHDTs RNAi</em> phenotype. We discuss tha<em>t </em>MtHDTs regulate expression of <em>MtHMGRs</em> and in this way affect Nod factor signalling and control nodule development.</p> <p>Similar to nodule symbiosis, during arbuscular mycorrhizal symbiosis cells in the cortex are also intracellularly infected. We show that <em>MtHDT2</em> is also induced in these arbuscule containing cells. Knock-down of <em>MtHDT2</em> (<em>MtHDT2i</em>) significantly reduces the intracellular infection of the hyphae on the mycorrhized root segments, indicating that MtHDT2 control mycorrhizal intracellular infection. We discuss whether MtHDTs can regulate mycorrhizal/rhizobial infection in a similar way.</p> <p>The data obtained in this thesis and the published information related to these subjects are discussed at the end. HDTs are key players in plant responses to environmental cues, whereas they respond to abiotic factors and biotic factors differently. They are also key regulators of plant growth and development that is clearly demonstrated in this thesis on examples of root and nodule development. I also propose a role of AtHDT1/2 in response to salt signal to fine-tune the switch from cell division to expansion in root tips during halotropism.</p>

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