Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) encounters versatile environmental conditions during its environmental, epiphytic and endophytic growth. As a successful pathogen and environmental bacteria, Pst DC3000 needs to recognize relevant biotic and/or abiotic conditions and form appropriate behavioral responses through transcriptional and post-transcriptional regulations. In this thesis I focused on flagellar motility, extracytoplasmic function (ECF) sigma factor AlgU and type III secretion system (T3SS) as the functions of interest and reviewed established understandings and new development regarding these systems in Pst DC3000 in chapters one and two. In chapter three I investigated the Pst DC3000 genome for novel motility regulators by using a competitive selection to enrich for mutants with altered swimming motility and using random barcode transposon-site sequencing (RB-TnSeq) to identify genes with significant roles in swimming motility. I identified oxidative stress related anti-sigma factor PSPTO_1042 (chrR) and hypothetical protein encoding PSPTO_4229 as novel motility-altering genes and characterized their impact on swimming motility. In chapter 4 I reported a new socially-induced motility behavior (referred to as baited expansion) where Pst DC3000 displayed socially-induced motility towards nearby colonies of Dickeya dianthicola or Escherichia coli. I determined that baited expansion behavior occurrence was dependent on a chemical gradient generated and maintained by the cognate bait colony and molybdenum cofactor was required for the behavior. In chapter five I investigated how Pst DC3000 transcriptome responds to pH levels the bacteria encounter during pathogenesis and plant-immunity in vitro. I determined that both T3SS and AlgU are activated by acidic pH of 5.5 which is close to the apoplastic pH of uninfected plants, and suppressed at alkalized pH of 7.8 which is similar to the apoplastic pH of plants undergoing activated pathogen-associated-molecular-pattern (PAMP)-triggered immunity. This pH-dependent control requires the presence of periplasmic proteases, AlgW and MucP, that function as part of the environmental sensing system that activates AlgU in specific conditions. Together these results provide a global perspective on regulation of flagellar motility and virulence in Pst DC3000.