The Auxin-Regulated Protein ZmAuxRP1 Coordinates the Balance between Root Growth and Stalk Rot Disease Resistance in Maize

To optimize fitness, plants must efficiently allocate their resources between growth and defense. Although phytohormone crosstalk has emerged as a major player in balancing growth and defense, the genetic basis by which plants manage this balance remains elusive. We previously identified a quantitative disease-resistance locus, qRfg2, in maize (Zea mays) that protects against the fungal disease Gibberella stalk rot. Here, through map-based cloning, we demonstrate that the causal gene at qRfg2 is ZmAuxRP1, which encodes a plastid stroma-localized auxin-regulated protein. ZmAuxRP1 responded quickly to pathogen challenge with a rapid yet transient reduction in expression that led to arrested root growth but enhanced resistance to Gibberella stalk rot and Fusarium ear rot. ZmAuxRP1 was shown to promote the biosynthesis of indole-3-acetic acid (IAA), while suppressing the formation of benzoxazinoid defense compounds. ZmAuxRP1 presumably acts as a resource regulator modulating indole-3-glycerol phosphate and/or indole flux at the branch point between the IAA and benzoxazinoid biosynthetic pathways. The concerted interplay between IAA and benzoxazinoids can regulate the growth–defense balance in a timely and efficient manner to optimize plant fitness. Expression of the maize auxin-regulated gene ZmAuxRP1 rapidly and transiently decreases in response to pathogen challenge, leading to retarded root growth and enhanced disease resistance. ZmAuxRP1 promotes the biosynthesis of indole-3-acetic acid (IAA) while it suppresses the formation of benzoxazinoid defense compounds. The concerted interplay between IAA and benzoxazinoids can regulate the growth–defense balance to optimize plant fitness.