Real-time monitoring of translocation of selected type-III effectors from Xanthomonas oryzae pv. oryzae into rice cells

Bian, H W; Zhang, Liyuan; Chen, Lei; Wang, Wenzhan; Ji, Hongtao; Dong, Hansong

doi:10.1007/s12038-019-9916-0

Cited by 7 publications

(16 citation statements)

References 39 publications

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“…Taken together, our findings in this study and previous works (Wang et al, 2018;Bian et al, 2019;Li et al, 2019;Zhang et al, 2019b) demonstrate that Hpa1, Hpa2, HrpF, and XopN are concomitant translocators of the TALE PthXo1 in the standard Xoo strain PXO99 A while infecting the susceptible rice variety Nipponbare. We further show that in addition to mediate PthXo1 translocation, the three translocators themselves also move into rice cells, wherein XopN has a high quantity and induces suppression of rice defense responses.…”

Section: Discussionsupporting

confidence: 88%

“…We have identified Hpa2, HrpF, and XopN as concomitant translocators of the Xoo TALE PthXo1, which was well studied with respect to its function in determining virulence of the standard Xoo strain PXO99 A on the susceptible variety Nipponbare (Yang et al, 2006;Wang et al, 2018;Bian et al, 2019;Li et al, 2019;Zhang et al, 2019b). Evidence that demonstrates the translocator role has been shown as quantitative changes of PthXo1 translocation in Nipponbare plants inoculated with the WT and genetically modified POX99 A strains in the presence and absence of Hpa2, HrpF, and XopN, respectively.…”

Section: Discussionmentioning

confidence: 99%

“…In agreement with this criterion, Hpa2, HrpF, and XopN regulate the virulent role of PthXo1 by mediating its translocation from bacteria into rice cells, but the three translocators are not required for PthXo1 secretion through the bacterial T3 pathway. Shortly before this study, we have already characterized Hpa1 as a translocator of Xoo TALEs PthXo1 and AvrXa10 trafficking from the bacteria into rice cells, wherein PthXo1 plays a virulent role, but AvrXa10 executes its avirulent function (Wang et al, 2018;Bian et al, 2019). Therefore, Xoo possesses at least four T3-translocators that function concomitantly to facilitate effector translocation.…”

Section: Discussionmentioning

confidence: 99%

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Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice

Zhang

Liu

et al. 2020

Front. Microbiol.

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Type III (T3) proteic effectors occupy most of the virulence determinants in eukaryote-pathogenic Gram-negative bacteria. During infection, bacteria may deploy a nanomachinery called translocon to deliver T3 effectors into host cells, wherein the effectors fulfill their pathological functions. T3 translocon is hypothetically assembled by bacterial translocators, which have been identified as one hydrophilic and two hydrophobic proteins in animal-pathogenic bacteria but remain unclear in plant pathogens. Now we characterize Hpa2, HrpF, and XopN proteins as concomitant T3 translocators in rice bacterial blight pathogen by analyzing pathological consequences of single, double, and triple gene knockout or genetic complementation. Based on these genetic analyses, Hpa2, HrpF, and XopN accordingly contribute to 46.9, 60.3, and 69.8% proportions of bacterial virulence on a susceptible rice variety. Virulence performances of Hpa2, HrpF, and XopN were attributed to their functions in essentially mediating from-bacteria-into-rice-cell translocation of PthXo1, the bacterial T3 effector characteristic of transcription factors targeting plant genes. On average, 61, 62, and 71% of PthXo1 translocation are provided correspondingly by Hpa2, HrpF, and XopN, while they cooperate to support PthXo1 translocation at a greater-than-95% extent. As a result, rice disease-susceptibility gene SWEET11, which is the regulatory target of PthXo1, is activated to confer bacterial virulence and induce the leaf blight disease in rice. Furthermore, the three translocators also undergo translocation, but only XopN is highly translocated to suppress rice defense responses, suggesting that different components of a T3 translocon deploy distinct virulence mechanisms in addition to the common function in mediating bacterial effector translocation.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice

Zhang

Liu

et al. 2020

Front. Microbiol.

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“…Therefore, PIPs are required to extend their function from substrate transport to plant infection and immunity when the circumstances demand it. Emerging evidence suggests the implication of OsPIP1;3 in rice infection by Xoo (Zhang et al, 2018; Bian et al, 2019; Li et al, 2019). In this case, OsPIP1;3 functions with the bacterial hydrophilic protein Hpa1, which belongs to the harpin-group proteins secreted by the T3 secretion pathway of Gram-negative plant-pathogenic bacteria (Wei et al, 1992; Tejeda-Dominguez et al, 2017; Zhang et al, 2018; Li et al, 2019).…”

Section: The Circumstantial Function Of a Pip In T3etmentioning

confidence: 99%

“…Two-domain harpins have potential to associate with the bacterial periplasm or plant cell walls to facilitate assembly of the T3 secretion machinery (Mushegian et al, 1996; Koraimann, 2003; Zhang et al, 2008; Dik et al, 2017; Hausner et al, 2017). One-domain harpins, including Hpa1, target plasma membranes (PMs), where they serve as T3 translocators to mediate T3ET (Kvitko et al, 2007; Bocsanczy et al, 2008; Wang X. et al, 2018; Bian et al, 2019; Li et al, 2019).…”

Section: The Circumstantial Function Of a Pip In T3etmentioning

confidence: 99%

Plant Aquaporins in Infection by and Immunity Against Pathogens – A Critical Review

2019

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Plant aquaporins (AQPs) of the plasma membrane intrinsic protein (PIP) family face constant risk of hijack by pathogens aiming to infect plants. PIPs can also be involved in plant immunity against infection. This review will utilize two case studies to discuss biochemical and structural mechanisms that govern the functions of PIPs in the regulation of plant infection and immunity. The first example concerns the interaction between rice Oryza sativa and the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Xoo). To infect rice, Xoo uses the type III (T3) secretion system to secrete the proteic translocator Hpa1, and Hpa1 subsequently mediates the translocation of T3 effectors secreted by this system. Once shifted from bacteria into rice cells, effectors exert virulent or avirulent effects depending on the susceptibility of the rice varieties. The translocator function of Hpa1 requires cooperation with OsPIP1;3, the rice interactor of Hpa1. This role of OsPIP1;3 is related to regulatory models of effector translocation. The regulatory models have been proposed as, translocon-dependent delivery, translocon-independent pore formation, and effector endocytosis with membrane protein/lipid trafficking. The second case study includes the interaction of Hpa1 with the H 2 O 2 transport channel AtPIP1;4, and the associated consequence for H 2 O 2 signal transduction of immunity pathways in Arabidopsis thaliana , a non-host of Xoo. H 2 O 2 is generated in the apoplast upon induction by a pathogen or microbial pattern. H 2 O 2 from this source translocates quickly into Arabidopsis cells, where it interacts with pathways of intracellular immunity to confer plant resistance against diseases. To expedite H 2 O 2 transport, AtPIP1;4 must adopt a specific conformation in a number of ways, including channel width extension through amino acid interactions and selectivity for H 2 O 2 through amino acid protonation and tautomeric reactions. Both topics will reference relevant studies, conducted on other organisms and AQPs, to highlight possible mechanisms of T3 effector translocation currently under debate, and highlight the structural basis of AtPIP1;4 in H 2 O 2 transport facilitated by gating and trafficking regulation.

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Rice aquaporin OsPIP2;2 is a water‐transporting facilitator in relevance to drought‐tolerant responses

et al. 2021

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In rice ( Oryza sativa ), the PLASMA MEMBRANE INTRINSIC PROTEIN (PIP) family of aquaporin has 11 members, OsPIP1;1 to OsPIP1;3, and OsPIP2;1 to OsPIP2;8, which are hypothesized to facilitate the transport of H 2 O and other small compounds across cell membranes. To date, however, only OsPIP1;2, OsPIP2;1, and OsPIP2;4 have been demonstrated for substrate selectivity in their source plant (rice). In this study, OsPIP2;2 was characterized as the most efficient facilitator of H 2 O transport across cell membranes in comparison with the other 10 OsPIPs. In concomitant tests of all OsPIP s, four genes ( OsPIP1;3 , OsPIP2;1 , OsPIP2;2 , and OsPIP2;4 ) were induced to express in leaves of rice plants following a physiological drought stress, while OsPIP2;2 was expressed to the highest level. After de novo expression in frog oocytes and yeast cells, the four OsPIP proteins were localized to the plasma membranes in trimer and tetramer and displayed the activity to increase the membrane permeability to H 2 O. In comparison, OsPIP2;2 was most supportive to H 2 O import to oocytes and yeast cells. After de novo expression in tobacco protoplasts, OsPIP2;2 exceeded OsPIP1;3, OsPIP2;1, and OsPIP2;4 to support H 2 O transport across the plasma membranes. OsPIP2;2‐mediated H 2 O transport was accompanied by drought‐tolerant responses, including increases in concentrations of proline and polyamines, both of which are physiological markers of drought tolerance. In rice protoplasts, H 2 O transport and drought‐tolerant responses, which included expression of marker genes of drought tolerance pathway, were considerably enhanced by OsPIP2;2 overexpression but strongly inhibited by the gene silencing. Furthermore, OsPIP2;2 played a role in maintenance of the cell membrane integrity and effectively protected rice cells from electrolyte leakage caused by the physiological drought stress. These results suggest that OsPIP2;2 is a predominant facilitator of H 2 O transport in relevance to drought tolerance in the plant.

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Real-time monitoring of translocation of selected type-III effectors from Xanthomonas oryzae pv. oryzae into rice cells

Cited by 7 publications

References 39 publications

Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice

Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice

Plant Aquaporins in Infection by and Immunity Against Pathogens – A Critical Review

Rice aquaporin OsPIP2;2 is a water‐transporting facilitator in relevance to drought‐tolerant responses

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