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Pentatricopeptide repeat (PPR) proteins, with tandem 30–40 amino acids, were characterized as one kind of nucleus coding protein. They have been demonstrated to play important roles in RNA editing, plant growth and development, and plant immunity. Although the PPR gene family has been characterized in some plant species, less is known about this family in peanut, especially their functions in response to Ralstonia solanacearum. In this study, we performed a genome-wide analysis to identify PPR genes and their functions in resistance to R. solanacearum. Here, 389, 481, and 1079 PPR genes were identified from Arachis duranensis, Arachis ipaensis, and Arachis hypogaea, respectively. Allopolyploidization was the main reason for the increased number of the AhPPR members. Gene duplication brought about 367 pairs of homologous genes of PPRs in A. hypogaea. Whole-genome replication, tandem repeats, scattered repeats, and unconnected repeats constituted the replication types. The substitution rates of nonsynonymous (Ka) versus synonymous (Ks) of all homologous pairs were less than 1.0, suggesting that the homologous AhPPRs underwent intense purifying selection pressure and remained conserved in both structure and function. RNA-seq and RT-qPCR analyses showed that AhPPR598 gene was highly expressed in the aerial part of peanut and involved in response to R. solanacearum. The transient expression of AhPPR598 in Nicotiana benthamiana induced the HR-mediated cell death, up-regulated expression of resistant marker genes, and enhanced the resistance to R. solanacearum, suggesting AhPPR598 was a positive regulator of immunity by regulating the JA and SA pathways. These results provide a new understanding of the origin, distribution, and evolution of the AhPPR gene family and potential gene resources for peanut-resistant breeding. [ABSTRACT FROM AUTHOR]