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1. Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae

   Brauer, Elizabeth K; Popescu, George V.; Singh, Dharmendra K.; Calviño, Mauricio; Gupta, Kamala; Gupta, Bhaskar; Chakravarthy, Suma; Popescu, Sorina C. (December 2018, PLoS biology)

   Kamoun, Sophien (Ed.)

   Plant protein kinases form redundant signaling pathways to perceive microbial pathogens and activate immunity. Bacterial pathogens repress cellular immune responses by secreting effectors, some of which bind and inhibit multiple host kinases. To understand how broadly bacterial effectors may bind protein kinases and the function of these kinase interactors, we first tested kinase–effector (K-E) interactions using the Pseudomonas syringae pv. tomato–tomato pathosystem. We tested interactions between five individual effectors (HopAI1, AvrPto, HopA1, HopM1, and HopAF1) and 279 tomato kinases in tomato cells. Over half of the tested kinases interacted with at least one effector, and 48% of these kinases interacted with more than three effectors, suggesting a role in the defense. Next, we characterized the role of select multi-effector–interacting kinases and revealed their roles in basal resistance, effector-triggered immunity (ETI), or programmed cell death (PCD). The immune function of several of these kinases was only detectable in the presence of effectors, suggesting that these kinases are critical when particular cell functions are perturbed or that their role is typically masked. To visualize the kinase networks underlying the cellular responses, we derived signal-specific networks. A comparison of the networks revealed a limited overlap between ETI and basal immunity networks. In addition, the basal immune network complexity increased when exposed to some of the effectors. The networks were used to successfully predict the role of a new set of kinases in basal immunity. Our work indicates the complexity of the larger kinase-based defense network and demonstrates how virulence- and avirulence-associated bacterial effectors alter sectors of the defense network. 

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2. Species-specific microsymbiont discrimination mediated by a Medicago receptor kinase

   https://doi.org/10.1126/sciadv.adp6436  

   Yu, Xiaocheng; Liu, Jinge; Qin, Qiulin; Zribi, Ikram; Yu, Jingyin; Yang, Shengming; Dinkins, Randy D; Fei, Zhangjun; Kereszt, Attila; Zhu, Hongyan (July 2024, Science Advances)

   Host range specificity is a prominent feature of the legume-rhizobial symbiosis.Sinorhizobium melilotiandSinorhizobium medicaeare two closely related species that engage in root nodule symbiosis with legume plants of theMedicagogenus, but certainMedicagospecies exhibit selectivity in their interactions with the two rhizobial species. We have identified aMedicagoreceptor–like kinase, which can discriminate between the two bacterial species, acting as a genetic barrier against infection by mostS. medicaestrains. Activation of this receptor-mediated nodulation restriction requires a bacterial gene that encodes a glycine-rich octapeptide repeat protein with distinct variants capable of distinguishingS. medicaefromS. meliloti. This study sheds light on the coevolution of host plants and rhizobia, shaping symbiotic selectivity in their respective ecological niches. 

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3. Regulation of biotic interactions and responses to abiotic stresses by MAP kinase pathways in plant pathogenic fungi

   https://doi.org/10.1007/s44154-021-00004-3  

   Zhang, Xue; Wang, Zeyi; Jiang, Cong; Xu, Jin-Rong (December 2021, Stress Biology)

   Abstract Like other eukaryotes, fungi use MAP kinase (MAPK) pathways to mediate cellular changes responding to external stimuli. In the past two decades, three well-conserved MAP kinase pathways have been characterized in various plant pathogenic fungi for regulating responses and adaptations to a variety of biotic and abiotic stresses encountered during plant infection or survival in nature. The invasive growth (IG) pathway is homologous to the yeast pheromone response and filamentation pathways. In plant pathogens, the IG pathway often is essential for pathogenesis by regulating infection-related morphogenesis, such as appressorium formation, penetration, and invasive growth. The cell wall integrity (CWI) pathway also is important for plant infection although the infection processes it regulates vary among fungal pathogens. Besides its universal function in cell wall integrity, it often plays a minor role in responses to oxidative and cell wall stresses. Both the IG and CWI pathways are involved in regulating known virulence factors as well as effector genes during plant infection and mediating defenses against mycoviruses, bacteria, and other fungi. In contrast, the high osmolarity growth (HOG) pathway is dispensable for virulence in some fungi although it is essential for plant infection in others. It regulates osmoregulation in hyphae and is dispensable for appressorium turgor generation. The HOG pathway also plays a major role for responding to oxidative, heat, and other environmental stresses and is overstimulated by phenylpyrrole fungicides. Moreover, these three MAPK pathways crosstalk and coordinately regulate responses to various biotic and abiotic stresses. The IG and CWI pathways, particularly the latter, also are involved in responding to abiotic stresses to various degrees in different fungal pathogens, and the HOG pathway also plays a role in interactions with other microbes or fungi. Furthermore, some infection processes or stress responses are co-regulated by MAPK pathways with cAMP or Ca 2+ /CaM signaling. Overall, functions of individual MAP kinase pathways in pathogenesis and stress responses have been well characterized in a number of fungal pathogens, showing the conserved genetic elements with diverged functions, likely by rewiring transcriptional regulatory networks. In the near future, applications of genomics and proteomics approaches will likely lead to better understanding of crosstalk among the MAPKs and with other signaling pathways as well as roles of MAPKs in defense against other microbes (biotic interactions). 

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4. Legionella pneumophila targets autophagosomes and promotes host autophagy during late infection

   https://doi.org/10.1101/2021.07.08.451723  

   Noll, Rebecca R; Pike, Colleen M; Lehman, Stephanie S; Williamson, Chad D; Neunuebel, M Ramona (July 2021, bioRxiv)

   Abstract Autophagy is a fundamental eukaryotic process that mediates clearance of unwanted molecules and facilitates nutrient release. The bacterial pathogenLegionella pneumophilaestablishes an intracellular niche within phagocytes by manipulating host cellular processes, such as autophagy. Effector proteins translocated byL. pneumophila’s Dot/Icm type IV secretion system have been shown to suppress autophagy. However evidence suggests that overall inhibition of autophagy may be detrimental to the bacterium. As autophagy contributes to cellular homeostasis and nutrient acquisition,L. pneumophilamay translocate effectors that promote autophagy for these benefits. Here, we show that effector protein Lpg2411 binds phosphatidylinositol-3-phosphate lipids and preferentially binds autophagosomes. Translocated Lpg2411 accumulates late during infection and co-localizes with the autophagy receptor p62 and ubiquitin. Furthermore, autophagy is inhibited to a greater extent in host cells infected with a mutant strain lacking Lpg2411 compared to those infected with wild-typeL. pneumophila,indicating that Lpg2411 stimulates autophagy to support the bacterium’s intracellular lifestyle. SummaryLegionella pneumophilatranslocates several effector proteins that inhibit autophagic processes. In this study, we find that the effector protein Lpg2411 targets autophagosomes during late stages of infection and promotes autophagy. 

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5. Programmed Proteolysis of Chemotaxis Proteins in Sinorhizobium meliloti : Features in the C-Terminal Region Control McpU Degradation

   https://doi.org/10.1128/JB.00124-20  

   Arapov, Timofey D.; Kim, Jiwoo; Cronin, Rachel M.; Pahima, Maya; Scharf, Birgit E. (August 2020, Journal of Bacteriology)

   Stock, Ann M. (Ed.)

   ABSTRACT Chemotaxis and motility are important traits that support bacterial survival in various ecological niches and in pathogenic and symbiotic host interaction. Chemotactic stimuli are sensed by chemoreceptors or m ethyl-accepting c hemotaxis p roteins (MCPs), which direct the swimming behavior of the bacterial cell. In this study, we present evidence that the cellular abundance of chemoreceptors in the plant symbiont Sinorhizobium meliloti can be altered by the addition of several to as few as one amino acid residues and by including common epitope tags such as 3×FLAG and 6×His at their C termini. To further dissect this phenomenon and its underlying molecular mechanism, we focused on a detailed analysis of the amino acid sensor McpU. Controlled proteolysis is important for the maintenance of an appropriate stoichiometry of chemoreceptors and between chemoreceptors and chemotactic signaling proteins, which is essential for an optimal chemotactic response. We hypothesized that enhanced stability is due to interference with protease binding, thus affecting proteolytic efficacy. Location of the protease recognition site was defined through McpU stability measurements in a series of deletion and amino acid substitution mutants. Deletions in the putative protease recognition site had similar effects on McpU abundance, as did extensions at the C terminus. Our results provide evidence that the programmed proteolysis of chemotaxis proteins in S. meliloti is cell cycle regulated. This posttranslational control, together with regulatory pathways on the transcriptional level, limits the chemotaxis machinery to the early exponential growth phase. Our study identified parallels to cell cycle-dependent processes during asymmetric cell division in Caulobacter crescentus . IMPORTANCE The symbiotic bacterium Sinorhizobium meliloti contributes greatly to growth of the agriculturally valuable host plant alfalfa by fixing atmospheric nitrogen. Chemotaxis of S. meliloti cells toward alfalfa roots mediates this symbiosis. The present study establishes programmed proteolysis as a factor in the maintenance of the S. meliloti chemotaxis system. Knowledge about cell cycle-dependent, targeted, and selective proteolysis in S. meliloti is important to understand the molecular mechanisms of maintaining a suitable chemotaxis response. While the role of regulated protein turnover in the cell cycle progression of Caulobacter crescentus is well understood, these pathways are just beginning to be characterized in S. meliloti . In addition, our study should alert about the cautionary use of epitope tags for protein quantification. 

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