Rapid activation kinetics of the NLR Swordholder underpin nonhost resistance to Phytophthora capsici in Nicotiana tabacum

Nonhost resistance (NHR) represents a durable phenomenon where plants resist nonadapted pathogens. While NHR holds substantial potential for engineering crops with broad-spectrum and durable resistance, its underlying molecular mechanism remains incompletely understood. The oomycete pathogen Phytophthora capsici is nonadapted to Nicotiana tabacum (Nt) but is virulent on the closely related Nicotiana benthamiana (Nb). Here, we demonstrated that both species encode the NLR Swordholder (Swh), which recognizes P. capsici AvrNt effector proteins. NtSwh restores NHR in ntswh mutants, whereas NbSwh confers only partial resistance. Mechanistically, NtSwh exhibits weaker autoinhibition mediated by its amino-terminal extension domains, enabling rapid immune signaling that prevent pathogen effector–mediated suppression; NbSwh’s stronger autoinhibition delays activation, permitting effector suppression. Heterologous expression of NtSwh in tomato enhances field resistance to P. capsici without yield penalty. These findings indicate that the kinetics of NLR can play a key role in defining NHR, in addition to the presence or absence of specific NLRs, providing insights into strategies for breeding durable crop immunity.