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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

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: "Cyst-ained" research into Heterodera parasitism.

Juvale, Parijat S / Baum, Thomas J

PLoS pathogens

2018 Volume 14, Issue 2, Page(s) e1006791

MeSH term(s)	Animals ; Crops, Agricultural/growth & development ; Crops, Agricultural/parasitology ; Host-Parasite Interactions ; Secernentea Infections/parasitology ; Soil/parasitology ; Tylenchoidea/physiology
Chemical Substances	Soil
Language	English
Publishing date	2018
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1006791
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Article: Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections

Noon, Jason B / Hewezi, Tarek / Baum, Thomas J

Journal of experimental botany. 2019 Mar. 11, v. 70, no. 5

2019

Abstract: Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396–GRF1/3 ... ...

Abstract	Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396–GRF1/3 module is a master regulator of syncytium development in model cyst nematode H. schachtii infection of Arabidopsis. Here, we investigated whether this regulatory system operates similarly in soybean roots and is likewise important for H. glycines infection. We found that a network involving nine MIR396 and 23 GRF genes is important for normal development of soybean roots and that GRF function is specified in the root apical meristem by miR396. All MIR396 genes are down-regulated in the syncytium during its formation phase while, specifically, 11 different GRF genes are up-regulated. The switch to the syncytium maintenance phase coincides with up-regulation of MIR396 and down-regulation of the 11 GRF genes specifically via post-transcriptional regulation by miR396. Furthermore, interference with the miR396–GRF6/8–13/15–17/19 regulatory network, through either overexpression or knockdown experiments, does not affect the number of H. glycines juveniles that enter the vascular cylinder to initiate syncytia, but specifically inhibits efficient H. glycines development to adult females. Therefore, homeostasis in the miR396–GRF6/8–13/15–17/19 regulatory network is essential for productive H. glycines infections.
Keywords	Arabidopsis ; Heterodera glycines ; Heterodera schachtii ; adults ; apical meristems ; cyst nematodes ; females ; gene expression regulation ; genes ; giant cells ; homeostasis ; juveniles ; models ; nematode infections ; plant diseases and disorders ; roots ; soybeans
Language	English
Dates of publication	2019-0311
Size	p. 1653-1668.
Publishing place	Oxford University Press
Document type	Article
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erz022
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Article ; Online: Homeostasis in the soybean miRNA396-GRF network is essential for productive soybean cyst nematode infections.

Noon, Jason B / Hewezi, Tarek / Baum, Thomas J

Journal of experimental botany

2019 Volume 70, Issue 5, Page(s) 1653–1668

Abstract	Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396-GRF1/3 module is a master regulator of syncytium development in model cyst nematode H. schachtii infection of Arabidopsis. Here, we investigated whether this regulatory system operates similarly in soybean roots and is likewise important for H. glycines infection. We found that a network involving nine MIR396 and 23 GRF genes is important for normal development of soybean roots and that GRF function is specified in the root apical meristem by miR396. All MIR396 genes are down-regulated in the syncytium during its formation phase while, specifically, 11 different GRF genes are up-regulated. The switch to the syncytium maintenance phase coincides with up-regulation of MIR396 and down-regulation of the 11 GRF genes specifically via post-transcriptional regulation by miR396. Furthermore, interference with the miR396-GRF6/8-13/15-17/19 regulatory network, through either overexpression or knockdown experiments, does not affect the number of H. glycines juveniles that enter the vascular cylinder to initiate syncytia, but specifically inhibits efficient H. glycines development to adult females. Therefore, homeostasis in the miR396-GRF6/8-13/15-17/19 regulatory network is essential for productive H. glycines infections.
MeSH term(s)	Animals ; Homeostasis ; MicroRNAs/metabolism ; Plant Diseases/parasitology ; Plant Proteins/metabolism ; RNA, Plant/metabolism ; Glycine max/genetics ; Glycine max/parasitology ; Tylenchida/physiology
Chemical Substances	MicroRNAs ; Plant Proteins ; RNA, Plant
Language	English
Publishing date	2019-02-04
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erz022
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Article ; Online: (with research data) Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients.

Noon, Jason B / Baum, Thomas J

BMC evolutionary biology

2016 Volume 16, Page(s) 74

Abstract: Background: Hoplolaimina plant-parasitic nematodes (PPN) are a lineage of animals with many documented cases of horizontal gene transfer (HGT). In a recent study, we reported on three likely HGT candidate genes in the soybean cyst nematode Heterodera ... ...

Abstract	Background: Hoplolaimina plant-parasitic nematodes (PPN) are a lineage of animals with many documented cases of horizontal gene transfer (HGT). In a recent study, we reported on three likely HGT candidate genes in the soybean cyst nematode Heterodera glycines, all of which encode secreted candidate effectors with putative functions in the host plant. Hg-GLAND1 is a putative GCN5-related N-acetyltransferase (GNAT), Hg-GLAND13 is a putative invertase (INV), and Hg-GLAND16 is a putative chorismate mutase (CM), and blastp searches of the non-redundant database resulted in highest similarity to bacterial sequences. Here, we searched nematode and non-nematode sequence databases to identify all the nematodes possible that contain these three genes, and to formulate hypotheses about when they most likely appeared in the phylum Nematoda. We then performed phylogenetic analyses combined with model selection tests of alternative models of sequence evolution to determine whether these genes were horizontally acquired from bacteria. Results: Mining of nematode sequence databases determined that GNATs appeared in Hoplolaimina PPN late in evolution, while both INVs and CMs appeared before the radiation of the Hoplolaimina suborder. Also, Hoplolaimina GNATs, INVs and CMs formed well-supported clusters with different rhizosphere bacteria in the phylogenetic trees, and the model selection tests greatly supported models of HGT over descent via common ancestry. Surprisingly, the phylogenetic trees also revealed additional, well-supported clusters of bacterial GNATs, INVs and CMs with diverse eukaryotes and archaea. There were at least eleven and eight well-supported clusters of GNATs and INVs, respectively, from different bacteria with diverse eukaryotes and archaea. Though less frequent, CMs from different bacteria formed supported clusters with multiple different eukaryotes. Moreover, almost all individual clusters containing bacteria and eukaryotes or archaea contained species that inhabit very similar niches. Conclusions: GNATs were horizontally acquired late in Hoplolaimina PPN evolution from bacteria most similar to the saprophytic and plant-pathogenic actinomycetes. INVs and CMs were horizontally acquired from bacteria most similar to rhizobacteria and Burkholderia soil bacteria, respectively, before the radiation of Hoplolaimina. Also, these three gene groups appear to have been frequent subjects of HGT from different bacteria to numerous, diverse lineages of eukaryotes and archaea, which suggests that these genes may confer important evolutionary advantages to many taxa. In the case of Hoplolaimina PPN, this advantage likely was an improved ability to parasitize plants.
MeSH term(s)	Acetyltransferases/genetics ; Animals ; Bacteria/genetics ; Biological Evolution ; Chorismate Mutase/genetics ; Gene Transfer, Horizontal ; Nematoda/classification ; Nematoda/enzymology ; Nematoda/genetics ; Phylogeny ; beta-Fructofuranosidase/genetics
Chemical Substances	Acetyltransferases (EC 2.3.1.-) ; beta-Fructofuranosidase (EC 3.2.1.26) ; Chorismate Mutase (EC 5.4.99.5)
Language	English
Publishing date	2016-04-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2041493-6
ISSN	1471-2148 ; 1471-2148
ISSN (online)	1471-2148
ISSN	1471-2148
DOI	10.1186/s12862-016-0651-y
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Article ; Online: A novel sugar beet cyst nematode effector 2D01 targets the Arabidopsis HAESA receptor‐like kinase

Verma, Anju / Lin, Marriam / Smith, Dante / Walker, John C. / Hewezi, Tarek / Davis, Eric L. / Hussey, Richard S. / Baum, Thomas J. / Mitchum, Melissa G.

Molecular Plant Pathology. 2022 Dec., v. 23, no. 12 p.1765-1782

2022

Abstract: Plant‐parasitic cyst nematodes use a stylet to deliver effector proteins produced in oesophageal gland cells into root cells to cause disease in plants. These effectors are deployed to modulate plant defence responses and developmental programmes for the ...

Abstract	Plant‐parasitic cyst nematodes use a stylet to deliver effector proteins produced in oesophageal gland cells into root cells to cause disease in plants. These effectors are deployed to modulate plant defence responses and developmental programmes for the formation of a specialized feeding site called a syncytium. The Hg2D01 effector gene, coding for a novel 185‐amino‐acid secreted protein, was previously shown to be up‐regulated in the dorsal gland of parasitic juveniles of the soybean cyst nematode Heterodera glycines, but its function has remained unknown. Genome analyses revealed that Hg2D01 belongs to a highly diversified effector gene family in the genomes of H. glycines and the sugar beet cyst nematode Heterodera schachtii. For functional studies using the model Arabidopsis thaliana–H. schachtii pathosystem, we cloned the orthologous Hs2D01 sequence from H. schachtii. We demonstrate that Hs2D01 is a cytoplasmic effector that interacts with the intracellular kinase domain of HAESA (HAE), a cell surface‐associated leucine‐rich repeat (LRR) receptor‐like kinase (RLK) involved in signalling the activation of cell wall‐remodelling enzymes important for cell separation during abscission and lateral root emergence. Furthermore, we show that AtHAE is expressed in the syncytium and, therefore, could serve as a viable host target for Hs2D01. Infective juveniles effectively penetrated the roots of HAE and HAESA‐LIKE2 (HSL2) double mutant plants; however, fewer nematodes developed on the roots, consistent with a role for this receptor family in nematode infection. Taken together, our results suggest that the Hs2D01–AtHAE interaction may play an important role in sugar beet cyst nematode parasitism.
Keywords	Arabidopsis ; Heterodera glycines ; Heterodera schachtii ; abscission ; cyst nematodes ; genes ; giant cells ; lateral roots ; mutants ; nematode infections ; parasitism ; plant pathology ; protein secretion ; stylets ; sugar beet
Language	English
Dates of publication	2022-12
Size	p. 1765-1782.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1464-6722
ISSN (online)	1364-3703
ISSN	1464-6722
DOI	10.1111/mpp.13263
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Article ; Online: Screening soybean cyst nematode effectors for their ability to suppress plant immunity.

Pogorelko, Gennady / Wang, Jianying / Juvale, Parijat S / Mitchum, Melissa G / Baum, Thomas J

Molecular plant pathology

2020 Volume 21, Issue 9, Page(s) 1240–1247

Abstract: The soybean cyst nematode (SCN), Heterodera glycines, is one of the most destructive pathogens of soybeans. SCN is an obligate and sedentary parasite that transforms host plant root cells into an elaborate permanent feeding site, a syncytium. Formation ... ...

Abstract	The soybean cyst nematode (SCN), Heterodera glycines, is one of the most destructive pathogens of soybeans. SCN is an obligate and sedentary parasite that transforms host plant root cells into an elaborate permanent feeding site, a syncytium. Formation and maintenance of a viable syncytium is an absolute requirement for nematode growth and reproduction. In turn, sensing pathogen attack, plants activate defence responses and may trigger programmed cell death at the sites of infection. For successful parasitism, H. glycines must suppress these host defence responses to establish and maintain viable syncytia. Similar to other pathogens, H. glycines engages in these molecular interactions with its host via effector proteins. The goal of this study was to conduct a comprehensive screen to identify H. glycines effectors that interfere with plant immune responses. We used Nicotiana benthamiana plants infected by Pseudomonas syringae and Pseudomonas fluorescens strains. Using these pathosystems, we screened 51 H. glycines effectors to identify candidates that could inhibit effector-triggered immunity (ETI) and/or pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). We identified three effectors as ETI suppressors and seven effectors as PTI suppressors. We also assessed expression modulation of plant immune marker genes as a function of these suppressors.
MeSH term(s)	Animals ; Host-Parasite Interactions ; Pathogen-Associated Molecular Pattern Molecules/metabolism ; Plant Diseases/immunology ; Plant Diseases/parasitology ; Plant Immunity ; Pseudomonas syringae/genetics ; Pseudomonas syringae/pathogenicity ; Pseudomonas syringae/physiology ; Glycine max/genetics ; Glycine max/immunology ; Glycine max/parasitology ; Nicotiana/genetics ; Nicotiana/immunology ; Nicotiana/microbiology ; Tylenchoidea/genetics ; Tylenchoidea/pathogenicity ; Tylenchoidea/physiology
Chemical Substances	Pathogen-Associated Molecular Pattern Molecules
Language	English
Publishing date	2020-07-16
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1364-3703
ISSN (online)	1364-3703
ISSN	1364-3703
DOI	10.1111/mpp.12972
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Article ; Online: An Effector from the Cyst Nematode

Vijayapalani, Paramasivan / Hewezi, Tarek / Pontvianne, Frederic / Baum, Thomas J

The Plant cell

2018 Volume 30, Issue 11, Page(s) 2795–2812

Abstract: Cyst nematodes are plant-pathogenic animals that secrete effector proteins into plant root cells to alter host gene expression and reprogram these cells to form specialized feeding sites, known as syncytia. The molecular mechanisms of these effectors are ...

Abstract	Cyst nematodes are plant-pathogenic animals that secrete effector proteins into plant root cells to alter host gene expression and reprogram these cells to form specialized feeding sites, known as syncytia. The molecular mechanisms of these effectors are mostly unknown. We determined that the sugar beet cyst nematode (
MeSH term(s)	Acetylation ; Animals ; Arabidopsis/genetics ; Arabidopsis/parasitology ; DNA, Ribosomal/metabolism ; Gene Expression Regulation, Plant ; Histone Deacetylases/genetics ; Histones/metabolism ; Host-Parasite Interactions ; RNA, Ribosomal/metabolism ; Tylenchoidea/pathogenicity
Chemical Substances	DNA, Ribosomal ; Histones ; RNA, Ribosomal ; Histone Deacetylases (EC 3.5.1.98)
Language	English
Publishing date	2018-10-17
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	623171-8
ISSN	1532-298X ; 1040-4651
ISSN (online)	1532-298X
ISSN	1040-4651
DOI	10.1105/tpc.18.00570
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Article ; Online: The plant-parasitic cyst nematode effector GLAND4 is a DNA-binding protein.

Barnes, Stacey N / Wram, Catherine L / Mitchum, Melissa G / Baum, Thomas J

Molecular plant pathology

2018 Volume 19, Issue 10, Page(s) 2263–2276

Abstract: Cyst nematodes are plant pathogens that infect a wide range of economically important crops. One parasitic mechanism employed by cyst nematodes is the production and in planta delivery of effector proteins to modify plant cells and suppress defences to ... ...

Abstract	Cyst nematodes are plant pathogens that infect a wide range of economically important crops. One parasitic mechanism employed by cyst nematodes is the production and in planta delivery of effector proteins to modify plant cells and suppress defences to favour parasitism. This study focuses on GLAND4, an effector of Heterodera glycines and H. schachtii, the soybean and sugar beet cyst nematodes, respectively. We show that GLAND4 is recognized by the plant cellular machinery and is transported to the plant nucleus, an organelle for which little is known about plant nematode effector functions. We show that GLAND4 has DNA-binding ability and represses reporter gene expression in a plant transcriptional assay. One DNA fragment that binds to GLAND4 is localized in an Arabidopsis chromosomal region associated with the promoters of two lipid transfer protein genes (LTP). These LTPs have known defence functions and are down-regulated in the nematode feeding site. When expressed in Arabidopsis, the presence of GLAND4 causes the down-regulation of the two LTP genes in question, which is also associated with increased susceptibility to the plant-pathogenic bacterium Pseudomonas syringae. Furthermore, overexpression of one of the LTP genes reduces plant susceptibility to H. schachtii and P. syringae, confirming that LTP repression probably suppresses plant defences. This study makes GLAND4 one of a small subset of characterized plant nematode nuclear effectors and identifies GLAND4 as the first DNA-binding, plant-parasitic nematode effector.
MeSH term(s)	Arabidopsis/microbiology ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Gene Expression Regulation, Plant ; Host-Parasite Interactions ; Plant Diseases/microbiology
Chemical Substances	Arabidopsis Proteins
Language	English
Publishing date	2018-07-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1464-6722
ISSN (online)	1364-3703
ISSN	1464-6722
DOI	10.1111/mpp.12697
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Article: Esophageal Gland RNA-Seq Resource of a Virulent and Avirulent Population of the Soybean Cyst Nematode

Maier, Tom R / Masonbrink, Rick E / Vijayapalani, Paramasivan / Gardner, Michael / Howland, Amanda D / Mitchum, Melissa G / Baum, Thomas J

Molecular plant-microbe interactions : MPMI

2021 Volume 34, Issue 9, Page(s) 1084–1087

Abstract: The soybean cyst ... ...

Abstract	The soybean cyst nematode
MeSH term(s)	Animals ; Cysts ; Plant Diseases ; RNA-Seq ; Glycine max/genetics ; Tylenchoidea/genetics
Language	English
Publishing date	2021-09-29
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-03-21-0051-A
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