Interactions of gene expression, alternative splicing, and DNA methylation in determining nodule identity

Niyikiza, Daniel; Piya, Sarbottam; Routray, Pratyush; Liu, Miao; Kim, Won‐Seok; Burch‐Smith, Tessa M.; Ader, David; Sams, Carl E.; Arelli, Prakash R.; Pantalone, Vincent R.; Krishnan, Hari B.; Hewezi, Tarek

doi:10.1111/tpj.14861

Cited by 29 publications

(40 citation statements)

References 104 publications

(129 reference statements)

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“…A total of 18 methylC-seq libraries, constructed from three biological samples of DNA isolated from nodules at 12, 22, and 36 dpi and the corresponding control root tissues (Niyikiza et al, 2020) were analyzed in this study. Low quality reads and adapters of methylC-seq data were removed with trimmomatic, version 0.35 (Bolger et al, 2014).…”

Section: Identification Of Differentially Methylated Regions Overlapping With Mirna Genesmentioning

confidence: 99%

“…Whole genome bi-sulfite sequencing reads of nodules collected at 12, 22, and 36 days post inoculation (dpi) with Bradyrhizobium diazoefficiens (strain USDA110) and the corresponding root tissues (Niyikiza et al, 2020) were mapped to the promoter FIGURE 1 | Absolute DNA methylation levels across miRNA genes in soybean nodules and roots at 12, 22, and 36 dpi. (A-I): Differences in global DNA methylation levels between nodules and roots over miRNA genes in the CG, CHG, and CHH sequence contexts at 12 (A-C), 22 (D-F), and 36-dpi (G-I).…”

Section: Global Hypermethylation Of Mirna Genes Occurs During Nodule Developmentmentioning

confidence: 99%

“…In contrast to M. truncatula, genome-wide analysis of DNA methylation profiles in three nodule developmental stages in soybean revealed global increases in DNA methylation levels in all sequence contexts as compared with corresponding root tissues (Niyikiza et al, 2020). Identification of the differentially methylated regions and the overlapping genes pointed to a major role of DNA methylation in regulating gene expression and alternative splicing events during nodule differentiation and development (Niyikiza et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…These changes are accompanied and mediated by massive changes in the expression of thousands of genes (Quist et al, 2015;Mergaert et al, 2020). Transcription factor of the GRAS, AP2/ERF, NAC, NF-Y, bZIP, C2H2, bHLH, MYB, and WRKY families are believed to be the key regulators responsible for gene expression changes during nodule differentiation, formation, and development (Schauser et al, 1999;Soyano and Hayashi, 2014;Kawaharada et al, 2017;Liu et al, 2020;Niyikiza et al, 2020;Tan et al, 2020). Also, microRNA (miRNA) genes have been shown to play key regulatory functions during nodulation (Hoang et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Title: Hypermethylation of miRNA Genes During Nodule Development

Piya

Lopes-Caitar

Kim

et al. 2021

Front. Mol. Biosci.

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DNA methylation has recently emerged as a powerful regulatory mechanism controlling the expression of key regulators of various developmental processes, including nodulation. However, the functional role of DNA methylation in regulating the expression of microRNA (miRNA) genes during the formation and development of nitrogen-fixing nodules remains largely unknown. In this study, we profiled DNA methylation patterns of miRNA genes during nodule formation, development, and early senescence stages in soybean (Glycine max) through the analysis of methylC—seq data. Absolute DNA methylation levels in the CG, CHH, and CHH sequence contexts over the promoter and primary transcript regions of miRNA genes were significantly higher in the nodules compared with the corresponding root tissues at these three distinct nodule developmental stages. We identified a total of 82 differentially methylated miRNAs in the nodules compared with roots. Differential DNA methylation of these 82 miRNAs was detected only in the promoter (69), primary transcript region (3), and both in the promoter and primary transcript regions (10). The large majority of these differentially methylated miRNAs were hypermethylated in nodules compared with the corresponding root tissues and were found mainly in the CHH context and showed stage-specific methylation patterns. Differentially methylated regions in the promoters of 25 miRNAs overlapped with transposable elements, a finding that may explain the vulnerability of miRNAs to DNA methylation changes during nodule development. Gene expression analysis of a set of promoter-differentially methylated miRNAs pointed to a negative association between DNA methylation and miRNA expression. Gene Ontology and pathways analyses indicate that changes in DNA methylation of miRNA genes are reprogrammed and contribute to nodule development through indirect regulation of genes involved in cellular processes and pathways with well-established roles in nodulation.

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Section: Identification Of Differentially Methylated Regions Overlapping With Mirna Genesmentioning

confidence: 99%

Section: Global Hypermethylation Of Mirna Genes Occurs During Nodule Developmentmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Title: Hypermethylation of miRNA Genes During Nodule Development

Piya

Lopes-Caitar

Kim

et al. 2021

Front. Mol. Biosci.

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“…For complementation of nip2;1, as well as to provide a mechanism for localization of a native protein construct by fluorescence microscopy, transgenic lines containing a transgene consisting of a NIP2;1-GFP translational fusion under the control of the NIP2;1 promoter were generated in the nip2;1 background. The promoter region of the NIP2;1 gene (from the translational start site to a site 2000 bp upstream) was generated by PCR of Arabidopsis genomic DNA with gene specific primers with added KpnI and AatII restriction sites 21 (Supplemental Table 1) to facilitate insertion into the binary vector pKGW_RedRoot_OCSA (Niyikiza et al, 2020). The modified destination vector was named pKGW_OCSA_NIP2;1Pro.…”

Section: T-dna Insertion Mutant Nip2;1 and Complementation Line A Seqmentioning

confidence: 99%

TheArabidopsis thalianaNIP2;1 Lactic Acid Channel promotes Plant Survival Under Low Oxygen Stress

Beamer

Routray

Choi

et al. 2020

Preprint

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Under anaerobic stress Arabidopsis thaliana induces the expression of a collection of core hypoxia genes that encode proteins associated with an adaptive response. Included in these core hypoxia genes is NIP2;1, which encodes a member of the "Nodulin-like Intrinsic Protein" (NIP) subgroup of the aquaporin superfamily of membrane channel proteins. Under normal growth, NIP2;1 expression is limited to the "anoxia core" region of the root stele, but shows substantial induction in response to low oxygen stress (as high as 1000-fold by 2-4 hr of hypoxia challenge), and accumulates in all root tissues. During hypoxia, NIP2;1-GFP, accumulates on the cell surface by 2 hr and then is distributed between the cell surface and internal membranes during sustained hypoxia, and remains elevated in root tissues through 4 hrs of reoxygenation recovery. T-DNA insertional mutant nip2;1 plants show elevation of lactic acid within root tissues, and a reduced efflux of lactic acid and acidification of the external medium. Together with previous biochemical evidence demonstrating that NIP2;1 has lactic acid permease activity, the present work supports the hypothesis that the protein facilitates the release of cellular lactate to the rhizosphere to prevent lactic acid toxicity. In support of this, nip2;1 plants show poorer survival to argon-induced hypoxia stress. Nip2;1 mutant plants also show elevated expression of ethanolic fermentation transcripts, as well as reduced expression the lactate metabolic enzyme GOX3, suggesting that the altered efflux of lactate through NIP2;1 regulates other pyruvate and lactate metabolism pathways.

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Changes in epigenetic features in legumes under abiotic stresses

Yung

Huang

et al. 2022

The Plant Genome

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Legume crops are rich in nutritional value for human and livestock consumption. With global climate change, developing stress‐resilient crops is crucial for ensuring global food security. Because of their nitrogen‐fixing ability, legumes are also important for sustainable agriculture. Various abiotic stresses, such as salt, drought, and elevated temperatures, are known to adversely affect legume production. The responses of plants to abiotic stresses involve complicated cellular processes including stress hormone signaling, metabolic adjustments, and transcriptional regulations. Epigenetic mechanisms play a key role in regulating gene expressions at both transcriptional and posttranscriptional levels. Increasing evidence suggests the importance of epigenetic regulations of abiotic stress responses in legumes, and recent investigations have extended the scope to the epigenomic level using next‐generation sequencing technologies. In this review, the current knowledge on the involvement of epigenetic features, including DNA methylation, histone modification, and noncoding RNAs, in abiotic stress responses in legumes is summarized and discussed. Since most of the available information focuses on a single aspect of these epigenetic features, integrative analyses involving omics data in multiple layers are needed for a better understanding of the dynamic chromatin statuses and their roles in transcriptional regulation. The inheritability of epigenetic modifications should also be assessed in future studies for their applications in improving stress tolerance in legumes through the stable epigenetic optimization of gene expressions.

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Interactions of gene expression, alternative splicing, and DNA methylation in determining nodule identity

Cited by 29 publications

References 104 publications

Title: Hypermethylation of miRNA Genes During Nodule Development

Title: Hypermethylation of miRNA Genes During Nodule Development

TheArabidopsis thalianaNIP2;1 Lactic Acid Channel promotes Plant Survival Under Low Oxygen Stress

Changes in epigenetic features in legumes under abiotic stresses

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