A MIF-like effector suppresses plant immunity and facilitates nematode parasitism by interacting with plant annexins

Zhao, Jianlong; Li, Lijuan; Liu, Qian; Liu, Pei; Li, Shuang; Yang, Dan; Chen, Yongpan; Pagnotta, Sophie; Favery, Bruno; Abad, Pierre; Jian, Heng

doi:10.1093/jxb/erz348

Cited by 66 publications

(75 citation statements)

References 107 publications

(133 reference statements)

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“…AtANN1 is now known to be involved in [Ca 2+ ] cyt elevation in response to chitin, salinity stress, heat stress, extracellular hydroxyl radicals and H 2 O 2 [ 26 , 27 , 28 , 50 , 51 , 52 , 53 ]. Here, in roots, it most likely operates downstream of AtDORN1, given the dependency of the root eATP- and eADP-induced [Ca 2+ ] cyt response on this receptor [ 5 ].…”

Section: Discussionmentioning

confidence: 99%

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

Mohammad-Sidik

Sun

Shin

et al. 2021

IJMS

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Extracellular ATP (eATP) has long been established in animals as an important signalling molecule but this is less understood in plants. The identification of Arabidopsis thaliana DORN1 (Does Not Respond to Nucleotides) as the first plant eATP receptor has shown that it is fundamental to the elevation of cytosolic free Ca2+ ([Ca2+]cyt) as a possible second messenger. eATP causes other downstream responses such as increase in reactive oxygen species (ROS) and nitric oxide, plus changes in gene expression. The plasma membrane Ca2+ influx channels involved in eATP-induced [Ca2+]cyt increase remain unknown at the genetic level. Arabidopsis thaliana Annexin 1 has been found to mediate ROS-activated Ca2+ influx in root epidermis, consistent with its operating as a transport pathway. In this study, the loss of function Annexin 1 mutant was found to have impaired [Ca2+]cyt elevation in roots in response to eATP or eADP. Additionally, this annexin was implicated in modulating eATP-induced intracellular ROS accumulation in roots as well as expression of eATP-responsive genes.

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Section: Discussionmentioning

confidence: 99%

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

Mohammad-Sidik

Sun

Shin

et al. 2021

IJMS

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“…Apparently, plant annexins contain protein domains important for regulation of secretion or binding to F-actin, GTP, calcium, and plasma membrane ( Konopka-Postupolska, 2007 ; Lizarbe et al., 2013 ). Plant annexins are also essential for signal transduction during plant growth and development ( Surpin et al., 2003 ), ion homeostasis ( Pittman, 2012 ), salt and drought stress tolerance ( Zhu et al., 2002 ; Hamaji et al., 2009 ; He et al., 2020 ), or plant defense ( Leborgne-Castel and Bouhidel, 2014 ; Zhao et al., 2019 ). Experiments using polyclonal annexin antibody in corn and pea provided evidence that annexins can mediate secretion of cell wall materials during plant growth and development ( Clark et al., 1994 ; Carroll et al., 1998 ).…”

Section: Introductionmentioning

confidence: 99%

Advanced Microscopy Reveals Complex Developmental and Subcellular Localization Patterns of ANNEXIN 1 in Arabidopsis

et al. 2020

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Annexin 1 (ANN1) is the most abundant member of the evolutionary conserved multigene protein superfamily of annexins in plants. Generally, annexins participate in diverse cellular processes, such as cell growth, differentiation, vesicle trafficking, and stress responses. The expression of annexins is developmentally regulated, and it is sensitive to the external environment. ANN1 is expressed in almost all Arabidopsis tissues, while the most abundant is in the root, root hairs, and in the hypocotyl epidermal cells. Annexins were also occasionally proposed to associate with cytoskeleton and vesicles, but they were never developmentally localized at the subcellular level in diverse plant tissues and organs. Using advanced light-sheet fluorescence microscopy (LSFM), we followed the developmental and subcellular localization of GFP-tagged ANN1 in post-embryonic Arabidopsis organs. By contrast to conventional microscopy, LSFM allowed long-term imaging of ANN1-GFP in Arabidopsis plants at near-environmental conditions without affecting plant viability. We studied developmental regulation of ANN1-GFP expression and localization in growing Arabidopsis roots: strong accumulation was found in the root cap and epidermal cells (preferentially in elongating trichoblasts), but it was depleted in dividing cells localized in deeper layers of the root meristem. During root hair development, ANN1-GFP accumulated at the tips of emerging and growing root hairs, which was accompanied by decreased abundance in the trichoblasts. In aerial plant parts, ANN1-GFP was localized mainly in the cortical cytoplasm of trichomes and epidermal cells of hypocotyls, cotyledons, true leaves, and their petioles. At the subcellular level, ANN1-GFP was enriched at the plasma membrane (PM) and vesicles of non-dividing cells and in mitotic and cytokinetic microtubular arrays of dividing cells. Additionally, an independent immunolocalization method confirmed ANN1-GFP association with mitotic and cytokinetic microtubules (PPBs and phragmoplasts) in dividing cells of the lateral root cap. Lattice LSFM revealed subcellular accumulation of ANN1-GFP around the nuclear envelope of elongating trichoblasts. Massive relocation and accumulation of ANN1-GFP at the PM and in Hechtian strands and reticulum in plasmolyzed cells suggest a possible osmoprotective role of ANN1-GFP during plasmolysis/deplasmolysis cycle. This study shows complex developmental and subcellular localization patterns of ANN1 in living Arabidopsis plants.

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“…The M. incognita effector MiMIF-2, which led A. thaliana more susceptible to nematode infection, impaired Ca 2+ influx induced by H 2 O 2 . Compared to wild type, A. thaliana expressing MiMIF-2 exhibited a decrease in Ca 2+ influx when stimulated with H 2 O 2 (Zhao et al, 2019). Here, we found that HaCRT1 suppressed plant immunity and increased the cytosolic Ca 2+ concentration.…”

Section: Discussionmentioning

confidence: 57%

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

Liu

Peng

et al. 2020

Front. Plant Sci.

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Cereal cyst nematodes are sedentary biotrophic endoparasites that secrete effector proteins into plant tissues to transit normal cells into specialized feeding sites and suppress plant defenses. To understand the function of nematode effectors in Heterodera avenae, here, we identified a calreticulin protein HaCRT1, which could suppress the cell death induced by Bax when expressed in Nicotiana benthamiana. HaCRT1 is synthetized in the subventral gland cells of pre-parasitic second-stage nematodes. Real-time PCR assays indicated that the expression of HaCRT1 was highest in parasitic second-stage juveniles. The expression of an HaCRT1-RFP fusion in N. benthamiana revealed that it was localized in the endoplasmic reticulum of the plant cell. The ability of H. avenae infecting plants was significantly reduced when HaCRT1 was knocked down by RNA interference in vitro. Arabidopsis thaliana plants expressing HaCRT1 were more susceptible than wild-type plants to Pseudomonas syringae. The induction of defense-related genes, PAD4, WRKY33, FRK1, and WRKY29, after treatment with flg22 was suppressed in HaCRT1-transgenic plants. Also, the ROS accumulation induced by flg22 was reduced in the HaCRT1-transgenic plants compared to wild-type plants. HaCRT1 overexpression increased the cytosolic Ca 2+ concentration in A. thaliana. These data suggested that HaCRT1 may contribute to the pathogenicity of H. avenae by suppressing host basal defense.

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A MIF-like effector suppresses plant immunity and facilitates nematode parasitism by interacting with plant annexins

Abstract: The plant-parasitic nematode Meloidogyne incognita secretes MIF-like proteins into plant tissues, and MiMIF-2 interacts with two plant annexins to suppress plant immune responses and promote parasitism.

Cited by 66 publications

References 107 publications

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

Annexin 1 Is a Component of eATP-Induced Cytosolic Calcium Elevation in Arabidopsis thaliana Roots

Advanced Microscopy Reveals Complex Developmental and Subcellular Localization Patterns of ANNEXIN 1 in Arabidopsis

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

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