Damage-associated responses of the host contribute to defence against cyst nematodes but not root-knot nematodes

Shah, Syed Asim; Anjam, Muhammad Shahzad; Mendy, Badou; Anwer, Muhammad; Habash, Samer S.; Lozano‐Torres, Jose L.; Grundler, Florian M. W.; Siddique, Shahid

doi:10.1093/jxb/erx374

Cited by 61 publications

(69 citation statements)

References 72 publications

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“…Likewise, several host secondary metabolism genes, such as phytoalexin deficient ( PAD3 ), indole glucosinolate o‐methyltransferase 1 ( IGMT1 ), and cytochrome P450 91A1 ( CYP81D1 ), were significantly upregulated in MAS compared with FAS. Intriguingly, we also found that PGIP‐mediated changes in host susceptibility to cyst nematodes involve the activation of genes encoding enzymes for host secondary metabolism (Shah et al, ).…”

Section: Discussionmentioning

confidence: 72%

“…Among them are members of the polygalacturonase‐inhibiting protein gene family ( PGIP1 and PGIP2 ), which are involved in perception and activation of damage‐associated defence responses. The expression of both PGIP1 and PGIP2 was stronger in MAS than in FAS, and loss‐of‐function pgip1 mutants showed a significant increase in the average number of females and a corresponding decrease in the average number of males as compared to Col‐0 (Shah et al, ). Likewise, several host secondary metabolism genes, such as phytoalexin deficient ( PAD3 ), indole glucosinolate o‐methyltransferase 1 ( IGMT1 ), and cytochrome P450 91A1 ( CYP81D1 ), were significantly upregulated in MAS compared with FAS.…”

Section: Discussionmentioning

confidence: 99%

“…Promoter::GUS constructs were introduced into Agrobacterium tumefaciens GV3101 for transformation of Arabidopsis Col‐0 plants by the floral dip method. T3 homozygous lines were generated and analysed for GUS expression as described recently (Shah et al, ). Four plants from each of three transgenic lines per construct were analysed at each time point.…”

Section: Methodsmentioning

confidence: 99%

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Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Anjam

Shah

Matera

et al. 2020

Plant Cell & Environment

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Plant-parasitic cyst nematodes induce hypermetabolic syncytial nurse cells in the roots of their host plants. Syncytia are their only food source. Cyst nematodes are sexually dimorphic, with their differentiation into male or female strongly influenced by host environmental conditions. Under favourable conditions with plenty of nutrients, more females develop, whereas mainly male nematodes develop under adverse conditions such as in resistant plants. Here, we developed and validated a method to predict the sex of beet cyst nematode (Heterodera schachtii) during the early stages of its parasitism in the host plant Arabidopsis thaliana. We collected root segments containing male-associated syncytia (MAS) or female-associated syncytia (FAS), isolated syncytial cells by laser microdissection, and performed a comparative transcriptome analysis. Genes belonging to categories of defence, nutrient deficiency, and nutrient starvation were over-represented in MAS as compared with FAS. Conversely, gene categories related to metabolism, modification, and biosynthesis of cell walls were over-represented in FAS. We used β-glucuronidase analysis, qRT-PCR, and loss-of-function mutants to characterize FAS-and MAS-specific candidate genes. Our results demonstrate that various plant-based factors, including immune response, nutrient availability, and structural modifications, influence the sexual fate of the cyst nematodes. K E Y W O R D S cyst nematodes, environmental sex determination, plant-nematode interaction, host-plant interaction

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Section: Discussionmentioning

confidence: 72%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Anjam

Shah

Matera

et al. 2020

Plant Cell & Environment

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“…CNs J2s are destructive, moving intracellularly and piercing cells with their stylets. In contrast, RKNs J2s cause comparatively little damage, as they move intercellularly through root tissue (Sijmons et al ., ; Wyss et al ., ; Shah et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Root endodermal barrier system contributes to defence against plant‐parasitic cyst and root‐knot nematodes

et al. 2019

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Plant-parasitic nematodes (PPNs) cause tremendous yield losses worldwide in almost all economically important crops. The agriculturally most important PPNs belong to a small group of root-infecting sedentary endoparasites that includes cyst and root-knot nematodes. Both cyst and root-knot nematodes induce specialized long-term feeding structures in root vasculature from which they obtain their nutrients. A specialized cell layer in roots called the endodermis, which has cell walls reinforced with suberin deposits and a lignin-based Casparian strip (CS), protects the vascular cylinder against abiotic and biotic threats. To date, the role of the endodermis, and especially of suberin and the CS, during plant-nematode interactions was largely unknown. Here, we analyzed the role of suberin and CS during interaction between Arabidopsis plants and two sedentary root-parasitic nematode species, the cyst nematode Heterodera schachtii and the root-knot nematode Meloidogyne incognita. We found that nematode infection damages the endodermis leading to the activation of suberin biosynthesis genes at nematode infection sites. Although feeding sites induced by both cyst and root-knot nematodes are surrounded by endodermis during early stages of infection, the endodermis is degraded during later stages of feeding site development, indicating periderm formation or ectopic suberization of adjacent tissue. Chemical suberin analysis showed a characteristic suberin composition resembling peridermal suberin in nematode-infected tissue. Notably, infection assays using Arabidopsis lines with CS defects and impaired compensatory suberization, revealed that the CS and suberization impact nematode infectivity and feeding site size. Taken together, our work establishes the role of the endodermal barrier system in defence against a soil-borne pathogen.

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“…Although the mechanism of sex determination is not yet fully understood, host factors such as defence activation and nutrient availability influence the sexual outcomes of cyst nematodes (Siddique et al, 2014b, Siddique et al, 2015, Shah et al, 2017. When there is a surplus of nutrients, more females develop.…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii

Radakovic

Anjam

Escobar

et al. 2017

Preprint

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SummarySedentary plant-parasitic cyst nematodes are obligate biotrophs that infect the roots of their host plant. Their parasitism is based on modification of root cells to form a hypermetabolic syncytium from which the nematodes draw their nutrients. The aim of this study was to identify nematode susceptibility genes in Arabidopsis thaliana and to characterize their roles in supporting the parasitism of Heterodera schachtii. By selecting genes that were most strongly upregulated in response to cyst nematode infection, we identified HIPP27 (HEAVY METAL-ASSOCIATED ISOPRENYLATED PLANT PROTEIN 27) as a host susceptibility factor required for beet cyst nematode infection and development. Detailed expression analysis revealed that HIPP27 is a cytoplasmic protein and that HIPP27 is strongly expressed in leaves, young roots and nematode-induced syncytia. Loss-of-function Arabidopsis hipp27 mutants exhibited severely reduced susceptibility to H. schachtii and abnormal starch accumulation in syncytial and peridermal plastids. Our results suggest that HIPP27 is a susceptibility gene in Arabidopsis whose loss-of-function reduces plant susceptibility to cyst nematode infection without increasing susceptibility to other pathogens or negatively affecting plant phenotype.

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Damage-associated responses of the host contribute to defence against cyst nematodes but not root-knot nematodes

Abstract: Expression of polygalacturonase-inhibiting protein (PGIP) genes and production of oligogalacturonides (OGs) form an important component of plant basal resistance against cyst nematodes, but not root-knot nematodes.

Cited by 61 publications

References 72 publications

Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Root endodermal barrier system contributes to defence against plant‐parasitic cyst and root‐knot nematodes

Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii

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