The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells

Leborgne-Castel, Nathalie; Lherminier, Jeannine; Der, Christophe; Fromentin, Jérôme; Houot, Valérie; Simon-Plas, Françoise

doi:10.1104/pp.107.111716

Cited by 80 publications

(69 citation statements)

References 55 publications

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“…During pathogen infection, endocytosis plays an important role in at least two instances: (i) perception of a bacterial flagellin and oomycete-derived cryptogein associated with endocytosis of its receptor and activation of downstream immune responses, respectively (35,42,43) and (ii) internalization of eukaryotic pathogen effector molecules in the host cell (44). SA is part of the immune response in plants and, therefore, it is plausible that the SA effect on endocytosis is related to its role in these processes.…”

Section: Discussionmentioning

confidence: 99%

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Tejos

Beck

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

100

117

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Removal of cargos from the cell surface via endocytosis is an efficient mechanism to regulate activities of plasma membrane (PM)-resident proteins, such as receptors or transporters. Salicylic acid (SA) is an important plant hormone that is traditionally associated with pathogen defense. Here, we describe an unanticipated effect of SA on subcellular endocytic cycling of proteins. Both exogenous treatments and endogenously enhanced SA levels repressed endocytosis of different PM proteins. The SA effect on endocytosis did not involve transcription or known components of the SA signaling pathway for transcriptional regulation. SA likely targets an endocytic mechanism that involves the coat protein clathrin, because SA interfered with the clathrin incidence at the PM and clathrin-deficient mutants were less sensitive to the impact of SA on the auxin distribution and root bending during the gravitropic response. By contrast, SA did not affect the ligand-induced endocytosis of the FLAGELLIN SENSING2 (FLS2) receptor during pathogen responses. Our data suggest that the established SA impact on transcription in plant immunity and the nontranscriptional effect of SA on clathrin-mediated endocytosis are independent mechanisms by which SA regulates distinct aspects of plant physiology.

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Section: Discussionmentioning

confidence: 99%

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Tejos

Beck

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

100

117

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“…If considerable overlap has been found in the responses to different elicitors, suggesting that they activate conserved basal defense responses (Jones and Dangl, 2006), the particular suite of early signaling events, or associated kinetics and intensity, varies depending on the specific elicitor (Garcia-Brugger et al, 2006). Cryptogein and flagellin trigger common signaling events such as ROS production, medium alkalinization, MAP kinase activation, calcium influx, endocytosis, or induction of gene expression GarciaBrugger et al, 2006;Chinchilla et al, 2007;Denoux et al, 2008;Leborgne-Castel et al, 2008), although some discrepancies exist between these two proteinaceous elicitors. For instance, both elicitors induce changes in nuclear and cytosolic Ca 2+ concentrations, yet the changes vary in magnitude and timing (Lecourieux et al, 2005).…”

Section: Cryptogein Transiently Induces a Modification In Tobacco Celmentioning

confidence: 99%

Modification of Plasma Membrane Organization in Tobacco Cells Elicited by Cryptogein

et al. 2013

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Lipid mixtures within artificial membranes undergo a separation into liquid-disordered and liquid-ordered phases. However, the existence of this segregation into microscopic liquid-ordered phases has been difficult to prove in living cells, and the precise organization of the plasma membrane into such phases has not been elucidated in plant cells. We developed a multispectral confocal microscopy approach to generate ratiometric images of the plasma membrane surface of Bright Yellow 2 tobacco (Nicotiana tabacum) suspension cells labeled with an environment sensitive fluorescent probe. This allowed the in vivo characterization of the global level of order of this membrane, by which we could demonstrate that an increase in its proportion of ordered phases transiently occurred in the early steps of the signaling triggered by cryptogein and flagellin, two elicitors of plant defense reactions. The use of fluorescence recovery after photobleaching revealed an increase in plasma membrane fluidity induced by cryptogein, but not by flagellin. Moreover, we characterized the spatial distribution of liquid-ordered phases on the membrane of living plant cells and monitored their variations induced by cryptogein elicitation. We analyze these results in the context of plant defense signaling, discuss their meaning within the framework of the "membrane raft" hypothesis, and propose a new mechanism of signaling platform formation in response to elicitor treatment.

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“…Important to note that rate of vesicular transport or secretion have not been measured in this study. Interestingly, Leborgne-Castel et al [41] reported ROS dependant increase of clathrin-mediated endocytosis after addition of cryptogein to tobacco Bright Yellow-2 (BY-2) cells followed by the elicitation of defence responses.…”

Section: Discussionmentioning

confidence: 99%

A Proteomic Approach to Evaluate the Effects of Endogenous Expression of Cryptogein Gene in Crypt-Transgenic Plants of Bacopa monnieri

Paul

Nandagopal

Agarwala

et al. 2017

JABB

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Cryptogein, a 10 kDa sterol scavenging protein secreted by the oomycete Phytophthora cryptogea [1], belongs to 'elicitin' class of elicitors [2]. Cryptogein has been used to study the underlying molecular mechanisms of disease resistance in tobacco. Application of purified cryptogein protein, even in nanomolar quantity causes hypersensitive response (HR)-like necrosis in tobacco plants [3] and also induces systemic acquired resistance (SAR) to P. parasitica var nicotianae [4].There are several reports on transformation with cryptogein (crypt) gene aimed to achieve the resistance against plant pathogens. Over expression of β-cryptogein induces HR in tobacco and triggers resistance against P. parasitica var nicotianae [5,6] and other pathogens. Effective increase in biomass and/ or secondary metabolites accumulation in crypt-transgenic cultures in a number of plant species have also been observed [7][8][9], where the crypt gene was either under the constitutive promoter [7] or under the inducible promoter [8]. AbstractCryptogein, a proteinaceous elicitor has been reported to affect growth and secondary metabolism in several plant species. We established two transgenic plant lines of Bacopa monnieri L., an indigenous medicinal species, following Agrobacterium tumefaciens mediated transformation. The transgenic plant lines obtained following transformation with strains LBA4404-nptII-crypt (plant line BmAt-ncrypt) and LBA4404-nptII (plant line BmAt-n), were maintained on selection media i.e. MS medium containing 100 mg/l Kanamycin. To evaluate the effects of endogenous expression of cryptogein gene in crypt-transgenic plants of B. monnieri, in the present study, a proteomic approach was employed. Using 2D-PAGE followed by MALDI TOF MS/MS, we found 54 spots with reproducible differences in abundance (≥ +2 or ≤ -0.5-fold) between the plant lines. Bioinformatics analyses helped their identification, functional annotation and categorization.Significantly upregulated gene expression (p≤ 0.5) of most of the key enzymes of triterpenoid saponin biosynthetic pathway (mevalonate kinase, mvk; mevalonate diphosphate decarboxylase, mdc; squalene synthase, sqs; β-amyrin synthase, bas and UDP-glycosyl transferase 2, ugt 2) in crypt-transgenic plant lines (BmAt-ncrypt) of B. Monnieri was observed as compared to non-transformed (Bm-NT) and empty vector control (BmAt-n) plant lines. Cryptogein-induced ROS production, a typical stress response of plant cells towards cryptogein, was significantly increased (p≤ 0.5) in specific activities and higher abundance of several anti-oxidant enzymes, such as SOD (3.0-5.0-fold), APX (2.3-3.0-fold) and CAT (2.6-fold) in BmAt-ncrypt. The upregulation of CaM (1.6-fold) and calcium-transporting ATPase-2 (2.0-fold) in BmAt-ncrypt indicate possible calcium-dependant cryptogein elicitation. A 3.0-fold increase in EIN3 levels with down-regulation of F-box protein, its regulator also indicate induction of JA-ET signalling pathway in crypt-transgenic plants. This study not only demonstrates involvement of ...

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The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells

Cited by 80 publications

References 55 publications

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Modification of Plasma Membrane Organization in Tobacco Cells Elicited by Cryptogein

A Proteomic Approach to Evaluate the Effects of Endogenous Expression of Cryptogein Gene in Crypt-Transgenic Plants of Bacopa monnieri

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