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Highly ABA-Induced 1 (HAI1)-Interacting protein HIN1 and drought acclimation-enhanced splicing efficiency at intron retention sites
Monday, 2019/11/04 | 08:07:57

Geeng Loo Chong, Mung Hsia Foo, Wen-Dar Lin, Min May Wong, and Paul E. Verslues

PNAS October 29, 2019 116 (44) 22376-22385


The ability of plants to acclimate and maintain productivity under changing environmental conditions is a topic of heightened concern because of climate change and increasing demands on agriculture. Plant stress acclimation involves multiple layers of gene regulation and posttranslational protein modifications. Pre-mRNA splicing patterns are greatly altered by stress, yet little is known about how stress signaling impinges upon the splicing machinery to mediate such changes. We found that one of the key stress signaling protein phosphatases can interact with and dephosphorylate a newly identified splicing regulator. This splicing regulator promotes growth during moderate-severity drought stress and mediates a dramatic shift toward increased splicing efficiency of stress and signaling-related genes which are prone to intron retention.


The Highly ABA-Induced 1 (HAI1) protein phosphatase is a central component of drought-related signaling. A screen for HAI1-interacting proteins identified HAI1-Interactor 1 (HIN1), a nuclear protein of unknown function which could be dephosphorylated by HAI1 in vitro. HIN1 colocalization and interaction with serine-arginine rich (SR) splicing factors and appearance of nuclear speckle-localized HIN1 during low water potential (ψw) stress suggested a pre-mRNA splicing-related function. RNA sequencing of Arabidopsis Col-0 wild type identified more than 500 introns where moderate severity low ψw altered intron retention (IR) frequency. Surprisingly, nearly 90% of these had increased splicing efficiency (decreased IR) during stress. For one-third of these introns, ectopic HIN1 expression (35S:HIN1) in unstressed plants mimicked the increased splicing efficiency seen in stress-treated wild type. HIN1 bound to a GAA-repeat, Exonic Splicing Enhancer-like RNA motif enriched in flanking sequence around HIN1-regulated introns. Genes with stress and HIN1-affected splicing efficiency were enriched for abiotic stress and signaling-related functions. The 35S:HIN1 plants had enhanced growth maintenance during low ψw, while hin1 mutants had reduced growth, further indicating the role of HIN1 in drought response. HIN1 is annotated as an MYB/SANT domain protein but has limited homology to other MYB/SANT proteins and is not related to known yeast or metazoan RNA-binding proteins or splicing regulators. Together these data identify HIN1 as a plant-specific RNA-binding protein, show a specific effect of drought acclimation to promote splicing efficiency of IR-prone introns, and also discover HAI1–HIN1 interaction and dephosphorylation that connects stress signaling to splicing regulation.


See https://www.pnas.org/content/116/44/22376

Figure 1:

HIN1 interacts with HAI1 as well as other Clade A PP2Cs and can be dephosphorylated by HAI1. (A) HAI1–HIN1 and HAI1–LIMYB interaction in yeast 2-hybrid assays. Colony lifts after β-galactosidase staining are shown. Strong, weak, and negative control interaction pairs provided with the ProQuest yeast 2-hybrid system were included for comparison. PYL10 was included as a positive control for HAI1 interaction. All interaction pairs showed consistent results in repeated assays. F.L., full length; E.V., empty vector. (B) Coimmunoprecipitation of YFP-tagged HAI1 and MYC-tagged HIN1. Both constructs were transiently expressed in Avr-PTO expressing Arabidopsis seedlings and immunoprecipitation performed 48 h after transfer of seedlings to fresh control plates (Cont.) or stress (−1.2 MPa) plates. Co-IP assays were also done with YFP-tagged EGR1 (a Clade E PP2C) as a negative control (SI Appendix, Fig. S1D), and both sets of assays included mock IP assays with untransformed Avr-PTO seedlings as a further negative control. IN, input; IP, immunoprecipitated sample. Results shown are representative of several replicate experiments. (C) Ratiometric BiFC quantification of relative interaction intensity (ratio of YFP fluorescence to that of the RFP reporter contained in the same vector). Experiments were performed by transient expression in Avr-PTO seedlings. After infiltration, seedlings were transferred to fresh control plates or to −1.2-MPa plates for 48 h before YFP and RFP fluorescence was quantified in individual cells. Data are means ± SE, n = 20 combined from 2 to 3 independent experiments. (D) Representative images of rBiFC assays reported in C. In all cases, interaction was observed in the nucleus. Arrows in the HAI/HIN1 YFP images show example of nuclei having faint HAI1–HIN1 interaction in the unstressed control or example of nuclei where the HAI1–HIN1 interaction was observed as nuclear speckles. Representative images of other interaction pairs are shown in SI Appendix, Fig. S2. (Scale bars, 20 μm.) (E) In vitro dephosphorylation assays. YFP-HIN1 immunoprecipitated from 35S:YFP-HIN1 plants in control and stress (−0.7 MPa, 96 h) treatments was dephosphorylated using Calf Intestinal Phosphatase (C.I.P.) or recombinant HAI1 (5 μg). Aliquots of the same samples were run on Phos-tag gel (Top) and SDS/PAGE (Bottom). Both blots were probed with antisera recognizing YFP. Red numbers along the left of the blots indicate phosphorylated forms of HIN1. The expected molecular weight of YFP-HIN1 is 81 kDa. The experiment was repeated with consistent results.

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