Du Plessis has been given a break for the series, while four other first-choice players Kagiso Rabada, Hashim Amla, Quinton de Kock and JP Duminy have also been rested ahead of the Test series.
Meanwhile, Dwaine Pretorius, who has been a regular member of the national ODI squad during the past season, is the only new cap in the format.
While Aaron Phangiso and Theunis de Bruyn have been left out of the side that took on Sri Lanka, Morne Morkel has been recalled following impressive return in the Champions Trophy.
"We have also been impressed as a panel by the quality of players coming through our franchise and South Africa 'A' system and we are ready to give further opportunities to Andile Phehlukwayo, Mangaliso Mosehle, Jon-Jon Smuts and Dane Paterson who all made their debuts in the recent series against Sri Lanka. Unfortunately, Lungi Ngidi could not be considered because of injury," Linda Zondi, CSA National Selection Panel convener, said.
"This is an exciting opportunity for the newcomers to play alongside world-class and experienced players like AB, Farhaan, David Miller, Imran Tahir, Morne Morkel, Chris Morris and Wayne Parnell," he added.
The first match in Southampton will be followed by games in Taunton (June 23) and Cardiff (June 25).
AB de Villiers (captain), Farhaan Behardien, Reeza Hendricks, Imran Tahir , David Miller , Morne Morkel, Chris Morris, Mangaliso Mosehle, Wayne Parnell , Dane Paterson, Andile Phehlukwayo, Dwaine Pretorius, Tabraiz Shamsi, Jon-Jon Smuts.
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