SDG8-Mediated Histone Methylation and RNA Processing Function in the Response to Nitrate Signaling

Li, Ying; Brooks, Matthew D.; Yeoh-Wang, Jenny; McCoy, Rachel M.; Rock, Tara M.; Pasquino, Angelo; Moon, Chang In; Patrick, Ryan M.; Tanurdžić, Miloš; Ruffel, Sandrine; Widhalm, Joshua R.; McCombie, W. Richard; Coruzzi, Gloria M.

doi:10.1104/pp.19.00682

Cited by 26 publications

(25 citation statements)

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“…Thus, the relationship between the levels of H3K36me3 and transcription does not seem to be absolute in Arabidopsis, and depends on the preponderance of different parameters, such as signaling molecules like SA. Therefore, predicting the transcriptional output from changes in H3K36 methylation seems at certain genes very uncertain and even more complex when considering recent findings involving SDG8 and H3K36 methylation in others gene regulatory mechanisms such as RNA processing and splicing (Pajoro et al, 2017;Li et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Four HKMTs, exclusively from the TrxG group were so far reported to directly or indirectly contribute to the regulation of plant immunity, with their corresponding mutant being more susceptible to some pathogens (Alvarez-Venegas et al, 2007;Berr et al, 2010;Palma et al, 2010;De-La-Peña et al, 2012;Xia et al, 2013;Lee et al, 2016). Among them, the H3K36 di-and tri-methyltransferase SET DOMAIN GROUP 8 (SDG8) was involved in many biological processes, including the regulation of flowering time, organ growth, ovule and anther development, seed development, carotenoid biosynthesis, brassinosteroid-regulated gene expression, light-and/or carbonresponsive gene expression and RNA processing in response to temperature or nitrate signaling (Soppe et al, 1999;Zhao et al, 2005;Dong et al, 2008;Xu et al, 2008;Cazzonelli et al, 2009b;Grini et al, 2009;Tang et al, 2012;Li et al, 2019). Regarding plant immunity, SDG8-mediated H3K36me3 was reported as being crucial for the transcriptional induction of a subset of JA/ET-inducible genes upon infection by necrotrophic fungi (Berr et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Arabidopsis SDG8 Potentiates the Sustainable Transcriptional Induction of the Pathogenesis-Related Genes PR1 and PR2 During Plant Defense Response

et al. 2020

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Post-translational covalent modifications of histones play important roles in modulating chromatin structure and are involved in the control of multiple developmental processes in plants. Here we provide insight into the contribution of the histone lysine methyltransferase SET DOMAIN GROUP 8 (SDG8), implicated in histone H3 lysine 36 trimethylation (H3K36me3), in connection with RNA polymerase II (RNAPII) to enhance Arabidopsis immunity. We showed that even if the sdg8-1 loss-of-function mutant, defective in H3K36 methylation, displayed a higher sensitivity to different strains of the bacterial pathogen Pseudomonas syringae, effector-triggered immunity (ETI) still operated, but less efficiently than in the wild-type (WT) plants. In sdg8-1, the level of the plant defense hormone salicylic acid (SA) was abnormally high under resting conditions and was accumulated similarly to WT at the early stage of pathogen infection but quickly dropped down at later stages. Concomitantly, the transcription of several defense-related genes along the SA signaling pathway was inefficiently induced in the mutant. Remarkably, albeit the defense genes PATHOGENESIS-RELATED1 (PR1) and PR2 have retained responsiveness to exogenous SA, their inductions fade more rapidly in sdg8-1 than in WT. At chromatin, while global levels of histone methylations were found to be stable, local increases of H3K4 and H3K36 methylations as well as RNAPII loading were observed at some defense genes following SA-treatments in WT. In sdg8-1, the H3K36me3 increase was largely attenuated and also the increases of H3K4me3 and RNAPII were frequently compromised. Lastly, we demonstrated that SDG8 could physically interact with the RNAPII C-terminal Domain, providing a possible link between RNAPII loading and H3K36me3 deposition. Collectively, our results indicate that SDG8, through its histone methyltransferase activity and its physical coupling with RNAPII, participates in the strong transcriptional induction of some defense-related genes, in particular PR1 and PR2, to potentiate sustainable immunity during plant defense response to bacterial pathogen.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Arabidopsis SDG8 Potentiates the Sustainable Transcriptional Induction of the Pathogenesis-Related Genes PR1 and PR2 During Plant Defense Response

et al. 2020

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“…It was hypothesized that SDG8-mediated placement of H3K36me3 affects transcriptional elongation or RNA processing. Following up on this, Li et al (2020) demonstrate that H3K36me3 placement is influenced by nitrogen availability and regulates the production of transcript isoforms, including the full-length isoform of CCT101 (a CONSTANS, CO-like, and TOC1 motif protein). Nitrogen depletion or the loss of SDG8 activity through mutation lowers H3K36me3 on nucleosomes within the CCT101 gene body and is associated with the production of a truncated RNA isoform, demonstrating that chromatin marks influence 39-end processing.…”

Section: Histone Modifications and 39-end Processingmentioning

confidence: 90%

The Dynamic Kaleidoscope of RNA Biology in Plants

2020

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ACKNOWLEDGMENTSWe thank all of the authors, reviewers, and editors, especially Sarah M. Assmann, who contributed to this Focus Issue. We thank Thanin Chantarachot and Sarah M. Assmann for comments on this editorial. LITERATURE CITEDArribas-Hernández L, Brodersen P (2020) Occurrence and functions of m 6 A and other covalent modifications in plant mRNA. Plant Physiol 182: 79-96 Bai B, van der Horst S, Cordewener J, America T, Hanson J, Bentsink L (2020) Seed stored mRNAs that are specifically associated to monosome are translationally regulated during germination. Plant Physiol 182: 378-392 Beck J, Lohscheider JN, Albert S, Andersson U, Mendgen KW, Rojas-Stütz MC, Adamska I, Funck D (2017) Small one-helix proteins are essential for photosynthesis in Arabidopsis. Front Plant Sci 8: 7 Bentley DL (2005) Rules of engagement: Co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol 17: 251-256 Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16: 727-741 Browning KS, Bailey-Serres J (2015) Mechanism of cytoplasmic mRNA translation. The Arabidopsis Book 13: e0176 Cao Y, Ma L (2019) To splice or to transcribe: SKIP-mediated environmental fitness and development in plants. Front Plant Sci 10: 1222 Chantarachot T, Bailey-Serres J (2018) Polysomes, stress granules, and processing bodies: A dynamic triumvirate controlling cytoplasmic mRNA fate and function. Plant Physiol 176: 254-269 Chaudhary S, Khokhar W, Jabre I, Reddy ASN, Byrne LJ, Wilson CM, Syed NH (2019) Alternative splicing and protein diversity: Plants versus animals. Front Plant Sci 10: 708 Crisp PA, Hammond R, Zhou P, Vaillancourt B, Lipzen AM, Daum C, Barry KW, de Leon N, Buell CR, Kaeppler SM, et al (2020) Variation and inheritance of small RNAs in maize inbreds and F1 hybrids. Plant

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“…The chromatin factor HNI9 (high nitrogen-insensitive 9), a conserved component of RNA polymerase II complex, is shown to suppress the AtNRT2.1 expression via histone H3 lysine 27 tri-methylation (H3K27me3) modifications under high N conditions (Widiez et al 2011). The sdg8-5 mutant that lacks histone methyltransferase SDG8 exhibits not only impaired regulation of ASN1 promoter (Thum et al 2008), but also impaired H3K36me3 modifications at genomic loci functionally relevant to NO 3 uptake, resulting in reduced metabolic and developmental responses to N treatments (Li et al 2020). A new study shows that the rice AP2 transcription factor NITROGEN-MEDIATED TILLER GROWTH RESPONSE 5 (NGR5) is positively regulated by N supply, and it interacts directly with PRC2 complex and consequently alters the genome-wide H3K27me3 pattern, thus regulating the expressions of N-responsive genes in response to N availability (Wu et al 2020b).…”

Section: Local Nitrate Signalingmentioning

confidence: 99%

Improving coordination of plant growth and nitrogen metabolism for sustainable agriculture

Han

et al. 2020

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The agricultural green revolution of the 1960s boosted cereal crop yield was in part due to cultivation of semi-dwarf green revolution varieties. The semi-dwarf plants resist lodging and require high nitrogen (N) fertilizer inputs to maximize yield. To produce higher grain yield, inorganic fertilizer has been overused by Chinese farmers in intensive crop production. With the ongoing increase in the food demand of global population and the environmental pollution, improving crop productivity with reduced N supply is a pressing challenge. Despite a great deal of research efforts, to date only a few genes that improve N use efficiency (NUE) have been identified. The molecular mechanisms underlying the coordination of plant growth, carbon (C) and N assimilation is still not fully understood, thus preventing significant improvement. Recent advances have shed light on how explore NUE within an overall plant biology system that considered the co-regulation of plant growth, C and N metabolisms as a whole, rather than focusing specifically on N uptake and assimilation. There are several potential approaches to improve NUE discussed in this review. Increasing knowledge of how plants sense and respond to changes in N availability, as well as identifying new targets for breeding strategies to simultaneously improve NUE and grain yield, could usher in a new green revolution.

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SDG8-Mediated Histone Methylation and RNA Processing Function in the Response to Nitrate Signaling

Cited by 26 publications

References 63 publications

Arabidopsis SDG8 Potentiates the Sustainable Transcriptional Induction of the Pathogenesis-Related Genes PR1 and PR2 During Plant Defense Response

Arabidopsis SDG8 Potentiates the Sustainable Transcriptional Induction of the Pathogenesis-Related Genes PR1 and PR2 During Plant Defense Response

The Dynamic Kaleidoscope of RNA Biology in Plants

Improving coordination of plant growth and nitrogen metabolism for sustainable agriculture

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