In E. coli K-12, absence of dephospho-PtsN, is thought to cause an L-leucine sensitive growth phenotype (LeuS) by hyperactivated K+ uptake mediated impairment of the expression of the ilvBN operon, encoding subunits of the L-valine (Val) sensitive acetohyrodxyacid synthase I (AHAS I), that renders residual AHAS activity susceptible to inhibition by Leu and K+.  This is thought to lead to AHAS insufficiency and a requirement for isoleucine (Ile). Herein we provide an alternate mechanism for LeuS of the ∆ptsN mutant. Genetic and physiological studies with suppressors of the LeuS, indicate that impaired expression of the ilvBN operon jointly caused by the absence of dephospho-PtsN and the presence of Leu coupled to Leu mediated repression of expression of AHAS III leads to AHAS insufficiency rendering residual AHAS activity susceptible to chronic Val stress that may be generated by exogenous Leu. Hyperactivated K+ uptake and an elevated α-ketobutyrate level, mediate elevation of ilvBN expression, and alleviate the LeuS. The requirement of dephospho-PtsN as a positive regulator of ilvBN expression, may buffer Ile biosynthesis against Leu mediated AHAS insufficiency and protect AHAS I function from chronic endogenous Val generated by Leu and could be realised in certain environments that impair AHAS function.