HaCRT1 of Heterodera avenae Is Required for the Pathogenicity of the Cereal Cyst Nematode

Liu, Jing; Peng, Huan; Su, Wen; Liu, Mao-Yan; Huang, Wenkun; Dai, Liangying; Peng, Deliang

doi:10.3389/fpls.2020.583584

Cited by 3 publications

(8 citation statements)

References 54 publications

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“…The Calr of the root-knot nematode Meloidogyne incognita suppresses PAMP-triggered immunity (PTI) whilst infecting its host (116); PTI can be considered the innate immune response of plants. A similar effect was encountered when studying the function of Heterodera avenae Calr (HaCalr) (117); the same study showed that treatment of plants with HaCalr reduced the intensity of the respiratory burst and facilitated H. avenae parasitism in early stages. Insects fall victim to parasitism as well: an important immunoprotective mechanism against parasites is the encapsulation of the invading organism, a process that requires hemocyte spreading to occur.…”

Section: Immunomodulatory Effects Of Parasite Calreticulinmentioning

confidence: 56%

The many faces of parasite calreticulin

2023

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Calreticulin from parasites and its vertebrate hosts share ~50% identity and many of its functions are equally conserved. However, the existing amino acid differences can affect its biological performance. Calreticulin plays an important role in Ca2+ homeostasis and as a chaperone involved in the correct folding of proteins within the endoplasmic reticulum. Outside the endoplasmic reticulum, calreticulin is involved in several immunological functions such as complement inhibition, enhancement of efferocytosis, and immune upregulation or inhibition. Several parasite calreticulins have been shown to limit immune responses and promote infectivity, while others are strong immunogens and have been used for the development of potential vaccines that limit parasite growth. Furthermore, calreticulin is essential in the dialogue between parasites and hosts, inducing Th1, Th2 or regulatory responses in a species-specific manner. In addition, calreticulin participates as initiator of endoplasmic reticulum stress in tumor cells and promotion of immunogenic cell death and removal by macrophages. Direct anti-tumoral activity has also been reported. The highly immunogenic and pleiotropic nature of parasite calreticulins, either as positive or negative regulators of the immune response, render these proteins as valuable tools to modulate immunopathologies and autoimmune disorders, as well as a potential treatment of neoplasms. Moreover, the disparities in the amino acid composition of parasite calreticulins might provide subtle variations in the mechanisms of action that could provide advantages as therapeutic tools. Here, we review the immunological roles of parasite calreticulins and discuss possible beneficial applications.

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Section: Immunomodulatory Effects Of Parasite Calreticulinmentioning

confidence: 56%

The many faces of parasite calreticulin

2023

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“…Meanwhile, OsCML31 and OsHMGB1 were fused with nYFP though cloning to pSPYNER173 vectors (Waadt et al, 2008). The A. tumefaciens strain EHA105 containing those recombined constructs were cultured and infiltrated into the leaves of N. benthamiana as previously described (Liu et al, 2020). ER‐GFP(CD3‐955) and ER‐RFP(CD3‐959) were used as endoplasmic reticulum markers (Nelson et al, 2007).…”

Section: Methodsmentioning

confidence: 99%

“…The constructs pYBA‐1143: MgCRT1 and pYBA‐1132: OsCML31 were transformed into A. tumefaciens EHA105 and co‐expressed in N. benthamiana leaves as previously described (Liu et al, 2020). Two days after infiltration, total protein was extracted with native extraction buffer (50 mM tris‐HCl at pH 6.8, 4.5% SDS, 7.5% β‐m2‐mercaptoethanol, 9 M urea, and protease inhibitor cocktail).…”

Section: Methodsmentioning

confidence: 99%

“…Mi‐CRT is produced in the subventral glands of Meloidogyne incognita , and it is secreted into the apoplast of plant tissues to suppress plant during M. incognita parasitism (Jaouannet et al, 2013; Jaubert et al, 2005). HaCRT1 is synthetised in the subventral gland cells of Heterodera avenae second‐stage nematodes (Liu et al, 2020). It was shown to be localised in the endoplasmic reticulum of the plant cell when it was transiently expressed in Nicotiana benthamiana leaves.…”

Section: Introductionmentioning

confidence: 99%

“…It was shown to be localised in the endoplasmic reticulum of the plant cell when it was transiently expressed in Nicotiana benthamiana leaves. HaCRT1 suppressed the expression of defense‐related genes and ROS accumulation in nonhost plant A. thaliana revealing that HaCRT1 interfere host basal defense (Liu et al, 2020). Despite that MiCRT and HaCRT1 have been demonstrated to suppress plant defense, the mechanistic basis of how nematode CRTs manipulate the host immunity is unknown, mainly due to lack of knowledge of their targets in planta .…”

Section: Introductionmentioning

confidence: 99%

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The nematode effector calreticulin competes with the high mobility group protein OsHMGB1 for binding to the rice calmodulin‐like protein OsCML31 to enhance rice susceptibility to Meloidogyne graminicola

Liu,

Zhang,

Wei

et al. 2024

Plant Cell & Environment

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The root‐knot nematode Meloidogyne graminicola secretes effectors into rice tissues to modulate host immunity. Here, we characterised MgCRT1, a calreticulin protein of M. graminicola, and identified its target in the plant. In situ hybridisation showed MgCRT1 mRNA accumulating in the subventral oesophageal gland in J2 nematodes. Immunolocalization indicated MgCRT1 localises in the giant cells during parasitism. Host‐induced gene silencing of MgCRT1 reduced the infection ability of M. graminicola, while over‐expressing MgCRT1 enhanced rice susceptibility to M. graminicola. A yeast two‐hybrid approach identified the calmodulin‐like protein OsCML31 as an interactor of MgCRT1. OsCML31 interacts with the high mobility group protein OsHMGB1 which is a conserved DNA binding protein. Knockout of OsCML31 or overexpression of OsHMGB1 in rice results in enhanced susceptibility to M. graminicola. In contrast, overexpression of OsCML31 or knockout of OsHMGB1 in rice decreases susceptibility to M. graminicola. The GST‐pulldown and luciferase complementation imaging assay showed that MgCRT1 decreases the interaction of OsCML31 and OsHMGB1 in a competitive manner. In conclusion, when M. graminicola infects rice and secretes MgCRT1 into rice, MgCRT1 interacts with OsCML31 and decreases the association of OsCML31 with OsHMGB1, resulting in the release of OsHMGB1 to enhance rice susceptibility.

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Functional characterization of the soybean cyst nematode effector SCN-27D09 using the model plant pathogenic fungus Magnaporthe oryzae-mediated delivery system

Yang

et al. 2022

Phytopathol Res

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Soybean cyst nematode (SCN, Heterodera glycines) is widely considered as the model plant-parasitic nematode, which secretes effector proteins to manipulate host responses. In this study, we cloned a dorsal gland-expressed effector protein SCN-27D09 that belongs to the same family as Hg10A07 in SCN. We used the model plant pathogen rice blast fungus (Magnaporthe oryzae) to quickly predict and characterize the functions of SCN-27D09. By using M. oryzae secretion system in barley, we confirmed that the signal peptide of SCN-27D09 has secretory activity and can guide the protein into the host cells. Heterologous expression of SCN-27D09 in M. oryzae significantly enhanced the susceptibility of barley to M. oryzae. SCN-27D09 can inhibit Bax-triggered cell death when expressed in Nicotiana benthamiana. Overexpression of SCN-27D09 in soybean hairy root also increased the susceptibility of soybean plants to SCN. Moreover, yeast two-hybrid and firefly luciferase complementation imaging assays showed that SCN-27D09 interacts with a soybean plant kinase GmIPK-2. Functional characterization of GmIPK-2 revealed its positive role in soybean resistance, indicating that SCN-27D09 might compromise the function of GmIPK-2 to facilitate nematode infection. Our results not only uncover the biological role of SCN-27D09 in suppressing plant defense responses and therefore promoting nematode parasitism, but also reaffirm the potential application of the model plant pathogenic fungus M. oryzae in investigating the pathogenic roles of candidate effectors of phytonematodes.

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HaCRT1 of Heterodera avenae Is Required for the Pathogenicity of the Cereal Cyst Nematode

Cited by 3 publications

References 54 publications

The many faces of parasite calreticulin

The many faces of parasite calreticulin

The nematode effector calreticulin competes with the high mobility group protein OsHMGB1 for binding to the rice calmodulin‐like protein OsCML31 to enhance rice susceptibility to Meloidogyne graminicola

Functional characterization of the soybean cyst nematode effector SCN-27D09 using the model plant pathogenic fungus Magnaporthe oryzae-mediated delivery system

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