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Article ; Online: Phytopathogens Reprogram Host Alternative mRNA Splicing.

Hewezi, Tarek

2024

Abstract: Alternative splicing (AS) is an evolutionarily conserved cellular process in eukaryotes in which multiple messenger RNA (mRNA) transcripts are produced from a single gene. The concept that AS adds to transcriptome complexity and proteome diversity ... ...

Abstract	Alternative splicing (AS) is an evolutionarily conserved cellular process in eukaryotes in which multiple messenger RNA (mRNA) transcripts are produced from a single gene. The concept that AS adds to transcriptome complexity and proteome diversity introduces a new perspective for understanding how phytopathogen-induced alterations in host AS cause diseases. Recently, it has been recognized that AS represents an integral component of the plant immune system during parasitic, commensalistic, and symbiotic interactions. Here, I provide an overview of recent progress detailing the reprogramming of plant AS by phytopathogens and the functional implications on disease phenotypes. Additionally, I discuss the vital function of AS of immune receptors in regulating plant immunity and how phytopathogens use effector proteins to target key components of the splicing machinery and exploit alternatively spliced variants of immune regulators to negate defense responses. Finally, the functional association between AS and nonsense-mediated mRNA decay in the context of plant-pathogen interface is recapitulated.
Language	English
Publishing date	2024-05-01
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	207934-3
ISSN	1545-2107 ; 0066-4286
ISSN (online)	1545-2107
ISSN	0066-4286
DOI	10.1146/annurev-phyto-121423-041908
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Article ; Online: Epigenetic Mechanisms in Nematode-Plant Interactions.

Hewezi, Tarek

Annual review of phytopathology

2020 Volume 58, Page(s) 119–138

Abstract: Epigenetic mechanisms play fundamental roles in regulating numerous biological processes in various developmental and environmental contexts. Three highly interconnected epigenetic control mechanisms, including small noncoding RNAs, DNA methylation, and ... ...

Abstract	Epigenetic mechanisms play fundamental roles in regulating numerous biological processes in various developmental and environmental contexts. Three highly interconnected epigenetic control mechanisms, including small noncoding RNAs, DNA methylation, and histone modifications, contribute to the establishment of plant epigenetic profiles. During the past decade, a growing body of experimental work has revealed the intricate, diverse, and dynamic roles that epigenetic modifications play in plant-nematode interactions. In this review, I summarize recent progress regarding the functions of small RNAs in mediating plant responses to infection by cyst and root-knot nematodes, with a focus on the functions of microRNAs. I also recapitulate recent advances in genome-wide DNA methylation analysis and discuss how cyst nematodes induce extensive and dynamic changes in the plant methylome that impact the transcriptional activity of genes and transposable elements. Finally, the potential role of nematode effector proteins in triggering such epigenome changes is discussed.
MeSH term(s)	Animals ; DNA Methylation ; Epigenesis, Genetic ; Genome ; Plants ; Tylenchoidea/genetics
Language	English
Publishing date	2020-05-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	207934-3
ISSN	1545-2107 ; 0066-4286
ISSN (online)	1545-2107
ISSN	0066-4286
DOI	10.1146/annurev-phyto-010820-012805
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Article ; Online: Editorial: epigenetic regulation of plant development and stress responses.

Hewezi, Tarek

Plant cell reports

2017 Volume 37, Issue 1, Page(s) 1–2

MeSH term(s)	Epigenesis, Genetic ; Gene Expression Regulation, Plant ; Histones/metabolism ; Plant Development/genetics ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Plants/genetics ; Plants/metabolism ; Stress, Physiological
Chemical Substances	Histones ; Plant Proteins
Language	English
Publishing date	2017-11-20
Publishing country	Germany
Document type	Editorial
ZDB-ID	8397-5
ISSN	1432-203X ; 0721-085X ; 0721-7714
ISSN (online)	1432-203X
ISSN	0721-085X ; 0721-7714
DOI	10.1007/s00299-017-2233-x
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Article ; Online: Cellular Signaling Pathways and Posttranslational Modifications Mediated by Nematode Effector Proteins.

Hewezi, Tarek

Plant physiology

2015 Volume 169, Issue 2, Page(s) 1018–1026

Abstract: Plant-parasitic cyst and root-knot nematodes synthesize and secrete a suite of effector proteins into infected host cells and tissues. These effectors are the major virulence determinants mediating the transformation of normal root cells into specialized ...

Abstract	Plant-parasitic cyst and root-knot nematodes synthesize and secrete a suite of effector proteins into infected host cells and tissues. These effectors are the major virulence determinants mediating the transformation of normal root cells into specialized feeding structures. Compelling evidence indicates that these effectors directly hijack or manipulate refined host physiological processes to promote the successful parasitism of host plants. Here, we provide an update on recent progress in elucidating the molecular functions of nematode effectors. In particular, we emphasize how nematode effectors modify plant cell wall structure, mimic the activity of host proteins, alter auxin signaling, and subvert defense signaling and immune responses. In addition, we discuss the emerging evidence suggesting that nematode effectors target and recruit various components of host posttranslational machinery in order to perturb the host signaling networks required for immunity and to regulate their own activity and subcellular localization.
MeSH term(s)	Animals ; Cell Wall/parasitology ; Cell Wall/ultrastructure ; Host-Parasite Interactions/physiology ; Indoleacetic Acids/metabolism ; Molecular Mimicry ; Nematoda/metabolism ; Nematoda/pathogenicity ; Phosphorylation ; Plant Proteins/metabolism ; Plants/metabolism ; Plants/parasitology ; Protein Processing, Post-Translational ; Signal Transduction
Chemical Substances	Indoleacetic Acids ; Plant Proteins
Language	English
Publishing date	2015-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1104/pp.15.00923
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Article: Overexpression of soybean

Mazarei, Mitra / Routray, Pratyush / Piya, Sarbottam / Stewart, C Neal / Hewezi, Tarek

Frontiers in plant science

2023 Volume 14, Page(s) 1186292

Abstract: Soybean ( ...

Abstract	Soybean (
Language	English
Publishing date	2023-05-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2023.1186292
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Article ; Online: The soybean immune receptor GmBIR1 regulates host transcriptome, spliceome, and immunity during cyst nematode infection.

Hawk, Tracy E / Piya, Sarbottam / Zadegan, Sobhan Bahrami / Li, Peitong / Rice, John H / Hewezi, Tarek

The New phytologist

2023 Volume 239, Issue 6, Page(s) 2335–2352

Abstract: BAK1-INTERACTING RECEPTOR LIKE KINASE1 (BIR1) is a negative regulator of various aspects of disease resistance and immune responses. Here, we investigated the functional role of soybean (Glycine max) BIR1 (GmBIR1) during soybean interaction with soybean ... ...

Abstract	BAK1-INTERACTING RECEPTOR LIKE KINASE1 (BIR1) is a negative regulator of various aspects of disease resistance and immune responses. Here, we investigated the functional role of soybean (Glycine max) BIR1 (GmBIR1) during soybean interaction with soybean cyst nematode (SCN, Heterodera glycines) and the molecular mechanism through which GmBIR1 regulates plant immunity. Overexpression of wild-type variant of GmBIR1 (WT-GmBIR1) using transgenic soybean hairy roots significantly increased soybean susceptibility to SCN, whereas overexpression of kinase-dead variant (KD-GmBIR1) significantly increased plant resistance. Transcriptome analysis revealed that genes oppositely regulated in WT-GmBIR1 and KD-GmBIR1 upon SCN infection were enriched primarily in defense and immunity-related functions. Quantitative phosphoproteomic analysis identified 208 proteins as putative substrates of the GmBIR1 signaling pathway, 114 of which were differentially phosphorylated upon SCN infection. In addition, the phosphoproteomic data pointed to a role of the GmBIR1 signaling pathway in regulating alternative pre-mRNA splicing. Genome-wide analysis of splicing events provided compelling evidence supporting a role of the GmBIR1 signaling pathway in establishing alternative splicing during SCN infection. Our results provide novel mechanistic insights into the function of the GmBIR1 signaling pathway in regulating soybean transcriptome and spliceome via differential phosphorylation of splicing factors and regulation of splicing events of pre-mRNA decay- and spliceosome-related genes.
MeSH term(s)	Animals ; Transcriptome/genetics ; Glycine max/genetics ; Glycine max/metabolism ; Gene Expression Profiling ; Nematode Infections ; Plant Diseases/genetics ; Tylenchoidea/physiology
Language	English
Publishing date	2023-06-20
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.19087
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Article ; Online: Conceptual Framework of Epigenetic Analyses of Plant Responses to Sedentary Endoparasitic Nematodes.

Hawk, Tracy / Zadegan, Sobhan Bahrami / Ozdemir, Selin / Li, Peitong / Pantalone, Vince / Staton, Meg / Hewezi, Tarek

Methods in molecular biology (Clifton, N.J.)

2024 Volume 2756, Page(s) 327–341

Abstract: Epigenetic modifications including miRNA regulation, DNA methylation, and histone modifications play fundamental roles in establishing the interactions between host plants and parasitic nematodes. Over the past decade, an increasing number of studies ... ...

Abstract	Epigenetic modifications including miRNA regulation, DNA methylation, and histone modifications play fundamental roles in establishing the interactions between host plants and parasitic nematodes. Over the past decade, an increasing number of studies revealed the key functions of various components of the plant epigenome in the regulation of gene expression and shaping plant responses to nematode infection. In this chapter, we provide a conceptual framework for methods used to investigate epigenetic regulation during plant-nematode interactions. We focus specifically on current and emerging methods used to study miRNA regulation and function. We also highlight various methods and analytical tools used to profile DNA methylation patterns and histone modification marks at the genome level. Our intention is simply to explain the advantages of various methods and how to overcome some limitations. With rapid development of single-cell sequencing technology and genome editing, advanced and new methodologies are expected to emerge in the near future to further improve our understanding of epigenetic regulation and function during plant-nematode interactions.
MeSH term(s)	Animals ; Epigenesis, Genetic ; Plant Diseases/genetics ; Plants/genetics ; Plants/parasitology ; DNA Methylation ; MicroRNAs/genetics ; Tylenchoidea/physiology
Chemical Substances	MicroRNAs
Language	English
Publishing date	2024-03-01
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3638-1_12
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Article ; Online: Expression Patterns of DNA Methylation and Demethylation Genes during Plant Development and in Response to Phytohormones.

Bennett, Morgan / Cleaves, Kailyn / Hewezi, Tarek

International journal of molecular sciences

2021 Volume 22, Issue 18

Abstract: DNA methylation and demethylation precisely and effectively modulate gene expression during plant growth and development and in response to stress. However, expression profiles of genes involved in DNA methylation and demethylation during plant ... ...

Abstract	DNA methylation and demethylation precisely and effectively modulate gene expression during plant growth and development and in response to stress. However, expression profiles of genes involved in DNA methylation and demethylation during plant development and their responses to phytohormone treatments remain largely unknown. We characterized the spatiotemporal expression patterns of genes involved in de novo methylation, methyl maintenance, and active demethylation in roots, shoots, and reproductive organs using β-glucuronidase (GUS) reporter lines. Promoters of DNA demethylases were generally more highly active at the mature root tissues, whereas the promoters of genes involved in DNA methylation were more highly active at fast-growing root tissues. The promoter activity also implies that methylation status in shoot apex, leaf primordia, floral organs, and developing embryos is under tight equilibrium through the activity of genes involved in DNA methylation and demethylation. The promoter activity of DNA methylation and demethylation-related genes in response to various phytohormone treatments revealed that phytohormones can alter DNA methylation status in specific and redundant ways. Overall, our results illustrate that DNA methylation and demethylation pathways act synergistically and antagonistically in various tissues and in response to phytohormone treatments and point to the existence of hormone-linked methylome regulation mechanisms that may contribute to tissue differentiation and development.
MeSH term(s)	DNA Methylation ; Gene Expression Regulation, Plant ; Genes, Plant ; Genes, Reporter ; Organ Specificity/genetics ; Plant Development/drug effects ; Plant Growth Regulators/metabolism ; Plant Growth Regulators/pharmacology ; Plants, Genetically Modified ; Promoter Regions, Genetic
Chemical Substances	Plant Growth Regulators
Language	English
Publishing date	2021-09-07
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms22189681
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Article ; Online: miR778 mediates gene expression, histone modification, and DNA methylation during cyst nematode parasitism.

Bennett, Morgan / Piya, Sarbottam / Baum, Thomas J / Hewezi, Tarek

Plant physiology

2022 Volume 189, Issue 4, Page(s) 2432–2453

Abstract: Despite the known critical regulatory functions of microRNAs, histone modifications, and DNA methylation in reprograming plant epigenomes in response to pathogen infection, the molecular mechanisms underlying the tight coordination of these components ... ...

Abstract	Despite the known critical regulatory functions of microRNAs, histone modifications, and DNA methylation in reprograming plant epigenomes in response to pathogen infection, the molecular mechanisms underlying the tight coordination of these components remain poorly understood. Here, we show how Arabidopsis (Arabidopsis thaliana) miR778 coordinately modulates the root transcriptome, histone methylation, and DNA methylation via post-transcriptional regulation of the H3K9 methyltransferases SU(var)3-9 homolog 5 (SUVH5) and SUVH6 upon infection by the beet cyst nematode Heterodera schachtii. miR778 post-transcriptionally silences SUVH5 and SUVH6 upon nematode infection. Manipulation of the expression of miR778 and its two target genes significantly altered plant susceptibility to H. schachtii. RNA-seq analysis revealed a key role of SUVH5 and SUVH6 in reprograming the transcriptome of Arabidopsis roots upon H. schachtii infection. In addition, chromatin immunoprecipitation (ChIP)-seq analysis established SUVH5 and SUVH6 as the main enzymes mediating H3K9me2 deposition in Arabidopsis roots in response to nematode infection. ChIP-seq analysis also showed that these methyltransferases possess distinct DNA binding preferences in that they are targeting transposable elements under noninfected conditions and protein-coding genes in infected plants. Further analyses indicated that H3K9me2 deposition directed by SUVH5 and SUVH6 contributes to gene expression changes both in roots and in nematode feeding sites and preferentially associates with CG DNA methylation. Together, our results uncovered multi-layered epigenetic regulatory mechanisms coordinated by miR778 during Arabidopsis-H. schachtii interactions.
MeSH term(s)	Animals ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Cysts/genetics ; Cysts/metabolism ; DNA Methylation/genetics ; Gene Expression ; Gene Expression Regulation, Plant ; Histone Code ; Methyltransferases/metabolism ; Plant Diseases/genetics ; Plant Roots/genetics ; Plant Roots/metabolism ; Tylenchoidea
Chemical Substances	Arabidopsis Proteins ; Methyltransferases (EC 2.1.1.-)
Language	English
Publishing date	2022-05-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1093/plphys/kiac228
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Article ; Online: GmSABP2-1 encodes methyl salicylate esterase and functions in soybean defense against soybean cyst nematode.

Lin, Jingyu / Wang, Weijiao / Mazarei, Mitra / Zhao, Nan / Chen, Xinlu / Pantalone, Vincent R / Hewezi, Tarek / Stewart, Charles Neal / Chen, Feng

Plant cell reports

2024 Volume 43, Issue 6, Page(s) 138

Abstract: Key message: The soybean gene GmSABP2-1 encodes methyl salicylate esterase and its overexpression led to significant reduction in development of pathogenic soybean cyst nematode. Soybean cyst nematode (SCN, Heterodera glycines) is one of the most ... ...

Abstract	Key message: The soybean gene GmSABP2-1 encodes methyl salicylate esterase and its overexpression led to significant reduction in development of pathogenic soybean cyst nematode. Soybean cyst nematode (SCN, Heterodera glycines) is one of the most devastating pests of soybean (Glycine max L. Merr.). In searching for SCN-defense genes, a soybean gene of the methylesterase (MES) family was found to be upregulated in an SCN-resistant soybean line and downregulated in an SCN-susceptible line upon SCN infection. This gene was designated as GmSABP2-1. Here, we report on biochemical and overexpression studies of GmSABP2-1 to examine its possible function in SCN resistance. The protein encoded by GmSABP2-1 is closely related to known methyl salicylate esterases. To determine the biochemical function of GmSABP2-1, a full-length cDNA of GmSABP2-1 was cloned into a protein expression vector and expressed in Escherichia coli. The resulting recombinant GmSABP2-1 was demonstrated to catalyze the demethylation of methyl salicylate. The biochemical properties of GmSABP2-1 were determined. Its apparent Km value was 46.2 ± 2.2 μM for methyl salicylate, comparable to those of the known methyl salicylate esterases. To explore the biological significance of GmSABP2-1 in soybean defense against SCN, we first overexpressed GmSABP2-1 in transgenic hairy roots of an SCN-susceptible soybean line. When infected with SCN, GmSABP2-1-overexpressing hairy roots showed 84.5% reduction in the development of SCN beyond J2 stage. To provide further genetic evidence for the role of GmSABP2-1 in SCN resistance, stable transgenic soybean plants overexpressing GmSABP2-1 were produced. Analysis of the GmSABP2-1-overexpressing lines showed a significant reduction in SCN development compared to non-transgenic plants. In conclusion, we demonstrated that GmSABP2-1 encodes methyl salicylate esterase and functions as a resistance-related gene against SCN.
MeSH term(s)	Glycine max/genetics ; Glycine max/parasitology ; Animals ; Plant Diseases/parasitology ; Plant Diseases/genetics ; Salicylates/metabolism ; Tylenchoidea/physiology ; Tylenchoidea/pathogenicity ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Plants, Genetically Modified ; Gene Expression Regulation, Plant ; Carboxylic Ester Hydrolases/metabolism ; Carboxylic Ester Hydrolases/genetics ; Disease Resistance/genetics
Chemical Substances	Salicylates ; methyl salicylate (LAV5U5022Y) ; Plant Proteins ; Carboxylic Ester Hydrolases (EC 3.1.1.-)
Language	English
Publishing date	2024-05-11
Publishing country	Germany
Document type	Journal Article
ZDB-ID	8397-5
ISSN	1432-203X ; 0721-085X ; 0721-7714
ISSN (online)	1432-203X
ISSN	0721-085X ; 0721-7714
DOI	10.1007/s00299-024-03224-9
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