Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation

Guo, Xiaoli; Wang, Jianying; Gardner, Michael; Fukuda, Hiroo; Kondo, Yuki; Etchells, J. Peter; Wang, Xiaohong; Mitchum, Melissa G.

doi:10.1371/journal.ppat.1006142

Cited by 62 publications

(81 citation statements)

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“…We observed significant similarities among several cellular processes differentially regulated in 30D08 transgenic lines and cyst nematode‐induced syncytia (Szakasits et al ., ), including cell cycle, hormone metabolism and cell wall modification. In addition, we identified a significant enrichment in the differential regulation of genes encoding several members of transcription factor families in Arabidopsis, including those known to participate in feeding site formation (Szakasits et al ., ; Jin et al ., ; Guo et al ., ; Piya et al ., ). Several biotic stress genes involved in jasmonic acid, salicylic acid, and glucosinolate biosynthesis were also upregulated in the 30D08 transgenic lines.…”

Section: Discussionmentioning

confidence: 98%

“…(Noon et al, 2016). Cyst nematodes also target plant developmental pathways by secreting effector proteins that mimic CLAVATA3/ESR (CLE) signaling peptides of plants (Mitchum et al, 2012;Guo et al, 2017) that interact with receptor-like kinases to initiate developmental changes (Chen et al, 2015;Guo et al, 2015). These nematodes may also directly alter the metabolism of host cells through the secretion of enzymes such as chorismate mutase (Doyle & Lambert, 2003) and effectors that target hormone transporter proteins (Lee et al, 2011) to affect changes in local hormone concentrations at feeding sites.…”

Section: Introductionmentioning

confidence: 99%

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The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

et al. 2018

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Cyst nematodes deliver effector proteins into host cells to manipulate cellular processes and establish a metabolically hyperactive feeding site. The novel 30D08 effector protein is produced in the dorsal gland of parasitic juveniles, but its function has remained unknown. We demonstrate that expression of 30D08 contributes to nematode parasitism, the protein is packaged into secretory granules and it is targeted to the plant nucleus where it interacts with SMU2 (homolog of suppressor of mec-8 and unc-52 2), an auxiliary spliceosomal protein. We show that SMU2 is expressed in feeding sites and an smu2 mutant is less susceptible to nematode infection. In Arabidopsis expressing 30D08 under the SMU2 promoter, several genes were found to be alternatively spliced and the most abundant functional classes represented among differentially expressed genes were involved in RNA processing, transcription and binding, as well as in development, and hormone and secondary metabolism, representing key cellular processes known to be important for feeding site formation. In conclusion, we demonstrated that the 30D08 effector is secreted from the nematode and targeted to the plant nucleus where its interaction with a host auxiliary spliceosomal protein may alter the pre-mRNA splicing and expression of a subset of genes important for feeding site formation.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

et al. 2018

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“…CLAVATA3 is involved in switching between proliferation and differentiation of stem cells in the root apical meristem by regulating the expression of members of the WUSCHEL-LIKE HOMEOBOX (WOX) transcription factor family. Recently, a new type of CLE effectors with similarity to TRACHEARY ELEMENT DIFFERENTION INHIBITORY FACTOR (TDIF) was identified in cyst nematodes (Guo et al, 2017). TDIF/WOX4 signalling promotes the proliferation of the procambial meristem cells and was shown to be involved in parasitism of cyst nematodes.…”

Section: Direct Modulation Of Hormone Homeostasis By Nematodesmentioning

confidence: 99%

Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes

2018

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SUMMARYParallel adaptations enabling the use of plant cells as the primary food source have occurred multiple times in distinct nematode clades. The hallmark of all extant obligate and facultative plant-feeding nematodes is the presence of an oral stylet, which is required for penetration of plant cell walls, delivery of pharyngeal gland secretions into host cells and selective uptake of plant assimilates. Plant parasites from different clades, and even within a single clade, display a large diversity in feeding behaviours ranging from short feeding cycles on single cells to prolonged feeding on highly sophisticated host cell complexes. Despite these differences, feeding of nematodes frequently (but certainly not always) induces common responses in host cells (e.g. endopolyploidization and cellular hypertrophy). It is thought that these host cell responses are brought about by the interplay of effectors and other biological active compounds in stylet secretions of feeding nematodes, but this has only been studied for the most advanced sedentary plant parasites. In fact, these responses are thought to be fundamental for prolonged feeding of sedentary plant parasites on host cells. However, as we discuss in this review, some of these common plant responses to independent lineages of plant parasitic nematodes might also be generic reactions to cell stress and as such their onset may not require specific inputs from plant parasitic nematodes. Sedentary plant parasitic nematodes may utilize effectors and their ability to synthesize other biologically active compounds to tailor these common responses for prolonged feeding on host cells.

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“…These pests present an increasing threat to global food security which is exacerbated by the imposition of restraints on the use of nematicides due to their unacceptable levels of hazard and ecotoxicity. Strategies to improve this situation are highly dependent on achieving a better understanding of the biology underpinning the interaction of these nematodes with their host plants [32,33].…”

Section: Discussionmentioning

confidence: 99%

Identification and characterisation of serotonin signalling in the potato cyst nematodeGlobodera pallidareveals new targets for crop protection

Crisford

Calahorro

Ludlow

et al. 2018

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Plant parasitic nematodes are microscopic pests that invade plant roots and cause extensive damage to crops worldwide. To investigate mechanisms underpinning their parasitic behaviour we used a chemical biology approach: We discovered that reserpine, a plant alkaloid known for its antagonism of the mammalian vesicular monoamine transporter VMAT and ability to impart a global depletion of synaptic biogenic amines in the nervous system, potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show that this effect of reserpine is mediated by an inhibition of serotonergic signalling that is essential for activation of the stylet, a lance-like organ that protrudes from the mouth of the worm and which is used to pierce the host root to gain access. Prompted by this we identified core molecular components of G. pallida serotonin signalling encompassing the target of reserpine, VMAT; the synthetic enzyme for serotonin, tryptophan hydroxylase; the G protein coupled receptor SER-7 and the serotonin-gated chloride channel MOD-1. We found that inhibitors of tryptophan hydroxylase, SER-7 and MOD-1 phenocopy the plant protecting action of reserpine. Thus targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes.

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Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation

Cited by 62 publications

References 53 publications

The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes

Identification and characterisation of serotonin signalling in the potato cyst nematodeGlobodera pallidareveals new targets for crop protection

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